As I have documented numerous times in these blogs, [see here, here, here, here, here, here, here and here] forests throughout the world are being reshaped by rising numbers of introduced, non-native pathogens. Once established, these diseases are nearly impossible to contain, much less eradicate.
While the worst effect of such bioinvasions is widespread mortality of host species, even “lesser” results produce significant changes in the impacted ecosystems.
I believe that the international phytosanitary “system” adopted by the World Trade Organization (WTO) and amended by the International Plant Protection Convention (IPPC) in the mid-1990s impedes efforts to prevent introductions of pathogens. These rules require unattainable levels of certainty about an organism’s impacts before it can be restricted. Scientists such as Haoran Wu and Kenneth Raffa have called for phytosanitary approaches that will be more effective because they are realistic, reflect the true level of threat, and the limits of current science. I agree and have repeated their calls.
How Well Is This “System” Keeping Pathogens At Bay?
- If the world’s phytosanitary system worked well, we should be seeing fewer high-risk forest pathogens being introduced to new countries. Instead, examples abound of pests invading new ecosystems in the post-WTO/IPPC era: Austropuccinia psdii — 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.
- Phytophthora ramorum – 8 to 14 additional introductions to California after its initial detection.
- Fusarium disease vectored by beetles in the Euwallaceae genus:
- Euwallacea fornicatus s.s.— detected in southern California in 2003, Hawai`i in 2007, Israel in 2009, in South Africa in 2012, in Australia in 2021, and in Argentina and Uruguay in 2023 and 2024 . The haplotype detected in South America and several European greenhouses differs from that established elsewhere.
- E. kuroshio detected in southern California in 2013; has spread to nearby Mexico
- E. interjectus detected in central California in 2024.
- Boxwood blight fungus Calonectria pseudonaviculata — first detected in the Caucuses in 2010 and the US in 2011. Now established in at least 24 countries in three geographic areas: Europe and western Asia; New Zealand; and North America. Boxwood blight has caused rapid and intensive defoliation of native stands of Buxus sempervirens. Although disease was detected in United Kingdom in the mid-1990s, the causal agent was not determined until 2002.
- Beech leaf disease caused by the nematode Litylenchus crenatae subsp. mccannii — detected near Cleveland, Ohio, in 2012. Has since spread east to the Atlantic Ocean, south to Virginia, north into Ottawa.
- Phytophthora austrocedrii — detected in nurseries in Ohio and Oregon in 2024. Previously known from Argentina and in England and Scotland. At the latter location it is causing mortality of native Juniperus and introduced Cupressaceae. See here and here.
Most of these pathogens were unknown at the time they were discovered – because they were causing disease in the invaded ecosystems.
In the Face of International Failures, How Can USDA’s APHIS Succeed?
When countries choose to prioritize preventing bioinvasions, they can impose more restrictive controls than those implemented by the WTO/IPPC system.
I urge USDA to more proactively use its authority to protect America’s plant resources. In particular, I urge USDA leaders to use the NAPPRA authority more effectively and quickly. This allows the agency to temporarily prohibit importation of plants that host potentially damaging pathogens. ). https://www.aphis.usda.gov/plant-imports/nappra
We Americans can’t protect our forests from pathogens without APHIS responding more promptly to recent detections of pathogens in North America and on Pacific islands. Recent events are not encouraging.
The agency did undertake an analysis of Phytophthora austrocedrii after it was detected in nurseries in two states. Unfortunately, in my view, APHIS and the states decided the pathogen was too widespread so they dropped any idea of regulating it. This was despite the apparent threat to junipers across the country. See here and here. P. austrocedri also attacks cypress trees, including Port-Orford cedar, Chamaecyparis lawsoniana. USFS scientists recently announced success in breeding POC trees resistant to a different pathogen.
There are no indications that APHIS will respond to detection of a new pathogen causing wilt disease in elms (Plenodomus tracheiphilus) recently discovered in Alberta, Canada. The pathogen is spread primarily through movement of infected plant material, including on asymptomatic material. Current U.S. regulations do not prohibit importation of plants or cut greenery in the Ulmus genus from Canada. Beyond the risk associated with elm material, I think it is probable that this pathogen also survives on plants in additional taxa, since it was formerly known for causing disease on citrus trees.
