plants as pest vectors – Page 2 – Center for Invasive Species Prevention

Plants for Planting – Major Pathway, Too Little Attention

*Phytopthora cinnamomi* on manzanita in California; photo courtesy of Ted Swiecki/Phytosphere

While I blog often about wood packaging the fact is that imports of live plant [= “plants for planting” in USDA’s terms] have historically posed a higher risk of introducing tree-killing pests. In 2012, Liebhold et al. found that nearly 70% of 455 damaging pests introduced to the continental U.S. as of 2006 had probably been introduced via plant imports. These included 95% of sap feeding and 89% of foliage feeding insects and about half of the pathogens. Imported plants not only carry a greater variety of pests than wood packaging; they also carry many more.

Introductions on imported plants for planting is not a rare event. An analysis of data in the Agriculture Quarantine Inspection Monitoring (AQIM) during 2009 found that the approach rate of pests on imported plants was apparently 12% (Liebhold et al. 2012) — more than 100 times higher than the 0.1% approach rate found by Haack et al. (2014) for wood packaging. This alarming statistic receives less attention than warranted because APHIS objected to the accuracy of other aspects of the study.

APHIS has adopted changes to its phytosanitary system for plants for planting in the decade since 2009. The question is, have these changes reduced the known risks associate with live plant imports – especially given skyrocketing imports? Are more measures necessary? Current data and analyses cannot provide a scientifically valid answer.

ohia rust on endangered Hawaiian native plant *Eugenia koolauensis*

First, most studies focus on insects – they even exclude pathogens. Among pathogens introduced in recent decades, probably by the plant trade, are several Phytophthoras, rapid ‘ōhi‘a death, beech leaf disease, boxwood blight. (I am assuming that the Fusarium dieback disease vectored by Euwallacea beetles was introduced via wood packaging.) There have been repeated detections of the Ralstonia solanacearum Race 3 biovar 2, a bacterium that attacks a range of herbaceous plants, despite APHIS requiring specific integrated pest management programs in producing nurseries located in Central America. Examples of recently introduced leaf feeders include the European beech leaf-mining weevil and elm zigzag sawfly.

I concede that it is difficult to study introduced pathogens. It is nearly impossible to compile a complete list of introduced fungi and related organisms since only the most damaging are typically detected and their native ranges are frequently undeterminable. However, European forest pathologists are much more active on these questions. Why? What can we do to focus Americans on the threats these organism pose?

Second, most studies analyzing the pest risk associated with plant imports use port inspection data. However, port inspection data are not reliable indicators of the pest approach rate – as explained by Liebhold et al. 2012 and Haack et al. 2014 (as it pertains to wood packaging). Thus, most of the analyses carried out by Liebhold et al. and MachLachlan et al. (2022) are based on the pests found by APHIS inspectors: actionable pests were detected on only 2.6% of the incoming plants that they inspected.

Here I discuss two recent discussions of the risk associated with imported plant for planting. One is an analysis of establishments of one order of insects in the United States over 200 years (MacLachlan et al. 2022; full citation at the end of the blog). Again, the focus is on insects! The other is a discussion of the pathway during the recent annual meeting of the Continental Dialogue on Non-Native Forest Insects and Diseases. link to posting of presentations This discussion raised some of the key questions, although no answers were provided.

U.S. imports of plants have increased by more than 400% since the 1960s; 35% in just the last 15 years (in 2007 the U.S. imported approximately 3.7 billion plants [Liebhold et al. 2012]; in 2021 it was about 5 billion [MacLachlan et al. 2022]. Yet establishments of new non-native insects associated with this pathway have not risen commensurately. MacLachlan et al. (2022) attempt to answer why this is so. However, pests are often not detected for several years or a decade after their introduction. Furthermore, I doubt that an analysis based on inspection data, not the more reliable AQIM data, can provide an accurate assessment.

To clarify the pest risk associated with plant imports, studies of some insect types, excluding pathogens, is not sufficient. Again, APHIS should update the Liebhold et al. study to determine the approach rate for all types of organisms that threaten North American tree species. Any such study should include trees on Hawai`i, Guam, Puerto Rico, and other U.S possessions and territories. These islands are usually excluded from analyses of imported pests, including Liebhold et al. 2012. I concede that there are probably scientific and data-management challenges but these islands are immensely important from a biodiversity point of view, and they are parts of the United States!

*Cycas micronesica* endemic to Guam; threatened by cycad scale & cycad blue butterfly; photo courtesy A. Gawel

MacLachlan et al. (2022) focused their analysis on the insect order Hemiptera, including the so-called true bugs, including cicadas, aphids, planthoppers, and leafhoppers. This is the insect order most frequently transported with imported plants. In addition, establishments of Hemiptera can be attributed to plant imports rather than to wood or other vectors. Of the 3,500 species of non-native insects established in North America (including the contiguous U.S. states, Alaska, and Canada), about 27% are Hemiptera. Many are serious pests, e.g., hemlock woolly adelgid and balsam woolly adelgid). Complicating the analysis, however, is the fact that some Hemiptera are inconspicuous so they are difficult to detect. In fact, MacLaughlan et al. 2022 estimate the median delay between introduction and detection to be 80 years! They believe that many introduced species remain undiscovered, ranging from 21% for Eurasian regions to 38% for the Neotropics and 52% for Australasia.

eastern hemlocks killed by hemlock woolly adelgied; Linville Gorge, NC; photo by Steven Norman, USFS

MacLachlan et al. (2022) compare the relationship between plant imports and discoveries of Hemiptera from 1800 to the present in an attempt to answer the puzzle of why new Hemiptera establishments have remained relatively steady despite quadrupled plant imports. Perhaps the pool of novel insect species in the source region has been depleted. Or other factors might have changed, such as

the commodities imported (plant species or types; or geographic source)
phytosanitary measures applied by the U.S.

MacLachlan et al. (2022) tracked plant imports since 1854 from seven ecological regions: Afrotropic, Asian Palearctic, Australasia, European Palearctic, Indomalaya, Nearctic, Neotropic. In the early decades, both imported plants and introduced Hemiptera detected in the U.S., came predominantly from European and Asian Palearctic regions. Now, however, almost no new Hemiptera species are being introduced on plants imported from the European and Asian Palearctic regions. Since the 1950s, estimated establishments from the Indomalaya region have remained relatively stable. Establishments from the Neotropic and Afrotropic regions rose following World War II and have remained relatively high. After also declining in the first half of the 20th century, establishments of new species from Australasia have recently increased.

Generally, the regions associated with declining establishments of new species (Eurasia) are experiencing relatively gradual increases in their exports to the U.S. Those regions which contribute relatively steady or increasing establishments (Neotropics, Indomalaya, Australasia, and Afrotropic) have each undergone rapid increases in exports to the U.S.

Establishment Risk Among Regions

Source regions vary in the type of plants they export (e.g., rootless cuttings v. whole plants) and in the volume of exports. They also differ in the composition of their indigenous and introduced insect populations. Imports from areas with an abundance of species capable of establishing and adapted to environmental conditions in North America pose greater establishment risk, although it is challenging to determine the risk associated with individual species.

Establishment risk of shipments from a particular region also changes over time. The number of potential new species of invaders might shrink as more and more arrive in North America. (This situation has no effect on the continued introduction of insect species already established in North America. These reintroductions might arrive in new areas – so expanding the area at risk; or their increasing number contributes to propagule pressure at establishment sites.) Another factor might be phytosanitary policies. Strengthening of phytosanitary measures might suppress the number of organisms that travel with the plant shipment, enter North America, and establish. The opposite might happen if phytosanitary measures are relaxed or if the sourcing or type of imports diversifies in ways that connect additional species in source regions with trade pathways.

