Growing Pathogen Threat from Southeast Asia – US Unprotected

APHIS can protect our native & agricultural plants – but will it?

Imports of large numbers of plants for planting from Southeast Asia represents a significant biosecurity risk for forestry, horticulture, and natural ecosystems in North America and Europe.  This threat is likely to grow unless APHIS takes action under its emergency authorities.

Recent pest introductions and related studies indicate that Southeast Asia is a newly-discovered center of origin for plant pathogens. Places of particular concern are Vietnam, southern Yunnan Province and Hainan Island of China, northern Laos, the eastern Himalayas, and Taiwan. Significant pathogens and associated insects apparently centered in these areas include the sudden oak death pathogen (Phytophthora ramorum) and other Phytophthora species; and several ambrosia beetles and associated fungi, including the laurel wilt fungus (Raffaelea lauricola) and its primary vector (Xyleborus glabratus), and the polyphagous (Euwallacea whitfordiaodendrus) and Kuroshio shot hole borers (Euwallacea kuroshio).

Southeast Asia is attractive to the plant trade because of the region’s high floral diversity, including such sought-after families as Ericaceae (rhododendrons). Indochina has more than 10,350 vascular plant species in 2,256 genera – equaling more than 20% of the world’s plant species (Jung et al. 2019).

Pathogens are notoriously difficult to detect during inspections at the time of shipment. One-time inspections of high volume imports are especially weak and prone to failure.

How do we protect America’s flora?

APHIS could — but has not yet — developed requirements that these countries institute integrated pest management procedures for their exporting nurseries – as provided under amendments to APHIS’ Q-37 regulation and ISPM#36. In any case, it is unlikely that such procedures would minimize the risk because many of the plants that would be imported would probably be wild-collected.

APHIS has – and should use – far more effective means to minimize risk. These are the Federal orders and listing process known as “not authorized for importation pending pest risk assessment” or NAPPRA. If – despite the scientific evidence – APHIS continues to allow high volumes of dangerous imports, the agency should immediately institute new phytosanitary controls to its inspection process. These include relying on risk-based inspection regimes and molecular high-through-put detection tools.

Supporting Material

SOD-killed tanoaks in Big Sur; photo provided by Matteo Garbelotto, UC Berkeley

Phytophthora species

A team of European pathologists, led by Thomas Jung and including Clive Brasier and Joan Webber (see full citation at the end of this blog) surveyed Phytophthora species by sampling rhizosphere soils in 25 natural and semi-natural forest stands, isolations from naturally fallen leaves, and waters in 16 rivers in temperate and subtropical montane and lowland regions of Vietnam during 2016 and 2017.

These studies detected 13 described Phytophthora species, five informally designated taxa, and 21 previously unknown taxa. Detections were made from soil samples taken from 84% of the forest stands and from all rivers.

As I reported in am earlier blog, P. ramorum and P. cinnamomi were among those species detected. Both the A1 and A2 mating types of both P. ramorum and P. cinnamomi co-occurred.

The survey also detected at least 15 species in other genera of oomycetes.

The scientists conclude that most of the 35 forest Phytophthora species detected are native to Vietnam or nearby surrounding areas, attributing species in Phytophthora clades (taxonomically related groups) 2, 5, 6, 7, 8, 9, and 10 as native to Indochina. Different clades were detected in high-elevation vs. lowland rivers, cooler (subtropical) vs. tropical streams, and in soils vs. streams. Given the relatively limited number and diversity of the sampled sites and ecosystem types, it is likely that the true Phytophthora diversity of Vietnam is markedly higher (Jung et al. 2019)  

Worrying diversity of Phytophthora has been detected in other areas of Southeast Asia. A 2013 survey in natural forests and streams of Taiwan detected 10 described species and 17 previously unknown taxa of which 9 were of hybrid origin. In three areas in northern Yunnan, a Chinese province adjacent to northern Vietnam, eight Phytophthora species were isolated from streams running through sclerophyllous oak forests; two were recovered from forest soil samples. In montane forests of the tropical island Hainan, located in the South China Sea close to Vietnam, six Phytophthora species were found (Jung et al. 2019).

These studies are being conducted in the context of scientists discovering numerous new species of Phytophthora in recent decades. Since 1999, the number of described species and informally designated taxa of Phytophthora has tripled. World-renowned experts Clive Brasier anticipates that between 200 and 600 species of Phytophthora are extant in natural ecosystems around the world (Jung et al. 2019).

In the Vietnam survey, P. ramorum was the most widespread species. While genetic studies indicate ancestral connections to the four P. ramorum lineages (genetic strains) introduced to North America or Europe, further studies are under way to clarify these relationships (Jung et al. 2019).

Jung and colleagues found P. cinnamomi to be the most common soilborne Phytophthora species at elevations above 700 m. Two genotypes of the P. cinnamomi A2 mating type are causing epidemics in numerous natural and managed ecosystems worldwide. There was some evidence that the more frost sensitive A2 mating type might be spreading into higher altitudes in Vietnam (Jung et al. 2019).

Most of the Phytophthora species detected in the rhizosphere were not associated with obvious disease symptoms. (The principal exception was the A2 mating type of P. cinnamomi in montane forests in northern Vietnam.) (Jung et al. 2019) This lack of disease greatly reduces the chances of detecting the oomycetes associated with any plants exported from the region – there are no symptoms.

Since southern Yunnan, northern Laos, and the eastern Himalayas belong to the same biogeographic area those areas might also harbor endemic P. ramorum populations. Further surveys are needed to confirm this hypothesis (Jung et al. 2019).

Phytophthora lateralis – causal agent of Port-Orford cedar root rot – also probably originated in the area, specifically Taiwan (Vettraino et al. 2017).

Implications for phytosanitary measures

Many of the native Asian forest Phytophthora species have co-evolved with a variety of tree genera also present in Europe and North America, including Fagaceae, Lauraceae, Aceraceae, Oleaceae, and Pinaceae. Numerous examples demonstrate a strong potential that trees in these families that have not previously been exposed to these Phytophthora species might be highly susceptible. Scientists have begun an extensive host range study of Phytophthora species from Asia and South and Central America. One part of this study found that five Asian Phytophthora species caused significant rot and loss of fine roots and lateral roots in three European species of chestnut and oak (Jung et al. 2019).

Other pathogens

Studies by separate groups of scientists have concluded that several beetle-fungus disease complexes are native to this same region.

Sassafras – photo by David Moynihan

Both the laurel wilt fungus Raffaelea lauricola and its primary vector Xyleborus glabratus probably originated in Southeast Asia; there are probably different strains or genetic makeups across their wide ranges. For example, Dreaden et al. 2019 found that the fungus population from Myanmar differed genetically from those found in Japan, Taiwan, and the United States. Others had already expressed concern about the possibility that new strains of R. lauricola might be introduced (Wuest et al. 2017, cited in Cognato et al. 2019).

Cognato et al. 2019 found that the beetle occurs in deciduous forests from southern Japan to Northeast India, so genetic variation across this range is likely. In fact, they have separated the species X. glabratus into three species. They found that some of the beetles might thrive at 40o North – the latitude of central Illinois, Indiana, and Ohio and southern Pennsylvania. The ability of the vector of laurel wilt disease to spread so far north poses an alarming threat to sassafras (Sassafras albidum) – which is a major understory tree in forests of these regions.

It is unknown whether these new species and X. glabratus lineages are associated with different fungal strains. In company with the pathologists cited above, Cognato et al. 2019 warn that preventing introduction of the three beetle species to other regions is prudent. Cognato et al. 2019 point out that if other beetle lineages from the southern extent of their range can tolerate hotter and drier conditions, they might pose a greater risk to host species in the more arid areas of California and Mexico. In addition, Central America is at great risk because of the numerous plant species in the vulnerable Lauraceae found there.

Also from the region are two beetle-fungus combinations killing trees in at least seven botanical families, including maples, oaks, and willows, in southern California. The polyphagous shot hole borer (Euwallacea whitfordiaodendrus) apparently is native to Vietnam (Eskalen et al. 2013) and the closely related Kuroshio shot hole borer (Euwallacea kuroshio) to Japan, Indonesia, and Taiwan (Gomez et al. 2018).  

What you can do

Getting APHIS to act

1) communicate concern about the risk to APHIS leadership and ask that the agency take action under its NAPPRA authority

2) communicate the same to intermediaries who can influence APHIS:

  • State phytosanitary agency – especially through regional plant boards and National Plant Board
  • Your Congressional representative and senators (especially if one or more serves on Agriculture or Appropriations committee)
  • Professional societies – American Phytophathological Society, Mycological Society, American Society of Entomologists, Society of American Foresters …

3) communicate the same to university leadership and ask that their lobbyists advocate to USDA

4) communicate the same to the media

2) Research on extent of North American tree species’ vulnerability to the Oomycetes and other associated microorganisms

Jung et al. 2019 say that studies are under way to identify potential pest-host relationships with important tree species. However, all the authors are Europeans. Is anyone carrying out tests on North American trees in the apparently most vulnerable families — Fagaceae, Lauraceae, Aceraceae, Oleaceae, and Pinaceae?

1) Communicate with colleagues, scientific societies, APHIS, Agriculture Research Service, National Institute of Food and Agriculture, and USFS to determine whether such tests are under way or planned.

2) In those cases where no studies are planned, work with above to initiate them.

Sources

Cognato, A.I., SM. Smith, Y. Li, T.H. Pham, and J. Hulcr. 2019. Genetic Variability Among Xyleborus glabratus Populations Native to Southeast Asia (Coleoptera: Curculionidae: Scolytinae: Xyleborini) and the Description of Two Related Species. Journal of Economic Entomology XX(XX), 2091, 1 – 11.

Dreaden, T.J., M.A. Hughes, R.C. Ploetz, A. Black and J.A. Smith. 2019. Genetic Analyses of the Laurel wilt Pathogen, Raffaelea lauricola, in Asia Provide Clues on the Source of the Clone that is Responsible for the Current USA Epidemic. Forests 2019, 10, 37

Eskalen, A., Stouthamer, R. Lynch, S.C., Twizeyimana, M., Gonzalez, A., and Thibault, T. 2013. Host range of Fusarium dieback and its ambrosia beetle (Coleoptera Scolytinae) vector in southern California. Plant Disease 97938-951.

