Category: plants as pest vectors

International Year of Plant Health: Time to Admit that the International Phytosanitary System is Failing

As I noted last November, the premise of the international phytosanitary system – the Agreement on the Application of Sanitary and Phytosanitary Standards (SPS Agreement) and the International Plant Protection Convention (IPPC) – is that importing countries should, and can, rely on exporting countries to take the actions necessary to meet the importing countries’ plant health goals. However, the experience with the International Standard on Phytosanitary Measures (ISPM) #15 and wood packaging casts doubt on this premise.

Exporters are not reliably ensuring the cleanliness of their wood packaging, putting American forests at risk. Indeed, some experts have concluded that continuing to implement ISPM#15 at current levels could triple the number of non-native wood-boring insects introduced into the U.S. by 2050 (Leung et al. 2014).

Too many shipments carry wood packaging that bears no ISPM#15 stamp. And too many pieces of wood packaging arrive with the ISPM#15 stamp, yet are not reliably pest-free. If we cannot clean up this pathway – which involves boards or even logs that are, after all, already dead — it bodes poorly for limiting pests imported with other commodities that are pathways for tree-killing pests – especially living plants (plants for planting). Living plants are much more easily damaged or killed by treatments than the dead wood used in packaging – so ensuring pest-free status of a shipment is even more difficult.  (A longer discussion of the SPS Agreement and IPPC is found in Chapter III of Fading Forests II, available here.

Here are the problems – and the latest evidence.

ALB larva in piece of wood packaging material

Too Many Shipments with Pest-Infested Wood Packaging Are Reaching the Country

My information on Customs and Border Protection (CBP) interceptions comes primarily from Kevin Harriger (see full reference at end of the blog). I will note when it comes from other sources.

In November 2019, Kevin Harriger reported that over the past three years, CBP detected a regulated pest, on average, in 30% of the wood packaging the agency intercepted because it was not compliant with ISPM#15. Non-compliance is defined as wood packaging that either lacks an official mark or is infested by a quarantine pest, or both.

From this and previous reports, I have 10 years of CBP interception data – from 2020 – 2019. These data thus begin four years after the U.S. began implementing ISPM#15 (in 2006) and 11 years after the U.S. began requiring China to treat wood packaging accompanying its exports (in 1999).

Over the period 2010 – 2018, CBP intercepted an average of 3,183 shipments with non-compliant wood packaging each year. On average, 2,100 (66%) of these shipments lacked the required ISPM#15 mark. A live quarantine pest was found in an average of 794 (25%) shipments. (There was some overlap in the categories).

In 2019, CBP intercepted a total of 2,572 non-compliant shipments (Stephen Brady, CBP, April 2020). Those lacking the ISPM#15 mark number 1,825 (71%). Shipments in which a live pest was found numbered 747 (29%).

The 2019 data show decreases, in absolute numbers, from earlier years in all categories: a 19% decrease below 1010-2018 average of shipments intercepted; a 13% decrease in number of shipments intercepted because the wood packaging lacked the ISPM#15 mark; a decrease of 6% in the number of shipments intercepted that had a quarantine pest. It is too early to say whether CBP’s stronger enforcement approach launched in November 2017 has resulted in a lower number of shipments in violation of ISPM#15 approaching our shores.

There has been a dispute about which categories of packaging are most likely to be infested. The categories are pallets, crates, spools for cable, and dunnage (wood used to brace cargo and prevent it from shifting). The CBP data available to me and the study by Krishnankutty et al. (2020b – see full reference at the end of this blog) shed no light on that issue.  

What is the actual number of infested containers approaching our shores? We know that CBP inspects, on average, 2% of incoming containers – so the above interception data reflect a small percentage of probable true approach rate.

The first issue is, how many containers arrive here?

I have been unable to find data for 2019 – much less 2020, when the media report that import volumes have crashed. Until recently, import volumes had been rising. According to a U.S. DOT report to Congress (see reference at the end of this blog), 25 U.S. maritime ports received 24,789,000 loaded shipping containers (measured as TEU – 20-foot equivalent) in 2018. The number of incoming containers had increased at the top three ports – Long Beach, Los Angeles, and New York / New Jersey – between 3% and 7% since 2016.

However, APHIS told me in November 2019 that CBP reports that only about 13 million loaded containers enter the country every year by rail, truck, air, or sea. While I can’t yet explain the discrepancy, one possible explanation is that DoT counts 40-foot containers as two 20-foot containers.

(Of course, pests introduced to Canada also threaten North America’s forests. Canada received fewer than 5 million containers via maritime trade in 2016 (Asbil pers. comm. 2018).

Two decade-old estimates of the proportion of incoming containers that hold wood packaging (Haack et al. 2017, Meissner et al. 2009) allow me to estimate the risk associated with these incoming containers. Meissner et al. found that 75% of maritime containers have wood packaging. Haack et al. estimated that the wood in 0.1% of those containers was infested. Applying these two factors, I conclude that as many as 18,590 of incoming containers in maritime trade could have been transporting a woodborer in the regulated families (Cerambycids, Buprestids, Siricids). I am hesitant to apply the calculation to CBP’s estimate because I don’t know how many of the 13 million containers entered by sea. However, if I assume that the same percentage of wood packaging applied to all the CBP-counted containers, I conclude that 9,750 of those containers held infested wood packaging – still a significant number.

The actual approach rate might be less – or more! Haack et al. (2014) did not include imports from China in their calculations. Given the history of interceptions, it appears probable to me that a recalculation of the approach rate that included China would probably raise the overall proportion.

Furthermore, 11 years have passed since Haack and Meissner made their calculations. During that time, ISPM#15 has been amended to make it more effective. The most important change was restricting the size of bark remnants that may remain on the wood. I have asked several times that APHIS commission a new analysis of Agriculture Quarantine Inspection Monitoring data to determine the pest approach rate before and after the CBP action in order to determine whether the more aggressive enforcement has led to reductions in non-compliant shipments at the border.

By comparing Dr. Haack’s estimate (see above) with the CBP data, I estimate that Customs is detecting and halting the importation of 4 – 8% of the shipments that actually contain pest-infested wood. Since CBP inspects only about two percent of incoming shipments, the higher detection rate demonstrates the value of CBP’s program to target likely violators – and deserves praise. But it is obviously too low a “catch” rate to provide an adequate level of protection for our forests. 

ISPS#15 Is Not Helping to Target Inspections

So – ISPM#15 still allows too many pests to arrive at our shores. Is ISPM#15 at least helping phytosanitary agencies target inspections? No, because both U.S. and European data demonstrate that a high proportion of shipments containing infested wood pieces bore the ISPM#15 stamp. Phytosanitary agencies cannot rely on the presence or absence of the stamp to indicate the pest risk level.