Although APHIS has classified Leptosillia pistaciae as a federal quarantine pest, I have learned of no response to detection of the pathogen on the native California shrub, lemonade berry (Rhus integrifolia), in 2019.
Has APHIS Changed its Practices in Response to Recent Detections?
We’ve known about gaps and weaknesses in APHIS’ approach for a long time. Here are specifics.
Has APHIS upgraded its attention to nematodes – as should have been prompted by detection of the beech leaf disease nematode (above) and as recommended by Kantor et al.?
Has APHIS changed any of its practices or policies in response to detection of plant and human pathogens associated with wooden handicrafts from countries other than China? Or wood pieces used for unanticipated purposes, e.g., to decorate aquaria? All 31 fungal taxa detected by one of these studies were viable despite having been subjected to various phytosanitary requirements.
USDA has no authority to regulate organisms that pose a risk to non-plant hosts, like us humans! Has APHIS contacted officials at the relevant agency?
Does APHIS respond to detections abroad when pests attack congeners of North American trees? I have blogged about several — see here, here, here and here — detected in Europe or Asia that attack cypress, magnolia, dogwood, Persea, and oaks. PestLens — an alert system created by APHIS — reported these.
How has APHIS incorporated the findings at various “sentinel garden” projects? And the wider implications of findings by Eliana Torres Bedoya and Enrico Bonello regarding findings on asymptomatic plants?
How is APHIS applying the impact assessment tools developed (for insects) by Ashley Schulz and Angela Mech? Has APHIS incorporated Kenneth Raffa’s advice about the strengths and weaknesses of various prediction tools?
I wonder whether APHIS has responded in any way to the rash of woodborer introductions on the west coast, including three species in the invasive shot hole borer complex and the Mediterranean oak borer. Has the agency explored the threat that the spotted poplar borer (Agrilus fleischeri) – another wood-boring beetle native to northern Asia – might pose to North American Populus species? Canada has twice intercepted the species on solid wood packaging material .
USDA APHIS is explicitly not a research agency. However, it claims that its decisions are science-based. In my view, this means APHIS has a responsibility to respond to scientific findings (such as those above) and to bring about research aimed at answering pertinent questions, e.g., those related to risks of pest introduction and establishment, effective detection and management technologies, etc.
APHIS has occasionally done this:
- It established the NORS-DUC research facility to study what aspects of nursery management facilitate establishment of Phytophthora ramorum.
- It enabled and participated in several studies of wood-borer introduction via wood packaging, including those by Robert Haack and colleagues (see blogs on this website under the category “wood packaging”).
- It enabled and participated in a study of introduction pathways that included plants-for-planting – relying on 2009 data. (Liebhold et al. 2012)
- Did APHIS support the study by Li et al. to evaluate the vulnerability of two oak and two pine species to 111 fungi associated with Old World bark and ambrosia beetles?
APHIS could do much more to determine whether North American trees are vulnerable to pathogens and arthropods detected on the congeners in trade partner countries. Opportunities include:
- studying which North American species might be vulnerable to the growing number of the 38 new Phytophthora species detected overseas. This would be a monumental task: 216 species have been recognized in the genus. I have focused specifically on the 38 species detected by Jung, Brasier, and others in Vietnam and now the 18 Phytophthora species detected in the Alps. (I have already noted that APHIS and the states dropped any idea of regulating one of those species, P. austrocedrii).
- Regarding P. ramorum specifically, scientists now recognize 12 genetic strains; 8 are in Southeast Asia, a ninth (EU2) in Europe. How likely is it that some of these will be introduced to the U.S.? Three strains are known to be established in western North American forests – NA1, NA2, and EU1.
In addition, new hosts continue to be identified. APHIS has pledged to update the host list annually. In the past I have criticized APHIS for not accepting hosts identified in the United Kingdom.