Considering all regional plant sources, MacLachlan et al. (2022) estimate that establishments per unit of additional imports – of Hemipterans – have shrunk because of a combination of increased imports, accumulated introductions associated with past imports, and the passage of time. These decreases are substantial – between 75.2% and 99.8% for the various regions from 1962 to 2012. For the Asian Palearctic and Neotropic regions, MacLachlan et al. (2022) determined that depletion of species pools is a contributing factor. Other factors are thought to explain the substantial decline in establishment likelihood for the other regions. However, note the caveats above re: lag times in detecting introductions.

However, despite that significant decrease in risk per unit of imports, the number of establishments has remained relatively constant over the past century. MacLachlan et al. (2022) attribute this pattern to the decreases in marginal risk from additional imports being offset by substantial increases in overall import levels and diversification of the origins of imports across regions, which exposed the U.S. to new source species pools.

MacLachlan et al. (2022) suggest that APHIS should target biosecurity resources to the specific commodity-country pairs associated with a demonstrated higher relative risk of introducing additional insect species.

MacLachlan et al. (2022) are unable to evaluate the efficacy of APHIS’ most important policy change: creation of the “Not Authorized for Importation Pending Pest Risk Assessment” (NAPPRA) program because it was adopted in 2011 and they analyzed data only through 2012. A decade later this policy restricts imports of about 250 taxa (Regelbrugge to Continental Dialogue). It is certainly time to evaluate its efficacy through a new study of pest approach rates in the “plants for planting” trade.

I do not think that U.S. phytosanitary policy should be based on an analysis of just one of at least three types of pests that travel via the pathway. We need analysis of the risk from pathogens, nematodes, viruses … and other orders of arthropods.

The Continental Dialogue on Non-Native Forest Insets and Pathogens

The Continental Dialogue on Non-Native Forest Insects and Pathogens hosted a discussion of the risk of pest introduction via the plant trade during its recent annual meeting. Participants asked: How can the international phytosanitary system curtail introductions of unknown organisms when it is based on risk assessments that address only species that are fully known and – usually – have proven to be invasive elsewhere.

*Rhodomyrtos psidioides* in eastern Australia killed by myrtle rust; photo by Peter Entwistle

In recent decades, tens of species of Phytophthora have been introduced to countries around the world. Myrtle rust (Austropuccinia psidii) has been introduced to 27 countries from the U.S. to Australia and South Africa. The two causal agents of boxwood blight has been introduced to at least 24 countries in three geographic areas: Europe and western Asia; New Zealand; and North America. The ash decline fungus has been introduced across Europe. Most of these species were unknown to science at the time of their introduction. Other species were known – but not believed to pose a threat because, in their native regions, their co-evolved hosts are not harmed.

For more than a decade, scientists have noted that the international phytosanitary system has failed to prevent this rapid worldwide spread of significant pathogens via the international nursery trade. Examples include Brasier 2008; Liebhold el. al. 2012; Santini et al. 2013; Roy et al. 2014; Eschen et al. 2015; Jung et al. 2015; Meurisse et al. 2019; O’Hanlon et al. 2021.

During the Continental Dialogue discussion, Craig Regebrugge, Vice President of AmericanHort (the principal nursery trade association) noted the economic importance of greenhouse and nursery production and the importance of offering novel plants to their customers. Also, he noted that U.S. retail nurseries import primarily unrooted plant cuttings. In so doing, they have a strong incentive to ensure that they are pest-free in order to avoid delays arising during inspections. Those delays would probably kill these highly perishable products. Most U.S. imports of “finished” plants come from Canada. There have been pest problems; one of the most recent examples is a moth that attacks boxwoods (Buxus), which is the top-selling shrub crop in the U.S. Earlier there was confusion over whether plants shipped from British Columbia had been infected by the sudden oak death pathogen.

Regelbrugge noted that the industry’s voluntary integrated pest management program – Systems Approach to Nursery Certification (SANC) – currently has about two dozen participating nurseries. Hoped-for adoption by more of the hundreds of production nurseries in the country has been delayed by COVID-related travel restrictions, but he hopes to restore momentum. The industry is looking for opportunities to strengthen the program through marketing messages.

Regelbrugge and a second speaker, Rebecca Epanchin-Niell of the University of Maryland, warned that prohibitions on imports will stimulate smuggling. Both raised concerns about direct-to-consumer sales by e-commerce vendors and sought ideas on how to change the behavior of both exporters and consumers.

Later Sarah Green of British Forest Research asked the APHIS representative whether the agency’s import procedures are working to prevent introductions. She pointed to the issues raised by the scientific sources I cited above: pest risk analyses address only known organisms, so this process cannot protect importers from unknown organisms. She noted that the United Kingdom is struggling to contain a number of introductions of previously unknown pathogens. Gary Lovett of the Cary Institute noted that this weakness of pest risk assessments also hampers U.S. attempts to prevent introductions – especially of pathogens. He called on the Dialogue to focus on the resource at risk – native and urban forests – and change our phytosanitary programs on this basis. He has advocated halting imports of plants that are congenerics of important North American tree species, in order to minimize the risk that pests that damage those genera will be introduced.

an American elm that has survived DED – at Longwood Gardens; photo by F.T. Campbell

Jiri Hulcr of the University of Florida tried to reassure Dialogue participants by stating that recent research has substantially reduced the threat from “unknown unkowns”. I applaud Dr. Hulcr’s efforts to reduce scientific uncertainty about the invasive potential of pathogens native to regions other than North America. His study might be the largest attempted by U.S.-based scientists. However, I note that his study assessed the threat posed by 55 insect-vectored fungi to two species of oak and two species of pines. The forests of the southeastern U.S. comprise many other tree genera! He also set a very high bar for defining a threat as serious: the damage to the host must be equivalent to that caused by Dutch elm disease or laurel wilt. Both have devastated their respective hosts. I believe U.S. phytosanitary policy must aim at protecting the full range of native species. Furthermore, levels of damage that affect the host’s role in the ecosystem – not just rapid mortality — should not be acceptable.

SOURCES

Epanchin-Niell, R., M. Springborn, an A. Lindsay. 2016. Resources No. 193 Fall 2016. http://www.rff.org/files/document/file/RFF_Resources_193_Web.pdf

Li, Y. C. Bateman, J. Skelton, B. Want, A. Black, Y-T. Huang, A. Gonzalez, M.A. Jusino, Z.J. Nolen, S. Freemen, Z. Mendel, C-Y. Chen, H-F. Li, M. Kolarik, M. Knizek, J-H. Park, W. Sittichaya, P.H. Thai, S-I. Ito, M. Torii, L. Gao, A.J. Johnson, M. Lu, J. Sun, Z. Zhang, D.C. Adams, J. Hulcr. 2021. Pre-invasion assessment of exotic bark beetle-vectored fungi to detect tree-killing pathogen. Phytopathology. https://doi.org/10.1094/PHYTO-01-21-0041-R

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

MacLachlan, M.J., A. M. Liebhold, T. Yamanaka, M. R. Springborn. 2022. Hidden patterns of insect establishment risk revealed from two centuries of alien species discoveries. Sci. Adv. 7, eabj1012 (2021).

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

www.fadingforests.org

Funding APHIS & USFS in FY23 – Senate Recommendations

The Senate Appropriations Committee has adopted its recommendations for funding APHIS and the US Forest Service in Fiscal Year 2023, which begins on October 1. The full Senate has not yet acted; most people expect that it will not act before October, so the agencies will have to operate under a “continuing resolution” for at least the first several months. Under a “CR”, funding is maintained at the current level.

SOD-infected rhododendron plants detected by state officials in Indiana in 2019

Funding for APHIS in FY23

The Senate Appropriations Committee issued a report [available here] that recognizes APHIS’ objective of protecting the animal and plant resources of the Nation from diseases and pests. These objectives are carried out through, inter alia, Safeguarding and Emergency Preparedness/Response and Safe Trade and International Technical Assistance.