Gomez, D.F., J. Skelton, M.S. Steininger, R. Stouthamer, P. Rugman-Jones, W. Sittichaya, R.J. Rabaglia, and J. Hulcr1/ 2018. Species Delineation Within the Euwallacea fornicatus (Coleoptera: Curculionidae) Complex Revealed by Morphometric and Phylogenetic Analyses. Insect Systematics and Diversity, (2018) 2(6): 2; 1–11

Jung, T., B. Scanu, C.M. Brasier, J. Webber, I. Milenkovic, T. Corcobado, M. Tomšovský, M. Pánek, J. Bakonyi, C. Maia, A. Baccová, M. Raco, H. Rees, A. Pérez-Sierra & M. Horta Jung. 2020. A Survey in Natural Forest Ecosystems of Vietnam Reveals High Diversity of both New and Described Phytophthora Taxa including P. ramorum. Forests, 2020, 11, 93   https://gcc02.safelinks.protection.outlook.com/?url=https%3A%2F%2Fwww.mdpi.com%2F1999-4907%2F11%2F1%2F93%2Fpdf&data=02%7C01%7C%7Cfcd843919a3348a4a56108d7974039ab%7Ced5b36e701ee4ebc867ee03cfa0d4697%7C0%7C1%7C637144174418121741&sdata=WayrZsxp3P9Kj0h1aDPZnzu4yjDGA2ZEuH9NZITFQF4%3D&reserved=

Vettraino,  A.M., C.M. Brasier, J.F. Webber, E.M. Hansen, S. Green, C.Robin, A. Tomassini, N. Bruni, A. Vannini. 2017. Contrasting microsatellite diversity in the evolutionary lineages of Phytophthora lateralis. Fungal Biology Vol. 121, Issue 2, February 2017, pp. 112-126

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.

New Ambrosia Beetle in California – Threat to Oaks?

valley oak at Jack London State Park (24 miles from Calistoga)

In November, scientists discovered a new ambrosia beetle in symptomatic valley oaks  (Quercus lobata) trees in Calistoga, Napa County. Some blue oaks (Q. douglasii) have also been attacked (Rabaglia et al. 2020). Trees associated with this outbreak showed wilting, defoliation, and broken branches. The infested wood was discolored, presumably by the fungus. The insect, Xyleborus monographus, is native to Europe.

Officials now know that this beetle is found throughout a 15-mile-long area in Napa and neighboring Lake and Sonoma counties. It has probably been there for several years (Rabaglia et al. 2020). One specimen of the beetle was trapped in Portland, Oregon in 2018, but no infestation was detected. The beetle has never been intercepted in California. Nor has it been found in traps designed to detect bark beetles which have been deployed in 11 counties – including several in the San Francisco Bay area but not including Napa or Sonoma.

Like all Xyleborus, adult females tunnel into tree’s trunks, carrying fungal spores in their mycangia (structures in the jaws in which microbes are harbored). Beetle larvae eat the fungi. Beetle reproduction is facilitated by sibling mating within the gallery and by the ability of unmated females to produce male offspring.

Sometimes the beetle’s associated fungi are pathogenic to living trees. One of the fungal species detected in the Calistoga infestation is Raffaelea montetyi, which is reported to be pathogenic to cork oak. The presence of this fungus had been reported in 2018, although the beetle species carrying it was not identified then. This is apparently the first report of this fungus in North America.

Known hosts of beetle X. monographus include European or Eurasian chestnut (Castanea sativa), beech (Fagus orientalis), and European and American oaks (including Q. lobata and Q. rubra).  The possible effects of the beetle and associated fungi on other oak species is unknown. Oaks are acknowledged to be important components of forests and woodlands in California. Ambrosia beetles often attack stressed trees. Since California forests are increasingly frequently stressed by drought, fire, and other pests, they might be especially vulnerable.

The California Department of Food and Agriculture is currently seeking comments on what pest rank to assign the insect.  The comment period closes on March 6th and I encourage you to consider providing your views.

In their draft document ranking risk, state officials note that a proven host — Q. lobata — is widespread in California and the insect is probably capable of establishing over much of the state. The possible economic impact was described as possibly affecting production of oaks in California nurseries and triggering quarantines.  (Does this mean CDFA expects impacts only on saplings? Is this realistic? CDFA made no mention of costs to urban areas for hazard tree management.)

The risk assessment notes that research by McPherson, et al. (2008) found that ambrosia beetles are attracted to oak trees already infected with sudden oak death (SOD) (Phytophthora ramorum). Therefore, X. monographus could have a synergistic impact with SOD on California oaks – which has already killed an estimated 1.9 to 3.3 million coast live and Shreve oaks.

SOURCE

Rabaglia, R.J. S.L. Smigh, P. Rurgman-Jones, M.F. Digirolomo, C. Ewing, and A. Eskalen. 2020. Establishment of a non-native xyleborine ambrosia beetle, Xyleborus monographus (Fabricius) (Coleoptera: Curculionidae: Scolytinae), new to North America in California. Zootaxa 478 (2): 269-276

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.

Add your comments – should APHIS open trade in maples from Korea?

exit hole of Anapolophora chinensis in Chinese penjing from circa 2001

APHIS has released a risk assessment in response to a petition from the Republic of Korea (ROK) seeking permission to export to the United States bunjae of three maple species (Acer buergerianum Miq., A. palmatum Thunb., and A. pseudosieboldianum Nakai).  The risk assessment is available here.  Scroll down to the deadline February 3.

Comments are accepted until 3 February. To comment, send an email to PPQPRAcomments@aphis.usda.gov. Include the name of the commodity assessed by the draft document (e.g., Korean maple bunjae) in the Subject line.

“Bunjae” is the Korean term for plants for planting equivalent to Japanese “bonsai” or Chinese “penjing”.  In this practice, trees are grown – often for years – using cultivation techniques such as pruning, root reduction, potting, defoliation, and grafting, to produce miniature specimens.

Importation of bunjae plants for planting in the Acer genus from several Asian countries was prohibited temporarily under the agency’s authority under the Plant Protection Act and regulations in 7 CFR 319.37, Subpart H- P4P to limit imports of a new suite of plant taxa as “not authorized pending pest risk analysis” (NAPPRA). 

The NAPPRA listing, finalized in 2013, followed numerous detections of Anoplophora and possibly other pests in penjing shipped from China to the United States, and one outbreak (in Takohma, Washington) that required expensive and destructive eradication measures. At that time, APHIS made the case that no effective mitigation existed to provide protection adequate to the risk. If APHIS is to agree to the ROK petition, it must demonstrate that any mitigation measures it accepts have overcome deficiencies identified in the original proposal to include Acer in the NAPPRA category.

APHIS will address risk management aspects, including and risk mitigation measures, after it has assessed stakeholder and country comments on each pest list or risk assessment. There will be an opportunity to comment on any proposed mitigation measures later.

The risk assessment now open for comment clearly demonstrates that the risks are severe. It concludes that 17 or 18 taxa or groups of species pose a “high” overall risk of introduction, establishment, and impacts.  Another 10 pose an overall “moderate” risk. In each case, the risk assessors concluded that the harvest and shipment procedures outlined in Section 1.4 of the Korean petition would not mitigate the risk. 

While the risk is greatest for maples (Acer spp.), many other types of plants also host pests evaluated in the risk assessment. Thus, the risk often affects fruit trees and grapes as well as alders, birches, dogwoods, elms, magnolias, oaks, poplars, walnuts, willows, rhododendron, even redwood.

My questions and concerns

I note that Table 3 of the risk assessment omits the Asian longhorned beetle (Anoplophora glabripennis), even ‘tho the species is discussed in the text and received an overall risk ranking of “high”. Is this a mistake? If the omission is deliberate, why is the reasoning not discussed in the risk assessment?

The assessments included in this document are brief and leave out many easily obtainable facts regarding damage, especially with regard to the Anoplophora, Lymantria, and Lycorma genera. The risk assessment notes when pest species are polyphagous, but it is uncertain how it incorporates that heightened risk of potential damage.

eradication clearcuts in Takoma, Washington in 2001
reason: escape of A. chinensis from Chinese penjing plants
while they were in “post entry quarantine”

I am also concerned about the document’s treatment of uncertainty.  First, “moderate uncertainty” is defined as “Additional or better evidence may or may not change rating.” How do the assessors evaluate this 50/50 tossup?  My concern is heightened by a statement in the text regarding two taxa, Cacopsylla albopontis & C. pseudosieboldiani. The assessment notes an absence of literature documenting that these taxa are pests in their native range, so their ability to cause damage if introduced to the U.S. is unknown. Consequently, the assessors did not analyze them further “as they are unlikely to cause unacceptable impacts.” As we all know, numerous arthropods and pathogens highly damaging in naïve environments – including in the US — were not pests / were barely known in their native ranges.

Regarding individual species, I note that the assessment says the wood-root fungus Daedalea dickinsii is usually found in older heartwood of roots, trunks, or branches. The assessors conclude that it is unlikely that this fungus would be associated with maple seedlings.  However, bunjae trees are not seedlings; they are deliberately miniaturized woody plants that are often years old.

Re: Anomala cuprea, the assessor seems to downplay the risk because the insect lacks a specific attraction to maples. While I agree that a generalist might be somewhat less likely to be on the bunjae when they are exported, a generalist might pose a threat to a wide range of woody plants if introduced. This higher level of possible impacts needs to be recognized in the assessment.

Several insect groups were excluded from further valuation despite being described as established in Korea and “only associated with Acer species”. Included in this group are several beetles, true bugs (including aphids and leafhoppers), and butterflies/moths (pp. 13-14 of the PRA). I found this language to be completely unclear. If the pests are in Korea and associated with maples, why were they not evaluated?  

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.

Last Chance! to comment on proposal to restrict imports of certain plant taxa

rust on `ohi`a; photo by J.B Friday, University of Hawaii

As I blogged in December, APHIS is seeking input on a proposal to place several plant taxa in the category “not authorized pending pest risk analysis” (NAPPRA). The purpose of this proposed listing is to prevent introduction of plant pests or probable invasive plant species.

I urge you to comment before the deadline – this Friday, January 24.

In comments prepared for the Center for Invasive species Prevention (CISP), I applauded APHIS’ continued reliance on this authority to improve phytosanitary protections for our natural and agricultural resources. I noted, however, several weaknesses in the proposal – including several pathogens that I think should have been included, but were not. I summarize these comments here. 

1) There have been lengthy delays in proposing and finalizing lists of species to be regulated under this authority. While I strongly support listing of all plants in the family Myrtaceae that are destined for Hawai`i in order to reduce the risk that additional strains of the `ohi`a rust pathogen Austropuccinia psidii might be introduced and prove more damaging to native Hawaiian vegetation than the strain already present on the islands. However, this proposal comes 15 years after the pathogen was detected in Hawai`i and six years after publication of scientific documentation of the existence of more damaging strains of the pathogen.

2) When lists have been presented, they failed to include all appropriate species.

I am disturbed that APHIS did not include in the NAPPRA proposal Ceratocystis lukuohia and Ceratocystis huliohia, two pathogens that are killing millions of ‘ōhi‘a trees in Hawai`i under the name “rapid ‘ōhi‘a death”.

3) APHIS must act under other regulatory provisions to close some of the gaps left by this proposal.

The listing of plants in the Myrtaceae (see number 1 above) under NAPPRA does nothing to halt imports of cut flowers and foliage, which are widely recognized to be the pathway by which the rust was introduced to Hawai`i.  APHIS notes that is should act under other regulatory authority to close this pathway; I hope you will urge APHIS to take such action quickly, preferably initially by issuing a Federal Order.