U.S. data:

  • During the period 2010-2015, CBP found that an average of 95% of pest-infested shipments bore the ISPM#15 mark (Harriger). Unfortunately, CBP data from more recent years don’t provide this breakdown.
  • In the past two years, CBP inspectors have repeatedly found pests in dunnage bearing the ISPM#15 mark.
  • Krishnankutty et al. (2020b) analyzed wood packaging from 42 countries of origin intercepted by CBP over six years (April 2012 – January 2018). They found that 87% of the interceptions bore the ISPM mark.

I blogged earlier about the velvet longhorned beetle (Trichoferus (=Hesperophanes) campestris) This pest, like others, has reached our shores and entered the country both before and after implementation of ISPM#15. The predictable result is that VLB is established in three states and has been detected in 14 others plus Puerto Rico (Krishnankutty, et al. 2020a). Apparently we have been lucky that this one isn’t as damaging as so many are!

European data:

For Europe, see Eyre et al. (2018). They concluded that the ISPM-15 mark was of little value in predicting whether harmful organisms were present.

This is alarming and we need to understand the reason – How much is caused by fraud? How much is caused by failure of treatment – either intrinsic weakness or incorrect application? APHIS researchers have found that larvae from wood subjected to methyl bromide fumigationwere more likely to survive to adulthood than those intercepted in wood that had been heat treated (Nadel et al. 2016).

Krishnankutty et al. (2020b) query whether the 2009 requirement that wood be debarked might be less effective in countering insect species that require bark only in the early stages of larval development. Half of the species intercepted in hardwood shipments (e.g., Anoplophora glabripennis, Phoracantha recurva) might fit this profile. They also appear to pose a higher threat since they are polyphagous and known to infest healthy hosts. While some of the softwood-inhabiting species also require bark, they not known to infest living trees and only a quarter were classified in the high-risk group. The Mech et al. 2020 finding that no wood-borers that specialize in conifers posed a high risk appears to support these different impacts.

Krishnankutty, et al. (2020b) also note the risk from pallet recycling. The wood might occasionally be infested by dry-wood borers. One puzzling example was wood packaging shipped from Brazil and bearing a Brazilian ISPM#15 stamp that was infested with a larva of T. campestris (VLB). This is an Asian species not recorded as being present in South or Central America. The authors speculate that the pallets were recycled in Brazil after inadequate treatment in their original places of manufacture.

Of the 17 wood borer species intercepted in hardwoods, three have reproducing populations in the U.S.: A. glabripennis, Phoracantha recurva and T. campestris. Krishnankutty et al. (2020b) say that they are unaware of any of the non-native buprestids and siricids intercepted in softwood SWPM being established in the US. (One Siricid that is established, Sirex noctillio, was not detected in the wood packaging analyzed in this study.)

What Can Be Done to Slow or Eliminate this Pathway?

CBP inspectors

CBP strengthened enforcement of ISPM#15 in November 2017. CBP’s enforcement actions increased by 400% from 2017 to 2018 (John Sagle, CBP, pers. comm). CBP has also expanded its outreach to shippers and others involved in international trade with the goal of reducing all types of non-compliance – lack of documentation, pest presence, etc. in both wood packaging and shipping containers. The outreach includes awareness campaigns targetting trade, industry, affiliated associations, CBP employees, and international partners (Harriger).

Certain countries have a long-standing record of non-compliance with ISPM#15 – as seen in interception records.

  • Haack et al. 2014 – Italy was the country of origin for most wood borers intercepted 1985 – 2000.
  • Haack et al. 2014 – the top 5 countries in the 2003 – 2009 period were Mexico (33.7%), Italy (14.2%), Canada (13.4%), Netherlands (4.4%), China (4.1%).
  • APHIS’ interception database for FY2011-2016 (provided to me) showed Mexico, China, Italy, and Costa Rica had the highest numbers of interceptions.
  • Krishnankutty et al. (2020b) found the highest numbers of interceptions came from Mexico, China, and Turkey.

These numbers reflect in part the huge volumes of goods imported from both Mexico and China. But China and Italy stand out for their poor performance. (The U.S. does not regulate – or inspect! – wood packaging from our third-largest trade partner Canada.)

Officials know which individual companies within these countries have a history of non-compliance. For example, 21 of the interceptions on wood packaging made from Populus trees in China (53%) were associated with stone, ceramic, and terracotta commodities. Anoplophora glabripennis was intercepted six times in Populus originating from a single wood-treatment facility in China (Krishnankutty et al. 2020b).

How reduce risk to U.S. forests?

Over the past year or two, I have suggested the following actions:

  1. USDA APHIS join Bureau of Customs and Border Protection in penalizing violators.
  2. Citing the need for setting a higher “level of protection”, APHIS & the Canadian Food Inspection Agency (CFIA) should prepare a risk assessment to justify adopting more restrictive regulations. The new regulations should prohibit use of packaging made from solid wood – at least from the countries with records of high levels of non-compliance (listed above).
  3. USDA Foreign Agriculture Service (FAS) should assist U.S. importers to determine which suppliers reliably provide compliant wood packaging.
  4.  USDA FAS and APHIS should help importers convey their complaints about specific shipments to the exporting countries’ National Plant Protection Organizations (NPPOs; departments of agriculture).
  5. APHIS should increase 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.
  6. APHIS should fund more studies and audits of wood packaging to document the current efficacy of the standard, including an urgent update of the Haack study of pest approach rate.

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.

The situation is even worse re: movement of plants for planting.

SOURCES

Asbil, W. Canadian Food Inspection Agency, pers. comm. August 2018.

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)

Haack, R. A., K. O. Britton, E. G. Brockerhoff, J. F. Cavey, L. J. Garrett, M. Kimberley, F. Lowenstein, A. Nuding, L. J. Olson, J. Turner, and K. N. Vasilaky. 2014. Effectiveness of the international phytosanitary standard ISPM no. 15 on reducing wood borer infestation rates in wood packaging material entering the United States. Plos One 9:e96611.