The Committee recommends the following funding for specific APHIS programs (in $millions)

PROGRAM	FY22 FUNDING	FY23 ADMIN REQ	HOUSE $	SENATE COMM RECOMM	CISP ASK
Border inspections (AQI appropriated)	33.849	36.725		36.650	X
Pest Detection	28.218	29.137	29.825	29.075	30
Methods Development	21.217	21.854	31.807	23.557	23
Specialty Crops	209.533	219.533	219.698	222.072	219
Tree & Wood pests	61.217	62.854	62.562	62.719	70
Subtotal, Plant health	379.144	385.560		397.603	X
Emerg. Prepare & Response	42.021	44.242		44.317	X

Specific programs mentioned:

Northern (~~Asian)~~ giant hornet eradication: $1.75 million to continue cooperation with Washington State to eradicate this pest; also to improve monitoring methods and lures, and build a rapid response platforms
sudden oak death (SOD): recognize that the EU1 and NA1 strains of this pathogen threaten Douglas-fir / tanoak forests and lead foreign governments to impose quarantines on U.S. timber exports. So APHIS should spend no less that FY22 funding to better understand threat and treatment methods in wildlands. This earmark disappoints because it focuses on APHIS’ role as certifying timber exports as pest-free rather than the spread of the pathogen within the U.S. via the nursery trade. The same language appears in the report’s discussion of the Agriculture Research Service (see below).

Pertinent action re: Agriculture Research Service

The Senate Committee report sets several priorities, including the following:

Invasive Pests: The Committee is concerned about the threats invasive pests pose to agriculture, the economy, environment, human health, and national security of the Pacific region. The Committee directs ARS to continue working with stakeholders in the region to assess options for combatting invasive species, including biocontrol research facilities, containment facilities, additional laboratory space.
Sudden oak death: the same language as for APHIS. Again, I wish the language referred to the pathogen’s spread via the nursery trade.

These numbers are disappointing; the increase for “specialty crops” demonstrates the lobbying clout of the nursery and berry industries! I appreciate the attention to sudden oak death – with the caveat I mentioned.

SOD-infected tanoaks in southern Oregon; photo by Oregon Department of Forstry

Forest Service

The Senate Appropriations Committee issued a report [available here] . The Senate Appropriations Committee recommends the following funding levels for USFS programs that address non-native forest pests and other invasive species (in $millions):

PROGRAM	FY22 FUNDING	FY ADMIN REQUEST	HOUSE $	S COMM RECOMM	CISP ASK
Research	296.616	317.733	$360.4	$302.773	317.733
State & Private Forest Health Protection TOTAL	48	59.232	$52.232	50	83
S&P FHP Federal lands	16,000	22,485	?	17,000	51
S&P FHP non-federal lands	32,000	36,747	?	33,000	32

R&D

The Senate wants to retain the current structure of five regional stations, International Institute of Tropical Forestry, and Forest Products Laboratory.

The Senate listed several research priorities. Two pertain to forest health: 1) needle pathogens, and 2) Northeastern States Research Cooperative working to sustain the health of northern forest ecosystems and biological diversity management. I am disappointed that no mention is made of the need to respond to 400 introduced tree-killing insects and pathogens.

planting to test ash trees’ resistance to emerald ash borer; photo courtesy of Jennifer Koch, USFS

S&P

The Senate Committee recommends a significant increase in S&P overall ($8 million above FY22 level), but not for Forest Health Management. This is disappointing.

The Committee is concerned about high tree mortality on National Forests due to bark beetle infestations and instructs USFS to work with states and tribes to prioritize insect prevention, suppression & mitigation projects.

The Committee expects the Forest Service and Bureau of Land Management (BLM) to continue efforts to treat sudden oak death in California and Oregon. It provides $3 million for this purpose, including for partnerships with private landowners.

Posted by Faith Campbell

www.fadingforests.org

Boxwood Blight – Another Failure of the Global Phytosanitary System

boxwood garden at Gunston Hall – home of founding father George Mason; Virginia; photo by Roger 4336 *via* Wikimedia

Boxwood blight is a disease caused by a group of fungal pathogens. While boxwoods are horticultural plants in the U.S. – important ones! – they are keystone forest species in several regions of the tropics and subtropics.

The situation with boxwood blight is yet another example of a too-frequent pattern for plant pathogens. This pattern applies even to plant taxa that are important to the ornamental horticulture industry – not only plants that are important in natural ecosystems. [See other blogs posted here under the category “plants as pest vectors”, e.g., here. The boxwood blight pathogens:

are of unknown origin;
have a wide range of known hosts; additional hosts probable;
have been introduced to many new sites over about 30 years;
have caused considerable economic, aesthetic, and ecological harm;
are a threat to centers of endemism;
have no known methods to treat plants in forests;
are spread by international plant trade;
complicate detection by having hosts that sometimes are asymptomatic; or symptoms can be suppressed by fungicides;
apparently few efforts to apply phytosanitary measures to prevent further spread.

Also typical: concerned scientists are trying to promote adoption of phytosanitary measures. This takes the form of a study by Barke, Coop and Hong (full citation at the end of the blog; unless otherwise stated, information in this blog is from this source). They use several models based largely on climatic factors to predict additional geographic areas where else boxwood blight might establish.

I think it is most unfortunate that the U.S. horticultural industry prefers to avoid federal regulation despite the significant costs to its members. Instead, it has advocated for a primarily voluntary response (see below). This undermines efforts to restructure regulatory programs to improve phytosanitary agencies’ management of pathogens. Since the U.S. is such a powerful player on this issue, reducing pressure on APHIS to find more effective measures has global implications. I recognize that preventing transmission of unknown and cryptic pathogens is an intrinsically difficult task. However, tackling this problem should be a top priority for people concerned about retaining healthy floral communities.

Specifics About Boxwood Blight

Boxwood blight is caused by two ascomycete fungi, Calonectria pseudonaviculata [synonym Cylindrocladium buxicola] and Calonectria henricotiae. Both can infect and blight boxwood foliage, resulting in rapid plant death. C. henricotiae is known from only five countries in Europe; C. pseudonaviculata is currently established in 24 countries in three geographic areas: Europe and western Asia; New Zealand; and North America (30 US states and British Columbia). The disease caused by C. pseudonaviculata could spread well beyond its currently invaded range in these regions.

range of *Buxus sempervirens*; via Wikimedia

Native plants in the family Buxaceae grow in tropical or subtropical areas around the world. Plants in the genera Buxus, Didymeles, Haptanthus, Pachysandra, Sarcococca, and Styloceras are found in some areas of western and southern Europe; Turkey and the Caucuses into Iran; several countries in southeast and east Asia (China, Japan, South Korea, Vietnam, Indonesia); coastal Australia; high elevation areas of Africa, including Madagascar; parts of South America (southern Brazil, Uruguay, northern Argentina, and southern Chile, and foothills of the Andes); parts of Central America and the Caribbean. Asia is home to about 40 species of Buxus, four species of Pachysandra, and 11 species of Sarcococca. In the Andes region, all five species of Styloceras are endemic. Central America and the Caribbean are home to about 50 species of Buxus; there are 37 species endemic to Cuba! Madagascar has nine endemic Buxus species.

Many Buxus species occur in small and isolated distributions resulting from both natural causes (e.g., island endemism) and anthropogenic disturbances (including deforestation and invasions of by other non-native pests, such as the box tree moth Cydalima perspectalis in Europe and western Asia).

In native stands of Buxus sempervirens in Georgia and northern Iran, where C. pseudonaviculata was detected in 2010, the disease has caused rapid and intensive defoliation of boxwood plants of different ages. [See also Lehtijarvi, Dogmus-Lehtijarvi and Oskay. Boxwood Blight in Turkey: Impact on Natural Boxwood Populations and Management Challenges. Baltic Forestry 2017, vol. 23(1)] Infected plants are also vulnerable to attacks by secondary opportunistic pathogens that can lead to eventual death. Damage to these forests could lead to reductions in soil stability and subsequent declines in water quality and flood protection, changes in forest structure and composition, and declines in Buxus-associated biodiversity (at least 63 species of lichens, fungi, chromista and invertebrates might be obligate).