4) APHIS has proposed 26 plant taxa for inclusion in the NAPPRA category because they might themselves be invasive. These proposals are generally well supported and deserve your support. Several plant taxa appear to pose significant ecological threats: two taxa of mangroves (Bruguiera gymnorhiza and Lumnitzera racemose); a vine that grows in Asian and Indian Ocean mangrove forests, Derris trifoliate; and several aquatic plants (Crassula helmsii, Elatine ambigua, Luziola subintegra, Philydrum lanuginosum, Stratiotes aloides); and Ligustrum robustum.

Remember that at least 50 species of aquatic plants are already considered invasive in the United States. At least eight species of Ligustrum are also invasive.

Update: Listing finalized

On June 2, 2021 APHIS finalized the NAPPRA listing originally proposed in November 2019.

The agency added to the category 26 plant taxa because they are invasive; all plants in the Myrtaceae family when destined to Hawai`i, and 43 other plant taxa that are hosts of 17 quarantine pests. 

The only change from the proposed action was to drop listing of the subfamily Bambusoideae because it is already regulated under NAPPRA to prevent introduction of other quarantine pests.

APHIS had received 132 comments from producers, importers, industry groups, conservationists, scientists, plant pathologists, ecologists, administrators, teachers, students, and private citizens. Most reportedly supported the proposed listing of Myrtaceae destined for Hawai`i and expressed no concerns about the proposed listing of most other taxa. I have blogged previously about the threat to Hawaii’s unique flora posed by the pathogen Australopuccinia psidii (the subject of this NAPPRA listing) and other non-native organisms – here and here.

A complete list of taxa listed under NAPPRA and the resulting restrictions on importation is posted at https://www.aphis.usda.gov/aphis/ourfocus/planthealth/import-information/permits/plants-and-plant-products-permits/plants-for-planting/ct_nappra  

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

Sudden Oak Death – Bad News All Around

SOD in California;
photo by Joseph O’Brien. courtesy of Bugwood

We know that the international trade in living plants is a major pathway by which tree-killing pathogens are being spread – some of them again and again. According to Grünwald et al. (2019), Phytophthora ramorum, the pathogen that causes Sudden Oak Death (SOD), has been introduced to North America and Europe – probably from Asia – at least five times. One lineage or genetic strain – EU1 – has been established on both continents (strains explained here). There is strong evidence of two separate introductions to Oregon, at least 12 to California.

Jung et al. 2015 state definitively that the international movement of infested nursery stock and planting of reforestation stock from infested nurseries have been the main pathway of introduction and establishment of Phytophthora species in European forests.  

Clive Btasier in Vietnam
photo from UK Forest Research

Jung et al. 2020 have demonstrated that P. ramorum probably originated in Vietnam.  This region appears to be a center of diversity for Phytophtoras and other Oomycetes: baiting of soil and streams resulted in the detection of 13 described species, five informally designated taxa, and 21 previously unknown taxa of Phytophthoras plus at least 15 species in other genera. Noting the risk associated with any trade in plants from this region, the authors re-iterated past appeals that the international phytosanitary system replace the “outdated and scientifically flawed species-by-species regulation approach based on random visual inspections for symptoms of described pests and pathogens” by instituting “a sophisticated pathway regulation approach using pathway risk analyses, risk-based inspection regimes and molecular high-throughput detection tools.”

Pathogen’s Spread Proves U.S. Domestic Regulations Governing Nursery Trade Are Inadequate

Last year I blogged about the most recent spread of Phytophthora ramorum through the nursery trade.  As of now, we know that shipments of potentially infected plants had been sent to 18 states. Infected stock had been detected in nurseries in seven of these (Iowa, Illinois, Indiana, Kansas, Missouri, Nebraska, Oklahoma) plus the source state, Washington [COMTF Newsletter August 2019].

Since then, I learned [COMTF newsletter for December 2019]   that these plants were infected by the NA2 strain of the pathogen. This is the first time that this strain has been shipped to states outside the West Coast. It is unclear what the impact will be if – as is likely – infested plants are still extant in purchasers’ yards. Both the NA1 strain (the strain established in most infested forests of California and Oregon) and the NA2 strain belong primarily to the A2 mating type, so the potential spread of NA2 lineages might not exacerbate the probability of sexual reproduction of the pathogen.

I applaud agencies’ funding of genetic studies to determine the lineage of the pathogen involved. It not only helps narrow the possible sources of infected plants, but also could be important in determining risk and management options.

I have long criticized USDA’s P. ramorum regulatory program – see Fading Forests III and my blogs discussing the most recent revisions to the regulations here and here. I believe that both the earlier regulations and the revisions finalized last May provide inadequate protection for America’s forests. 

The updated regulations do take a couple of important positive steps. First, APHIS is now authorized to sample water, soil, pots, etc. – and to act when it finds evidence of the pathogen’s presence. APHIS also now mandated nurseries found to be infested to carry out a “critical control point analysis” to determine practices which facilitated establishment and persistence of P. ramorum.

However, these improvements are severely undermined by continuing the five-year-old practice of limiting close scrutiny to only those nurseries that tested positive for the pathogen in the recent past. The flaw in this approach was starkly demonstrated by the pathogen’s spread in 2019. The Washington State nursery that was the source of the infected plants had not previously been positive, so it was under routine nursery regulation, not the more stringent federal P. ramorum program.

Too often various iterations of the regulations have allowed infected plants to be shipped. Between 2003 and 2011, a total of 464 nurseries located in 27 states tested positive for the pathogen, the majority as a result of shipments traced from infested wholesalers (Campbell). The number of nurseries found to have infected plants has since declined, but not dropped to zero. These include 34 nurseries in 2010 (COMTF February 2011 newsletter), 21 in 2012, and 17 in 2013 (Pfister). During 2014, state inspectors detected the SOD pathogen in 19 nurseries – 11 in the three west-coast states and eight in other parts of the country (Maine-1, New York-2, Texas-1, and Virginia-4) COMTF newsletter December 2014). Despite the continuing presence of the pathogen in the nursery trade, APHIS formalized existing practices that narrowed the regulators’ focus to only those nurseries with a history of pathogen presence. This approach has been shown to fail – we need APHIS and the states to find a way to broaden their scrutiny.

The most immediate impact of the continuing presence of P. ramorum in the nursery trade is the burden borne by eastern states’ departments of agriculture. They are obligated to seek out in-state nurseries that might have received infected plants; inspect those plants; and destroy the infected plants, test nearby plants, and try to find and retrieve plants that had been sold. The heaviest, and most direct, burden is borne by the receiving nurseries. Anger about bearing this burden for 15 years doubtless prompted the National Plant Board to adopt a tart resolution calling on APHIS to carry out a review of its communications to the states during the 2019 incident. The NPB also questioned whether current program processes and guidance are effective in preventing spread of this pathogen. 

Unfortunately, the NPB had not commented formally on the rule change when it was proposed.

The states’ frustration is exacerbated by the fact that under the Plant Protection Act, when APHIS takes a regulatory action it prevents states from adopting more stringent regulations. While the law allows for exceptions if the state can demonstrate a special need, none of the five applications for an exemption pertaining to P. ramorum was approved (Porter and Robertson 2011). I have been unable to find evidence of petitions submitted in the nine years since 2011.

In Case You Needed A Reminder: P. ramorum is a Dangerous Pathogen – as Proved by the Situation in the West states and Abroad

Continuing Intensification of the Already Bad Infestations in the West

tanoak mortality in Big Sur
photo courtesy of Matteo Garbelotto, UC Berkeley

As of 2014 (see COMTF November 2018 newsletter available here), perhaps 50 million trees had been killed by P. ramorum in California and Oregon. The vast majority were tanoaks (Notholithocarpus densiflorus)  – an ecologically important tree. 

Since 2014, the disease has intensified and spread in response to recent wet winters. In 2016 (see COMTF

November 2016 newsletter here) disease was detected for the first time in a fifteenth California county and new outbreaks or more severe infestations were recorded in seven other counties.  In 2019, SOD was detected in the sixteenth county. Tanoak mortality in California increased by more than 1.6 million trees across 106,000 acres in 2018.

Perhaps more disturbing, the disease has also intensified on the eastern side of San Francisco Bay – an area thought to be less vulnerable because it is drier and where there are fewer of the principal sporulation host, California bay laurel (see COMTF March 2017 newsletter here).

A second disturbing event is the detection in Oregon forests of the EU1 strain of Phytophthora ramorum. The August 2015 detection was the first instance of this strain being detected in a forest in North America. Oregon authorities prioritized removing EU1-infected trees and treating (burning) the immediate area, which had expanded to more than 355 acres – all within the quarantine area in Curry County. The legislature provided $2.3 million for SOD treatments for 2017-2019 (Presentation by Chris Benemann of Oregon Department of Agriculture to the Continental Dialogue on Non-Native Forest Insects and Diseases; reported here).

The EU1 lineage is a different mating type than the NA1 lineage already established in Oregon. Scientists should study P. ramorum populations in Vietnam and Japan, where both mating types are present, to determine whether they are reproducing sexually. There is also the risk that the EU1 lineage might be more aggressive on conifers – as it has been in the United Kingdom (Grünwald et al. 2019).

The EU1 infestation was introduced to the forest from a nursery. The nursery had carried out the APHIS-mandated Confirmed Nursery Protocol, then closed.  I ask, what does this apparent transmission from nursery to forest say about the risk of transmission? Does it raise questions about the efficacy of the confirmed nursery protocol to clean up the area? Remember that a pond at the botanical garden in Kitsap, Washington has repeatedly tested positive, despite several applications of the clean-up protocols.

(For a discussion of the implications of mixing the various strains of P. ramorum, visit here)

These disasters remind us how sad it is that California and federal officials did not adopt aggressive management efforts aimed at slowing the pathogen’s spread at an early stage of  the epidemic. Experts on modeling the epidemiology of plant disease concluded three years ago that the sudden oak death epidemic in California could have been slowed considerably if aggressive and well-funded management actions had started in 2002 (Cunniffe, Cobb, Meentemeyer, Rizzo, and Gilligan 2016).

The Oregon Department of Forestry commissioned a study of the economic impact of the P. ramorum infestation that found few economic impacts to date, but potentially significant impacts in the future. It also noted potential harms to tribal cultural values and the “existence value” of tanoak-dominated forests and associated obligate species.

Situation Abroad

The situation in Europe is even worse than in North America. Two strains of P. ramorum are widespread in European nurseries and in tree plantations and wild heathlands of western the United Kingdom and Ireland. and here and here.  Jung et al. 2015 found 56 Phytophthora taxa in 66% of 2,525 forest and landscape planting sites across Europe that were probably introduced to those sites via nursery plantings.

larch plantation in UK killed by P. ramorum
photo from UK Forest Research

In Australia, Phytophthora dieback has infected more than one million hectares in Western Australia. More than 40% of the native plant species of the region are vulnerable to the causal agent, P. cinnamomi

 and here.  

