plants as pest vectors – Page 3 – Center for Invasive Species Prevention

On the Rise: US Imports & the Risks of Tree-killing Pests

containers at Port of Long Beach; photo courtesy of Bob Kanter, Port of Long Beach

Here I update information on two of the major pathways by which tree-killing pests enter the United States: wood packaging and living plants (plant for planting).

Wood Packaging

Looking at wood packaging material, we find rising volumes for both shipping containers – and their accompanying crates and pallets; and dunnage.

Crates and pallets – Angell (2021; full citation at the end of the blog) provides data on North American maritime imports in 2020. The total number of TEUs [a standardized measure for containerized shipment; defined as the equivalent of a 20-foot long container] entering North America was 30,778,446.U.S. ports received 79.6% of these incoming containers, or 24,510,990 TEUs. Four Canadian ports handled 11.4% of the total volume (3,517,464 TEUs; four Mexican ports 8.9% (2,749, 992 TEU). Angell provides data for each of the top 25 ports, including those in Canada and Mexico.

To evaluate the pest risk associated with the containerized cargo, I rely on a pair of two decade-old studies. Haack et al. (2014) determined that approximately 0.1% (one out of a thousand) shipments with wood packaging probably harbor a tree-killing pest. Meissner et al. (2009) found that about 75% of maritime shipments contain wood packaging. Applying these calculations, we estimate that 21,000 of the containers arriving at U.S. and Canadian ports in 2020 might have harbored tree-killing pests.

While the opportunity for pests to arrive is obviously greatest at the ports receiving the highest volumes of containers with wood packaging, the ranking (below) does not tell the full story. The type of import is significant. For example, while Houston ranks sixth for containerized imports, it ranks first for imports of break-bulk (non-containerized) cargo that is often braced by wooden dunnage (see below). Consequently, Houston poses a higher risk than its ranking by containerized shipment might indicate.

Also, Halifax Nova Scotia ranks 22^nd for the number of incoming containerized shipments (258,185 containers arriving). However, three tree-killing pests are known to have been introduced there: beech bark disease (in the 1890s), brown spruce longhorned beetle (in the 1990s), and European leaf-mining weevil (before 2012) [Sweeney, Annapolis 2018]

The top ten ports receiving containerized cargo in 2020 were

Port 2020 market share 2020 TEU volume

Los Angeles 15.6% 4,652,549

Long Beach 13% 3,986,991

New York/New Jersey 12.8% 3,925,469

Savannah 7.5% 2,294,392

Vancouver BC 5.8% 1,797,582

Houston 4.2% 1,288,128

Manzanillo, MX 4.1% 1,275,409

Seattle/Tacoma 4.1% 1,266,839

Virginia ports 4.1% 1,246,609

Charleston 3.3% 1,024,059

Import volumes continue to increase since these imports were recorded. U.S. imports rose substantially in the first half of 2021, especially from Asia. Imports from that content reached 9,523,959 TEUs, up 24.5% from the 7,649,095 TEUs imported in the first half of 2019. The number of containers imported in June was the highest number ever (Mongelluzzo July 12, 2021).

Applying the calculations from Haack et al. (2014) and Meissner et al. (2009) to the 2021 import data, we find that approximately 7,100 containers from Asia probably harbored tree-killing pests in the first six months of the year. (The article unfortunately reports data only for Asia.) Industry representatives quoted by Mongelluzzo expect high import volumes to continue through the summer. This figure also does not consider shipments from other source regions.

Dunnage on the pier at Port of Houston; photo by Port of Houston

Infested dunnage – Looking at dunnage, imports of break-bulk (non-containerized) cargo to Houston – the U.S. port which receives the most – are also on the upswing. Imports in April were up 21% above the pandemic-repressed 2020 levels.

Importers at the port complain that too often the wooden dunnage is infested by pests, despite having been stamped as in compliance with ISPM#15. CBP spokesman John Sagle confirms that CBP inspectors at Houston and other ports are finding higher numbers of infested shipments. CBP does not release those data, so we cannot provide exact numbers (Nodar, July 19, 2021).

The Houston importers’ suspicion has been confirmed by data previously provided by CBP to the Continental Dialogue on Non-Native Insects and Diseases. From Fiscal Year 2010 through Fiscal Year 2015, on average 97% of the wood packaging (all types) found to be infested bore the stamp. CBP no longer provides data that touch on this issue.

Detection of pests in the dunnage leads to severe problems. Importers can face fines up to the full value of the associated cargo. Often, the cargo is re-exported, causing disruption of supply chains and additional financial losses (Nodar, July 19, 2021).

In 2019 importers and shippers from the Houston area formed an informal coalition with the Cary Institute of Ecosystem Studies to try to find a solution to this problem. The chosen approach is for company employees to be trained in CBP’s inspection techniques, then apply those methods at the source of shipments to identify – and reject – suspect dunnage before the shipment is loaded. In addition, the coalition hopes that international inspection companies, which already inspect cargo for other reasons at the loading port will also be trained to inspect for pests. Steps to set up such a training program were interrupted by the COVID-19 pandemic, but are expected to resume soon (Nodar, July 19, 2021).

Meanwhile, the persistence of pests in “treated” wood demands answers to the question of “why”. Is the cause fraud – deliberate misrepresentations that the wood has been treated when it has not? Or is the cause a failure of the treatments – either because they were applied incorrectly or they are inadequate per se?

ISPM#15 is not working adequately. I have said so. Gary Lovett of the Cary Institute has said so (Nodar July 19, 2021). Neither importers nor regulators can rely on the mark to separate pest-free wood packaging from packaging that is infested.

APHIS is the agency responsible for determining U.S. phytosanitary policies. APHIS has so far not accepted its responsibility for determining the cause of this continuing issue and acting to resolve it. Preferably, such detection efforts should be carried out in cooperation with other countries and such international entities as the International Plant Protection Convention (IPPC) and International Union of Forest Research Organizations (IUFRO). However, APHIS should undertake such studies alone, if necessary.

In the meantime, APHIS and CBP should assist importers who are trying to comply by facilitating access to information about which suppliers often supply wood packaging infested by pests. The marks on the wood packaging includes a code identifying the facility that carried out the treatment, so this information is readily available to U.S. authorities.

Plants for Planting

A second major pathway of pest introduction is imports of plants for planting. Data on this pathway are too poor to assess the risk – although a decade ago it was found that the percentage of incoming shipments of plants infested by a pest was 12% – more than ten times higher than the proportion for wood packaging (Liebhold et al. 2012).

According to APHIS’ annual report, in 2020 APHIS and its foreign collaborators inspected 1.05 billion plants in the 23 countries where APHIS has a pre-clearance program. In other words, these plants were inspected before they were shipped to the U.S. At U.S. borders, APHIS inspected and cleared another 1.8 billion “plant units” (cuttings, rooted plants, tissue culture, etc.) and nearly 723,000 kilograms of seeds. Obviously, the various plant types carry very different risks of pest introduction, so lumping them together obscures the pathway’s risk. The report does not indicate whether the total volume of plant imports rose or fell in 2020 compared to earlier years.

SOURCES

Angell, M. 2021. JOC Rankings: Largest North American ports gained marke share in 2020. June 18, 2021. https://www.joc.com/port-news/us-ports/joc-rankings-largest-north-american-ports-gained-market-share-2020_20210618.html?utm_campaign=CL_JOC%20Port%206%2F23%2F21%20%20_PC00000_e-production_E-103506_TF_0623_0900&utm_medium=email&utm_source=Eloqua

Haack R.A., Britton K.O., Brockerhoff, E.G., Cavey, J.F., Garrett, L.J., et al. (2014) Effectiveness of the International Phytosanitary Standard ISPM No. 15 on Reducing Wood Borer Infestation Rates in Wood Packaging Material Entering the United States. PLoS ONE 9(5): e96611. doi:10.1371/journal.pone.0096611

Liebhold, A.M., E.G. Brockerhoff, L.J. Garrett, J.L. Parke, and K.O. Britton. 2012. Live Plant Imports: the Major Pathway for Forest Insect and Pathogen Invasions of the US. www.frontiersinecology.org

Meissner, H., A. Lemay, C. Bertone, K. Schwartzburg, L. Ferguson, L. Newton. 2009. Evaluation of Pathways for Exotic Plant Pest Movement into and within the Greater Caribbean Region. A slightly different version of this report is posted at 45^th Annual Meeting of the Caribbean Food Crops Society https://econpapers.repec.org/paper/agscfcs09/256354.htm

Mogelluzzo, B. July 12, 2021. Strong US imports from Asia in June point to a larger summer surge.

Nodar, J. July 19, 2021. https:www.joc.com/breakbulk/project-cargo/breakbult-volume-recovery-triggers-cbp-invasive-pest-violations_20210719.htm

Posted by Faith Campbell

We welcome comments that supplement or correct factual information, suggest new approaches, or promote thoughtful consideration. We post comments that disagree with us — but not those we judge to be not civil or inflammatory.

For a detailed discussion of the policies and practices that have allowed these pests to enter and spread – and that do not promote effective restoration strategies – review the Fading Forests report at http://treeimprovement.utk.edu/FadingForests.htm

International Phytosanitary System Impedes Prevention

*Eugenia koolauensis* (endangered) damaged by ohia rust; photo courtesy of the U.S. Army Natural Resources Program, Oahu

I have written often about failings of the international phytosanitary systems – starting with my report Fading Forests II in 2004, and continuing in many blogs. As the International Year of Plant Health comes to an end, I do so again. I begin with a key recommendation.

Australia’s experience dealing with myrtle rust (Austropuccina psidii) demonstrates the need to integrate agencies responsible for conservation of natural ecosystems into the determination and implementation of phytosanitary policy.