Barke, Coop and Hong expect excessive heat and seasonal dryness at one extreme and excessive cold at the other to limit areas in North America and Europe/central Asia where the disease can establish. Areas with oceanic rather than continental climates are probably more vulnerable. However, heat and aridity barriers could be overcome by artificial irrigation of horticultural plantings.

Indeed, the conditions favoring C. pseudonaviculata establishment – warm temperatures and high humidity or water on the leaves – are commonly found in production nurseries. Overhead irrigation exacerbates the risk. Production nurseries also have large numbers of host plants in close proximity – so it is easy for disease to spread (Douglas).

I am reminded that the causal agent of sudden oak death, Phytophthora ramorum, has been spread from production nurseries located in hot, dry areas that were considered unsuitable to the pathogen – because conditions inside the nursery were suitable.

wild *Buxus* on island of Corsica; photo by Sten Porse *via* Wikimedia

As I noted, the origin of C. pseudonaviculata is unknown. Barke, Coop and Hong think it is most likely in eastern Asia, which is thought to be the likely native region of box tree moth. However, they cannot rule out some other center of diversity for Buxaceae species e.g., the Caribbean or Madagascar.

Barke, Coop and Hong call for additional studies to

Explore potential effects of climate change on establishment risk, especially higher latitude areas expected to see increasing humidity, precipitation, and rising temperatures.
Determine ability of C. pseudonaviculata microsclerotia to survive higher temperatures, e.g. in parts of the U.S. Deep South that may have ideal growing conditions during cool seasons.
Modify the CLIMEX model developed for this study to predict the potential distribution of C. henricotiae, a closely related but genetically distinct species with greater tolerance of higher temperatures.

They call for a strict phytosanitary protocol for risk mitigation of accidental intro, with effective surveillance for early detection, and development of a recovery plan.

Regulatory (non) Response

Boxwood blight was first detected in the United Kingdom in mid-1990s; then in New Zealand in 2002. Only then was the causal agent determined. It was first detected in the U.S. in October 2011 (in Connecticut). It was quickly determined to be established in the mid-Atlantic region. Apparently the British, other European countries, and APHIS all decided the pathogen was too widespread to regulate (Douglas).

The U.S. is relying on a voluntary program. The nursery industry, through its Horticultural Research Institute (HRI), and the National Plant Board developed guidance for best management practices – updated as recently as 2020.

boxwood blight symptoms; Oregon State University; *via* Flickr

In contrast, APHIS has acted to regulate the boxwood tree moth, Cydalima perspectalis. The moth was first detected in North America near Toronto in 2018. U.S. nurseries in six states received infected plants in spring 2021. On May 26, 2021, APHIS prohibited importation of host plants from Canada, including boxwood (Buxus spp), Euonymus (Euonymus spp), and holly (Ilex spp).

In July 2021, the moth was detected in Niagara County, New York. It was thought that the moths had flown or been blown into the area from Canada. New York adopted an intrastate quarantine of three counties (Erie, Niagara, and Orleans) in December 10, 2021. APHIS followed with an interstate quarantine on March 23, 2022.

SOURCES

Barke, B.S., L. Coop and C. Hong. 2022. Potential Distribution of Invasive Boxwood Blight Pathogen (Calonectria pseudonaviculata) as Predicted by Process-Based and Correlative Models. Biology 2022, 11, 849. https://doi.org/10.3390/biology11060849 www.mdpi.com/journal/biology

Douglas, S.M. Fact sheet; Connecticut Agricultural Experiment Station https://portal.ct.gov/-/media/CAES/DOCUMENTS/Publications/Fact_Sheets/Plant_Pathology_and_Ecology/2020/Boxwood-Blight-(1).pdf?la=en&hash=A4C6AF39765F27FDDEB5B4DC3FD3B6F3

Posted by Faith Campbell

www.fadingforests.org

Comment to APHIS on its Strategic Plan

APHIS is seeking stakeholder input to its new strategic plan to guide the agency’s work over the next 5 years.

The strategic plan framework is a summary of the draft plan; it provides highlights including the mission and vision statements, core values, strategic goals and objectives, and trends or signals of change we expect to influence the agency’s work in the future. APHIS is seeking input on the following questions:

Are your interests represented in the plan?
Are there opportunities for APHIS to partner with others to achieve the goals and objectives?
Are there other trends for which the agency should be preparing?
Are there additional items APHIS should consider for the plan?

range of American beech – should APHIS be doing more to protect it from 3 non-native pests?

The strategic plan framework is available at https://www.regulations.gov/document/APHIS-2022-0035-0001

To comment, please visit: https://www.regulations.gov/docket/APHIS-2022-0035

Comments must be received by July 1, 2022, 11:59pm (EST).

Posted by Faith Campbell

or www.fadingforests.org

SOD – Frightening Genetics

tanoak killed by SOD; photo by Joseph O’Brien, via Bugwood

I am belatedly catching up with developments regarding sudden oak death (SOD; Phytophthora ramorum). The situation is worsening, with three of the four existing strains now established in U.S. forests. Nursery outbreaks remain disturbingly frequent.

This information comes primarily from the California Oak Mortality Task Force’s (COMTF) newsletters posted since October; dates of specific newsletters are shown in brackets.

Alarming presence of variants & hybridization

The long-feared risk of hybridization among strains has occurred. Canadian authorities carrying out inspections of a British Columbia nursery found a hybrid of European (EU1) and North American (NA2) clonal lineages. These hybrids are viable, can infect plants and produce spores for not only long-term survival but also propagation. So far the hybrid has been found in a single nursery; it has not spread to natural forests. The pathogen is considered eradicated in that nursery, so it is hoped it cannot reproduce further. [December 2021 newsletter, summarizing research by R. Hamelin et al.]

Noted British forest pathologist Clive Brasier warned in 2008 about the risk of hybrids evolving in nurseries which harbor multiple strains of related pathogens. (See full citation at end of the blog.)

The threat is clear: three of the four known variants are already established in forests of the Pacific Northwest – NA1, NA2, and EU1. (For an explanation of P. ramorum strains and mating types, go here.)

In Oregon, the EU1 strain was detected in a dying tanoak (Notholithocarpus densiflorus) tree in the forests of Curry County in 2015. Genetic analysis revealed that the forest EU1 isolates were nearly identical to EU1 isolates collected in 2012 from a nearby nursery during routine monitoring. This detection was considered to be evidence that multiple distinct P. ramorum introductions had occurred. The scientists expressed concern that the presence of this strain – which is of the A1 mating type while the widely established NA1 population of the pathogen in the forest is of the A2 mating type — makes the potential for sexual recombination more likely. Therefore, the state prioritized eradication of the EU1 forest infestation [Grünwald et al. 2016]. (For an explanation of P. ramorum strains and mating types, go here.)

The NA2 strain was detected in 2021, 33 km north of the closest known P. ramorum infestation. Because Oregonians genotype all detections on the leading front of the infection, they completed Koch’s postulates and found this surprising result [February 2022]. NA2 is thought to be more aggressive than the NA1 lineage [February 2022]. Surveys and sampling quickly determined that the outbreak is well established — 154 positive detections [February 2022] across more than 500 acres [October 2021]. Oregon Department of Forestry immediately began treatments; the goal is to prevent overlap with existing NA1 and EU1 populations. [April 2022; summarizing research by Peterson et al.] Given the number of infected trees and the new variant, Oregon pathologists believe this to be a separate introduction to Oregon forests that has been spreading in the area for at least four years [February 2022].

Scientists [April 2022; summarizing research by Peterson et al.] again note evidence of repeated introductions of novel lineages into the western US native plant communities; this region is highly vulnerable to Phytophthora establishment, justifying continued monitoring for P. ramorum not only in nurseries but also in forests.