Barber et al. 2013 reported 9 species of Phytophthora associated with a wide variety of host species in urban streetscapes, parks, gardens, and remnant native vegetation in urban settings in Western Australia. Phytophthora species were recovered from 30% of sampled sites.

In New Zealand, the endemic – and huge, long-lived – kauri tree (Agathis australis) is also suffering severe impacts from Phytophtoras and other pathogens (Bradshaw et al. 2020)

See the IUFRO Working Party 7.02.09 ‘Phytophthora Diseases of Forest Trees’ global overview (Jung et al. 2018), which covers 13 outbreaks of Phytophthora-caused disease in forests and natural ecosystems of Europe, Australia and the Americas.

The situation in the Eastern United States is Unclear

After 15 years of the nursery trade carrying P. ramorum to nurseries – and possibly yards and other plantings – in states east of the 100th Meridian, what is the risk that these forests will become infested? No one knows. We do known that the pathogen has been detected from 11 streams in six eastern states – four in Alabama; one in Florida; two in Georgia; one in Mississippi; one in North Carolina; and two in Texas. P. ramorum has been found multiple times in eight of these streams – two steams in Alabama, one each in Mississippi and North Carolina (see COMTF April 2019 newsletter available here). While established vegetative infections have not been detected, the question remains: how is the pathogen persisting? Scientists agree that P. ramorum cannot persist in the water; it must be established on some plant parts (roots?) or in the soil. Still, Grünwald et al. (2019) report that there is little evidence of plant infections resulting from stream splash in Oregon.

Unfortunately, fewer states are participating in the stream surveys – which are operated by the USDA Forest Service. In 2010, 14 states participated; in 2018, only seven (Alabama, Georgia, Mississippi, North Carolina, Pennsylvania, South Carolina, and Texas). Florida and Tennessee recently dropped out. The number of streams surveyed annually also has dropped – from 95 at the highest to only 47 in 2018 (see COMTF April 2019 newsletter available here). This reduced scrutiny makes it less likely that any infestation on plants will be detected. Risk maps (reproduced in Chapter 5 of Fading Forests III here) developed over more than a decade indicate that forests in the southern Appalachians and Ozarks are vulnerable to SOD.

Risks to other plants

The risk from Phytophthoras is not just P. ramorum and trees! Swiecki et al. 2018 report a large and increasingly diverse suite of introduced Phytophthora species pose an ever greater threat to both urban and non-urban plant communities in California. These threats are linked to planting of nursery stock. See also the information posted here.

Jung et al. 2018 cite numerous other authors’ findings of multiple Phytophthoras in Oregon and. California nurseries as well as in nurseries in various eastern states.

Nor is Phytophthoras the only pathogenic genus to pose a serious risk to America’s trees. I remind you of the fungus Fusarium euwallacea associated with the Kuroshio and polyphagous shot hole borers, which is known to kill at least 18 species of native plants in California and additional species in South Africa.   The laurel wilt fungus kills many trees and shrubs in the Lauraceae family. ‘Ohi‘a or myrtle rust kills several shrubs native to Hawai`i and threatens a wide range of plants in the Myrtaceae family in Australia and New Zealand; rapid ‘ohi‘a death fungi (Ceratocystis huliohia and Ceratocystis lukuohia)  [All described here] are killing the most widespread tree on the Hawaiian Islands.

Solutions – complete & implement modernized international and domestic phytosanitary regulations

Clearly, standard phytosanitary practice of regulating pests known to pose a threat does not work when many – if not most – of the damaging pests are unknown to science until introduced to a naïve ecosystem where they start causing noticeable levels of damage. We need a more proactive approach – as has long been advocated by forest pathologists, including Clive Brasier 2008 and later, Santini et al. 2013, Jung et al. 2016, Eschen et al. 2017.

National and international phytosanitary agencies have taken some steps toward adopting policies and programs that all hope will be more effective in preventing the continued spread of these highly damaging tree-killing pests. First, APHIS has had authority since 2011 – through the Not Authorized for Importation Pending Pest Risk Assessment (NAPPRA) program — to prohibit temporarily imports of plants suspected of transporting known damaging pathogens until the agency has conducted a pest risk analysis. However, utilization has lagged: only three sets of species have been proposed for listing in NAPPRA in the eight and a half years since the program was instituted in 2011. The third list of proposed species is currently open for public comment.

Another weakness is that the program still focuses on organisms known to pose a risk.

Second, in 2018 APHIS completed a decades-long effort to revise its plant import regulations (the “Q-37” regulations). APHIS now has authority to require foreign suppliers of living plants to carry out “hazard analysis and critical control point” programs and adopt integrated pest management strategies to ensure that the plants are pest-free during production and transport.

However, implementation of this new authority depends on APHIS negotiating agreements with individual countries that would govern specific types of plants exported to the U.S. APHIS has not yet announced completion of any programs under this authority. Nor is it clear which taxa or countries APHIS will prioritize.

APHIS’ action was anticipated by the international plant health community. In 2012, member states in the International Plant Protection Convention adopted International Standard for Phytosanitary Measure 36 (ISPM#36)  The standard sets up a two-level system of integrated measures, which are to be applied depending on the pest risk identified through pest risk analysis or a similar process. The “general” integrated measures are widely applicable to all imported plants for planting. The second level includes additional elements designed to address higher pest-risk situations that have been identified through pest risk analysis or other similar processes. 

However, the preponderance of international efforts to protect plant health continues to rely on visual inspections that look for species on a list of those known to be harmful. Yet we know that most damaging Phytophthoras were unknown before their introduction to naïve ecosystems.

Furthermore, use of fungicides and fungistatic chemicals – that mask infections but do not kill that pathogen – is still allowed before shipment.

(For more complete analyses of the Q-37 revision and ISPM#36, see chapters five and four, respectively, of Fading Forests III.)

The nursery industry is working with state regulators and APHIS to develop a voluntary program utilizing  integrated measures – the Systems Approach to Nursery Certification (SANC) program. https://sanc.nationalplantboard.org/

SOURCES

Bradshaw et al. 2020. Phytophthora agathidicida: research progress, cultural perspectives and knowledge gaps in the control and management of kauri dieback in New Zealand. Plant Pathology (2020) 69, 3–16 Doi: 10.1111/ppa.13104

Brasier CM. 2008. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathology 57: 792–808.

Brasier, C.M, S. Franceschini, A.M. Vettraino, E.M. Hansen, S. Green, C. Robin, J.F. Webber, and A.Vannini. 2012. Four phenotypically and phylogenetically distinct lineages in Phytophthora lateralis

Fungal Biology. Volume 116, Issue 12, December 2012, Pages 1232–1249

Campbell, F.T. Calculation by F.T. Campbell from tables in U.S. Department of Agriculture, Animal and Plant Health Inspection Service – National Plant Board.  2011.  Phytophthora ramorum Regulatory Working Group Reports.  January 2011.

Cunniffe, N.J., R.C. Cobb, R.K. Meentemeyer, D.M. Rizzo, and C.A. Gilligan. Modeling when, where, and how to manage a forest epidemic, motivated by SOD in Calif. PNAS, May 2016 DOI: 10.1073/pnas.1602153113

Grünwald, N.J., J.M. LeBoldus, and R.C. Hamelin. 2019. Ecology and Evolution of the Sudden Oak Death Pathogen Phytophthora ramorum. Annual Review of Phytopathology date? #?

Jung T, Orlikowski  L, Henricot B, et al. 2016. Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. Forest Pathology 46: 134–163.

Jung, T., A. Pérez-Sierra, A. Durán, M. Horta Jung, Y. Balci, B. Scanu. 2018. Canker and decline diseases caused by soil- and airborne Phytophthora species in forests and woodlands. Persoonia 40, 2018: 182–220   Open Access!

Jung, T. et al. 2015. Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora disease. Forest Pathology. November 2015; available from Resource Gate

Jung, T., B. Scanu, C.M. Brasier, J. Webber, I. Milenkovic, T. Corcobado, M. Tomšovský, M. Pánek, J. Bakonyi, C. Maia, A. Baccová, M. Raco, H. Rees, A. Pérez-Sierra & M. Horta Jung. 2020. A Survey in Natural Forest Ecosystems of Vietnam Reveals High Diversity of both New and Described Phytophthora Taxa including P. ramorum. Forests, 2020, 11, 93 https://gcc02.safelinks.protection.outlook.com/?url=https%3A%2F%2Fwww.mdpi.com%2F1999-4907%2F11%2F1%2F93%2Fpdf&data=02%7C01%7C%7Cfcd843919a3348a4a56108d7974039ab%7Ced5b36e701ee4ebc867ee03cfa0d4697%7C0%7C1%7C637144174418121741&sdata=WayrZsxp3P9Kj0h1aDPZnzu4yjDGA2ZEuH9NZITFQF4%3D&reserved=

Knaus, B.J., V.J. Fieland, N.J. Grunwald. 2015. Diversity of Foliar Phytophthora  Species on Rhododendron in Oregon Nurseries. Plant Disease Vol 99, No. 10 326 – 1332

Pfister, S. USDA APHIS. Presentation to the National Plant Board, August 2013

Porter, R.D. and N.C. Robertson. 2011. Tracking Implementation of the Special Need Request Process Under the Plant Protection Act. Environmental Law Reporter. 41.

Santini A, Ghelardini L, De Pace C, et al. 2013. Biogeographic patterns and determinants of invasion by alien forest pathogens in Europe. New Phytologist 197: 238–250.

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

Tsao PH. 1990. Why many Phytophthora root rots and crown rots of tree and horticultural crops remain undetected

Will Chaos Replace International Trade Rules?

The United Nations has designated 2020 as the International Year of Plant Health.  I welcome the possibility of heightened awareness – although it could result in promises that are more optimistic than facts warrant.

APHIS and probably other national and international phytosanitary bodies have planned events to draw attention to the importance protecting of plant health. For example, the APHIS website lists numerous meetings, some of which are special events, e.g., Safeguarding 2020: North American Safeguarding and Safe Trade Conference in Washington, DC, in August. Another event is a continuation of the Entomological Society of America’s Grand Challenges event, “Pre-border Prevention:  A New Conversation on Invasive Pest Pathways Through Trade” – which will take place in Orlando in November.

I repeat that we should support the international phytosanitary community’s efforts to raise political leaders’ awareness of the importance of preventing phytosanitary disasters.

However, at the same time, the international system that, for more than two decades, has governed trade, with all its associated phytosanitary risks and regulations, is falling apart.

The World Trade Organization – which is the basis for international trade rules – is under unprecedented threat. United States has blocked nomination of individuals to the World Trade Organization’s Dispute Panel. As of December 10, 2019 the Panel no longer has a quorum. As a result, experts expect countries to revert to the pre-WTO practice of bullying trade “partners” with whom they have a quarrel. They will probably erect tariffs and other barriers in order to force other parties to concede. Phytosanitary requirements might again be governed by individual countries’ bilateral agreements, leading to confusion and perhaps a “race to the bottom” in the name of facilitating trade.