These environmental agencies should be active participants in setting up surveillance and diagnostics protocols and on-the-ground surveillance, and should be directly involved in emergency response. Federal agricultural agencies have technical expertise in biosecurity but lack expertise in key elements of environmental management. In the Australian context, this recommendation is made by several studies cited by Carnegie and Pegg (2018) – full citation at the end of this blog. I strongly endorse the recommendation for the United States. In the U.S., the appropriate agencies would include USDA’s Forest Service and the Department of Interior’s Fish and Wildlife Service.

While the USDA Forest Service is (apparently) more involved in US phytosanitary efforts than its Australian counterpart, its voice in setting USDA phytosanitary policy is limited to the most narrow details, e.g., treatment protocols for wood packaging.

Carnegie and Pegg note a second common problem: the ongoing decline in forest entomology and pathology capacity in government agencies. This decline has long been decried by U.S. natural resource experts as depriving agencies of needed expertise – but we have not yet managed to raise agency budgets so as to reverse it.

The forests of Australia, New Zealand, nearby islands, and South Africa formed during the period of the supercontinent Gondwana – 300 million years ago. While the threat to these unique forests from non-native pests is severe, so far it arises from a limited number of organisms. These are Phytophthora cinnamomi, Austropuccinia psidii, polyphagous shot hole borer and Fusarium fungus (in South Africa), and – in the future, laurel wilt disease. All these organisms threaten multiple hosts. In contrast, the threat to America’s forests comes from more than 100 highly damaging non-native insects, pathogens, and nematodes already here. Some threaten multiple hosts. Plus there is the constant risk of new introductions. Surely our federal conservation agencies have important resources to defend and expertise to contribute to the effort.

Flaws in the System

The international phytosanitary rules adopted by both the World Trade Organization’s Agreement on the Application of Sanitary and Phytosanitary Measures [WTO SPS Agreement] and the International Plant Protection Convention [IPPC] are fundamentally flawed. That is, they require regulatory officials to be unrealistically certain about an organism’s “pest” potential before regulating it. Yet uncertainty is likely to be at its highest at two critical times: before invasion or at its earliest stage. These times are precisely when phytosanitary actions are likely to be most effective.

The effect of this demand for certainty is exacerbated by decision-makers’ caution when confronted with the potential that their action might harm an economic interest. The vast majority won’t impose a regulation until they are sure that the organism under consideration poses a major threat to plant health.

Yet at the same time, most phytosanitary officials rarely carry out the scientific studies that might answer such questions about the risk.

For example, USDA APHIS has created its own Catch 22. It has not funded laboratory tests to get preliminary information on how vulnerable North American tree genera are to the 38 new Phytophthora species detected in Southeast Asia [see earlier blog]. European scientists are doing this testing; it is unclear whether their work is supported by European governments. American scientists could build on the Europeans’ work since our continents share many plant genera – but since vulnerability might vary at the species level, we still must assess North American species separately. At the same time as APHIS is not sponsoring such tests, it refuses to propose acting under its NAPPRA authority link to temporarily prohibit imports of Asian hosts of the Phytophthoras because it lacks information demonstrating the risk they pose to North American plants!

Sometimes, other agencies step in to fill the gap. Thus, the USDA Forest Service funded research to demonstrate that strains of the ‘ōhi‘a rust pathogen not yet introduced to the U.S. posed a risk to native plants in Hawai`i. (See the linked description and additional information later in this blog.) The Forest Service has also funded “sentinel gardens” – plantings inside the U.S. and abroad that are closely monitored to detect new pests.

British forest pathologist Clive Brasier (white hair) searching for *Phytophthora* species in Vietnam

Three pathogens illustrate the problems clearly:

1) brown alga in the Phytophthora genus;

2) myrtle (or ohia or eucalyptus) rust Austropuccinia psidii; and

3) the ophiostomatoid laurel wilt fungus Raffaelea lauricola.

These organisms present a variety of challenges to various countries. Individually and together, these pathogens threaten to transforms forest floras around the world.

Spread: the first two are spread internationally by movement of plants for planting but also spread locally by rain or wind. The third, laurel wilt fungus, arrived in the U.S. when its insect vector, the redbay ambrosia beetle Xyleborus glabratus, hitched a ride in solid wood packaging material.

How countries prepared for pathogen invasion – not always successfully

Numerous plant pathogens in the Phytophthora genus have long had the attention of phytosanitary officials. However, the species that causes sudden oak death (P. ramorum) was unknown when it was introduced to North America and Europe in the late 1980s or early 1990s. The established phytosanitary measures on two continents failed to detect and prevent its introduction.

areas of Australia vulnerable to myrtle rust; Australian Department of Agriculture and Water Resources

The myrtle rust pathogen was already recognized by phytosanitary officials in Australia, New Zealand, and New Caledonia as a severe potential threat, especially to Eucalyptus in both natural forests and plantations. Its appearance in Hawai`i in 2005 raised the level of concern. However, that awareness neither prevented its entry to Australia (probably, although not certainly, on imported plants or foliage) nor prompted its detection early enough for eradication. New Zealand and New Caledonia became infested by wind transport of the pathogen from Australia. [For a thorough discussion of the Australia’s extensive preparations for possible introduction of this pathogen, see Carnegie and Pegg 2018, full citation at the end of this blog.]

The laurel wilt fungus was unknown before it was detected in Georgia, U.S.A. Phytosanitary officials were certainly aware of the pest risk associated with wood packaging material (see Fading Forests II, chapter 3) but at the time the invasion was detected – 2003 – U.S. regulations required that the wood be debarked only, not treated to kill pests.

redbay tree killed by laurel wilt in Georgia

Pathogens are more difficult to detect and manage than insects. They also get less attention. I can think of three possible reasons: 1) Usually we can’t see a pathogen – we literally can’t put a face on the “enemy”. 2) Disease intensity can vary depending on ecological factors, so it is more difficult to understand than an insect feeding on a plant. 3) In recent decades, many invading insects have been linked to a singlepathway of introduction — wood packaging — while pathogens enter through association with a myriad of imports, especially a variety of imported plants. A single pathway is a concept that is easier to understand and address. Because pathogens get little attention, it is more difficult to obtain data quantifying their risks.

The rapid spread and high mortality of laurel wilt in one host – redbay trees (Persea borbonia) – and threat to a second—sassafras (Sassafras albidum) – have alerted scientists to this threat. The pathogen apparently threatens trees and shrubs in the Lauraceae family that are native to regions other than Southeast Asia. These areas include the tropical Americas, Australia, Madagascar, and islands in the eastern Atlantic (Azores, Canary Islands, and Madeira). I understand that Australian phytosanitary officials are aware of this risk, but I don’t know about officials in the other regions. For example, laurel wilt is not listed among the pathogens thought to pose the greatest risk in Europe, i.e., the A1 list of the European and Mediterranean Plant Protection Organization (EPPO)

Why do some organisms suddenly disperse widely? Who is figuring out why?

The myrtle rust pathogen Austropuccinia psidii experienced a burst of introductions after 2000: it was detected in Hawai`i in 2005, Japan in 2009, Australia in 2010, China in 2011, New Caledonia and South Africa in 2013, Indonesia and Singapore in 2016, and New Zealand in 2017. It is believed to have been carried to Hawai`i on cut vegetation for the floral trade; to New Caledonia and New Zealand by wind from Australia across the Tasman Sea. The introduction pathway to Australia has never been determined, although it first was detected in a nursery. I don’t have information on how it was introduced to Japan or China. Has anyone tried to figure out what triggered this expansion? Was it some fad in horticulture or floriculture? Would it not be useful to learn what happened so we can try to prevent a repetition?

Similar sudden dispersals occurred during roughly the same period for Phytophthora ramorum and the erythrina gall wasp (Quadrastichus erythrinae). The latter spread across the Indian and Pacific oceans within a dozen years of its discovery. Again, was there some fad that prompted international trade in host material? Or did the insect suddenly start utilizing transport facilities such as aircraft interiors or holds? Has anyone tried to figure this out? I doubt anyone is even searching for and recording the presence of the gall wasp now that it is so widespread.

Is the fungal genus Ceratocystis experiencing a similar dispersal burst now? Australian authorities (Carnegie and Pegg 2018) have noted Ceratocystis wilts threatening Acacia and Eucalyptus, as well as Metrosideros.

Efforts often wane at the management and restoration stages.

In the cases of all three pathogens, governments have reduced their efforts once they determined that they could not eradicate the pest.

In North America, USDA APHIS regulates movement of nursery stock with the goal of preventing spread of P. ramorum to the East. The agency has reduced the stringency of its regulations several times over the 18 years it has been regulated. These changes have been made at the urging of the nursery industry in California and Oregon, which are where the pathogen is present. Two years ago, a major regulatory failure resulted in infected plants being shipped to more than 100 retailers in more than a dozen states. This had huge costs to dozens, if not hundreds, of nurseries and state regulatory agencies. Yet APHIS has neither published a straightforward and complete analysis of what went wrong, nor promised to correct any weaknesses revealed by such an analysis. Another apparent regulatory failure is the appearance of the EU1 strain of P. ramorum in the country; this seems to indicate that introductions to North America have occurred more recently than the initial introduction in the late 1980s or early 1990s.

In Hawai`i, concern about the potential impact of myrtle rust on the Islands’ dominant native tree species, ‘ōhi‘a (Metrosideros polymorpha), spurred action. Although myrtle rust spread to all the islands within months, the state imposed an emergency rule prohibiting importation to the state of Myrtaceae plants or cut foliage in 2008. This action was relatively rapid, although it was three years after detection of the pathogen. The rule aimed to prevent introduction of possibly more virulent strains. However, it expired in 2009 (emergency rules are effective for only one year).