Harriger, K. Executive Director for the Agriculture Programs and Trade Liaison office, Department of Homeland Security Bureau of Customs and Border Protection (CBP), presentations to the Continental Dialogue on Non-Native Forest Insects and Diseases, over appropriate years. https://continentalforestdialogue.org/events/

Krishnankutty, S.M., K. Bigsby, J. Hastings, Y. Takeuchi, Y. Wu, S.W. Lingafelter, H. Nadel, S.W. Myers, and A.M. Ray. 2020a. Predicting Establishment Potential of an Invasive Wood-Boring Beetle, Trichoferus campestris (Coleoptera:) in the United States. Annals of the Entomological Society of America, XX(X), 2020, 1–12

Krishnankutty,  S., H. Nadel, A.M. Taylor, M.C. Wiemann, Y. Wu, S.W. Lingafelter, S.W. Myers, and A.M. Ray. 2020b. Identification of Tree Genera Used in the Construction of Solid Wood-Packaging Materials That Arrived at U.S. Ports Infested With Live Wood-Boring Insects. Commodity Treatment and Quarantine Entomology

Leung, B., M.R. Springborn, J.A. Turner, E.G. Brockerhoff. 2014. Pathway-level risk analysis: the net present value of an invasive species policy in the US. The Ecological Society of America. Frontiers of Ecology.org

Mech,  A.M., K.A. Thomas, T.D. Marsico, D.A. Herms, C.R. Allen, M.P. Ayres, K.J. K. Gandhi, J. Gurevitch, N.P. Havill, R.A. Hufbauer, A.M. Liebhold, K.F. Raffa, A.N. Schulz, D.R. Uden, & P.C. Tobin. 2019. Evolutionary history predicts high-impact invasions by herbivorous insects. Ecol Evol. 2019 Nov; 9(21): 12216–12230.

Meissner, H., A. Lemay, C. Bertone, K. Schwartzburg, L. Ferguson, L. Newton. 2009. Evaluation of Pathways for Exotic Plant Pest Movement into and within the Greater Caribbean Region. Caribbean Invasive Species Working Group (CISWG) and USDA APHIS Plant Epidemiology and Risk Analysis Laboratory

Nadel, H. S. Meyers, J. Molongoski, Y. Wu, S. Lingafelter, A. Ray, S. Krishnankutty, A. Taylor. 2017. Identification of Port Interceptions in Wood Packing Material Cumulative Progress Report, April 2012 – June 2017

USDA APHIS interception database – pers. comm. January 2017.

USDA APHIS press release dated September 12, 2018

U.S. Department of Agriculture, Press Release No. 0133.20, January 27, 2020

US Department of Transportation. Port Performance Freight Statistics in 2018 Annual Report to Congress 2019 https://rosap.ntl.bts.gov/view/dot/43525

Wu, Y., S.M. Krishnankutty, K.A. Vieira, B. Wang. 2020. Invasion of Trichoferus campestris (Coleoptera: Cerambycidae) into the United States characterized by high levels of genetic diversity and recurrent intros. Biological Invasions Volume 22, pages1309–1323(2020)

Yemshanov, D., F.H. Koch, M. Ducey, K. Koehler. 2012. Trade-associated pathways of alien forest insect entries in Canada. Biol Invasions (2012) 14:797–812

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.

SOD – questions that need answers

SOD in the nurseries

infected rhododendron
photo by Jennifer Parke
Oregon State University

As you may remember, in May 2019, we became aware of a troubling outbreak of the sudden oak death pathogen Phytophtora ramorum in the nursery trade. The discovery was made by Indiana authorities, who carefully inspected plants being sold in the state.

Briefly, 28 states initially learned that they might have received plants from the suspect sources. Later, APHIS determined that plants exposed to the pathogen had been sent to 18 states – Alabama, Arkansas, Iowa, Illinois, Indiana, Kansas, Kentucky, Michigan, Missouri, Nebraska, North Carolina, Ohio, Oklahoma, Pennsylvania, Tennessee, Texas, Virginia, and West Virginia. Of these, seven (Iowa, Illinois. Indiana, Kansas, Missouri, Nebraska, Oklahoma) plus Washington were known to have received P. ramorum-positive nursery stock. [California Oak Mortality Task Force Newsletter August 2019]

The 2019 episode was just the latest of several occasions since 2004 in which infected plants have been widely distributed by the nursery trade, despite federal and state regulations.

APHIS delays in explaining the situation and what actions it was taking led the states to complain through a letter from the National Plant Board.

For discussions of the 2019 espisode, see my earlier blog or the California Oak Mortality Task Force newsletter for February 2020.

What have we learned from this episode?

1) Three West coast states – California, Oregon, and Washington – are a usual source for the nursery trade of plant taxa that happen to host the P. ramorum pathogen plants. These states’ climates are conducive to growth of these plants and of the pathogen. After repeated nursery outbreaks over 16 years, I think it is time to question continued reliance on such a high-risk source for these plants.

2) APHIS funds the federally-mandated inspection programs in the three states through the “specialty crops” line of the agency’s annual appropriations. Funding levels have apparently remained steady in recent years (COMTF Feb 2020), despite increases in the overall funding for the “specialty crops” line in recent years. I – and some of you! – have lobbied for these increases precisely in order to address the P. ramorum threat. Why has the funding not been increased?

3) While APHIS allocated $352,945 (COMTF February 2020) from the Plant Pest and Disease Management and Disaster Prevention program to help states carry out nursery surveys in 14 states following the 2019 incident, some of the affected states were not included in the program and some states that had not received suspect plants were. States that did not get funding in Fiscal Year 2020 (2020 award report) included three where P. ramorum-positive plants were detected: Iowa, Illinois, and Indiana; and one state that had a scare – Pennsylvania received plants but none tested positive. Seven states received P. ramorum survey funds through the Plant Pest and Disease Management and Disaster Prevention program although they had not received positive plants in the 2019 incident. These were Maryland, Massachusetts, Nevada, New York, North Dakota, Rhode Island, and South Carolina.

The Plant Pest and Disease Management and Disaster Prevention program distributes $70 million annually, and is not subject to annual appropriations. Does a national crisis play any role in determining which projects get funded? Or are decisions made entirely on a proposal by proposal basis and so depend on states’ priorities and individuals’ grant-writing skills?

4) Even now, on the verge of a new plant shipping season (if one occurs given the Covid-19 virus shutdowns), I have seen no public information clarifying how the inspection systems in Washington, British Columbia, and at the U.S. border failed to detect the infested plants before they were shipped. Trace-back efforts carried out by state and U.S. authorities pointed to a nursery in British Columbia as the original source of the infested plants. However, the Canadian Food Inspection Service (CFIA) determined that no Canadian nursery shipped infected plants to the U.S. in 2018 or 2019. See the next paragraph for a description of APHIS’ efforts to resolve this discrepancy.