Collapse of the WTO rules alarms me – despite my having criticized WTO restrictions on strong national phytosanitary measures over the past 25 years. (The restrictions were imposed by the WTO’s Agreement on the Application of Sanitary and Phytosanitary Measures – the SPS Agreement). For more details, see Fading Forests II.  All-out country vs. country trade battles seldom put a priority on preventing the movement of pests. At least under WTO SPS, there has been a process for addressing pest problems.

Most phytosanitary issues – including development of international standards – are addressed under the International Plant Protection Convention. The IPPC is a separate organization from the WTO, so it might continue to function with fewer disruptions. Still, much of its clout comes from its recognition by the WTO SPS as the standard-setting body for plant health matters.

Rome – home of the IPPC

Of course, there are benefits associated with individual countries’ acting independently.  Might the current collapse of trade rules allow the U.S. to adopt more stringent regulations governing introduction pathways of concern to us — for example, wood packaging? Can we hope that an administration focused on “America First” take aggressive phytosanitary actions to protect our agriculture and environment?

Unfortunately, I see no indications that the U.S. Department of Agriculture – much less other agencies – might seize this opportunity.

The United Kingdom has an even greater opportunity to act independently, since it is “Brexiting” the European Union in January 2020. In theory, the UK is now free to adopt its own phytosanitary measures. A House of Lords committee held extensive hearings to explore options in 2018. 

Clive Brasier

While eminent plant pathologist Clive Brasier and others urged the UK to adopt more stringent rules based on a precautionary approach – for example, by banning imports of semi-mature trees with large root balls – the committee noted that the British government has often said that it wants to maintain “seamless” trade with the EU. It therefore seems unlikely that the UK will seize this opportunity to erect more effective phytosanitary barriers to prevent pest introductions to the islands.

Meantime, the European Union is making some mildly encouraging changes. Europe (including the UK) has the highest number of introduced tree-killing non-native pathogens of any continent – five times more than North America (Ghelardini 2017). Europe has a much more leaky phytosanitary system for plant imports than does the United States. See also Jung et al. (2015), Roy et al. (2014), the Montesclaros Declaration.

participants at the Montesclaros negotiation

In response to growing awareness of the plant pest threat, EU officials have gone through a multi-year process to strengthen phytosanitary rules governing movement of plants for planting (living plants, such as nursery stock). The process was described in Klapwijk et al. (2016) and discussed in my blog in October 2016. The new rules took effect in December 2019. The new European Commission regulation simplifies and harmonizes the “plant passport” system, under which plants are moved among EU member states. Plant imports that pose the greatest risk – called “priority pests” – are subject to enhanced measures concerning surveys, action plans for their eradication, contingency plans and simulation exercises. Plants for planting and plant products being imported into the EU will be subject to varying levels of restrictions, including prohibition of importation of those posing the highest risk. Less risky plants must be accompanied by a phytosanitary certificate issued by the phytosanitary agency of the exporting country (House of Lords report). The new system no longer depends on a list of harmful plant pests, but instead “sets out the conceptual nature of quarantine pests” and empowers the Commission to adopt measures to control certain pests (Klapwijk et al. (2016)).

Three years ago, Klapwijk et al. (2016) praised the new approach as a significant step forward. However, they note that the new rules still don’t provide for precautionary assessments of high-risk commodities. Nor do they actually restrict import of the highest-risk commodities, such as imports of large plants or plants in soil (my emphasis). Such restrictions still must be enacted separately. Organisms whose pest status is unknown will continue to be allowed into the EU. (See discussions of the impact of failing to curtail imports of “unknown unknowns” by Brasier (2008) and in Fading Forests II.

(While the U.S. also does not address organisms with unknown pest potential, it is much more stringent regarding sizes of plants, presence of soil or other growing media, and other issues. Furthermore, it has the NAPPRA process, which facilitates a more rapid response to emerging pest threats.)

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.

SOURCES

Brasier CM. 2008. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathology 57: 792–808.

Ghelardini, L., Luchi, N., Pecori, F., Pepori, A.L., Danti, R., Della Rocca, G., Capretti, P., Tsopelas, P. , Santini, A. 2017.  Ecology of invasive forest pathogens. Biological Invasions. June 2017

Jung, T. et al. 2015 “Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora disease” Forest Pathology. November 2015;

Klapwijk,  M., Hopkins, A.J.M., Eriksson, L. Pettersson, M., Schroeder, M., Lindelo¨w, A., Ro¨nnberg, J. Keskitalo, E.C.H.,  Kenis, M. 2016. Reducing the risk of invasive forest pests and pathogens: Combining legislation, targeted management and public awareness. Ambio 2016, 45(Suppl. 2):S223–S234  DOI 10.1007/s13280-015-0748-3

Roy, B.A., Alexander, H.M., Davidson, J., Campbell, F.T., Burdon, J.J., Sniezko, R., and Brasier, C. 2014. Increasing forest loss worldwide from invasive pests requires new trade regulations. Frontiers in Ecology  https://cpb-us-e1.wpmucdn.com/blogs.uoregon.edu/dist/1/11561/files/2018/07/Roy-et-al-2014-Frontiers-12p4898.pdf

APHIS seeks comments on NAPPRA proposals

APHIS proposes to place numerous plant taxa  on its list of plants for planting whose importation is “not authorized pending pest risk analysis” (NAPPRA).  Unfortunately, the proposal comes too late for some pests; doesn’t apply to at least one significant pathway of entry; excludes some highly damaging newly detected pathogens; and too often applies only to agricultural pests. Nevertheless, the proposal is worth supporting – while mentioning those caveats.  

APHIS is accepting comments on the data sheets justifying the proposed listings until 24 January. The Data sheets can be obtained here.  We encourage you to comment.

APHIS’ Regulatory Framework

Under APHIS’ regulations in ‘‘Subpart— P4P’’ (7 CFR 319.37 through 319.37–14 …), APHIS prohibits or restricts the importation of “plants for planting” – living plants, plant parts, seeds, and plant cuttings – to prevent the introduction of “quarantine pests” into the US. A “quarantine pest” is defined in § 319.37–1 as a plant pest or noxious weed that is of potential economic importance to the United States and not yet present in the country, or is present but not widely distributed and is being officially controlled.

§ 319.37–2a authorizes APHIS to identify those plant taxa whose importation is not authorized pending pest risk analysis (NAPPRA) in order to prevent their introduction into the United States. If the plant taxon has been determined to be a probable invasive species, its importation is restricted from all countries and regions. If the taxon has been determined to be a host of a plant pest, the list includes (1) names of affected taxa, (2) the foreign places from which these taxa’s importation is not authorized, and (3) the quarantine pests of concern.

APHIS finalized a rule giving itself the authority to place plant taxa in the NAPPRA program in 2011; it has previously used this process twice to restrict imports of plant taxa – most recently in 2017.

Plant Taxa that Host a Damaging Pest or Pathogen

The proposed restrictions would apply to two plant families — Myrtaceae taxa (when destined to Hawai`i), and the subfamily Bambusoideae (bamboo); plus 43 other taxa that are likely to transport damaging insects, pathogens, or viruses.

ohia in bloom; National Park Service photo

1) All plants in the family Myrtaceae that are destined for Hawai`i.

The proposed restriction is intended to counter the risk that additional strains of the `ohi`a rust pathogen Austropuccinia psidii might be introduced and prove more damaging to native Hawaiian vegetation than the strain already present on the islands. (See description of `ohi`a rust here.

`Ohi`a rust was detected in Hawai`i in 2005. Detection was followed by scientific studies to determine whether different strains exist and, if so, whether they posed a threat to Hawaiian vegetation. Under the circumstances, the proposed action is disturbingly tardy.

Worse, the pathogen was probably introduced to Hawai`i on imports of flower and foliage cuttings, rather than entire plants or propagules. Unfortunately, the section of APHIS’ regulations that governs imports of plants that can be grown (“plants for planting”) does not apply to imports of cuttings (including flowers). In the Federal Register notice, APHIS says it will issue a separate proposal to tighten regulations on imports of cuttings and flowers. I hope they move expeditiously on this rulemaking –  which will be more cumbersome in even the best case because it requires a full rulemaking, not the expedited notice and comment process allowed under the NAPPRA program.

It is disturbing that the proposal does not include the two Ceratocystis species that are killing millions of `ohi`a trees in Hawai`i link to DMF writeup. It is true that these were identified relatively recently – in 2017. However, other plant taxa proposed for inclusion in the NAPPRA category were also detected or determined to be the cause of a disease as recently as 2017.

ohia trees killed by Ceratocystis; Island of Hawaii; photo by J.B. Friday, University of Hawaii

2) APHIS proposes to include another pest that might attack a native Hawaiian plant, Phyllanthus distichus. Another species in the genus, P. saffordii is endemic to Guam; it is listed as endangered under the federal Endangered Species Act. Other Asian gooseberries in the Phyllanthus genus are grown in backyards in Hawai`i and other semitropical areas and there is some interest in expanding commercial uses.

3) APHIS proposes to include several plant taxa important in tropical agriculture because of the threat that imports of those plants will transport diseases or pests. These include two pathogens that threaten production of macadamia nuts (Neopestalotiopsis macadamiae and Pestalotiopsis macadamiae); and pests of breadfruit, lychee, and durian.

4) Some of the plant taxa that APHIS hopes to protect from new pests or pathogens by placing hosts in the NAPPRA category are invasive. These include – in Hawai`i – Syzygium jambos (rose apple).  It is named as a host of two pests targetted by the proposed action – the `ohi`a rust pathogen Austropuccinia psidii and armored scale insect Myrtaspis syzygii.

Euonymus bungeanus (winterberry euonymus) is in the same genus as several plant species invasive across the continent.  APHIS proposes to restrict its importation in order to prevent introduction of the  Euonymus yellow mottle associated virus (EuYMaV), which has only that plant species as a known host.

5) APHIS also proposes to add to the NAPPRA category several plant taxa that could transport the Elm mottle virus (EMoV) because of the threat the virus poses to several European elm species – and presumably also to North American elms. The virus also attacks hydrangea and lilac.

In several cases, some of the primary hosts of the target pest or pathogen are already in NAPPRA for other reasons from some origins. Nearly all the woody hosts are already required to undergo post-entry quarantine – which presumably APHIS now considers to provide inadequate protection.

6) Also proposed are diseases or pests that threaten grapevines and tomatoes.

Several of the proposed taxa are already present in the US (including `ohi`a rust). Other proposed listings appear to be precautionary actions to protect plant taxa that USDA expects to be increasingly important economically in the future.