SOD in Oregon; photo by Oregon Department of Forestry

The EU1 strain is also present in northern California, specifically in Del Norte County. It was detected there in 2020. Despite removal of infected and nearby host trees (tanoaks) and treatment with herbicide to prevent resprouting, the EU1 strain was again detected on tanoaks in 2021. The detected strain is genetically consistent with the EU1 outbreak in Oregon forests. Oddly, the usual strain found in North American forests, the NA1 strain, was not detected in Del Norte Co. in 2021 [February 2022].

One encouraging research finding [April 2022; summarizing research by Daniels, Navarro, and LeBoldus] is that established treatment measures have had significant impact on both the NA1 & EU1 lineages. They found on average 33% fewer positive samples at treated sites where NA1 is established; 43% reduction in P. ramorum prevalence at EU1 sites. Prevalence of P. ramorum in soil was not affected by treatment.

SOD Spread in Forests

In California, the incidence of new Phytophthora ramorum infections fell in 2021 to a historic low – estimated 97,000 dead trees across 16,000 acres, compared to ~885,000 dead trees across 92,000 acres in 2019 [April 2022]. It is agreed that the reason is the wave of mortality sparked by the very wet 2016-2017 winter has subsided and has been followed by several years of drought [February 2022].

data showing decline in new SOD detections in California in 2021 (no data collected in 2020)

In Oregon, however, SOD continues to spread. In 2010, the OR SOD Program had conceded that eradication was no longer feasible. Instead, authorities created a Generally Infested Area (GIA) where removal of infested tanoaks was now optional (not mandated) on private and state-owned lands. Since then, SOD has continued to spread and intensify within the designated zone. The GIA has been expanded eight times since its establishment in 2012; it now it covers 123 sq. mi. There has also been an immediate increase in tanoak mortality [December 2021].

In 2021, two new infestations were detected outside the GIA. One outbreak is on the Rogue River-Siskiyou National Forest along the Rogue River, 6 miles north of any previously known infestation. The second is just outside Port Orford [February 2022], 33 km north of the closest known infestation. This second infestation is composed of the NA2 variant [see above]. The Oregon Department of Agriculture (ODA) established emergency quarantines at these sites and began eradication efforts at both sites. The Oregon legislature appropriated $1.7 million to Oregon Department of Forestry to carry out an integrated pest management program to slow spread of the disease [February 2022].

Scientific research indicates that this situation might get worse. While it has long been recognized that California bay laurel (= Oregon myrtle) (Umbellularia californica) and tanoak are the principal hosts supporting sporulation and spread, it has now been determined that many other native species in the forest can support sporulation. Chlamydospore production was highest on bigleaf maple (Acer macrophyllum)and hairyCeanothus (Ceanothus oliganthus). All the other hosts produced significantly fewer spores than tanoak and myrtle [October 2021; summarizing research by Rosenthal, Fajardo, and Rizzo]

Furthermore, studies that aggregate observations of disease on all hosts, not paying attention to their varying levels of susceptibility, might lead scientists to misinterpret whether the botanic diversity slows spread of the pathogen [October 2021 summarizing research by Rosenthal, Simler-Williamson, and Rizzo].

Monitoring to detect any possible spread to the East

SOD risk map based on climate & presence of host species; USFS

The USDA Forest Service continues its Cooperative Sudden Oak Death Early Detection Stream Survey in the East. In 2021, 12 states participated – Alabama, Florida, Georgia, Illinois, Maryland, Mississippi, North Carolina, Pennsylvania, South Carolina, Texas, West Virginia, and Wisconsin. Samples were collected from 79 streams in the spring. Two streams were positive, both in Alabama. Both are associated with nurseries that were positive for P. ramorum more than a decade ago [October 2021].

Continued infestations in the nurseries

USDA Animal and Plant Health Inspection Service (APHIS) reported that in 2021, the agency supported compliance activities, diagnostics, and surveys in nurseries in 22 states. P. ramorum was detected at 17 establishments. Eight were new; nine had been positive previously. These included seven nurseries that ship intrastate – all had been positive previously. Six were already under compliance agreements. Also positive were three big box stores – none previously infected; and six nurseries that sell only within one state – five new. Infections at the big box outlets and half the intrastate nurseries were detected as a result of trace-forwards from other nurseries.

P. ramorum was detected in 300 samples in 2021 – 144 from plants in the genus Viburnum; 106 from Rhodendron (including azalea); and much lower numbers from other genera.

APHIS funds states for annual nursery surveys, compliance activities, and diagnostics through the: Plant Protection Act Section 7721 and the Cooperative Agricultural Pest Survey (CAPS) program. Table 4 lists states receiving survey funds. APHIS also supported compliance and diagnostic activities in California, Louisiana, Oklahoma, Oregon, Pennsylvania, Washington, and several states through Florida.

APHIS’ report – which provides few additional details about the nursery detections – can be found here.

California:

The California Department of Food and Agriculture (CDFA) reported that three of the eight nurseries regulated under either the federal or state sudden oak death program tested positive in 2021. This was down from five positive nurseries in 2020 [February 2022]. (In the past, numbers of nurseries testing positive have declined during droughts, risen during wet years.) At one interstate-shipping nursery 145 positive Viburnum tinus plants were detected by regulators in December 2021. Apparently the detection efforts were prompted by a trace-back from a nursery in an (unnamed) other state [April 2022].

Oregon:

Oregon continues to struggle with the presence of Phytopththora ramorum in the state’s nurseries. Early in 2021 the situation looked good. Three of eight interstate shippers and two intrastate shippers “passed” their sixth consecutive inspection with no P. ramorum detected so they were released from state and federal program inspection requirements. A fourth interstate-shipping nursery had ceased operating. By the end of the year, however, circumstances had deteriorated. One of the four interstate shippers still under regulatory scrutiny appeared to be badly infested. After routine autumn monitoring detected an infected plant, subsequent delimitation samplings detected 30 additional positive foliar samples and a large number (24) of samples were inconclusive. By spring 2022 six nurseries had to be inspected following trace-forwards from out-of-state nurseries. No P. ramorum was detected in five of these nurseries; the sixth had one positive foliar sample, so it is now under more stringent regulatory supervision [April 2022].

Washington:

Washington has only one interstate shipping nursery that is regulated under APHIS’ program; it tested negative in autumn 2021 [December 2021]. Meanwhile, USDA & Washington Department of Agriculture (WSDA) decided to deregulate the Kitsap County Botanical Garden where P. ramorum had been detected in 2015. Since then, more than 5,000 samples have been collected; 99.1% have tested negative. The last positive plant sample was collected in February 2016. Under a compliance agreement, the botanical garden will continue the best management practices deemed successful in eradicating the pathogen [December 2021]. However, water at the site continues to test positive [February 2022]. These water detections – in Washington and Alabama (above) – raise troubling questions.

Meanwhile, in late winter [April 2022], WSDA had to conduct two trace-forward investigations on plants that shipped from (unnamed) out-of-state nurseries. As of the April newsletter, 13 samples from four locations were all negative.

A stubborn problem has been the persistence of SOD infections in nurseries after the Confirmed Nursery Protocol has been carried out. Research indicates the reason might be that the pathogen is still there in the form of soilborne inoculum in buried, infested leaf debris [December 2021 newsletter; summarizing research by Peterson, Grünwald, and Parke].

Another native tree identified as host

Dieback on golden chinquapin, Chrysolepis chrysophylla, a slow growing, evergreen tree native to the U.S. west coast has been confirmed as caused by Phytophthora ramorum. The detection was in a part of Marin County, California heavily infested by P. ramorum since early in the epidemic. Affected trees were large overstory trees. Unlike other hosts in the Fagaceae, there were no external bole cankers [April 2022 newsletter; summarizing research by Rooney-Latham, Blomquist, Soriano, and Pastalka].