According to information in the Oregon Department of Agriculture report for 2019, plant imports from Canada are inspected by DHS Customs and Border Protection (CBP) agriculture specialists, not by APHIS. Apparently, CBP has been relying on rules applicable to fruits and vegetables (Q-56) rather than the more stringent provisions of the plants for planting regulation (Q-37). Alerted by Oregon to the importation of 15 Euonymus plants infested by a federally-designated quarantine pest (a thrips), the National Plant Board sent a letter to APHIS in August 2019 asking that it correct CBP’s inspection process.

In March 2020, APHIS sent a letter to the states saying it had amended its Manual and guidance to CBP agricultural inspectors to clarify that all plants for planting must be handled in accordance with the more stringent Q-37 regulations. Furthermore, APHIS is working with CFIA to clarify understanding of each other’s P. ramorum procedures. The letter states that APHIS might consider prohibiting importation of P. ramorum hosts from Canada until CFIA demonstrates that it has adopted effective management measures.

This action by APHIS demonstrates a new seriousness in addressing P. ramorum. I hope this gravitas will persist and carry through to 1) strengthening theregulatory conditions governing domestic production and sales see following section); 2) providing financial and other support to the states (see above about the “specialty crops” appropriation); 3) funding additional studies to clarify the host list and modes of transmission; and 4) using its authority under NAPPRA to curtail imports of plants from Vietnam and other areas where there are large numbers of newly detected Phytophthora species that might threaten North American plant species.  

infested plants detected by Indiana inspectors

I question sufficiency of inspection and mitigation regime

(as described in the February 2020 COMTF newsletter)

When alerted to the infected plants turning up in Indiana, in May 2019, Washington State Department of Agriculture (WSDA) began trace-back investigations. The large wholesale shipping nursery that supplied the plants appears to have acted quite responsibly – it destroy 54,000 plants, cooperated in the Critical Control Point assessment, and implemented mitigation actions. However, I am disturbed to read that the destruction of plants in the 10-meter quarantine radius from plants detected to be infected was a voluntary action. Why don’t the regulations require destruction of nearby hosts?

Descriptions of the western states’ inspection systems – those tied to this specific nursery episode and routine inspections under federal and state P. ramorum programs – indicate to me that P. ramorum is circulating in nurseries in the west coast states, but is evading detection. I cite examples from all three states.

One of the positive nurseries in California in 2019 had been found to be positive in previous years and is considered to be in compliance with quarantine regulations. Yet these measures have not been sufficient to ensure that the nursery is pathogen-free now – as illustrated by its testing positive in 2019.

In Oregon, a retail nursery found to have infected plants destroyed all host material located in the block. Is this action sufficient to ensure that the nursery is now pathogen free? What about the soil, water, cull piles, etc.?  Oregon trace-back surveys led to various suppliers that had previously not been known to be infested. This leads me to think that the pathogen is circulating below regulators’ attention.

In the wake of the 2019 crisis, Washington State Department of Agriculture (WSSA) inspected “opt-out” nurseries – those that had decided not to join APHIS’ program to ship interstate, but continued to ship within the state. WSDA relied on visual inspection only of host material; the agency collected no samples from plants or nursery soils, water, or plant waste (Feb 2020 COMTF). Given all we know about the difficulty of detecting P. ramorum, I think we need more intense inspections that do sample soils, water, and any nearby plant waste (cull piles).

Meaning of Stream Detections?

The P. ramorum pathogen continues to turn up regularly in water bodies. At a botanical garden in Washington State, plant samples have been negative since February 2016. However, water baits from a small pond were positive in 2019 and previous years. Washington’s Sammamish Riverhas been positive since 2007. In the Southeast, seven streams tested positive in 2019. Most if not all have been positive consistently or at least repeatedly for years. All these positive streams are associated with nurseries previously positive for the pathogen. However, plants in the vicinities of these streams show no symptoms.

The same is true in Vietnam: P. ramorum was found in seven out of eight high-elevation streams sampled, but none of the plants belonging to families that have proved highly vulnerable in North America and Europe had any disease symptoms (Jung et al, 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). The Jung et al. 2020 findings are discussed in the COMTF Feb. 2020 newsletter and my recent blog.

SOD in the woods

dead coast live oak in California
Joseph O’Brien, USFS

The COMTF February 2020 newsletter summarizes the worrying increase in disease in California woodlands in recent years, which followed the record wet spring of 2017. Aerial surveys documented a big increase in dead tanoak trees and affected acreages in 2018, followed by a smaller increase in 2019 – although still much higher than in 2017. [Details: in 2017, 21,000 dead trees were mapped across 18,000 acres; in 2018, 1.6 million dead trees across 106,000 acres; in 2019, 885,000 dead trees across 92,000 acres.]

California officially records as infested only those counties where infestations have been confirmed by California Department of Food and Agriculture or county Agricultural Commissioners. California currently lists 15 counties as infested. Recent observations by academics or other non-officials of Phytophthora ramorum in Del Norte and San Luis Obispo counties have not yet been confirmed by officials so neither is included in the official quarantine. I understand the need to be certain about reported detections, but we should remember that the disease is probably more widespread than official data indicate.

The newsletter reports Oregon’s treatment efforts – which have totaled 7,300 acres since 2001. I am pleased that Oregon Department of Forestry now has an Environmental Quality Incentives Program (EQIP) project with the USDA Natural Resources Conservation Service and that both the Bureau of Land Management and USDA Forest Service are treating infected areas.

treatment of SOD-infested site
in Oregon
USFS

Still, the quarantine area now covers 31% of Curry County, the EU1 lineage is established in the forest, and ODF and its partners lack sufficient resources to treat all infected areas.

Washington State doesn’t have (known) forest infestations, but it continues to find the pathogen in water bodies; the Sammamish River in King County has been positive since 2007.

In the East, seven states (Alabama, Florida, Georgia, Mississippi, North Carolina, South Carolina, and Texas) participated in the USFS Cooperative Sudden Oak Death Early Detection Stream Survey in 2019. A total of 48 streams were surveyed. P. ramorum was detected from seven streams – five in Alabama, one in Mississippi, and one in North Carolina. All positive streams were associated with nurseries previously positive for the pathogen.

Finally, the newsletter summarizes an article providing advice on managing SOD’s impacts – specifically, conservation of tanoak.

SOURCES

February 2020 issue of the California Oak Mortality Task Force newsletter http://www.suddenoakdeath.org/wp-content/uploads/2020/02/COMTF-Report-February.pdf

Oregon Department of Agriculture Plant Protection and Conservation 2019 annual report

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.