Plant Taxa Proposed Because They Appear Likely to be Invasive

APHIS has proposed 26 plant taxa for inclusion in the NAPPRA category because they might themselves be invasive. Of greatest ecological concern are two taxa of mangroves which had been introduced by early 20th century plant explorer David Fairchild and have since been detected to be spreading in South Florida. These are Bruguiera gymnorhiza and Lumnitzera racemose. Also of concern is a vine that grows in Asian and Indian Ocean mangrove forests, Derris trifoliate.

Bruguiera gymnorhiza;
Wikimedia Commons

Several proposed species are aquatic plants that can form dense mats.

Other taxa proposed appear to possibly threaten pastures or other agricultural uses.

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.

ISPM#15 – The Stamp is Not Effective as a Clue to Whether Wood Packaging is Pest-Free

For more than a decade, most countries in the world have required that crates, pallets, spools, and dunnage made from wood be treated in accordance with the requirements of the International Standard for Phytosanitary Protection (ISPM)#15 that this treatment be certified by applying an approved stamp to the wood. The goal of the program is to “reduce significantly the risk of introduction and spread of most quarantine pests that may be associated with that material.”

However, experience and studies in both the United States and Europe demonstrate that the ISPM#15 stamp is not a reliable indicator of whether the wood packaging is pest-free.

1) In the United States, over a period of nine years – Fiscal Years 2010 through 2018 – U.S. Customs and Border Protection (CBP) detected 9,500 consignments harboring a pest in a regulated taxonomic group. Of the shipments found with infested wood packaging, 97% bore the ISPM#15 mark (See Harriger reference at the end of the blog). The wood packaging was from nearly all trading countries. 2) In the past two years, CBP inspectors have repeatedly found pests in dunnage bearing the ISPM#15 mark – as reported by U.S. importers of “break bulk” cargo into Houston. While most of the criticism of non-compliant wood packaging refers to countries in Asia and the Americas, at least one of the Houston importers obtains its dunnage in Europe.

3) In Europe, a two-year intensive survey of wood packaging associated with shipments of stone from China to the 28 European Union countries over the period 2013-2016 again found that 97.5% of consignments found to harbor pests bore the ISPM#15 mark (Eyre et al. 2018). The scientists concluded that the ISPM-15 mark was of little value in predicting whether harmful organisms were present. (Eyre et al. 2018, p. 712)

As I have noted in previous blogs and policy briefs, the only in-depth study of the “approach rate” of pests in wood packaging, based on data which is now a decade old, found that 0.1% of incoming wood packaging transported a regulated pest (Haack et al. 2014). Given current trade volumes, as many as 17,650 containers per year (or 48 per day) transporting tree-killing insects might be entering the U.S. (My calculation of this estimate is explained in the blog on “risks of introduction” here.)

The Haack study excluded imports from Mexico, Canada, and China. The first and third countries have records of poor compliance with ISPM#15 requirements, so the “approach rate” for all incoming shipments might well have been higher.

The study of European imports focused on shipments of stone from China – which were deliberately chosen to represent types of imports presenting a high risk of transporting pests. Across Europe, over the four-year period, quarantine pests were detected in 0.9% of the consignments – somewhat higher than the U.S. number, as could be expected. However, there were large variations among participating countries’ findings. Austria and France found 6.95% of consignments inspected were infested, while half of European Union countries found none!

These differences demonstrate the importance of thorough inspections.

The data also indicate that the problem is not decreasing. Austria detected pests in nearly one-fifth (19.6%) of inspected shipments in 2016 – the final year of the study! However, during that same year, only 1.5% of wood packaging lacked the ISPM#15 mark.

So How Should the International Phytosanitary Community React to This Failure?

Data cited in numerous studies indicate that ISPM#15 has probably succeeded in reducing the presence of pests in wood packaging. This progress is good – but insufficient. Our forests need further reductions.

In the meantime, however, the international standard has demonstrably failed to provide a secure method to evaluate the pest risk associated with wood packaging accompanying any particular shipment. The presence of the stamp on pieces of wood packaging does not reliably show that the wood is pest-free. Officials need to determine why. Is it fraud? That would mean deliberately placing the stamp on wood that had not been treated, which U.S. CBP staffers think is occurring (Harriger). The European Union audit team that visited China also thought they detected instances of fraud. They concluded that “the current system of official controls in China does not adequately ensure that SWPM which forms part of consignments of goods exported to the EU is marked and treated according to ISPM No. 15” (Eyre et al. 2018, p. 713). On the other hand, the US importers in Houston say they are pressing their European suppliers to provide pest-free dunnage.

What more could we ask them to do to ensure that they are not receiving fraudulently marked materials?

Perhaps the problem has a different cause. Are the treatments themselves are less effective than expected? One APHIS study found that twice as many larvae reared from wood treated by methyl bromide fumigation survived to adulthood than larvae reared from heat-treated wood; the reason is unclear (Nadel et al. 2016). Unfortunately, it is apparently impractical to determine whether wood was heat treated by looking for changes in the chemical profile of the wood (Eyre et al. 2018).

Nor can we expect inspection of 100% of all risky consignments or detection of 100% of quarantine pests in those consignments that are inspected. Therefore, the European study authors concluded that inspection is best considered as a means of gathering evidence of risk and a deterrent rather than a means of completely preventing pest movement (Eyre et al. 2018).

The European study authors called for review of ISPM#15 as a control system and to investigate compliance at the source (Eyre et al. 2018 p. 714).

What is APHIS doing?

As I have noted previously – here and here – while U.S. CBP adopted a policy in 2017 under which it can penalize importers for each consignment not in compliance with ISPM#15, APHIS has not followed Custom’s lead on this. Instead, APHIS will apply a penalty only when an importer has accrued five violations over the period of a year. (The two agencies are acting under separate legal authorities.) This is yet another example of APHIS taking a less protective stance – as I described in earlier blogs.

Since Customs is now applying the letter of the law, the most useful step would probably be for APHIS (and the USDA Foreign Agriculture Service) to ramp up efforts to assist U.S. importers which are trying to comply. The importers are begging USDA to provide better information to them about foreign suppliers of wood packaging and dunnage. Which have good vs. poor records? USDA could also help importers trying to complain about specific shipments to the exporting countries’ National Plant Protection Organizations (NPPOs; departments of agriculture).  In addition, APHIS could augment its pressure on foreign NPPOs and the International Plant Protection Convention more generally to ascertain the reasons ISPM#15 is failing and to fix the problems.

APHIS has not been idle. The North American Plant Protection Organization (including Canada and Mexico) has sponsored two workshops intended to educate NPPOs and exporters in Asia and the Americas about the standard’s requirements. APHIS is planning to address wood packaging in an international symposium organized under the auspices of the International Year of Plant Health in July 2020 – I will provide details when they become available.

APHIS is collaborating with the Entomological Society of America to host a workshop on wood packaging at the ESA annual meeting in November 2020 – I will provide details when they become available. The Continental Dialogue on Non-Native Forest Insects and Diseases plans to link its annual 2020 meeting to this workshop.

More immediately, the Continental Dialogue on Non-Native Forest Insects and Diseases will have presentations on the wood packaging issue at its annual meeting in just 11 days! in Cleveland

In preparation for the 2020 meetings, APHIS should fund more studies and audits of wood packaging to document the current efficacy of the standard (that is, the pest approach rate); remember, Haack’s study relied on data which are now a decade old. Not only has time passed … Both the standard and U.S. enforcement policies have changed since 2009.

Significance of the Wood Packaging Problems

The apparent failure of the ISPM#15 standard to provide a reliable means to certify treatment raises obvious issues regarding the risk of pest introductions. However, the implications are much broader.

The premise of the international phytosanitary system – the Agreement on the Application of Sanitary and Phytosanitary Standards (SPS Agreement) and International Plant Protection Convention (IPPC) – is that importing countries should rely on exporting countries to take the actions necessary to meet the importing countries’ plant health goals. The ISPM#15 experience casts doubt on this premise. The exporters are not reliably ensuring the cleanliness of their wood packaging. Worse, wood packaging is easier to treat than fruits, vegetables, and living plants (plants for planting). The latter commodities are much more easily damaged or killed by treatments than are boards or even logs – which are, after all, already dead! (A longer discussion of the SPS Agreement and IPPC is found in Chapter III of Fading Forests II, available here.

I hope that the international phytosanitary community will take advantage of the heightened attention and effort associated with the International Year of Plant Health in 2020 to re-examine all aspects of the current global phytosanitary system.

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.

SOURCES

Eyre, D., R. Macarthur, R.A. Haack, Y. Lu, and H. Krehan. 2018. Variation in Inspection Efficacy by Member States of SWPM Entering EU. Journal of Economic Entomology, 111(2), 2018, 707–715)

Kevin Harriger, US CBP. Presentations to the annual meetings of the Continental Dialogue on Non-Native Forest Insects and Diseases over appropriate years. See, e.g., https://continentalforestdialogue.org/continental-dialogue-meeting-november-2018/

Nadel, N., S. Myers, J. Molongoski, Y. Wu, S. Linafelter, A. Ray S. Krishnankutty, and A. Taylor. 2016. Identificantion of Port Interceptions in Wood Packaging Material: Cumulative Progress Report, April 2012 – August 2016

https://www.joc.com/breakbulk/ispm-15-enforcement-leaves-shippers-no-good-nswers_20190717.htmlhttps://www.joc.com/breakbulk/enhanced-enforcement-ispm-15-costing-us-importers-millions_20190725.html

Congressional Funding for Key USDA Programs (Assuming it Ever Passes)

Fiscal Year 2020 began on 1 October. Congress has not yet passed funding bills (appropriations) for the full year. Agencies are operating now on a short-term continuing resolution which expires on November 21st. Meanwhile, representatives of the House and Senate will meet to reconcile the differences between the two bodies’ appropriations bills in hope that a year-long bill can be finalized by that time.

(Disagreement between President Trump and the Congress about funding for the border wall might prevent adoption of full-year appropriations bills and lead to another government shutdown.)

I report here the differences between House and Senate bills funding the USDA APHIS and Forest Service programs that are vital to addressing non-native forest pests.

APHIS

Over the years, I have complained that inadequate funding is a major cause of shortfalls in APHIS’ efforts to detect new invasions by tree-killing pests and to respond to those invasions in effective ways.

While funding levels are still too low, at least Congress is holding funding steady for APHIS for Fiscal Year 2020 (which began three weeks ago, on October 1st). Both House and Senate bills maintain funding for two crucial programs at the FY19 levels:

  • “tree and wood pests” program – $60 million (this matches the FY19 level; it is $4 million above the funding provided in previous years); and
  • “Pest Detection” – $27.4 million.

The House provided slightly higher funding than the Senate for two other programs:

  • “specialty crops” (including sudden oak death) – $186.5 million in the House bill, $186 million in the Senate bill; and
  • “methods development” – $21.686 million in the House bill, $20.686 million in the Senate bill.