Concerned about the possible impacts of various strains, the USDA Forest Service sponsored studies in Brazil. Based on their findings, Hawai`i adopted a new permanent rule in 2020. It prohibited importation of plants or foliage of all Myrtaceae species.

Also, APHIS proposed in November 2019 a federal regulation to support the state’s action through its NAPPRA authority. However, it took seven years to resolve regulators’ concerns about the possible presence and virulence of various strains. During this time importation of high-risk materials was not prohibited. As of this writing, it has been 18 months since APHIS proposed the NAPPRA listing, so federal rules still allow imports of high-risk material.

a surprisingly bad outbreak of rust on ‘ōhi‘a in 2016; cause unclear but possibly related to extremely wet weather; photo by J.B. Friday

Meanwhile, the focus of on-the-ground conservation and restoration efforts in Hawai`i has shifted to different pathogens, those causing rapid ‘ōhi‘a death dontmovefirwood.org

In Australia and New Zealand, federal officials determined within months of detection that myrtle rust was too widespread to be eradicated. They now focus on trying to prevent introduction of additional strains. Within the country, Australia prohibits movement of Myrtaceae (hosts of myrtle rust) to the two states so far free of the pathogen (South and West Australia). However, some scientists believe enforcement of these regulations is too lax. In New Zealand, nurseries are reported to be very careful to produce plants free of the pathogen. Is this sufficient?

The Australian government also funds seed collection and other ex situ conservation efforts. But little funding has been available even for impact studies. In Australia, funding from both state (New South Wales) and federal authorities became available only after designation of three plant species as endangered. The federal government also has not designated myrtle rust as a “key threatening process,” which would have opened access to significant funds and possibly prompted more vigorous regulatory efforts. The rust is included as part of the process “novel biota threat to biodiversity”, but scientists and activists consider this to be insufficient. A conservation strategy https://www.anpc.asn.au/myrtle-rust/ was developed by a coalition of non-governmental organizations and state experts. While never adopted by the federal government, this plan became the basis for a state strategy adopted by New South Wales in 2018 – eight years after the pathogen was first detected. For a thorough discussion of weaknesses in the Australian phytosanitary system’s response to the myrtle rust introduction, see Carnegie and Pegg 2018, full citation at the end of this blog.

In June 2021, the Australian Center for Invasive Species Solutions (CISS) and the office of the Chief Environmental Biosecurity Officer (CEBO) released a revised National Environment and Community Biosecurity RD&E Strategy. The sponsors sought feedback on the strategy from biosecurity and biodiversity researchers, investors, practitioners, the community, government and industry. Comments are due by 16 July 2021. The strategy is posted at https://haveyoursay.awe.gov.au/necbrdes

In New Zealand, the science plan for myrtle rust was described as advisory. The little funding available precludes resistance breeding and seed collection. There is not even a national program to track the rust’s spread.

Difficulties in Assessing Impact

Myrtle rust affects largely new growth of host plants, including flowers and seedlings and root sprouts. Thus, in many – but not all – host species the threat is primarily to reproduction rather than immediate mortality of mature plants. This delay in impacts complicates assessments of the threat posed by the rust.

NGO Action in Australia

After several years’ effort to build a broader coalition to support implementation of the NGO Action Plan, the Plant Biosecurity Science Foundation sponsored an international workshop in March 2021. The goal was to increase understanding of the rust and its impact and who is doing what. Time was devoted to discussions on how coordinate efforts to both raise awareness and spur government action. State and federal officials played prominent roles in both preparation of the Action Plan and the workshop – and did not shy away from criticizing Australia’s handling of the threat. The descriptions of myrtle rust’s impacts presented at the conference were much more dire than those of a few years ago. Information on impacts has accumulated slowly due to the few scientists doing the work. See https://www.apbsf.org.au/myrtle-rust/

Greater alarm about this pathogen is warranted.

Australia – Evidence of Disaster

According to speakers at the workshop, myrtle rust is causing an expanding disaster in Australia, where the flora is dominated by Myrtaceae. As of spring 2021, myrtle rust is widespread and well established in several 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. At this time, 382 of Australia’s Myrtaceae species – in 57 genera – are known to host the rust. 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. However, experts predict extinction of 16 rainforest species within a generation. (For comparison, only 12 plant species in Australia have become extinct since arrival of the first Europeans 200 years ago.) Several speakers at the conference stressed the speed at which rust is putting plant taxa in peril. Wetlands dominated by Melaleuca are apparently under immediate threat.

[For a thorough discussion of the rust’s impact on plant communities, see Carnegie and Pegg 2018, full citation at the end of this blog.]

New Zealand The vulnerability of each of the 27 – 30 native plant species remains unclear three years after the rust’s introduction.

New Caledonia The highly endemic flora of this small island group appears to be at great risk.

In Hawai`i, the rust has devastated one endangered plant species (Eugenia koolauensis) and damaged a non-endangered congener, E. reinwardtiana. The strain currently on the Islands does not threaten the dominant native tree species, ‘ōhi‘a (Metrosideros polymorpha).

Southern Africa

*Syzygium cordatum* South African plant in the Myrtaceae; photo courtesy of Bram van Wyk

South Africa has 24 native plant species in the Myrtaceae. I have been unable to learn the vulnerability of these species to the rust. South Africa relies heavily on plantation of Eucalyptus, some species of which might be vulnerable to the rust. The variant of the rust detected in South Africa 2013 is unique.

*Hetropyxis* sp. – South African plant in the Myrtacae; photo by Daniel L. Nikrent

Posted by Faith Campbell

SOURCES

Angus J. Carnegie, A.J. and G.S. Pegg. 2018. Lessons from the Incursion of Myrtle Rust in Australia. Annual Review of Phytopathology · August 2018

Jung, T.; Horta Jung, M.; Webber, J.F.; Kageyama, K.; Hieno, A.; Masuya, H.; Uematsu, S.; Pérez-Sierra, A.; Harris, A.R.; Forster, J.; et al.. The Destructive Tree Pathogen Phytophthora ramorum Originates from the Laurosilva Forests of East Asia. J. Fungi 2021, 7, 226. https://doi.org/10.3390/ open access!

Sudden Oak Death – two informative articles

I am alerting you to two publications about our “favorite” tree-killing pathogen, Phytopthora ramorum (sudden oak death).

SOD-infected rhododendron in a nursery in Indiana; photo by Indiana Department of Natural Resources

The Role of Nurseries in Spreading SOD

The first article informs the general public and raises important questions: “The Diseased Rhododendrons That Triggered a Federal Plant Hunt” by Ellie Shechet in The New Republic.

Ellie reviews the 2019 episode in which P. ramorum-infected rhododendron plants were shipped to retailers in the East and Midwest. Her article is based on interviews with state plant health and APHIS officials, several scientists and advocates (including me), and the executive director of the Oregon Association of Nurseries (OAN). Ellie notes that infected plants were found at more than 100 locations across 16 states.

Ellie notes that despite the risk to native plants in the eastern deciduous forest and the financial cost of implementing control actions (14 million plants were inspected in Washington State alone), plants have a “green” reputation; they are not recognized as potentially causing environmental harm.

The politics of the situation also are reviewed. She writes that the OAN representative has testified that he helped write the more relaxed regulatory approach that APHIS adopted by “federal order” in 2014 and formalized in changes to the regulations in 2019. APHIS denies this. [The article does not include the information that during this period, state regulatory officials detected P. ramorum-infected plants in between four and ten Oregon nurseries each year.] Ellie notes that individual consumers buying plants have few tools to try to ensure that plants they buy are not infected by SOD or other pathogens.

The fact is that the climate in the coastal areas of California, Oregon, Washington, and British Columbia is conducive to SOD, so the risk of diseased plants being produced there and sold is constant. The current APHIS regulations do not adequately address this, in my view!

Science: High Risk of Phytophthora Introductions from Southeast Asia

The second article reports results of intense scientific effort: Thomas Jung, Joan Webber, Clive Brasier, and other European plant pathologists report more completely on searches for P. ramorum and other Phytophthora species in East Asia. See the full citation at the end of this blog. [I blogged about their preliminary report a little over a year ago.] Jung et al. conclude that P. ramorum probably originates from the laurosilva forests growing in an arc from eastern Myanmar, across northern Laos, Vietnam, and southwestern China (Yunnan) to Shikoku & Kyushu islands in southwest Japan. The article notes that two other Phytophtoras – P. lateralis (cause of fatal disease on Port-Orford cedar) and P. foliorum – appear to be from the same area. Field science by this team has found 38 previously unknown Phytophthora species in these same forests – and expect that more are present.

Clive Brasier in Vietnam; UK Forestry Research

They warn that the lack of information about potential pathogens in many developing countries presents a high risk of introduction to naïve environments through burgeoning horticultural trade – especially since the World Trade Organization requires that a species be named and identified as posing a specific threat before phytosanitary regulations can be applied. [I addressed the issue of international phytosanitary rules in Fading Forests II; see the link at the end of the blog.]