While APHIS is not well-funded, it has largely escaped budget slashing by “DOGE,” other Trump Administration cuts, and congressional decreases. Scientific expertise at the USDA Forest Service has been shrinking for decades (see Chapter 6). Now, loss of expertise has reached crisis levels. The result will be less capacity to assist APHIS in evaluating pest risks and research needs.
Earlier, I noted the importance of APHIS using its full NAPPRA authority. Unfortunately, the record is not encouraging here, either.
Since the agency gained this authority in 2011, it has adopted lists of species temporarily prohibited for importation only three times – in 2013, 2017, and 2021. I complained that the last action was tardy and provided insufficient protection to Hawai’i’s unique flora arising from multiple strains of the ‘ōhi‘a rust pathogen Austropuccinia psidii and here. Even worse, four years after promising to close the loophole that allowed continued imports of cut flowers and foliage – the most likely pathway by which the rust was introduced to Hawai`i, APHIS has not proposed the necessary rule.
Pathogens are more difficult to detect and manage than invasive insects. The “disease triangle” is complex! Numerous pathways are involved! But they also get less attention – and this reflects unwise decisions by agency leaders. I suggest that they should respond to this complexity by adding resources. Voglmayr et al. (full reference at the end of this blog) also called for more attention to pathogens. Kantor et al. noted that nematodes are also neglected.
Of course, I have repeatedly urged APHIS leadership to enhance enforcement of regulations governing imports of wood packaging. One suggestion is that it prohibit importation of Chinese wood packaging because of its 25-year record of not complying with – first – U.S. and Canadian regulations and – later – the international regulation known as ISPM#15.
Information Gaps Impede APHIS’ Domestic Program
I have criticized APHIS’ failure to find answers to several questions important to managing the sudden oak death pathogen, Phytophthora ramorum. Like the many questions listed earlier, these also need priority attention.
APHIS has regulated interstate movement of nursery stock to contain P. ramorum for over 20 years. I appreciate its creation of NORS-DUC. But it is also responsible for protecting natural systems in regions not yet invaded, e.g, in the East. APHIS should have studied these issues years ago, given the frequency with which pests spread nationwide via the nursery trade.
Other pathogen systems also have genetic variation that might be important in determining pest-host relationships. As of 2022, scientists had identified 43 haplotypes (genetic variants) of E. fornicatus s.s. worldwide, with the greatest diversity in several Asian countries (P. Rugman-Jones, pers. comm). Other species of plant pathogens also have several haplotypes.
Forests At Risk Outside of North America
North American forests are not alone in being besieged by non-native pathogens. Their numbers have been rising also in Europe and Oceania. The record is less clear in Africa, South America, and Asia.
Reports of tree pathogens in Europe began rising suddenly after the 1980s – admittedly 15 years before the WTO took effect. By 2012, more than half of infectious plant diseases in Europe were caused by introduction of previously unknown pathogens https://www.nivemnic.us/?p=5164
Antonelli et al. (full citation at the end of this blog) report that three previously undetected species of Phytophthora have been detected in European nurseries since 2016. Voglmayr et al. reported that the number of alien fungi in Austria increased 4.6-fold over 20 years. Eighty percent were plant pathogens. The introductory pathway was unclear for the vast majority. They note that differences in research efforts probably explain some discrepancies.
The ash decline pathogen, Hymenoscyphus fraxineus, has apparently been present in eastern Europe since the 1980s, so its spread has probably not been facilitated by the downsides of the WTO/IPPC system.
Other sources report recent introductions of insects to Europe. Musolin et al. reported that 192 species of phytophagous non-native insects had been documented in European Russia as of 2011. They included the emerald ash borer detected in Moscow in 2003. Some of these insects were probably introduced to Europe (outside Russia) before the WTO/IPPC system came into effect. Examples are two insects from North America that were detected in 1999 and 2000, respectively – the western coniferous seed bug, Leptoglossus occidentalis, which vectors a pathogenic fungus Sphaeropsis sapinea (=Diplodia pinea); and the oak lace bug, Corythucha arcuata.