Progress – Now Threatened – On Protecting Our Cacti

prickly pear cacti in Big Bend National Park
photo by Blake Trester, National Park Service

The cacti that are such important components of desert ecosystems across nearly 2 million square miles straddling the U.S.-Mexico border are under threat from non-native insects – as I have noted in earlier blogs. Of course, cacti are important in other ecoregions, too – I wrote recently about the columnar cacti in the dry forests of Puerto Rico.

Flat-padded prickly pear cacti of the genus Opuntia are threatened by the cactus moth, Cactoblastis cactorum.

In 1989, the cactus moth was found in southern Florida, to which it had spread from the Caribbean islands (Simonson 2005). Recently, the moth was found to have spread west as far as the Galveston, Texas, area and near I-10 in Columbus, Texas, about 75 miles west of central Houston (Stephen Hight, pers. com.) Two small outbreaks on islands off Mexico’s Caribbean coast have been eradicated.

In Florida, the cactus moth has caused considerable harm to six native species of prickly pear, three of which are listed by the state as threatened or endangered.

When the cactus moth reaches the more arid regions of Texas, it is likely to spread throughout the desert Southwest and into Mexico. In the American southwest, 31 Opuntia species are at risk; nine of them are endemic, one is endangered. Mexico is the center of endemism for the Opuntia genus. In Mexico, 54 Opuntia species are at risk, 38 of which are endemic (Varone et al. 2019; full citation at end of this blog).

The long-term effects of the cactus moth on these North American Opuntia are unknown because there may be substantial variations in tolerance. The attacks observed in the Caribbean islands have shown great variability in various cactus species’ vulnerability (Varone et al. 2019).

The Opuntia cacti support a diversity of pollinators as well as deer, javalina (peccaries), tortoises, and lizards. Prickly pears also shelter packrats and nesting birds (which in turn are fed on by raptors, coyotes, and snakes), and plant seedlings. Their roots hold highly erodible soils in place (Simonson 2005).

While scientists have been concerned about the possible impacts of the cactus moth since it was detected in Florida 30 years ago, a substantial response began only 15 years later. The U.S. Department of Agriculture began trying to slow the spread of the cactus moth in 2005 (Mengoni Goñalons et al. 2014), with a focus on surveys and monitoring, host (cactus) removal, and release of sterile males. This program was successful at slowing the moth’s spread and eradicating small outbreaks on offshore islands of Alabama, Mississippi, and Mexico.

Cactus moth damage to native cacti in Florida
photo by Christine Miller, UF/IFAS

However, the moth continued to spread west and the program never received an appropriation from Congress. The primary funding source was a US – Mexico Bi-National Invasive Cactus Moth Abatement Program. Both countries contributed funds to support the research and operational program to slow the spread in the U.S. Funds were provided through USDA Animal and Plant Health and Inspection Service (APHIS) and the Mexican Secretariat of Agriculture, Livestock, Rural Development, Fisheries and Food (SEGARPA). Unfortunately, funding was reduced by both entities and became inadequate to maintain the Bi-National Program.

Therefore, in 2012, APHIS abandoned its regional program and shifted the focus to biocontrol. This is now considered the only viable control measure in the desert Southwest where vulnerable cacti are numerous and grow close together. The biocontrol project has been funded since 2012 through the Plant Pest and Disease Management and Disaster Prevention program (which receives funding through the Farm Bill). It has received a total of slightly more than $2 million over seven years. More than half the funds went to the quarantine facility to support efforts to rear non-target hosts and verify the biocontrol agent’s host specificity. About a quarter of the funds supported complementary work of an Argentine team (both the cactus moth and the most promising biocontrol agent are native to Argentina). Much smaller amounts have supported U.S.-based scientists who have studied other aspects of the cactus moth’s behavior and collected and identified the U.S. moths being tested for their possible vulnerability to attack by a biocontrol wasp.

Here are details of what these dedicated scientists achieved in just the past seven years at the relatively low cost of roughly $2 million. Unfortunately, the project now faces a funding crisis and we need to ensure they have the resources to finish their work.

Some Specifics of the BioControl Program

After literature reviews, extensive collections, and studies in the cactus moth’s native habitat in Argentina (Varone et al. 2015), a newly described wasp, Apanteles opuntiarum (Mengoni Goñalons et al. 2014), has been determined to be host specific on Argentine Cactoblastis species and the most promising candidate for biocontrol. Wasps were collected in Argentina and sent to establish a colony in a quarantine facility in Florida to enable host specificity studies on North American Lepidoptera (Varone et al. 2015).

Quarantine host specificity studies and development of rearing technology has not been straightforward. Initially, it was difficult to achieve a balanced male/female ratio in the laboratory-bred generations; this balance is required to maintain stable quarantine laboratory colonies for host range testing. This difficulty was overcome. A second challenge was high mortality of the cactus-feeding insects collected in the Southwest that were to be test for vulnerability to the biocontrol wasp. These desert-dwellers don’t do well in the humid, air-conditioned climate of the quarantine facility! For these difficult-to-rear native insects, scientists developed a molecular genetics method to detect whether eggs or larvae of the cactus moth parasitoid were present inside test caterpillars after they were exposed to the wasps. For easy to rear test insects, caterpillars are exposed to the wasps and reared to adulthood. Host specificity tests have been conducted on at least five species of native U.S. cactus-feeding caterpillars and 11 species of non-cactus-feeding caterpillars (Srivastava  et al. 2019; Hight pers.comm.).

To date there has been no instance of parasitism by Apanteles opuntiarum on either lepidopteran non-target species or non-cactus-feeding insects in the Florida quarantine or in field collections in Argentina (Srivastava et al. 2019; Varone et al. 2015; Hight pers.comm.).

The scientists expected to complete host-specificity testing in the coming months, then submit a petition to APHIS requesting the release of the wasp as a biocontrol agent. Unfortunately, the project’s request for about $250,000 in the current year was not funded. This money would have funded completion of the host specificity testing, preparation of a petition to APHIS in support of release of the biocontrol agent into the environment, and preparation of the release plan.

Meanwhile, what can we expect regarding the probable efficacy of the anticipated biocontrol program?

Some of the wasp’s behavioral traits are encouraging. The wasp is widely present in the range of the cactus moth, and persisted in these areas over the years of the study. The wasp can deposit multiple eggs with each “sting”. Multiple wasps can oviposit into each cactus moth without detriment to the wasp offspring. Unmated wasp females produce male offspring only, whereas mated females produce mixed offspring genders. In the field, female wasps attack cactus moth larvae in a variety of scenarios: they wait at plant access holes to sting larvae when they come outside to defecate; they attack larvae when they are moving on the surface of the pads; they can sting the youngest cactus moth larvae through the thin plant wall of mined the pads; and they enter large access holes created by older larvae and attack larger larvae. The wasps are attracted by the frass (excrement) left on the outside of the cactus pads by cactus moth larvae (Varone et al. 2020).