Other Pathogen Risks from the Region

Phytophthoras transported on imported plants are not the only pathogens that could come from Asia. The vectors and associated pathogens causing laurel wilt disease across the Southeast and Fusarium disease in California are believed also to originate in the same region of Asia. Unlike the Phytophthoras, which are transported primarily through the trade in plants for planting, these fungi travel with the vector beetles in wood packaging material. U.S. imports of goods from Asia – often packaged in wooden crates or pallets – have skyrocketed since July 2020. The ports of Los Angeles-Long Beach, which receive 50% of U.S. imports from Asia, handled 6.3 million TEU (twenty-foot equivalent containers) from Asia during the period July 2020 through February 2021. The average of close to 800,000 TEU per month for eight consecutive months is unprecedented. Other ports also saw increased import volumes from Asia during this period. [I discussed these shifts in my blog in January.] Imports from Asia in 2020 accounted for 67.4% of total US imports from the world. Imports from China specifically accounted for 42.1% of total US imports. [Data on import volumes is from several reports posted by the Journal of Commerce at its website: https://www.joc.com/maritime-news/]

SOURCE

Posted by Faith Campbell

Decision!! California Department of Food & Agriculture Upgrades Ranking of Phytophthora occultans

In January 2021, the California Department of Food and Agriculture announced the pest rating for Phytophthora occultans, one of two species of Phytophthora it was reviewing. (Once at the website, click on “comment” – next to name Heather Sheck.)

I blogged about this action in December.

Five people or organizations submitted comments. The most comprehensive comments were submitted by Elizabeth Bernhardt, Ph. D. and Tedmund Swiecki Ph.D. of Phytosphere Research. Another scientist was Tyler Bourret, who had been the first to detect P. occultans in California when working as a student in 2015-16. The third scientist was Jennifer Parke, a plant pathologist at Oregon State University who has worked with Phytophthora species in agriculture and wildland settings for 36 years. Additional comments were submitted by the Phytophthoras in Native Habitats Work Group and me.

All commenters raised some issues. First was the lack of information on the true distribution of P. occultans in California. CDFA restated that it that relies on official records and survey information, and that those records support a “low” rating.

Several issues relate to the definitions that CDFA applies in assigning ranks. They are so restrictive that – in my view – they result in underestimates of pathogens’ potential impacts.

One example is how CDFA recognizes first detections of a pathogen. As Bernhardt and Swiecki point out, CDFA’s consideration of only “official” samples prevents timely action to protect California’s agriculture and native vegetation. In the case of P. occultans, CDFA took no action for two years after the pathogen was first reported in the state. This detection had been confirmed by a CDFA laboratory.

A second example is host range. CDFA says it assigns a host range rating of “wide” (rating of “3”) only to pathogens that have host ranges of hundreds of species. This means that pathogens with dozens of known hosts across several plant families are given a ranking of “moderate” (2). Furthermore, the agency considers only “official” samples in defining hosts. This approach precludes consideration of the high probability that additional hosts would be found in future, including federally listed species in the genera Ceanothus and Arctostaphylos. Bernhardt and Swiecki named two additional hosts based on field work. CDFA responded to the second point by adding a reference to the likely expansion of the host range in the “Uncertainty” section of the document.

Similarly, CDFA gives a reproductive potential rating of “3” only to pathogens spread by a vector or that infect seeds.

CDFA staffers who manage specific pests lack authority to change these too stringent ranking criteria. The agency leadership need to adopt more realistic criteria.

CDFA responded by accepting many of the additional factors raised primarily by Bernhardt and Swiecki. This resulted in raising the overall score from 11 to 14, and changing the ranking from “C” to “B”.

Posted by Faith Campbell

Let’s shape the Biden Administration’s & New Congress’ Policies on Non-Native Forest Pests!

We have a great opportunity to shape future efforts to counter non-native forest pests and diseases. Administration officials are most open to new ideas when they first take office. The same is true of new Congressional leadership.

So now is the time to suggest needed changes!

The USDA Secretary-designate is Tom Vilsack. Of course, he was USDA Secretary during the Obama Administration … so he is not entirely “new” to the issues. However, perspectives and priorities have changed, so now is a good time to urge him to consider new approaches. Furthermore, the Senate Agriculture Committee will hold confirmation hearings for him; we can ask the Senators to advocate for our views during this proceeding.

The House Agriculture Committee has a new Chair, David Scott – from the suburbs of Atlanta, Georgia. Again, this provides an opportunity to suggest new approaches and topics for hearings.

I assume you all are knowledgeable about the numbers and impacts of non-native forest insects and pathogens in the United States, and of the pathways by which they are introduced and spread. If you are not, peruse my blogs about wood packaging or plants as vectors (click on the appropriate “categories” listed at the bottom of the archive of blogs). Or read Fading Forests III (see the link at the end of this blog) and the article I coauthored early this year on improving forest pest management programs.

On the basis of my long experience, I suggest that you encourage USDA Secretary-designate Vilsack, Senators on the Agriculture Committee, and House Agriculture Committee Chair David Scott to consider the following recommendations:

Actions Congress could take

Congress could amend the Plant Protection Act [7 U.S.C. §7701, et seq. (2000)] to prioritize the protection of natural and agricultural resources over the facilitation of trade. This might be done by amending the “findings” section of the statute to give higher priority to pest prevention.
The Agriculture Committees of both the House and Senate could hold hearings on the importation of forest pests. They could determine if the USDA is doing an adequate job protecting the country from insect pests and diseases, and how our defenses could be strengthened. One component of the hearings could focus on whether current funding levels and mechanisms are adequate to support vigorous responses to new pest incursions.
Congress could commission a study of the feasibility, costs and benefits of establishing a “Center for Forest Pest Control and Prevention” to coordinate research and policy on this issue.
Congress could increase funding for the appropriate USDA APHIS and Forest Service programs and activities to enable vigorous containment and eradication responses targeting introduced forest pests and diseases.
Congress could increase funding for USDA research on detection of insects and pathogens in shipping; insect and disease monitoring/surveillance; biological control; alternatives to packaging made from wooden boards; management of established pests; and resistance breeding to enable restoration of impacted tree species.

Actions Secretary-designate Vilsack could initiate without legislative action (once he is confirmed)

Introductions of pests in the wooden crates, pallets, etc., goods come in

APHIS could take emergency action to prohibit use of wood packaging by importers of goods from countries with a record of poor compliance with ISPM#15. This action is allowed under authority of the Plant Protection Act [7 U.S.C. §7701, et seq. (2000)] and Article 5.7 of the World Trade Organization’s Agreement on the Application of Sanitary and Phytosanitary Measures.
APHIS could strengthen enforcement of current regulations by aggressively prosecuting repeat offenders. For instance, APHIS could begin imposing administrative financial penalties on importers each time their wood packaging is non-compliant with ISPM#15.
APHIS could work with Department of Homeland Security Bureau of Customs and Border Protection (CBP) to improve information available to U.S. importers about which foreign suppliers of SWPM and shippers have good vs. bad records of compliance with ISPM#15.
DHS CBP could release information on country of origin and treatment facility for ISPM#15-stamped SWPM that is found to be infested with pests.
USDA APHIS could begin a phased transition from solid wood packaging to alternative materials that cannot carry wood-boring pests. APHIS could initiate a pest risk assessment to justify making such an action permanent. Imports could be packaged in alternative materials, e.g., manufactured wood products (e.g. plywood), metal, or plastic.

Nursery Plant (“Plants for Planting”) Pathway

APHIS could apply authorities under NAPPRA and other existing authorities to curtail imports of plants that pose a high risk of introducing insects and pathogens that would threaten tree species that are important in natural and urban forests in the U.S. At a minimum, APHIS should restrict imports of live plants that are in the same genus as native woody plants of the U.S.
APHIS could work with the Agriculture Research Service and National Institute of Food and Agriculture to determine which taxa of woody vegetation native to the U.S. are vulnerable to pathogens present in natural systems of trade partners. Particularly important would be the many Phytophthora species found by Jung and colleagues in Vietnam, Taiwan, Chile, and other countries. Once the studies are sufficiently complete, APHIS could utilize authority under NAPPRA to prohibit importation of plants from those source countries until effective phytosanitary measures can be identified and adopted.

Other Actions

APHIS could develop procedures to ensure the periodic evaluation of pest approach rates associated with wood packaging and imports of “plants for planting” and highlight areas of program strengths and weaknesses. A good place to start would be to update the study by Haack et al. (2014), which estimated the approach rate in wood packaging a decade ago.
The USDA could expand early detection systems for forest pests, such as the APHIS CAPS program and the Forest Service EDRR program. These programs should be better coordinated with each other and should make better use of citizen observations collected through smartphone apps, professional tree workers such as arborists and utility crews, and university expertise in pest identification and public outreach. An effective program would survey for a broad range of pests as well as for suspicious tree damage, and would be focused on high-risk areas such as forests around seaports, airports, plant nurseries, and facilities such as warehouses that engage in international trade.
The USDA could initiate a “Sentinel Plantings“ network of US tree species planted in gardens abroad and monitored for potential pests and diseases.

Posted by Faith Campbell

Korea seeks (again!) to export high-risk trees to America

dwarfed *Ulmus davidiana*; photo by Krzsztof Zianek; Wikipedia Commons

USDA APHIS is seeking public input on a risk assessment that is intended to evaluate the risk of allowing importation of dwarf elm trees (bunjae) from South Korea. Importation of these trees is currently prohibited under APHIS’ authority to require a risk assessment before importation under the NAPPRA program. Upon receiving the Korean request, APHIS must decide whether to maintain the prohibition, or alter it. The risk assessment can be obtained here. Comments are due January 11, 2021.

I urge those with expert knowledge about phytophagous insects, nematodes, and fungal and other pathogens to prepare your own comments to APHIS.

[A year ago, Korea sought permission to export dwarfed maple trees to the U.S. CISP commented on APHIS’ risk assessment at that time; see my blog here. I believe APHIS has not yet decided whether to allow such imports. Many of the same issues apply here.]

After reviewing the risk assessment, I conclude that there are too many high-risk pests to support removing the taxon from the current restrictions. The history of introductions on dwarfed trees in the past supports this conclusion. The most conspicuous is the citrus longhorned beetle (Anoplophora chinensis) – the reason for the original NAPPRA listing – but there have been others, too.