SOURCES

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

Grunwald, N.J., M.M. Larsen, Z.N. Kamvar, P.W. Reeser, A. Kanaskie, J. Laine and R. Wiese. 2016. First Report of the EU1 Clonal Lineage of Phytophthora ramorum on Tanoak in an Oregon Forest. Disease Notes. May 2016, Vol. 100, No. 5, p. 1024

Posted by Faith Campbell

Integrating Invasion & Phytosanitary Sciences & Practice

vegetation killed by *Phytophthora cinnamomi* in West Australia

Some invasive species practitioners have been trying to develop a standardized framework for describing bioinvasions. Their goal is to overcome disparities in approaches developed by scientists working with various taxonomic groups in hopes of improving understanding of, and communication about, bioinvasions. Prominent among these efforts is the “Unified Framework for Bioinvasion” published by Blackburn et al. in 2011 (full citation at end of blog).

Now several forest pathologists (Paap et al; full citation at end of blog) say that this framework does not adequately integrate forest pathogens. This omission is particularly unfortunate given the prominence of forest pathogens as damaging invaders – e.g., chestnut blight in Europe and North America; white pine blister rust in North America; sudden oak death in North America and Great Britain; myrtle rust and Phytophthora cinnamomi in Australia. (See profiles of all these pathogens here; I note additional examples in North America, such as laurel wilt disease.)

Paap et al think that this omission impedes understanding of both forest pests and invasive species in general. Also, they say that integrating microorganisms into the broader Blackburn framework would help forest pathologists better understand how and why invasions occur, where they occur, and how they can be stopped or mitigated.

Furthermore, they note the importance of integrating the diverging terminologies used by invasive species practitioners and plant pathologists and their separate regulatory bodies – the Convention on the Conservation of Biological Diversity (CBD) and the International Plant Protection Convention (IPPC). I concur, since nations’ programs regulating plant diseases and their vectors operate under the IPPC rubric.

Figure 2 and Table 1 lay out Paap et al.’s proposed modification of Blackburn’s framework, and detail strategies linked to management goals appropriate for the stages of plant disease development.

Tanoak mortality in southern Oregon caused by *P. ramorum* – a pathogen completely unknown until it was introduced to North America and Europe; photo by Oregon Department of Forestry

However, such integration will be impeded by many difficulties (I have re-ordered these points):

1) The first – which underlies all others — is the paucity of data on microbial taxa, which undermines the pest risk analyses and other systems developed for assessing and managing other types of invasive species. That is,

Many of the vast number of microbial taxa have not yet been described.
Even species that have been describe often cannot be ascribed to a specific geographic origin. This information gap undercuts efforts to determine whether a disease outbreak is caused by an “introduced” organism.

2) Microbial species are usually detected only when disease impacts become obvious. However, an outbreak might not signal a new or spreading “introduction”. While invasive species must—by definition—cross a geographic boundary (through the assistance of human actions), pathogens can cause disease outbreaks through breaching a wider range of boundaries, including ecological and evolutionary ones. Thus, the disease outbreak doesn’t always fit the definition of “invasive species”.

3) Substantial differences exist in training and goals between fields. Forest pathologists are usually trained in plant pathology (often focused on crops) rather than in forestry or ecology. Their goal is to manage the pathogen. Invasion scientists tend to focus on natural ecosystems, study animal and plant invasions, and seek understanding of the invasion process.

4) A related issue is that the two fields operate under separate regulatory bodies that have different emphases and aims. Paap et al. note that while the IPPC ostensibly includes impacts on natural environments, its members’ priority is plants of economic importance. The World Trade Organization’s Agreement on the Application of Sanitary and Phytosanitary Measures (WTO SPS) seeks primarily to minimize disruption of trade resulting from plant health regulation. On the other hand, the CBD explicitly considers invasive species’ impact to the natural environment (Aichi Biodiversity Target 9). [To read my critique of the WTO SPS and IPPC, read the Fading Forests reports (link at end of this blog), especially FF II.]

They note that in 2004, the IPPC and CBD secretariats established a Memorandum of Cooperation to promote synergy and to avoid duplication. Paap et al. appear disappointed that despite development of joint work plans, phytosanitary programs are still focused largely on crop pathogens.

Disease development – a complex set of circumstances that makes risk assessment less reliable

Since I am not a pathologist (or even a biologist), I learned a lot about the complexities of plant pathology from Paap et al.

While I am certainly familiar with the “disease triangle” concept, I had not thought about certain implications. For example, pathogens can cause severe disease outbreaks by evading any one of three types of barriers: geographic, environmental, or evolutionary. Transport of the micro-organism to a new ecosystem (leaping the geographic barrier and meeting the definition of an “introduction” in invasive species terminology) certainly can facilitate disease outbreaks. However, evolutionary and environmental barriers might also be overcome in other ways.

The result is that a plant disease can develop under multiple scenarios following the introduction of an alien pathogen. These scenarios are:

disease on a coevolved host growing as an alien species in the new environment, for example plantations of trees grown for timber (pathogen reunion);
disease on a naïve host that is itself alien to the geographic region in question (host jump);
disease on an alien host (naïve or coevolved) which supports disease on a host native to the new geographic area that could not be sustained in the absence of the alien host;
disease on alien and native hosts; and
disease on a host native to the new geographic area but not on an alien host.

Countries’ efforts to conduct pest risk analyses are unlikely to be straightforward – or even possible – with so many disease scenarios

Paap et al. proceed to compare introductory pathways under the CBD categorization and plant pathology. In doing so they point out several aspects of introduction, establishment, and spread that are specific to pathogens. For example, trees’ long life spans and inability to adapt as rapidly as the micro-organism increase their vulnerability to devastating disease outbreaks following the arrival of a novel pathogen.

Participants in the Montesclaros meeting that drafted an early critique of international phytosanitary procedures

Paap et al. reinforce points made by other critics of current phytosanitary programs. (See my earlier blogs under the category “plants as pest vectors”.) In particular, they point out the weakness of visual inspection and note that new molecular assays can detect only known microorganisms. An additional complication is that DNA can persist in soil and plant tissue after death of the organism, leading to false positives. RNA is cannot yet be used as a viability marker.

Paap et al. provide three case studies to illustrate in greater depth several major challenges encountered when managing invasive forest pathogens. Most of these weaknesses are well known to forest pathologists.

1. The inconspicuous nature of microorganisms

As noted by Paap et al. and other authors, the difficulty detecting microbes is exacerbated by the huge volumes of goods, especially live plants, in international trade; the small proportion of those plants that can be inspected; the weakness of visual examination; application of fungicides and fertilizers before export that suppress symptoms. The chosen example is the oomycete genus Phytophthora, specifically P. ramorum.

2. Cryptic status of many species

Current biosecurity programs rely on naming the organism and its place of origin. This is actually impossible for many microorganisms. The tardy response to ash dieback (Hymenoscyphus fraxineus) in Europe illustrates the delay in determining the causal agent and its geographic origin. During this nearly two-decade period the possibility of preventing spread was lost.

3. Rapid evolution

Rapid evolution of the introduced pathogen can overcome resistance in a host. The example described is Cronartium ribicola (causal agent of white pine blister rust) on Western white pine (Pinus monticola) and sugar pine (P. lambertiana). They also mention the threat from hybridization between previously isolated populations, specifically Phytophthora x alni causing a devastating decline of black alder in Europe.

Sugar pine in Sequoia National Park; photo by S. Rae via Flickr

Paap et al. call for increased research to increase our knowledge of microbial diversity, especially in taxonomically rich and poorly studied ecosystems. They praise sentinel plantings as a powerful tool for early warning of pathogen threats.

SOURCES

Blackburn, T.M., P. Pysek, S. Bacher, J.T. Carlton, R.P. Duncan, V. Jarosik, et al. A proposed unified framework for biological invasions. Trends Ecol Evol. 2011; 26(7):333-9.