However, I wonder about the extent to which the cactus moth is controlled by parasitoids in Argentina. Cactoblastis eggs are killed primarily by being dislodged during weather events (rain and wind) and by predation by ants. First instar larvae are killed primarily by the native Argentine cactus plants’ own defenses – thick cuticles and release of sticky mucilage when the young larvae chew holes into the pads where they enter and feed internally. As larvae feed and develop inside the pads, the primary cause of mortality is natural enemies.

Of all the parasitoid species that attack C. cactorum, A. opuntiarum is the most abundant and important. When the larvae reach their final state (6th instars), they leave the pads and find pupation sites in plant litter near the base of the plants. It is at this stage that the parasitism from A. opuntiarum is detected in the younger larvae that were attacked while feeding inside pads. As the moth larva begins to spin silk into which to pupate, larvae of the wasp erupt through the skin of the caterpillar and pupate within the silk spun by the moth. Predation by generalists (ants, spiders, predatory beetles) accounted for high mortality of the unprotected last instar and pupae (Varone et al. 2019).

Finally, the cactus moth has three generations per year when feeding on O. stricta in the subtropical and tropical coastal areas of the Americas and the Caribbean. In Argentina, on its native host, the moth completes only two generations per year (Varone et al. 2019).

 How to Get the Program Support Needed

Opuntia in Big Bend National Park
Photo by Cookie Ballou,
National Park Service

To date, no organized constituency has advocated for protection of our cacti from non-native insect pests. Perhaps now that the Cactoblastis moth is in Texas, the threat it represents to our desert ecosystems will become real to conservationists and they will join the struggle. The first step is to resolve the funding crisis so that the agencies can complete testing of the biocontrol agent and gain approval for its release. So now there is “something people can do” – and I hope they will step forward.

I hope Americans are not actually indifferent to the threat that many cacti in our deserts will be killed by non-native insects. Many are key components of the ecosystems within premier National Parks, and other protected areas. Cacti also are beautiful treasures in botanical gardens. I hope conservationists will agree that these threats must be countered, and will help to ensure funding of the final stages of the biocontrol tests.

Sources

Mengoni Goñalons, C., L. Varone, G. Logarzo, M. Guala, M. Rodriguero, S.D. Hight, and J.E. Carpenter. 2014. Geographical range & lab studies on Apanteles opuntiarum (hymenoptera: braconiDae) in AR, a candidate for BC of Cactoblastis cactorum (Lepidoptera: Pyralidae) in North America. Florida Entomologist 97(4) December 2014

Simonson, S.E., T. J. Stohlgren, L. Tyler, W. Gregg, R. Muir, and L. Garrett. 2005. Preliminary assessment of the potential impacts and risks of the invasive cactus moth, Cactoblastis cactorum Berg, in the U.S. and Mexico. Final Report to the International Atomic Energy Agency, April 25, 2005 © IAEA 2005

Srivastava, M., P. Srivastava,  R. Karan, A. Jeyaprakash, L. Whilby, E. Rohrig, A.C. Howe,  S.D. Hight, and L. Varone. 2019. Molecular detection method developed to track the koinobiont larval parasitoid Apanteles opuntiarum (Hymenoptera: Braconidae) imported from Argentina to control Cactoblastis cactorum (Lepidoptera: Pyralidae). Florida Entomologist 102(2): 329-335.

Varone, L., C.M. Goñalons, A.C. Faltlhauser, M.E. Guala, D. Wolaver, M. Srivastava, and S.D. Hight. 2020. Effect of rearing Cactoblastis cactorum on an artificial diet on the behavior of Apanteles opuntiarum. Applied Entomology DOI: 10.1111/jen.12731.

Varone, L., G. Logarzo, J.J. Martínez, F. Navarro, J.E. Carpenter, and S.D. Hight. 2015. Field host range of Apanteles opuntiarum (Hymenoptera: Braconidae) in Argentina, a potential biocontrol agent of Cactoblastis cactorum (Lepidoptera: Pyralidae) in North America. Florida Entomologist — Volume 98, No. 2 803

Varone, L., M.B. Aguirre, E. Lobos, D. Ruiz Pérez, S.D. Hight, F. Palottini, M. Guala, G.A. Logarzo. 2019. Causes of mortality at different stages of Cactoblastis cactorum in the native range. BioControl (2019) 64:249–261

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.

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.

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

Hawaiian Dry Forests – Glimmer of Hope for one tree, Alarm for a shrub

wiliwili flower
photo by Forrest and Kim Starr, courtesy of creative commons

Hawaii’s dryland forest is a highly endangered ecosystem. More than 90% of dry forests are already lost due to habitat destruction and the spread of invasive plant and animal species. However, a new publication documents some recovery of wiliwili trees from one major pest. At the same time, a new pest is spreading and killing naio, a critical dryland shrub.  Both pests originated in countries that have rarely if ever been a source of U.S. pests. This is worrying because phytosanitary agencies have their hands full with imports from the usual sources. The role of California as a source of invasive species in Hawai`i has long deserved federal attention – but as far as I know has not received it.

Hope for Wiliwili Trees

The Hawaiian endemic wiliwili tree, Erythrina sandwicensis, occurs in lowland dry forests on all the major islands from sea level to 600 m. Wililwili is a dominant overstory tree in these habitats. (Unless otherwise noted, the principal source is Kaufman et al. in press – full citation at end of blog.)

The tree has been severely affected by the introduced Erythrina gall wasp, Quadrastichus erythrinae (EGW). The gall wasp was detected on Oahu in 2005 and quickly spread to the other Hawaiian islands.  

Arrival of the EGW on Oahu was part of the insect’s rapid global range expansion.  Originally from East Africa, it was first detected in the Mascarene Islands and Singapore in 2003. At the time, it was unknown to science. Within a few years it had spread across Asia, many Pacific islands (including Hawai`i), and to the Americas, including Florida in 2006, Brazil in 2014 (Culik 2014), and Mexico in 2017 (Palacios-Torres 2017). Although apparently restricted to the Erythrina genus as host, it has lots of opportunities. This genus has 116 species distributed across tropical and subtropical regions: 72 species in the Americas, 31 in Africa, and 12 in Asia.