In the report accompanying its bill, the House called for two additional funding options to address emergencies. First, it set up a contingency fund of $470,000 to control outbreaks of insects, plant diseases, animal diseases and pest animals and birds to meet emergency conditions. Second, the report repeated language from past reports that authorizes the Secretary to take “such sums as may be deemed necessary” from other USDA programs in order to counter pest emergencies threatening any segment of U.S. agricultural production.

The Senate report addressed several high-profile tree pests. It called for complete eradication of the Asian longhorned beetle; mandated that APHIS report on its efforts to eradicate ALB and spotted lanternfly and to minimize spread of the polyphagous and Kuroshio shot hole borers; and to assist states that have recently detected the emerald ash borer. (This language is helpful, but it falls short of what I previously advocated – that APHIS continue efforts to prevent EAB spread, especially through movement of firewood.)  The Senate report also urged APHIS to maintain FY19 level funding addressing the sudden oak death pathogen, in particular to improve understanding of the two strains of the pathogen present in Oregon’s forests link to blog to inform control and management techniques in wildlands. (Actually, management in wildlands falls largely to the Forest Service, with scientific input from both Agriculture Research Service and – to some extent – the NORS-DUC research nursery managed by APHIS.)

For a lengthier justification of my funding requests, see my earlier blog  on APHIS funding

Funding for Resistance Breeding through NIFA

As I pointed out in my blog in May, the 2018 Farm Bill included an amendment (Section 8708) that establishes a new priority for a grant program managed by the National Institute of Food and Agriculture. The amendment would support restoration to the forest of native tree species that have suffered severe levels of mortality caused by non-native insects, plant pathogens, or other pests. The amendment affects the Competitive Forestry, Natural Resources, and Environmental Grants Program under Section 1232(c)(2) of the Food, Agriculture, Conservation, and Trade Act of 1990 (16 U.S.C. 582A-8, as amended. However, this program  has not been funded for more than a decade. In my blog, I asked you to support a $10 million appropriation to NIFA to fund a competitive grant program for such forests restoration.

Neither the House nor the Senate provided funding for this program.

USFS

The House bill provides $277,155,000 for USFS Research and Development – nearly $20 million more than the Senate bill ($257,640,000). The House report links this increase to the recognition of the increasing risk to urban, rural, and wildland forests from insect and disease outbreaks and invasive plant infestations.  The report calls on the Forest Service to develop a research program that addresses several priorities critical to forest health, including preventing the spread of disease and invasive species.

USFS engagement on pest issues with other federal agencies and state, local government, and private land managers is carried out through the Forest Health Management program under the State and Private Forestry division. The Senate bill and report are confusing because they have separated out salaries and other expenses. As a result, I can’t compare its figures to those in previous years or to those from the House. Partly for this reason, I urge you to support the House bill, which is quite clear in appropriating $103,736,000 for Forest Health Management, which is a programmatic increase of $19 million above the FY19 level and $29,919,000 above the budget request. I am encouraged by the House’ report, which encourages the Forest Service to address high priority invasive species, pests, and diseases, including the emerald ash borer and bark beetle infestations.

For longer explanations, see my earlier blog on USFS funding.

These bills show an increasing awareness of forest pest issues in key funding committees in both the House and Senate.  Let’s reinforce this message – and spread it to the rest of Congress. Please contact your senators and representative and ask them to support these funding levels.

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.

Thirty Years of Tree Pest Analysis, Continued – Risks of New Introductions

It is widely recognized that invasions of non-native species occur as a consequence of international trade (see Seebens et. al. 2017 – full citations at the end of this blog). This is as true for non-native forest pests as for any other bioinvader – see Aukema et al. 2010; Liebhold et al. 2012, Lovett et al. 2016. In fact, gross domestic product – as an indicator of levels of trade — is a better predictor of the number of forest pest invasions in a given country than the country’s amount of forested land (Roy et al. 2014).

shipping containers at port of Long Beach, California

As I noted in my previous blog, I began studying and writing about the threat to North America’s forests from non-native insects and pathogens in the early 1990s. I reported my analyses of the evolving threat in the three “Fading Forests” reports – coauthored by Scott Schlarbaum – in 1994, 2003, and 2014. These reports are available here.

I document here that both introduction and spread of pests within the country have continued apace. While significant efforts have been made to prevent introductions (described briefly under the “Invasives 101” tab of the CISP website), they have fallen short. As I noted in Fading Forests III, programs aimed at preventing spread of pests within the country remain fragmented and often are unsuccessful.

The Challenge: Huge Volumes of goods are moving, providing opportunities for pests

Since 1990, volumes of imported goods more than quintupled. Within the U.S., a total of 17,978 million tons of goods were transported in 2015; 10,776 million tons of this total by truck. About one-third of this total – 5,800 million tons – was moved farther than 250 miles. These vehicles moved on a public roads network of 4,154,727 miles (US DOT FFA). Consequently, once a pest enters the U.S., it can be moved quickly into every corner of the country.

Introductions

By and large, establishment of tree-killing pests has occurred at a fairly steady rate of about 2.5 per year, with “high-impact” insects and pathogens accumulating at 0.43 per year (Aukema et al. 2010). Since introductions did not rise commensurately with rising import volumes, Lovett et al. (2016) concluded that the recently adopted policies for preventing introductions referenced above are having positive effects but are insufficient to reduce the influx of pests in the face of ever-growing global trade volumes. The study’s authors went on to say that absent more effective policies, they expect the continued increase in trade will bring many new establishments of non-native forest pests.

One group of forest pests did not enter at a steady rate, but rather entered at a higher rate since 1985 – wood-boring insects. Experts concluded that the increase probably reflected increases in containerized shipping (Lovett et al. 2016). At the global level, the rate of fungal invasions has also recently been reported to be increasing rapidly (Roy et al. 2014).

Asian longhorned beetle

Geography of trade patterns also matters. Opening of trade with China (in 1979) offered opportunities for pests from a new source country which has a similar climate and biology. Roy et al. describe the importance of phylogenetic relatedness of pests and of tree hosts in explaining tree species’ vulnerability to introduced pests. The most vulnerable forests are those made up of species similar to those growing in the source of the traded goods – i.e., the temperate forests of the northeastern U.S. – when goods are imported from similar forested areas of Europe and Asia. Chinese-origin wood-boring pests began to be detected around 1990. This already short interval probably underestimates how quickly pests began arriving; detection methods were poor in those years, so a pest was often present for close to a decade before detection.

Between 1980 and 2016, at least 30 non-native species of wood- or bark-boring insects in the Scolytinae / Scolytidae were newly detected in the United States (Haack and Rabaglia 2013; Rabaglia et al. 2019).  Over the same period, approximately 20 additional tree pests were introduced to the continental states (Wu et al. 2017; Digirolomo et al. 2019; R. Haack, pers. comm.) plus about seven to America’s Pacific islands. Not all of the new species are highly damaging, but enough are. See my previous blog here.

Many of the tree-killing pests were probably associated with pathways other than wood packaging. These include 6 of the 7 Agrilus species, sudden oak death pathogen, three pests of palm trees, the spotted lanternfly, beech leaf disease; and the pests introduced to America’s Pacific Islands.

HIGH-RISK PATHWAYS OF INTRODUCTION

Already in the 1990’s it was evident that better preventing pest introductions would depend on shutting down the variety of pathways by which they move around the world.   At that time, attention focused on imports of logs and nursery stock (nursery stock makes up one component of a broader category called by phytosanitary agencies “plants for planting”). Both logs and “plants for planting” had well-established histories of transporting pests and import volumes were expected to grow. We have since learned that there are many more pathways!

Plants for Planting

Imports of “plants for planting” (phytosanitary agencies’ term, which encompasses nursery stock, roots, bulbs, seeds, and other plant parts that can be planted) have long been recognized as a dangerous pathway for introduction of forest pests. For example, this risk was the rationale for adopting the 1912 Plant Quarantine Act. Charles Marlatt, Chairman of USDA’s Federal Horticultural Board (see “Then and Now” in Fading Forests III here), wrote about the risk in National Geographic in April 1911 (urging adoption of the 1912 law) and again in August 1921. See also Brasier (2008), Roy et al. (2014), Liebhold et al. (2012), Jung et al. (2016).

Japanese cherry trees being burned because of scale infestation
January 28, 1910; Agriculture Research Service

Of the 91 most damaging non-native forest pest species in the U.S. (Guo et al. 2019), about 62% are thought to have entered North America with imports of live plants. These include nearly all the sap-feeding insects, almost 90% of the foliage-feeding insects, and approximately half of the pathogens introduced during the period 1860-2006 (Liebhold et al. 2012). Specific examples include chestnut blight, white pine blister rust, Port-Orford-cedar root disease, balsam woolly adelgid, hemlock woolly adelgid, beech scale, butternut canker, dogwood anthracnose, and sudden oak death. In more recent years, introductions via this pathway possibly include ‘ōhi‘a rust, rapid ‘ōhi‘a death pathogens, and beech leaf disease. The gypsy moth, while a foliage feeder, was not introduced via imports of live plants.

The APHIS annual report for 2018 reported that in that year we imported 18,502 shipments containing  more than 1.7 billion plant units (plants, bulbs, in vitro materials, etc.).

Liebhold et al. 2012, relying on 2009 data, found that about 12 percent of incoming plant shipments had symptoms of pests – a rate more than 100 times greater than that for wood packaging. Worse, a high percentage of the pests associated with a shipment of plants is not detected by the federal inspectors. The meaning of this finding is unclear because the study did not include any plant genera native to temperate North America and APHIS points out that infestation rates varied considerably among genera in the study. However, APHIS has not conducted its own analysis to document the “slippage rate” on imports of greatest concern to forest conservationists, i.e., imports of woody plants. I provide details on pests detected on imports of woody plants in recent in my blog here.

Clearly the risk of pest introductions continued at least until recently. I reviewed an APHIS database listing pests newly detected in the country during the period 2009-2013. I concluded that approximately 37 of the 90 “new” pests listed in the database (viruses, fungi, aphids and scales, whiteflies, mites) were probably introduced via imports of plants, cuttings, or cut foliage or flowers. I discussed these matters in greater detail here.

Adoption of a new regulatory regime governing imported plants for planting  (Q-37 regulation) in 2018 is too recent to for us to see its impact. But the new regulation sets up a process under which APHIS can impose more protective regulations on specific types of plants or plants from certain countries of origin to counter a perceived concerning level of risk. Until APHIS begins activating its new powers by negotiating more protective regulations governing plant imports from high-risk sources, it seems unlikely there will be any meaningful change in the introduction rates.

Crates, Pallets, and Other Forms of wood packaging (solid wood packaging, or SWPM)

Recognition of the risk associated with wood packaging is much more recent. In 1982, a USDA risk assessment concluded that the wood boring insects found in crates and pallets were not of great concern (USDA APHIS and Forest Service, 2000). However, contradictory indications were quickly documented – including from APHIS’ own port interception data – which the agency began collecting in 1985. Over the 16-year period 1985-2000, 72% of the 6,825 bark beetles (Scolytidae) intercepted by APHIS were found on SWPM (Haack 2002). Cerambycids (longhorned beetles) and buprestids (jewel beetles) make up nearly 30% of insects detected in wood packaging over the last 30 years (Haack et al. 2014).