Paap, T., M.J. Wingfield, T.I. Burgess, J.R.U. Wilson, D.M. Richardson, A. Santini. 2022. Invasion Frameworks: a Forest Pathogen Perspective. FOREST PATHOLOGY https://doi.org/10.1007/s40725-021-00157-4

Posted by Faith Campbell

British & Irish Efforts to Prevent or Combat Pathogens

I often blog about the forest pest situation in the UK because its scientists provide lots of easily accessible information. This blog has new information on Britain and – I am pleased to add – on Ireland!

European ash trees alongside the Malham Cove path in Yorkshire; KA via geograph

UK Overview

British woodlands cover just 13% of total land area (just over one-third of the European average of 37%). Their value is increasingly recognized—especially their role in combating climate change through carbon sequestration, flood mitigation and urban cooling. Realization of these benefits is driving new policy to increase woodland cover. In 2019–2020, 13,700 ha of new woodland was created in the United Kingdom (Green et al. 2021). The U.K. government has pledged to plant 30,000 ha of broadleaf and coniferous woodland every year as part of its climate change mitigation strategy (Donald et al. 2021). One example, the ‘northern forest’ scheme, involves planting 50 million native trees over 25 years (Green et al. 2021).

Risks Associated with Conservation Plantings or Translocations

On-going conservation planting efforts plus these ambitious new plans prompted Donald et al. (2021) to assess risk that pathogens might be introduced into the environment as a result of putting native plants in natural habitats. The focus of their study is the planting of common juniper (Juniperus communis)in habitats throughout England, Scotland, and Wales.

Juniper killed by *Phytophthora austrocedri*; photo from British Forest Research

Juniper is one of three native conifers in the UK. It has been in decline for decades, which conservationists hope to reverse. Now, though, juniper populations are experiencing significant mortality from disease. In 2012, the causal agent was determined to be the non-native pathogen Phytophthora austrocedri. The presence of a single genotype in ~60 geographically separate locations across Scotland and England lends support to idea that the pathogen is being introduced to these sites through some human mechanism. Phytophthora austrocedri has not [yet] been detected in Northern Ireland.

British and European nurseries have contained many Phytophthora pathogens. Hence Donald et al. (2021) sought to determine whether the pathogen is being introduced through use of nursery stock in these well-intentioned plantings. (I have blogged about a similar problem in California restoration plantings.)

The authors found that 19% of P. austrocedri detections are within 2 km of a known planting. The more frequently junipers were planted at a site, and the more cuttings planted during each planting effort, the higher the likelihood that nearby junipers would be infested by P. austrocedri. They conclude that transplanting material is a significant risk pathway for the introduction of disease. The key factor appeared to be the origin of the material. A higher percentage of stock at sites with P. austrocedri outbreaks for which data were available had been raised in a central location by the organization doing the planting or obtained from commercial nurseries. No P. austrocedri was detected in Wales. There, unlike in Scotland or England, the majority of plants were sourced from a commercial nursery that only grew juniper collected from Welsh populations and did not trade with other retailers.

Planting juniper has risen rapidly since the mid-1990s. The highest percentage of planting events co-occurring with disease outbreaks were conducted in 2000–2009. It is likely that there is a time lag between planting and disease detectability. If so, the even larger planting effort since 2010 probably will produce many more P. austrocedri outbreaks that will become visible in the future. And that might not be the end. Planting guidelines have been revised based on pathogen detection. However, the entities doing the planting have not changed their approach, especially regarding site selection.

Donald et al. (2021) also found serious data gaps in these programs beyond the health of propagules. They found:

1) very incomplete knowledge of which organizations are doing the planting;

2) poor attention to traceability of source material; and

3) very little follow-up to check the success of planting projects.

The authors concluded that planting projects have had mixed success in restoring juniper populations. They called for changes in planting strategy to reduce the risks of pathogen introduction.

They also note that efforts to slow the spread of P. austrocedri – for which there is no treatment – are more expensive and less likely to succeed than measures aimed at ensuring that nurseries are free of Phytophthoras. California native plant nurseries have shown that nurseries can maintain Phytophthora-free stock.

Risk of Nursery-spread Pathogens & Willingness of UK Nurseries to Adopt BMPs

Great Britain has experienced an accelerating series of Phytophthora outbreaks and disease epidemics affecting British trees. Introductions detected just since early 2000s include P. ramorum, P. kernoviae, P. lateralis, P. austrocedri and P. pseudosyringae. In all the above cases, imported planting material either is confirmed or strongly implicated as the likely route of intro (Green et al. 2021).

To address this threat – and with massive planting projects proposed – in 2016 the British forest research entity initiated the multidisciplinary ”Phyto-threats” project. Its goal was to understand the drivers of rising Phytophthora infestations and opportunities for mitigating them. The project:

(i) examined Phytophthora distribution and diversity in different nursery management systems;

(ii) assessed the social and economic feasibility of a nursery accreditation programs to curb the risk; and

(iii) identified Phytophthora risks by modelling introduction, establishment and spread of species in relation to biological characteristics, environmental factors and trade flows.

The assessment of Phytophthora presence in nurseries involved collecting 3,624 water and root samples from 163 host genera growing in plant nurseries across the U.K. over a three-year period. Sampling was not random but targetted to facilities thought to harbor Phytophthora. About half of the samples tested positive. They identified 63 species of Phytophthora. Among the most commonly detected species are several that are considered pathogenic — P. cinnamomi, P. cryptogea/pseudocryptogea, P. syringae, P. cactorum, P. cambivora, P. plurivora and P. nicotianae. P. ramorum was found in 12 samples; P. lateralis and P. austrocedri were each found in 10 samples. Several Phytophthora species are potential new records for the U.K. (i.e., P. castanetorum, P. palmivora, P. pseudotsugae,P. tentaculata,P. terminalis, P. uliginosa).

They also saw evidence for Phytophthora root infections in newly arrived plants imported from the European Union.

Their finding raised question about whether Phytophthora can be transported in peat-free potting media, that is, coconut fiber or coir.

The widespread presence and the diversity of Phytophthora found in nurseries was linked to high-risk management practices. These included: careless disposal of culled plants, the near presence of trees along nursery boundaries, and, especially, open water sources. [These factors are essentially identical to infection-facilitating factors found by researchers in California, Oregon, and Washington State. See advisory issued by Oregon State University Extension.]

The project also assessed the feasibility of nursery accreditation programs. The authors consulted widely with nursery owners and customers and conducted a cost-benefit analysis. Regarding nursery practices, owners claimed they were already addressing issues related to water storage in enclosed tanks, clean/covered storage of growing media, installation of drains or free-draining gravel beds, raised benches, and tool disinfestation stations. Therefore the new analysis focused on seven other topics: water testing for pathogens; water treatment s; quarantine holding areas for imported plants; composting or incineration of culled plants; boot and vehicle washing stations; and purchase from only trusted or accredited UK suppliers.

The study found that nurseries would support an accreditation program. However, their support required that costs not be “prohibitive”, actions required not be “unreasonable”, the scheme provide a safety net; and that measures exist to deter non-compliance. Nursery staff wanted to see evidence of consumer demand – a willingness to drive farther to buy “clean” plants, or to pay higher prices for them. The cost-benefit analysis reached a worrying conclusion: nurseries would benefit financially from introducing best practices only when the program would prevent introduction of a wider range of pests and pathogens, not only Phytophthoras. Green et al. (2021) note that the overall net benefit to society from nurseries adopting best practices would be much more substantial. That is, healthy trees are important in meeting carbon sequestration goals. They did not explore whether society should subsidize nurseries’ participation in BMP accreditation programs.