The severe damage to wiliwili (and to non-native Erythrina trees planted in urban areas and as windbreaks) prompted Hawaiian officials to immediately initiate efforts to find a classical biological control agent. The process moved rapidly. A candidate – a parasitic wasp species new to science, Eurytoma erythrinae – was found in East Africa in 2006. Host specificity testing was carried out. Scientists quickly learned to rear the parasitic wasp in laboratories. Release of the biocontrol agent was approved in November 2008 – only three and a half years after the EGW was detected on Oahu.

The biocontrol agent’s impact was quickly apparent. Establishment was confirmed within 1–4 months at all release locations throughout Hawai`i. Reduced pest impacts to trees were detected within two years. By 2018, only 33% of the foliage was damaged on the majority of wiliwili trees. Damage to non-native Erythrina had also declined.

Results of Biocontrol Agent’s Release

The biocontrol agent’s efficacy in reducing EGW’s impacts on trees has been evaluated for 10 years after the agent’s release. Monitoring was conducted at sites on four of the six main islands. (The monitoring program and its findings are described in Kaufman et al. in press).

I wonder how many other biocontrol agents have been monitored so closely for such a long time? Shouldn’t they all be?

Given the uniqueness and importance of such long-term assessment, it is worth looking at the data in detail.

1) Foliar Damage and Tree Health

In 2008, before release of the biocontrol agent, more than 70% of young shoots in wiliwili trees that were inspected were severely infested. The damage rating of “severe” fell from about 80% of trees in 2008 to about 40% in 2011. About 20% of trees surveyed – at sites on all islands – had no gall damage.

By three years after release of the biocontrol agent (2011), mortality rates attributed to stress from the EGW infestation for trees in natural areas fell to 21%. Mortality rates for trees in botanical gardens was somewhat higher – 34%. Kaufman et al. proposed several possible reasons: a) lingering presence of systemic insecticides that might have harmed the biocontrol agents early in the releases; b) year-round sustenance for the EGW as a result of the i) presence of alternative hosts and ii) supplemental irrigation which maintained fresh foliage on the trees.

Less intensive monitoring occurred during 2013 – 2018. It showed continuing substantial suppression of EGW damage on Erythrina foliage, although levels varied among locations. Sites with the lowest precipitation and higher temperatures throughout the year had the slowest recovery of wiliwili. Still, trees are now producing vegetative flushes and healthier canopies during non-dormant periods.

2) Flower and Seed Damage

Successful reduction of infestations in flowers and seedpods was less immediate. Still, by 2011, seed-set had increased from less than 3% of trees setting and maturing seed, to almost 30% with mature seed. The proportion of trees bearing inflorescences also increased, with more than 60% of trees blooming three years after introduction of the biocontrol agent. There was also a slow but steady increase in seed production.

However, in 2019, it remains unclear how infestation of seedpods will affect germination and therefore future plant recruitment.

More worrying, little recruitment was observed over the 10 years. Hawaiian authorities have completed tests on, and are preparing a petition for release of, a second biocontrol agent, Aprostocitus nites. It is hoped that it will further suppress EGW in flowers and seedpods.  

Still, poor recruitment is likely due to the combined impacts of multiple invasive species in native environments. A significant factor is a second insect pest – a bruchid, Specularius impressithorax – which can cause loss of more than 75% of the seed crop. I hope authorities are seeking methods to reduce this insect’s impacts.

The Hawaiian species group of the IUCN has given the wiliwili tree the Reed Book designation of “vulnerable”.

Worries for Naio

naio in bloom
photo by Forrest and Kim Starr, courtesy of creative commons

Naio (Myoporum sandwicense)is an integral component of native Hawaiian ecosystems, especially in dry forests, lowlands, and upland shrublands. However, it is also found in mesic and wet forest habitats. Naio is found on all of the main Hawaiian Islands at elevations ranging from sea level to 3000 m. The loss of this species would be not only a significant loss of native biological diversity but also a structural loss to native forest habitats.

The invasive non-native Myoporum thrips, Klambothrips myopori, was detected on the Big Island (Hawai‘i Island) in 2009 – four years after it was first detected on ornamental Myoporum species in California. At the time of the California detection, the species was unknown to science. It is now known that this species is native to Tasmania.

The thrips feeds on and causes galls on plants’ terminal growth and can eventually lead to death of the plant.

For close to a decade, the Myoporum thrips was restricted to the Big Island.  It has now been found on Oahu (Wright pers. comm.) Alarmed by the high mortality of plants in California, in September 2010, the Hawaii Department of Lands and Natural Resources Division of Forestry and Wildlife and the University of Hawai‘i initiated efforts to determine spatial distribution, infestation rates, and overall tree health of naio populations on the Big Island. Monitoring took place at nine protected natural habitats for four years. This monitoring program was supported by the USFS Forest Health Protection program. (See also the chapter on naio by Kaufman et al. 2019 in Potter et al. 2019 – full citation at the end of this blog.)

naio damaged by thrips
photo by Leyla Kaufman, University of Hawaii

The monitoring confirmed that the myoporum thrips has spread and colonized natural habitats on the leeward side of Hawai`i Island. Infestation rates increased considerably at all sites over the duration of the four-year sampling period. Trees experiencing high infestation levels also showed branch dieback.

Medium-elevation sites (between 500–999 m) had the highest infestations and dieback: over 70% of the shoots  had the worst damage.. At two sites, over 70% of the monitored trees have died.

Even though flowers and fruits were still seen at all sites, little to no plant recruitment was observed at these sites. Thus another plant species important in this endangered plant community is in decline.

Few management strategies are available for this pest. They include preventing spread to other islands and early detection followed by rapid application of pesticides.

 Implications and Conclusions

The Erythrina gall wasp and myoporum thrips are only two of the thousands of invasive species established in Hawai`i. Island ecosystems, especially Hawai`i,  are well recognized as especially vulnerable to invasive species. It has been estimated that on average 20 new arthropod species become established in Hawai`i every year.

East Africa and Tasmania are new sources for invasive species. Phytosanitary agencies need to adjust their targetting of high-risk imports to recognize this reality. Regarding the Hawaiian introduction of the thrips, there was probably made an intermediary stop in California – which is not unusual. (See also ohia rust.)

I applaud Hawaiian officials’ quick action to counter these pests. I wish their counterparts in other states did the same.

There are multiple threats to Hawaii’s dry forests, including habitat modification and fragmentation; wild fires; seed predation by rodents; predation on seeds, seedling, and saplings by introduced ungulates (e.g. feral goats, pigs and deer); competition with invasive weeds; and damage by invasive insect pests and diseases.