Detection of outbreaks of the Asian longhorned beetle and other woodborers in the mid-1990s made it clear that wood packaging was, indeed, a high-risk pathway.

Of the 91 most damaging non-native pest species in the US, 30% probably arrived with wood packaging material or other wood products (Liebhold et al. 2012). This group includes many of the most damaging pests, the deadly woodborers – Asian longhorned beetle, emerald ash borer, redbay ambrosia beetle,  possibly the polyphagous and Kuroshio shot hole borers.

CBP agents inspecting a pallet

As noted above, introductions of wood borers have risen in recent decades, widely accepted as associated with the rapid increase in containerized shipping after 1980. In 2009 it was estimated that 75% of maritime shipments were packaged in crates or pallets made of wood (Meissner et al. 2009). A good history of the global adoption of containerized shipping is Levinson, M. The Box: How the Shipping Container Made the World Smaller and the World Economy Bigger (Princeton University Press 2008)

The simultaneous opening of trade with China (in 1979) offered opportunities for pests from a new source country which has a similar climate and biology. Chinese-origin wood-boring pests began to be detected around 1990. This already short interval probably underestimates how quickly pests began arriving; detection methods were poor in those years, so a pest was often present for close to a decade before detection.

I have already documented numerous times that, despite the U.S.’ implementation of the International Standard of Phytosanitary Measures (ISPM) #15 in 2006, live quarantine pest woodborers continue to enter the U.S. in wood packaging. The best estimate is that 0.1% of wood packaging entering the United States is infested with wood-borers considered to be quarantine pests (Haack et al. 2014). More than 22 million shipping containers entered the U.S. via maritime trade in 2017 (US DoT). As noted, an estimated 75% of sea-borne containers include wood packaging. Applying the 0.1% estimate to these figures results in an estimate that as many as 17,650 containers per year (or 48 per day) transporting tree-killing insects enter the U.S.

Over a period of nine years – Fiscal Years 2010 through 2018 – U.S. Customs and Border Protection (CBP) detected more than 28,600 shipments with wood packaging that did not comply with ISPM#15 (Harriger presentations to the annual meetings of the Continental Dialogue on Non-Native Forest Insects and Diseases). While most of the non-compliant shipments were wood packaging that lacked the required mark showing treatment per ISPM#15, in 9,500 cases the wood packaging actually harbored a pest in a regulated taxonomic group.

Disturbingly, 97% of the shipments that U.S. CBP found with infested wood packaging bear the ISPM#15 mark certifying that wood had been fumigated or heat-treated (Harriger 2017). CBP inspectors tend to blame this on widespread fraud in use of the mark. On the other hand, one study found that larvae can survive both treatments – although the frequency of survival was not determined. It was documented that twice as many larvae reared from wood treated by methyl bromide fumigation survived to adulthood than larvae reared from heat-treated wood; the reason is unclear (Nadel et al. 2016).

The APHIS’ record of interceptions for the period FYs 2011 – 2016 contained 2,547 records for insect detections on wood packaging. The insects belonged to more than 20 families. Families with the highest numbers of detections were Cerambycids – 25% of total; Curculionidae – 23% (includes Dendroctonus, Ips, Orthotomicus, Scolytinae, Xyleborus, Euwallacea); Scolytidae – 17% (includes true weevils such as elm bark beetles); Buprestids – 11%; and Bostrichidae – 3%. Not all of the insects in these groups pose a threat to North American plant species.

One encouraging data point is that since 2010, there have been no detections of species of bark and ambrosia beetles new to North America in the traps deployed by the USDA Forest Service Early Detection and Rapid Response program (Rabaglia 2019). The 2014 recognition of the Kuroshio shothole borer apparently did not result from this trapping program.

There have been several changes in the wood packaging standard and its implementation by CBP since 2009, the year Haack et al. 2014 analyzed the “pest approach rate”. APHIS has not carried out a study to determine whether these recent changes have reduced the approach rate below Haack’s estimate of 0.01%.  Consequently, we do not know whether these changes have reduced the risk of pest introductions.

Other Pathways That Transport  Fewer Pests –  Some of Which Have High Impacts

Insects that attach egg masses to hard surfaces can be transported by ship superstructures, containers, and hardsided cargoes such as cars, steel beams, and stone. While relatively few species have been moved in this way, some have serious impacts. The principal examples are the gypsy moths from Asia, which feed on 500 species of plants (Gibbon 1992). 

The United States and Canada have a joint program – under the auspices of the North American Plant Protection Organization (see RSPM #33) aimed at preventing introduction of species of Asian gypsy moths. The NAPPO standard originally went into force in March 2012. Under its terms, ships leaving ports in those countries during gypsy moth flight season must be inspected and cleaned before starting their voyage.

Gypsy moth populations rise and fall periodically; it is much more likely that egg masses will be attached to ships during years of high moth population densities. These variations are seen in U.S. and Canadian detection reports – as reported here.

While most AGM detections are at West Coast ports, [here;  and here] the risk is not limited to that region. AGM have been detected at Wilmington, NC; Baltimore, MD; Charleston, SC; Savanna and Brunswick, GA; Jacksonville, FL; New Orleans, LA; Houston and Corpus Christi, TX; and even McAlester, OK.  

Nor is the risk limited to the ships themselves. In 2014, more than 500 Asian gypsy moth egg masses were found on four shipments of imported steel slabs arriving at ports on the Columbia River in Washington.

Between 1991 and 2014, AGM was detected and eradicated on at least 20 occasions in locations across the United States (USDA AGM pest alert). Additional outbreaks have been discovered and eradication efforts undertaken in more recent years.

A second example is the spotted lanternfly (SLF) (Lycorma delicatula), which was first detected in southeast Pennsylvania in autumn 2014. It is native to Asia; it is believed to have entered the country as egg masses on imported stone.

While SLF is clearly a pest of agriculture – especially grapes and tree fruits – its importance as a forest pest is still unclear. Many native forest trees appear to be hosts during the insect’s early stages, including maples, birches, hickories, dogwoods, beech, ash, walnuts, tulip tree, tupelo, sycamore, poplar, oaks, willows, sassafras, basswood, and elms. Adult lanternflies strongly prefer the widespread invasive species tree of heaven (Ailanthus altissima).

As of August 2019, SLF was established in parts of five states: Delaware, Maryland, New Jersey, Pennsylvania, and Virginia. It was detected as having spread to a 14th county in Pennsylvania; five new counties in New Jersey. APHIS is working with state departments of Agriculture in these states, as well as supporting surveys in New York, North Carolina, and West Virginia (USDA APHIS DA-2019-20, August 7, 2019). Apparently the detections of a few adults – alive or dead – in Connecticut and New York had not evolved into an outbreak. See description and map here.

Imports of logs – roundwood – seem inherently risky. Certainly Dutch elm disease was introduced via this pathway. However, there have been few pest introductions linked to this pathway in recent years, probably because we import most of our unprocessed lumber from Canada. (I provide considerable data on U.S. roundwood imports in Fading Forests III here.)

Decorative items and furniture made of unprocessed wood certainly have the potential to transport significant pests (USDA APHIS 2007). Examples include boxes and baskets; wood carvings; birdhouses; artificial Christmas trees or other plants; trellises; lawn furniture. To date, apparently, no high-impact pest has been introduced via this pathway, although pests intercepted on shipments have included Cerambycids from Asia, e.g., velvet longhorned beetle and here.

Alarmed by high numbers of infested shipments from China, APHIS first suspended imports of such items temporarily; then adopted a regulation (finalized in March 2012 – USDA APHIS 2012).

APHIS has not taken action to prevent introductions on such items imported from other countries – although the North American Plant Protection Action adopted a regional standard making the case for such action and outlining a risk-based approach (NAPPO RSPM#38).

Snails on Shipping Containers

Snails have been detected on shipping containers and wood packaging for decades. In 2015, APHIS stepped up its efforts to address this risk through bilateral negotiations with Italy and launching regional and international efforts to develop guidance for ensuring pest-free status of shipping containers (Wendy Beltz, APHIS, presentation to National Plant Board, 2018 annual meeting).

SPREAD WITHIN THE UNITED STATES

Major pathways for human-assisted spread of pests within the country are sales of plants for planting, movement of unprocessed wood – especially firewood, and hitchhiking on transport vehicles. Since most forest pests are not subject to federal quarantine, any regulatory programs aimed at preventing spread depend on cooperation among the 50 states. None of these pathways is regulated adequately to prevent pests’ spread. See Chapter 5 of Fading Forests III here.

And since neither federal nor state agencies do significant enforcement of existing regulations, preventing spread often depends upon pest awareness of, and voluntary compliance by, individuals and companies.

Even pests subject to a federal quarantine are not prevented from spreading. Plants exposed to the sudden oak death pathogen were shipped to 18 states in spring 2019.

SOD-infected rhododendron plant; Indiana Department of Natural Resources

A collaborative effort by the nursery industry, APHIS, and states (Systems Approach to Nursery Certification, or SANC) is striving to close gaps linked to the standard practice of inspecting plants at the time of shipping, but full implementation of this voluntary program is still years away.

Transport of firewood has been responsible for movement of pests both short distances, e.g., goldspotted oak borer in southern California; and long distances – e.g., emerald ash borer to Colorado. APHIS attempted to develop a certification program but the industry was unable to put one together (see Chapter 5 of Fading Forests III). Current federal and state regulations of firewood are tied to the emerald ash borer quarantine, which APHIS has proposed to terminate. Wood for turning and woodworking has also been linked to movement of pests, e.g., walnut twig beetle/thousand cankers disease from the west to Pennsylvania.

emerald ash borer

Truck transport of a variety of goods has transported European gypsy moths from the infested areas in the east to the west coast. Transport of stone probably moved spotted lanternfly from southeastern Pennsylvania to Winchester, Virginia.

SOURCES

Aukema, J.E., D.G. McCullough, B. Von Holle, A.M. Liebhold, K. Britton, & S.J. Frankel. 2010. Historical Accumulation of Nonindigenous Forest Pests in the Continental United States. Bioscience. December 2010 / Vol. 60 No. 11

Brasier, C.M. 2008. The biosecurity threat to the UK and global environment from international trade in plants.  Plant Pathology (2008) 57, 792-808

Bray, A.M., L.S. Bauer, T.M. Poland, R.A. Haack, A.I. Cognato, J.J. Smith. 2011. Genetic analysis of emerald ash borer (Agrilus planipennis Fairmaire) populations in Asia and North America. Biol. Invasions (2011) 13:2869-2887

Gibbon, A. 1992. “Asian Gypsy Moth Jumps Ship to United States.” Science. Vol. 235. January 31, 1992.

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