The risk assessment has some strengths. I applaud the assessors for noting in each pest review that since the proposed imports are propagative material, all the pests will arrive on living hosts. The assessment then discusses – briefly! – the mechanisms by which the pest or pathogen could disperse to infest new trees – e.g., flight, rain splash, irrigation water. However, I think the assessment is sometimes too cautious in describing probable invasive risks.

I also find several important weaknesses in both the risk assessment process generally and specific findings.

Weaknesses of the Risk Assessment Process

The assessors do not discuss the potential efficacy of pest-management actions taken by the exporter or by USDA at ports of entry. They outlined production and harvesting practices that they assumed would apply to the exported plants. They warned that the risk assessment finding could not be applied to plants produced or handled other under conditions.

I am troubled by the assessors’ decision not to consider the plants’ ages and sizes. There is evidence that age and size are very important in determining the likelihood of pest presence. Perhaps the decision reflects the assumption that the exported plants would be less than four years old. Still, the assessors should have been transparent about the reasoning behind this decision.

The assessment underestimates “uncertainty”. One manifestation is the decision to provide little information about whether pests or pathogens known to attack several Eurasian species of Ulmus might also attack North American elm species. This gap arises, I believe, from the International Plant Protection Organization (IPPC) and APHIS requirement that risk analysts consider only pest-host relationships described in the literature or inferred from port interception data. I find this narrow approach to be a weakness, given how many unknown pest-host relationships have proved to be highly damaging. This issue arises specifically in the reviews of the nematode Meloinema kerongense and several powdery mildews (Erysiphe kenjiana, E. ulmi and Podosphaera spiralis) – all of which are identified as affecting at least some elm species.

Perhaps the missing information has fewer consequences here, since the NAPPRA process does not require that APHIS prove the pest-host relationship for every pest evaluated in order to justify retaining the prohibition on importation. The well-documented history of detecting the citrus longhorned beetle in artificially dwarfed trees and as a pest of the Ulmus genus provides more than sufficient justification to retain trade restrictions. Still, if APHIS is conducting a formal risk assessment, it should be thorough. Anything else sets an unfortunate precedent.

Finally, in cases when some of the hosts considered are commercial crops – e.g., fruit trees – the assessment often does not include forest trees as economically important resources at risk.

Questions re: some of specific pests in the analysis

3.2.1. Cerambycidae (Coleoptera)

The risk assessment notes the minimal information available regarding several cerambycid beetles present in Korea that are capable of feeding on elm trees. Collectively, these beetles have a wide host range — Acer, Alnus, Citrus, Ficus, Hibiscus, Juglans, Malus, Morus, Quercus, Populus, Prunus, Pyrus, Salix, Sorbus, and Ulmus. The beetles can thrive in the climate present across most of the Lower 48 states (USDA Plant Hardiness Zones 6-9). The risk assessment does mention the risk to urban and forest trees. It also mentions British detection of A. chinensis larvae in twigs of imported maple trees, but for some reason does not mention past U.S. detections and introductions of this beetle in maple bonsai/bunjae trees in Tukwila, Washington. Is this because the detections were 20 years ago? Does the passage of time make the detections any less relevant?

trees removed for CLB eradication in Tukwila, Washington

3.2.2. Archips xylosteana (Lepidoptera: Tortricidae)

The analysis of this tortricid moth notes its broad host range, including Abies, Acer, Betula, Fraxinus, Populus, Quercus, Salix, Sorbus, Tilia, and Ulmus. Yet the analysis makes no mention of the potential impact of moth larval feeding on the buds and flowers of forest trees. Nor does it discuss the moth’s impact in Canada, where it is established. The Canadian experience seems quite pertinent and is an obvious omission.

3.2.3. Meloinema kerongens

This nematode is present on elms in Korea. The assessors could find no information on the damage it causes to its hosts there. Again, there is no discussion of possible vulnerability of American elms. Apparently the nematodes are considered likely to survive the importation process, when the trees will be bare root. The assessors say that since the dwarfed trees (once imported) are likely to be planted in pots, that might limit the nematodes’ dispersal into native soil habitats and ability to infect new trees. This finding is troubling because it is likely that nematodes or their eggs could be present in the pots’ soil, and if that soil leaks from the pot or is disposed of during repotting or with other actions, pests could become established in native soil.

3.2.5. Helicobasidium mompa

This fungus causes root rot on multiple genera in 44 plant families. The list of hosts includes Pinus spp., Populus spp., Prunus spp., and Quercus spp. It appears to thrive in a wide climatic range covering virtually the entire Lower 48 states (USDA Plant Hardiness Zones 2-11). The fungus is spread via rain or irrigation water. I note that experience with the Phytophthora genus of brown algae has demonstrated how difficult it can be to control pathogens that spread in rain or irrigation water – in both nurseries and the wild.

Other Potential Pests

I urge experts to review the long list of pests not analyzed—especially the nematodes that inhabit the root and rhizosphere. Analysts did not analyze them because they are ectoparasites; they decided that ectoparasites were unlikely to remain with the dwarfed trees when they are shipped bare-root.

I also wonder whether the mistletoe Viscum album – a parasitic plant – might be spread onto the dwarfed trees by birds perching on branches or shelter structures above the production facilities. Assessors thought that dormant mistletoe on the plants would not be easily detected during visual inspection at the ports.

Posted by Faith Campbell

SOD – Regulations Should Reflect Disease’s Complexity

Syringa vulgaris Chmurka 2018-05-06 1352.jpg Wikimedia Commons

As we know, the SOD pathogen Phytophthora ramorum infects more than 100 plant species [APHIS host list posted here]. Some are killed, some not. Some support production of spores (=sporulation), and thus promote spread of the disease – either in nurseries and plantings, or in the wild. Conditions under which P. ramorum infects specific plant species also varies.

In both the ornamental plant industry and natural environments, transmission is driven mostly by foliar hosts.

Matteo Garbelotto and colleagues have carried out studies aimed at improving our understanding of the differences in host-pathogen interactions, and their meaning vis a vis persistence and spread of the disease – especially in wildland situations. The experiments were carried out five or more years ago, funded by the Farm bill Section 7721 funding. See the full reference at the end of this blog.

The team ranked 25 ornamental plant species representing ten families for susceptibility to P. ramorum and infectivity (spore production). They also tested potential differences among three of the genetic lineages of the pathogen—NA1 (prevalent in U.S. forests), NA2 (found in some nurseries in Pacific coast states), and EU1 (found in nurseries and – since 2015 – in some wildland forests in Oregon). The team also studied the effect of temperature on infectibility. Their goal was to help focus regulations so they will be more effective.

The studies clearly show that the relationship between P. ramorum and various hosts is complex – both susceptibility and infectibility vary depending on the host species, pathogen genetic lineage, and environmental conditions, especially temperature. Results of testing of leaves for the presence of the pathogen were affected by such experimental choices as the concentration of zoospores, temperature, plant host, pathogen genotype, and by the interaction between host and pathogen genotype. Stem results were mostly affected by host and host-pathogen genotype interaction.

Hosts bearing the most severe infections do not always support the highest levels of sporulation, so they are not necessarily the most likely to spread the disease.

Regulators also cannot always generalize re: the pathogen’s impact on plant hosts based on the hosts’ taxonomic relationship. Results were fairly similar for congeneric species within the genera Rosa, Prunus, and Syringa, but quite different for species within the genera Ilex, Gaultheria, and Osmanthus.

It is clear that basing regulatory or best management practices on any one pathogen-host-environment relationship is likely to lead to failure, leaving our forests inadequately protected

The findings that pertain most directly to early detection of infections and those that otherwise promote spread of the pathogen are my focus here.

Hosts that Support Sporulation / Spread of Disease

At least five host species are much more infectious than Rhododendron catawbiense. Hosts that support the highest levels of sporulation were Syringa vulgaris, Hamamelis intermedia, and Syringa meyeri. Hosts that support medium-high levels of sporulation were Rosa gymnocarpa and Syringa pubescens subsp. patula.

Two of the Syringa species support high levels of sporulation, but rank low on overall susceptibility. Rosa gymnocarpa ranked fourth for levels of sporulation, but only fifteenth for overall susceptibility. At least six other species join this group of taxa that are highly infectious without displaying noticeable symptoms. Note than none of these top disease drivers is included in the so-called “filthy five” genera which are the focus of federal and state detection efforts. These genera are Rhododendron spp., Camellia spp., Viburnum spp., Pieris spp., and Kalmia spp.

One of the “filthy five” is Rhododendron catawbiense. It is often used as a standard against which to compare other species’ vulnerability. R. catawbiense supports a somewhat lower level of sporulation than do the species listed in the preceding paragraph. Again, disease severity is not a reliable cue to the likelihood of supporting sporulation and disease spread. Thus, the Hamamelis intermedia was the only species that scored high for both sporulation and susceptibility.

Temperatures Affect Infection Rates

A temperature of 20°C [68^o F] was found to be ideal for maximum sporulation by all three genotypes. However, the NA1 genotype was a relatively good sporulator at 12^oC [53^oF]. The NA2 genotype sporulates prolifically at 25°C [77^oF], but produces fewer sporangia than the other two genotypes at 12^oC. These findings suggest which genotype might pose a greater risk in warmer or cooler regions than those supporting the current wildland infestations in California and Oregon. Thus, if NA2 spreads via the nursery trade to warmer regions, such as the area of the Southeast identified by various risk maps developed in the past [See maps on pages 14 – 16 in chapter 5 of Fading forests III, available here], it might pose a higher risk. This discovery intensifies concern arising from the fact that many of the P. ramorum-infected plants shipped to Indiana – and presumably other eastern states – in 2019 were of the NA2 lineage. States that received infected plants in 2019 included Alabama, Arkansas, Kentucky, Missouri, North Carolina, Tennessee, Virginia, and West Virginia.