Australia was slow to respond to detection of myrtle rust, Austropuccina psidii. Few federal resources were made available to study its impacts – although the Australian flora includes at least 1,500 species in the vulnerable plant family. Carnegie and Pegg said this experience demonstrated the need to integrate the work of agencies responsible for conservation of natural ecosystems with those determining and implementing phytosanitary policy. New Zealand initially responded more assertively, but also found little funding to support resistance breeding or even to track the rust’s spread.
The record is less clear regarding Africa, South America, and Asia.
Africa
Sitzia et al. expressed concern that bark and ambrosia beetles threaten to cause significant damage to tropical forests. Several factors contribute to these threats: the long history of plant movement between tropical regions; conversion of tropical forests that disturbs canopies, understory plant communities, and soils; and, generally, regions with fewer resources to prevent or respond to invasions.
In Africa, Graziosi et al. reported on the cumulative economic impact of invasive species and the continent’s limited capacity to prevent or respond to introductions. They don’t discuss whether pests attacking plantations of non-native trees followed those trees from their point of origin. They found that some introduced insects pose significant threats to native tree species. They mentioned the Cypress aphid, Cinara cupressi, which was attacking both native African cedar, Juniperus procera, and exotic cypress plantations. All the examples appear to have been introduced before the WTO/IPPC system took effect. All the examples appear to have been introduced before the WTO/IPPC system took effect.
Graziosi et al. point out that South Africa plays a central role because it imports significant volumes of goods that can transport pests. At most immediate risk is South Africa’s highly diverse and endemic flora. For example Phytophthora cinnamomi is attacking native Proteaceae, which are important components of the unique Cape Floral Kingdom. Other pathogens are attacking native conifers in the Podocarpus genus, Ekebergia capensis (Meliaceae), and Syzygium trees. However, pests first introduced to South Africa often spread. Graziosi et al. name several insects and pathogens of Eucalyptus and the wood-boring pest of pine Sirex noctilio.
Pests in Asia
Available information about China is not definitive. The FAO reports that half of the most damaging forest pests are non-indigenous. They were estimated to occur over an area of 1.3 million ha and to kill over 10 million trees per year. However, the three tree-killing pests which receive the most attention are the pinewood nematode (Bursaphelenchus xylophilus), red turpentine beetle (Dendroctonus valens), and fall webworm (Hyphantria cunea). These were all introduced before the World Trade Organization was founded.
The FAO notes several non-native insects that attack native trees in India, but all were introduced decades before the World Trade Organization began. There is no discussion of tree pathogens.
Thu et al. report a growing number of pest outbreaks damaging plantations of non-indigenous trees in Vietnam. In most cases the pests are indigenous to the country. They report that almost nothing is known about pests that attack species in the highly diverse native forests.
The September 2025 meeting of the International Forest Quarantine Research Group (IFQRG) had a session devoted to the topic “Risk of international trade in plants for planting”. The specific presentations are titled
- “Using molecular tools to elucidate the pathways of cryptic pests on plants for planting”
- “Risk-based approach to the movement of germplasm into Australia: the luxury afforded to an affluent continent” (note my earlier blog criticizing Australian efforts re forest pests)
- “Challenges in the validation of methods for detection of quarantine pathogen – P. ramorum”
- “Challenges in surveillance and detection of quarantine fungal tree pathogens in European Union”
- “Pathogens in trade and the risk of establishment – update”
I hope that some of these discussions begin to tackle the crucial questions I raised in this blog and earlier. Also, I hope IFQRG continues to explore these important questions.
As Wu and Raffa et al. have said, Earth’s forests cannot afford delay in finding solutions to the challenges posed by introductions of novel pathogens to naïve systems.
SOURCES
Antonelli, C.; Biscontri, M.; Tabet, D.; Vettraino, A.M. 2023. The Never-Ending Presence of
Phytoph Spp in Italian Nurseries. Pathogens 2023, 12, 15. https://doi.org/10.3390/pathogens12010015
Voglmayr, H., A. Schertler, F. Essl, I. Krisai-Greilhuber. 2023. Alien and cryptogenic fungi and oomycetes in Austria: an annotated checklist (2nd edition). Biol Invasions (2023) 25:27–38 https://doi.org/10.1007/s10530-022-02896-2
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
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