With so much of Hawaii’s dry forests already lost, the release of biocontrol agents targetting specific pests is only one element of a much-needed effort. Long-term protection of wiliwili and naio depends on greater efforts to reduce all threats and to stimulate natural regeneration of this ecosystem. These programs could include predator-proof fencing to keep out ungulates; baiting rodents and snails; and active collection. Breeding, and planting of threatened plant species in an effort to protect both the individual species and the habitat.

SOURCES

Culik, M.P., D. dos Santos Martins, J. Aires Ventura & V. Antonio Costa. The invasive gall wasp Quadrastichus erythrinae (Hymenoptera: Eulophidae) in South America: is classical biological control needed?

Kaufman, L.V.,  J. Yalemar, M.G. Wright. In press. Classical biological control of the erythrina gall wasp, Quadrastichus erythrinae, in Hawaii.: Conserving an endangered habitat. Biological Control. Vol. 142, March 2020

Palacios-Torres, R.E., J. Malpica-Pita, A.G. Bustamante-Ortiz, J. Valdez-Carrasco, A. Santos-Chávez, R. Vega-Muñoz and H. Vibrans-Lindemann. 2017. The Invasive Gall Wasp Quadrastichus erythrinae Kim in Mexico. Southwestern Entomologist.

Potter, K.M. B.L. Conkling. 2019. Forest Health Monitoring: National Status, Trends, and Analysis 2018. Forest Service Research & Development Southern Research Station General Technical Report SRS-239

Kaufman, L.V, E. Parsons, D. Zarders, C. King, and R. Hauff. 2019. CHAPTER 9. Monitoring Myoporum thrips, Klambothrips myopori (Thysanoptera: Phlaeothripidae), in Hawaii

Wright, Mark. 2005. Assistant Professor and Extension Specialist, University of Hawaii. Personal communication.

 

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.

Sudden Oak Death update

P. ramorum-infected rhododendron plants
Indiana Department of Natural Resources

As you may remember, in June and July I blogged about a troubling outbreak of sudden oak death pathogen Phytophtora ramorum in the nursery trade. The discovery was made by Indiana authorities, who carefully inspected plants being sold in the state. They discovered that rhododendron plants imported from an Oklahoma wholesaler included infected plants.

By the end of May, Indiana state inspectors had destroyed more than 1,500 rhododendrons and prohibited sale of another 1,500 plants  pending determination of their health. [source: Indianapolis Star 29 May, 2019]  Over the next months, APHIS determined that more than 50 rhododendron plants found in Indiana nurseries had been infected [California Oak Mortality Task Force Newsletter August 2019 ].

In the spring and summer, APHIS and state authorities alerted 28 states that they might have received plants from the suspect sources – the suppliers of the Oklahoma wholesaler — one nursery in Washington State and two nurseries from Canada. In the end, APHIS determined that plants exposed to the pathogen had been sent to 18 states – Alabama, Arkansas, Iowa, Illinois, Indiana, Kansas, Kentucky, Michigan, Missouri, Nebraska, North Carolina, Ohio, Oklahoma, Pennsylvania, Tennessee, Texas, Virginia, and West Virginia. As of late July, P. ramorum-positive nursery stock had been detected in nurseries in seven of these (Iowa, Illinois. Indiana, Kansas, Missouri, Nebraska, Oklahoma) plus  Washington [California Oak Mortality Task Force Newsletter August 2019].

As I pointed out in the earlier blog, this is just the latest of several occasions since 2004 in which infected plants have been widely distributed by the nursery trade, despite federal and state regulations. Also, at the time of this outbreak, APHIS had just formalized several steps relaxing the regulations that had been implemented through Federal Orders adopted in recent years. (See the earlier blog for details.)

APHIS actions

I wonder at APHIS’ delay in explaining to stakeholders the situation– and what it is doing about it!  APHIS provided minimal information to me – by email rather than a public announcement; this email came a month after Indiana announced detection of the pathogen to the public (as reported in my blog).  APHIS issued an official notice even later, in mid-July [California Oak Mortality Task Force (COMTF) Newsletter August 2019]. Neither notice was timely, given the serious risks to both nursery and naturally growing plants from the pathogen.

It is now November and principal questions have not yet been answered. How did the inspection systems in Washington and British Columbia fail to detect the outbreaks before the plants were shipped? This lapse is especially worrisome because APHIS requires testing of soil and standing water, not just visual inspection of plants. Furthermore, rhododendrons are well known to be vulnerable to the pathogen and therefore are a specified focus of detection efforts!

The October COMTF newsletter includes a report by the Washington State Department of Agriculture that a nursery found positive in May will carry out a Critical Control Points (CCP) assessment. An “extensive fall certification survey” will also be conducted. Presumably, these efforts are aimed at determining how the outbreak occurred.

The Canadian Food Inspection Service (CFIA) described – briefly – its nationwide survey program. CFIA reported that one nursery was determined to be P. ramorum-positive in 2018, three in 2019. CFIA says that trace-forwards and trace-backs demonstrate that no Canadian nursery shipped infected plants to the U.S. in 2018 or 2019. So, apparently, none of the infected plants came from the Canadian nurseries.

I hope that Washington State and APHIS will soon determine the probable causes of the outbreak. APHIS should then promptly inform all stakeholders and engage them in developing improved programs and policies to minimize the likelihood that similar problems will occur again.

Phytosanitary officials from the states are apparently also seeking additional information from APHIS about what went wrong and how the agency plans to fix the problems. See the resolution adopted by the National Plant Board here

California Action

A much more positive development is that the California Department of Food and Agriculture (CDFA) has introduced a Voluntary P. ramorum Pre-Quarantine Program. This is a voluntary inspection program specifically for nurseries in California counties that are not currently regulated for the pathogen – but that might be put under regulation in the future. Inspections and sampling will be administered by county regulatory officials and samples will be processed by the CDFA Plant Pest Diagnostics Center. If P. ramorum is detected at a participating nursery, the PQP nursery may become a federally regulated establishment.

Broader Implications

As I pointed out in Fading Forests III, APHIS and the states have struggled to prevent spread of tree-killing pests once they have established in the country. Even regulated pests – such as Phytophthora ramorum and the emerald ash borer — have escaped the regulations. APHIS and/or the states have chosen not to engage on other pests, such as redbay ambrosia beetle and laurel wilt disease and the polyphagous and Kuroshio shot hole borers and associated Fusarium fungus. In other cases, some states have acted – and asked APHIS to not get involved – e.g., thousand cankers disease of walnut. This situation heightens the risk to our urban, rural, and wildland forests. Americans need a hard-nosed discussion of how we can improve coordinated efforts to prevent pests’ spread.

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.