Considering individual host species, Gaultheria shallon, R. catawbiense, Osmathus delayayi and Hamamelis intermedia supported good sporulation at the higher temperatures whereas Laurus nobilis, Syringa vulgaris, and Magnolia stellata supported better sporulation in cooler climates. Note that H. intermedia and S. vulgaris support prolific sporulation; the latter is a “symptomless superspreader”.

Garbelotto et al. note that Magnolia stellata is both highly susceptible and highly infectious at 12°C and thus able to spread the infection in colder areas. This advice to limit use of this species in cooler areas runs counter to horticultural experts’ guidance to plant this shrub in USDA Hardiness Zones 4–9 – which include virtually all the lower 48 except the most northern parts of Montana, North Dakota, and Minnesota. Clearly, star magnolia is a popular plant in colder regions. At the other end of the spectrum, Gaultheria shallon, Hamamelis intermedia, and Mahonia aquifolia were both highly susceptible and infectious at 25 °C, thus their use should be limited in warmer areas. All three include warm regions in their native ranges.

Early Detection

There are two ways to carry out early detection surveys.

(1) The first is detection of infection in plants themselves. Garbelotto et al. determined that 14 plant species are highly or moderately susceptible to infection even with relatively limited inoculum sources. Intense monitoring of these species would be likely to detect new infestations. Three of the highly susceptiblespecies, namely Syringa meyeri, Syringa pubescens subsp. patula and Hamamelis intermedia, are potentially more susceptible than R. catawbiense.

Hamamelis x intermedia ‘Angelly’ 01.JPG Wikimedia Commons

Based on the relative ease of pathogen re-isolation from the following host species after they had been inoculated at low levels, Syringa meyeri, Syringa pubescens subsp. patula, Hamamelis intermedia, Syringa vulgaris, Osmanthus delavayi, and Magnolia grandiflora indicated that a larger number of plants in the production facility had become infected.

(2) A second approach to early detection monitoring would be to focus on those host taxa able to support the most robust sporulation when infected by low levels of inoculum. This approach emphasizes curtailing spread.

As I noted above, Garbelotto et al. conclude that five species could spur significantly faster disease spread due to higher transmission rates coupled with higher susceptibility rates. These five species are Syringa vulgaris, S. meyeri, and S. pubescens subsp. patula; Hamamelis intermedia; and Rosa gymnocarpa. Note than none of these disease drivers is included in the so-called “filthy five” genera on which regulators focus now detection efforts.

Several species appeared less diseased, but supported more vigorous sporulation (e.g., Syringa vulgaris, S. pubescens subsp. patula and Rosa gymnocarpa). Others were more diseased but supported less sporulation (e.g., Prunus laurocerasus and Prunus lusitanica). Therefore, nursery managers and regulators should not rely on visual assessment of disease intensity to judge spread risk.

Other Information

Comparing the three genotypes, EU1 was most aggressive in terms of disease incidence at both low and high inoculum loads. At low levels of inoculum, NA1 lineage was comparable in terms of disease severity.

However, at higher inoculum loads NA1 was clearly the most infectious based on the number of sporangia produced on infected hosts. Garbelotto et al. conclude that the co-mingling of the EU1 and NA1 lineages in Oregon forests might result in a highly destructive forest disease, as both virulence and transmission potential would be maximized. There is the further risk that the presence of the two genetic lineages, which have different mating types, might enable sexual reproduction/ genetic exchange between the two lineages.

Sources

Matteo Garbelotto, M., D. Schmidt, T. Popenuck. 2020. Pathogenicity and infectivity of Phytophthora ramorum vary depending on host species, infected plant part, inoculum potential, pathogen genotype, and temperature. Plant Pathology 2020;00.1

Phytophthora ramorum – a deadly forest pathogen, surviving and spreading as three strains in North America. “Plant Pathology” Highlight. https://www.bspp.org.uk/phytophthora-ramorum-a-deadly-destructive-forest-pathogen-surviving-and-spreading-as-three-strains-in-north-america-on-more-than-100-ornamental-hosts-from-leaf-to-stem-across-a-range-of-t/

Posted by Faith Campbell

“Year of Plant Health” – Opportunity to Review International Phytosanitary Programs’ Effectiveness

The U.N. Food and Agriculture Organization has declared 2020 to be the International Year of Plant Health. APHIS, U.N. FAO, and others planned celebratory events — most now postponed.

The designation prompts consideration of whether the current global phytosanitary system – created in 1995 – is succeeding in preventing movement of invasive plant pests and invasive plants. Join me in this evaluation!

I focus on evaluating the most widespread invasive pests killing trees – and the pathways on which they travel. Some of the most damaging tree pests, of course, were moved around the world decades ago. But too many have been transported after the modern plant health system was developed in the mid-20^th Century with the adoption of the original International Plant Protection Convention (IPPC) in 1951.

Of course, this is also the period when trade volume exploded, resulting in new source countries, new products, and new technologies that facilitated newly rapid movement of goods and accompanying pests. See my earlier blog here and the book by Marc Levinson, The Box: How the Shipping Container Made the World Smaller and the World Economy Bigger. It is well-documented that rising trade volumes, new trade connections, new products have and will continue to exacerbate unintended movement of species (Seebens et al., 2018).

The phytosanitary regime was massively revised in the mid-1990s through adoption of the World Trade Organization and the Agreement on Sanitary and Phytosanitary Standards (SPS Agreement). Two principal changes were to constrain individual countries’ freedom to establish their own phytosanitary regulations and to require evidence of risk rather than allowing action on the basis of “if in doubt, keep it out”. I have written a critique of the new system in Fading Forests II. See Chapter 3, available here.

USDA officials burn infested cherry trees – gifts from Japan
Washington, D.C. 1912

Has the new regime allowed spread of pests, as I predicted in my critique?

Of course, the explosion of global trade has made prevention of species introductions far more difficult. So the rising numbers of introductions cannot be blamed entirely on the SPS Agreement. Still, it is vital to review pest status in order to see whether the SPS Agreement is succeeding in protecting Earth’s flora. Here, I am looking at only one type of bioinvader. Many more types need to be evaluated, even among plants and plant pests. Nor do I pretend that my list is comprehensive even in the category I focus on – tree-killing insects, nematodes, and pathogens.

My definition of “global invader” is an insect, pathogen, or nematode that has been moved from its known or probable place of origin to at least two novel continents or widespread island groups.

Before the SPS Agreement

Of course, many highly damaging forest insects and pathogens spread widely before the eruption of global trade in the second half of the 20^th Century. Examples include several pathogens:

American chestnut bred to be resistant to blight
photo by F.T. Campbell

Phytophthora cinnamomi – Europe, North America, Oceania, South America
Cryphonectria parasitica – Europe and North America; Oceania probably much later
Dutch elm disease causal agents Ophiostoma ulmi & novo-ulmi (the vectors are sometimes native insects) – Europe, North America, Oceania;

And some insects:

Hylastes ater – Oceania, South America, Africa
Scolytus multistriatus (Dutch elm disease vector) – North America 1909; later to Oceania; mid-20^th Century to Africa

There have also been initial introductions of some organisms that would become “global” later:

Phytophthora lateralis – North America before 1950

During the period 1950 – 1995 –when trade began exploding and countries were adopting their own phytosanitary regulations as allowed under the original IPPC – the following pests were introduced “globally”:

P. ramorum in Big Sur, California
photo by Matteo Garbelotto

Phytophthora ramorum was introduced from Southeast Asia to Europe and North America.
Hylurgus ligniperda – Oceania, South America, Africa, Asia after 1950; North America before 1995
Phoracantha recurva – detected in various geographies after 1995, but almost certainly introduced to North America, South America, Europe, Africa, and Oceania before that date
Palm pests – red palm weevil (Rhynchophorus ferrugineus) to most areas of the Old World and Oceania where palms grow; coconut rhinoceros beetle (Oryctes rhinoceros) around Africa, Mauritius, Reunion; Oceania;

Again, there were initial introductions of numerous insects in wood packaging and on “plants for planting” that would expand to “global” ranges after 1995:

Anoplophora glabripennis

To North America: Anoplophora glabripennis;, Agrilus planipennis; Austropuccinia psidii; Phoracantha recurve; Glycaspis brimblecombei
To Asia: Pine wood nematode Bursaphelenchus xylophilus
To Oceania, South America – Sirex noctillio;

After the SPS Agreement

There has been an apparent explosion of spread since adoption of SPS Agreement in 1995. No doubt these introductions were made possible by the concurrent explosion of trade volumes and more pest-friendly shipping practices (e.g., use of shipping containers and more rapid transportation). The principal vector appears to be plants for planting. About 50% of new plant pathogen invasions are associated with plants for planting (Jimu et al. 2016). Wood packaging is a strong second vector.

Tree-killing pests of which I am aware that have apparently spread globally after 1995 include:

Insects

Aulacaspis ysumatsui – North America, Caribbean, Pacific Ocean islands, Oceania, Africa, Europe, various islands off Southeast Asia that are probably outside original range

*Erythrina humeana* in the Manie van der Schijff Botanical Garden, Pretoria
vulnerable to Euwallacea / Fusarium complex

Quadrastichus erythrinae – North America, Southeast Asia, islands in the Indian and Pacific oceans

Euwallacea fornicatus complex, esp. Euwallacea whitfordiodendrus and E. kuroshio and their Fusarium symbionts Fusarium euwallaceae, Graphium euwallaceae, & Paracremonium pembeum – North America, Africa

Several insects that attack Eucalyptus have been widely introduced to areas where plantations of these species have been planted, e.g.,

Blue gum chalcid wasp or eucalyptus gall wasp Leptocybe invasa – throughout Africa, the Middle East, Asia, the Pacific Region, Europe, South America, Mexico, and the United States [CABI]
Red gum lerp psyllid (Glycaspis brimblecombei) Europe 2009 [EPPO]
Eucalyptus snout beetles Gonipterus spp complex à two species introduced to five continents (Schroder et al. 2019).
Eucalyptus gall wasp(Ophelimus maskelli) – Mediterranean Region, the Middle East, South Africa, Europe, U.S., New Zealand [CABI]

Continued spread of species that had been introduced to a single new continent before 1995:

Pine wood nematode Bursaphelenchus xylophilus – to Europe
Phytophthora lateralis – to Europe and South America
Myrtle rust Austropuccinia psidii – to Pacific oceanic islands and Oceania
Anoplophora glabripennis and A. chinensis – to Europe
Sirex noctillio – to North America
Agrilus planipennis – to Russia and western Europe
Red palm weevil (Rhynchophorus ferrugineus) – to North America (California- eradicated)
Coconut rhinoceros beetle (Oryctes rhinoceros) – to Pacific islands, e.g., Guam and Hawai`i

I note that several studies have identified large numbers of introduced species in certain categories, although the dates of introduction are uncertain. Some were probably introduced before 1995. Here I cite the following:

Jung et al. (2015) found 59 putative Phytophthora taxa in forest and landscape planting sites in Europe; none had been detected by inspectors at the European Union borders.
Jimu et al. (2019) report global spread of Eucalyptus pathogens carried by the trade in seed and cuttings to support establishment of new plantations and breeding programs.
Numerous species of Phytophthora across North America – about 60 species in California native plant nurseries; eleven species in Minnesota (both from Swiecki et al. 2018); Parke et al. (2014) identified 28 Phytophthora taxa in four Oregon nurseries.
Nine species of Phytophthora associated in urban streetscapes, parks, gardens, and remnant native vegetation in urban settings in Western Australia (Barber et al. 2013).

So What’s the Bigger Picture?

I have blogged frequently about the weaknesses of the international standard governing wood packaging; go here.

Clearly the weaknesses of the international phytosanitary system are not limited to the wood packaging pathway. And I repeat that the phytosanitary system is under severe challenge by trade volumes and practices – at least before the Covid-19 pandemic. Still, it is clear that the international phytosanitary system has failed in achieving its purpose: to provide adequate protection in response to this challenge.

I have two suggestions:

1) I hope that the most affected countries will take action per their authority under Section 5.7 of the SPS Agreement. This allows emergency action to prevent further introductions via the principal pathways and from the geographic origins posing the greatest threats (e.g., China for wood packaging, Southeast Asia for Phytophthora pathogens).

2) I hope further that all the nearly 200 countries that are parties to the SPS Agreement and the IPPC will rapidly institute an analysis of the current phytosanitary system to quickly identify amendments to the agreements that would better enable countries to protect their plants from non-native pests.

SOURCES

Barber, P.A., T. Paap, T.I. Burgess, W. Dunstan, G.E.St.J. Hardy. 2013. A diverse range of Phytophthora species are associated with dying urban trees. Urban Forestry & Urban Greening 12 (2013) 569-575

Jimu, L., M. Kemler, M.J. Wingfield, E. Mwenje, and J. Roux. 2016. The Eucalyptus stem canker pathogen Teratosphaeria zuluensis detected in seed samples. Forestry 2016 89 316-324 https://academic.oup.com/forestry/article/89/3/316/1749105

Jung, T., L. Orlikowski, B. Henricot, P. Abad‐Campos, A. G. Aday. O. Aguín Casal, J. Bakonyi, S. O. Cacciola, T. Cech, D. Chavarriaga, T. Corcobado, A. Cravador, T. Decourcelle, G. Denton, S. Diamandis, H. T. Doğmuş‐Lehtijärvi, A. Franceschini, B. Ginetti, S. Green, M. Glavendekić, J. Hantula, G. Hartmann, M. Herrero, D. Ivic, M. Horta Jung, N. Keca, V. Kramarets, A. Lyubenova, H. Machado, G. Magnano di San Lio, P. J. Mansilla Vázquez, B. Marçais, I. Matsiakh, I. Milenkovic, S. Moricca, Z. Á. Nagy, J. Nechwatal, C. Olsson, T. Oszako, A. Pane, E. J. Paplomatas, C. Pintos Varela, S. Prospero, C. Rial Martínez, D. Rigling, C. Robin, A. Rytkönen, M. E. Sánchez, A. V. Sanz Ros, B. Scanu, A. Schlenzig, J. Schumacher, S. Slavov, A. Solla, E. Sousa, J. Stenlid, V. Talgø, Z. Tomic, P. Tsopelas, A. Vannini, A. M. Vettraino, M. Wenneker, S. Woodward, A. Peréz‐Sierra. 2016. Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora disease. Forest Pathology. November 2015.

Levinson, M. The Box: How the Shipping Container Made the World Smaller and the World Economy Bigger Princeton University Press 2008

Schroder, M. Slippers, B., Wingfield, M.J., Hurley, B.P, Invasion history and management of Eucalyptus snout beetles in the Gopterus scutellatus species complex. 2019. Journal of Pest Science

Parke, J.L., B.J. Knaus, V.J. Fieland, C.Lewis, and N.J. Grünwald. 2014. Phytophthora Community Structure Analyses in Oregon Nurseries Inform Systems Approaches to Disease Management. Phytopathology Vol. 104, No 10.

Schroder, M. Slippers, B., Wingfield, M.J.,Hurley, B.P, Invasion history and managementof Eucalyptus snout beetles in the Gopterus scutellatus species complex. 2019. Journal of Pest Science

Seebens, H., T.M. Blackburn, E.E. Dyer, P. Genovesi, P.E. Hulme, J.M. Jeschke, S. Pagad, P. Pyse, M. van Kleunen, M. Winter, M. Ansong, M. Arianoutsou, S. Bacher, B. Blasius, E.G. Brockerhoff, G. Brundu, C. Capinha, C.E. Causton, L. Celesti-Grapow, W. Dawson, S. Dullinger, E.P. Economo, N. Fuentes, B. Guénard, H. Jäger, J. Kartesz, M. Kenis, I. Kühn, B. Lenzner, A.M. Liebhold, A. Mosen, D. Moser, W. Nentwig, M. Nishino, D. Pearman, J. Pergl, W. Rabitsch, J. Rojas-Sandoval, A. Roques, S. Rorke, S. Rossinelli, H.E. Roy, R. Scalera, S. Schindler, K. Stajerová, B. Tokarska-Guzik, K. Walker, D.F. Ward, T. Yamanaka, and F. Essl. 2018. Global rise in emerging alien species results from increased accessibility of new source pools. PNAS Plus. Available at http://www.nature.com/articles/ncomms14435

Swiecki, T.J., E.A. Bernhardt, and S.J. Frankel. 2018. Phytophthoraroot disease and the need for clean nursery stock in urban forests: Part 1 Phytophthora invasions in the urban forest and beyond. Western Arborist Fall 2018.

Wondafrash, M., B. Slippers, A. Nambazimana, I. Kayumba, S. Nibouche, S. van der Lingen, B.A. Asfaw, H. Jenya, E.K. Mutitu, I.A. Makowe, D. Chungu, P. Kiwuso, E. Kulimushi, A. Razafindrakotomamonjy, P.P. Bosu, P. Sookar & B.P. Hurley. 2020. Distribution and genetic diversity of five invasive pests of Eucalyptus in sub-Saharan Africa. Biological Invasions Vo. 22, pp. 2205-2221 (2020)

Coconut rhinoceros beetle – https://www.cabi.org/isc/datasheet/37974 + websites for Guam and Hawai`i

Red palm weevil – https://cisr.ucr.edu/invasive-species/red-palm-weevil

Posted by Faith Campbell

Why such scattershot responses to myrtle rust?

myrtle rust infestation;
source: New Zealand Department of Agriculture alert May 2017

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.

ohia rust on E. kooaulensis
photo by Edward Eickhoff via Flickr

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)

Calamity in Pacific Island Forests

We know the dire threats to Hawaiian forests from pathogens. Some threaten the most widespread tree – ohia. Others are insects threatening trees and shrubs in the remnant dryland forests.

The forests of smaller islands of the Pacific also appear to be facing severe threats – although I have been unable to find information on the current situation.

Guam and its Neighbors

The forests of Guam, Palau, and others in the Western Pacific are among those threatened.

They are geographically isolated and hard to reach, but that distance has not protected them from biological invaders. Their predicament illustrates the dominant role of global movement and trade in spreading pests. In this case, it’s mostly trade in ornamental plants.

These islands have unique flora and fauna. And true to invasive species experts’ expectations, they are vulnerable to bioinvaders. Guam’s most famous invasive species is the brown tree snake (Boiga irregularis), which over a few decades eradicated many bird species and the only native terrestrial mammal, the fruit bat.

Less known, but equally damaging, have been a group of insects that are decimating Guam’s native forest flora.

The most widespread arboreal species in the forests of Guam and neighboring islands is the Micronesian cycad, Cycas micronesica. Its range is Micronesia, the Marianas Group including Guam and Rota Islands; and several of the western Caroline Islands, e.g., Palau and Yap (Marler, Haynes, and Lindstrom 2010).

These forests have already absorbed severe habitat destruction as the sites of fierce fighting in World War II and – in some cases – construction of large military bases. Still, cycads were the most common species in the forest as late as 2002 (Moore, A., T. Marler, R. Miller, and L. Yudin. Date uncertain).

The Worst Pest: Asian Cycad Scale

The most severe current threat to the cycads are introduced insects, especially the Asian cycad scale Aulacaspis ysumatsui.

The cycad scale is native to Southeast Asia. It was first detected on Guam in 2003, when officials noticed that cycads planted near hotels had begun to die. However, this scale had already been spreading thanks to the trade in ornamental cycads. It was detected in Florida in 1996, on Hawai`i in 1998. It continued to spread rapidly in the western Pacific: to Rota in 2007, Palau in 2008 (University of Guam 2012). By late 2019, the scale had spread globally – numerous islands and neighboring mainland areas in the Caribbean (including Puerto Rico and US Virgin Islands), several US states in the Southeast, California, and Taiwan (Moore, Marler, Miller, and Yudin. Date uncertain.) and South Africa. (vanWilgen, et. al. 2020) Also, see the map prepared by CABI.

In every case, the scale has apparently been spread on nursery stock. It is difficult to contain by standard phytosanitary measures – visual inspection – because the scale is tiny and hides deep in the base of the plant’s stiff leaves and other crevices. (Marler and Moore 2010)

By 2005 the scale was killing the native cycad on Guam. Within four years, the millions of C. micronesica on Guam were reduced by more than 90% (Marler, T.E. and K.J. Niklas. 2011). The last time cycads on Guam reproduced in any significant number was in 2004 (Marler and Niklas 2018).

The severe impact of the scale was so rapid that the International Union for Conservation of Nature and Natural Resources (IUCN) changed its listing of C. micronesica from “near threatened” in 2003 to “endangered” in 2006. (IUCN Red List of Threatened Species Online 2008).

Scientists have made several attempts to introduce a biocontrol agent. However, the most promising – the lady beetle Rhyzobius lophanthae – has failed to control the scale, despite having become virtually ubiquitous on Guam. The beetle is too big to reach the significant proportion of scale insects living in small cracks and voids within the plant structures. Evidence from another cycad species indicates that the beetles also don’t prey on scale insects living beneath trichomes (fine hairlike structures on the leaves) or on parts of the plant close to the ground. (Moore, Marler, Miller, and Yudin. Date uncertain.).

Attempts to introduce a second biocontrol organism – the parasitoid wasp Aphytis lignanensis – were stymied by the presence of R. lophanthae (Moore, Marler, Miller, and Yudin. Date uncertain).

Micronesian cycad
photo by Lauren Gutierrez

Other Invasive Species Attacking Cycads

The cycad blue butterfly (Chilades pandava) was detected in 2005 and spread throughout Guam within months (IUCN 2009). Also, it’s been found on Saipan (1996) and Rota (2006). The butterfly is native to southern Asia from Sri Lanka to Thailand and Indonesia. High populations can cause complete defoliation of new foliage. Repeated defoliations can kill the plant. Cycads on Guam are particularly vulnerable because the scale has already caused loss of most of their leaves. Butterfly larvae are often protected by ants (Anonymous).

On cultivated plants the butterfly can be controlled by microbial insecticides containing Bacillus thuringiensis kurstaki (Moore). Scientists at the University of Guam are exploring use of injected insecticides (Moore). They have found an egg parasite, but parasitism levels are low. Any biocontrol agent targetting larvae would have to contend with the ants (Anonymous).

A longhorned beetle (Dihammus (Acalolepta) marianarum) and a snail (Satsuma mercatorius) are also feeding on the cycads (Marler 2010).

The Indo-Malayan termite Schedorhinotermes longirostris was detected in 2011. The termites weaken the cycad stems, which are then toppled by feeding by introduced deer. The termites are also damaging the cycad’s reproductive structures (megastrobili). Termite attacks on cycads surprised scientists since cycads do not form true wood. The termite had probably been introduced recently because, as of 2011, it had been detected only near the Andersen Air Force Base airport (Marler, Yudin, and Moore 2011).

More Isolated – but Still Overrun

Scattered across the Pacific are groups of atolls, including Palmyra and Rose.

Despite their distance from other islands, they have all been visited by mariners for centuries. As a result, they have non-native species, including insects that attack trees.

The tree most affected is pisonia – Pisonia grandis.

The principal insect is another scale, Pulvinaria urbicola. There are some reports that the scale is farmed by ants; species mentioned include several introduced species such as the yellow crazy ant, Paratrechina longicornis.

The scale is probably from the West Indies. Once it reached the Pacific, it might have been distributed to additional islands on seabirds, which travel long distances between the atolls.

The scale’s impact is unclear.

At first, in the mid-2000s, impacts seemed dire. It was reported to be causing widespread tree death on Palmyra and Rose atolls, islands around northeastern Australia, in the Seychelles, and possibly in Tonga.

However, in 2018, scientists reported that eradication of rats on Palmyra Atoll had resulted in an immediate spurt of reproduction of a tree. Numbers of “native, locally rare tree” seedlings (possibly but not explicitly said to be Pisonia grandis) jumped from 140 pre-eradication to 7,756 post-eradication (in 2016). The study made no mention of the scale.

Rose Atoll has only one small island (6.6 ha) with vegetation. Before 1970, it was dominated by Pisonia grandis, but by 2012, there were only seven trees on the island. Several possible causes of this decline have been suggested. Other than the scale, suggested causes include storms, drought, rising sea level / saltwater incursion, and imbalance of bird guano-derived nutrients in the soil. [All information about Rose Atoll is from Peck et al., 2014)

A survey carried out in April 2012 and November 2013 detected 73 species of arthropods from 20 orders on Rose Island, including nine ant species (all but one non-native). Two of these ants – Tetramorium bicarinatum and T. simillimum – were detected tending the scales on Pisonia.

The survey found no evidence of natural enemies of the Pulvinaria scales.

The scientists tested treatment of Pisonia with the systemic insecticide imidacloprid. This treatment apparently reduced scale populations considerably for several months, but then they began to build up again.

In contrast to Palmyra, Polynesian rats (Rattus exulans) were eliminated from Rose Atoll in 1990–1991 – so their role in destroying the trees had ended 20 years before the study. What does the continued decline of the Pisonia trees in subsequent decades suggest for the future of Pisonia trees on Palmyra?

I have sought updates on the tree-pest situations on Guam and the other Pacific islands, but my queries have not received a reply.

SOURCES

Anonymous. 2015. Cycad blue butterfly fact sheet.

Brooke, USFWS, pers. comm. June 3, 2005

CABI November 2019. Aulacaspis yasumatsui (cycad aulacaspis scale (CAS)) or the Asian cycad scale. https://www.cabi.org/isc/datasheet/18756 (was formerly Commonwealth Agricultural Bureaux (CAB) International; now apparently just uses acronym)

Marler, T.E. pers. comm. August 15, 2012

Marler, T.E. 2010. Cycad mutualist offers more than pollen transport. American Journal of Botany, 2010; 97 (5): 841. Viewed as materials provided by University of Guam, via EurekAlert; accessed 6 August, 2012.

Marler, T., Haynes, J. & Lindstrom, A. 2010. Cycas micronesica. The IUCN Red List of Threatened Species 2010: e.T61316A12462113. http://dx.doi.org/10.2305/IUCN.UK.2010-3.RLTS.T61316A12462113.en Accessed 22 April, 2020.

Marler, T.E., and A. Moore. 2010. Cryptic Scale Infestations on Cycas revoluta Facilitate Scale Invasions. HortScience. 2010; 45 837-839. Retrieved August 6, 2012 from www.eurekalert.org

Marler, T.E., L.S. Yudin, A. Moore. 1 September 2011. Schedorhinotermes longirostris (Isoptera: Rhinotermitidae) on Guam Adds to Assault on the Endemic Cycas micronesica. https://bioone.org/journals/florida-entomologist/volume-94/issue-3/024.094.0339/Schedorhinotermes-longirostris-Isoptera–Rhinotermitidae-on-Guam-Adds-to-Assault/10.1653/024.094.0339.full

Marler, T.E. and K.J. Niklas. 2011. Reproductive Effort and Success of Cycas micronesica K.D. Hill Are Affected by Habitat. International Journal of Plant Sciences, 2011; 172 (5): 700. Viewed as materials provided by University of Guam, via EurekAlert; accessed 6 August, 2012.

Moore, A. Cycad blue butterfly fact sheet. http://www.guaminsects.net/gisac2015/index.php?title=Cycad_blue_butterfly_fact_sheet accessed 20-4/24

Moore, A., T. Marler, R. Miller, and L. Yudin. Date? Biological Control of Cycad Scale, Aulacaspis yasumatsui, Attacking Guam’s Endemic Cycad, Cycas micronesica. Western Pacific Tropical Research Center University of Guam. Powerpoint http://guaminsects.myspecies.info/sites/guaminsects.myspecies.info/files/CycadScaleBiocontrolAustin.pdf

Peck, R., P. Banko, F. Pendleton, M. Schmaedick, and K. Ernsberger. 2014. Arthropods of Rose Atoll with Special Reference to Ants and Pulvinaria urbicola scales (Hemiptera: Coccidae) on Pisonia grandis trees. Hawaii Cooperative Studies Unit. University of Hawaii. Technical Report HCSU-057 December 2014

University of Guam (2012, August 2). Invasive insects cause staggering impact on native tree. ScienceDaily. Retrieved August 6, 2012, from www.sciencedaily.com-/releases/2012/08/120803094527.htm).

vanWilgen, B.W.,J. Measey, D.M. Richardson, J.R. Wilson, T.A. Zengeya. Editors. 2020. Bioinvasions in South Africa. Invading Nature. Springer Series in Invasion Ecology 14.

Posted by Faith Campbell