Ireland and Northern Ireland

The island of Ireland (Ireland and Northern Ireland) is thought to have fewer plant pests than other European countries due to its island status and because of its national and international phytosanitary regulations. O’Hanlon et al. (2022) do not mention another possible factor: the likelihood that import volumes to Ireland were probably much lower until the recent vitalization of the Republic’s economy.

O’Hanlon et al. (2022) sought to establish baseline information so scientists can track changes as trade increases and the climate changes. Their search of the literature and unpublished sources identified 396 forest pests on the island, including 11 bacteria, 20 oomycetes, 150 fungi and 215 arthropods. They believe these figures are all probably underestimates. At least 44 of the pests or pathogens are probably non-native to Ireland. (Determining original ranges is difficult, especially for pathogens.)

The Republic of Ireland is one of the least forested countries in Europe. Forests cover ~ 11% of the land area. In Northern Ireland, it is even less: ~ 8%. These forests are predominantly plantations of exotic species. In the Republic, Picea sitchensis makes up 51% of the forest area, Pinus contorta another 10%. Other exotic species planted are Picea abies (4%) and Larix kaempferi. In Northern Ireland, ~ 62% of the forest area is composed of conifer mixtures. Planting of P. sitchensis has accelerated recently, probably as a result of removal of ash and larch because of their vulnerability to pests already established on the island.

Sitka spruce plantation in U.K. Adam Ward, Geograph.org.uk

O’Hanlon et al. (2022) note the great vulnerability of these monocultures to pests. They found 51 pests native to Ireland that are associated with non-indigenous tree genera. They are also concerned about pests introduced from other parts of Europe. For example, green spruce aphid (Elatobium abietinum, native to Central and Eastern Europe) is already attacking Sitka spruce. A second pest of spruce, Ips typographus, which is native to much of Europe but not the British/Irish isles, is not yet established on the island. Northern Ireland imports bark and wood from Europe for processing. Ips typographus has been associated with at least one such shipment.

Non-native forest pests and pathogens also threaten tree species native to Ireland. These include:

Dutch elm disease caused by fungi from the genus Ophiostoma vectored by bark beetles of the genus Scolytus. The second outbreak, caused by the more aggressive pathogen 0. novo-ulmi, was detected in Britain in 1965 and in Ireland in 1977. It caused considerable mortality of elms in Northern Ireland throughout 1970s.

Phytophthora ramorum was recognized as a threat to forests in Europe only in 2010, when extensive mortality of Japanese larch was detected in Britain. The Republic of Ireland has only the EU1 lineage of the species. Northern Ireland has both the EU1 and EU2 lineages – the former only in nurseries.

Phytophthora disease of alder (caused by several Phytophthora species) was confirmed in Ireland in 2001. However, symptoms of the disease were noted as far back as 1995. It is likely that there are many other Phytophthora species present but not yet recorded.

Ash dieback disease (causal agent Hymenoscyphus fraxineus) on European ash (Fraxinus excelsior) has spread across Europe from Poland beginning in the 1990s. It was confirmed on the Irish island in 2012. Authorities made significant attempts to eradicate the disease, but were not successful. It is now recorded in every county in both Northern Ireland and Ireland. Damage to the economy, environment, and society are expected to be large. The Irish government had helped plant more than 13,000 ha of ash between 1992 and 2012. An estimated 2.9 million ash trees are in Northern Irish hedgerows. British scientists say more than 1,000 fauna species are associated with ash trees.

A second pest on ash — ash sawfly (Tomostethus nigritus) — was detected in Northern Ireland in 2016; it has defoliated hundreds of trees in Belfast.

In recent years, forest pest incursions have increased at a relatively steady rate, comparable to other countries, including Britain. In the 1970s, 26 species were reported; in the 1980s, 27; in the 1990s, 16; in the 2000s, 37; between 2010 and 2017, 28. See the graph in Fig. 2

There is a strong link between pest and pathogen findings in Britain and Ireland. O’Hanlon et al. (2021) list 16 insects and pathogens detected in Britain after 1960 which were later detected in Ireland. The list includes H. fraxineus, 0. novo-ulmi, Phytophthora ramorum, and Phytophthora lateralis. The average delay was 10 years. The authors note that the two islands share similar ecological conditions and hosts, are nearby, plus there is substantial travel and exchange of goods between them. For example, in 2018 an estimated 30,000 metric tonnes of conifer roundwood was sent from Scotland to Northern Ireland for processing.

There are very limited physical checks on plants or plant products moving between Ireland and Northern Ireland. The exception is conifer wood that is not bark-free. European Union regulations require that such shipments be accompanied by a plant passport that certifies that the wood has been inspected by a professional operator authorized by the NPPO of the exporting country. What rules will apply now, after BREXIT, remains unclear. Because of concerns about re-igniting sectarian conflict, most political figures want the border on the island to be almost invisible.

The Europhyt database for the period February 2006 – November 2016 documented interception of numerous high-risk pests at the British and Irish borders, including Anoplophora chinensis and A. glabripennis; I. typographus; Monochamus alternatus; H. fraxineus; and P. ramorum O’Hanlon et al. (2021). believe many more go undetected. O’Hanlon et al. (2021) report specifically on detections on commodities from China, especially on wood packaging. One detection on imported plants of interest to me is that of Discula destructiva (dogwood anthracnose). The article does not mention the origin of the shipment. The native British dogwood, Cornus sanguinea, would presumably be vulnerable to this Asian fungus, which has already caused widespread mortality of woodland dogwoods in North America.

*Cornus sanguinea*; photo by Hans Hillewaert

In addition to reviewing the current situation, O’Hanlon et al. (2021) note pertinent facts about current policy and future science. First, while the two political units on the island have a history of plant pathology expertise, there has recently been a reduction in the number of practicing forest pathologists, mycologists and entomologists. (I and others have complained about the same deterioration in expertise in the United States.)

Second, they describe the years of delay before official recognition that the pathogen Gremmeniella abietina was present in Northern Ireland. This delay resulted from officials refused to accept data from molecular detection tools.

O’Hanlon et al. (2021) add their voice to others criticizing the international phytosanitary system (they cite six major publications: Brasier 2008; Liebhold el. al. 2012; Santini et al. 2012; Eschen et al. 2015; Jung et al. 2016; Meurisse et al. 2019). The failures are (i) visual inspections can miss asymptomatic infections, (ii) limited resources mean only a small proportion of commodities can be inspected, (iii) allowing the use of fungicides masks disease symptoms on plants, (iv) list-based regulations don’t address undescribed organisms and (v) countries vary in how aggressively they carry out the required phytosanitary procedures. O’Hanlon et al. (2021) conclude that “Until these issues are addressed it is likely further increases in the numbers of non-native pests and pathogens of trees will increase.”

The authors note that Eschen et al. (2018) suggested that risk analysis should focus on the commodity (commodity risk assessment) rather than on an individual pest. I have made a similar suggestion, although less clearly worded.

Finally, O’Hanlon et al. (2021) note that climate change is expected to increase the island’s vulnerability to tree-killing pests and pathogens due to fewer frost days, more rain in winter, increased chance of drought in summer, increased average annual temperatures, and more frequent weather extremes. These changes are likely to affect the amount of damage caused by both native and introduced pests organisms. Range shifts in both pests and pathogens and their natural enemies; physiological or behavioral responses in the pests; phenological changes in the hosts; and increased stress on the trees will combine to affect damage.

SOURCES

Donald, F.; Purse, B.V.; Green, S. 2021. Investigating the Role of Restoration Plantings in Introducing Disease—A Case Study Using Phytophthora [UK] Forests 2021, 12, 764

Green, S., D.E.L. Cooke, M. Dunn, L. Barwell, B. Purse, D.S. Chapman, G. Valatin, A. Schlenzig, J. Barbrook, T. Pettitt, C. Price, A. Pérez-Sierra, D. Frederickson-Matika, L. Pritchard, P. Thorpe, P.J.A. Cock, E. Randall, B. Keillor and M. Marzano. 2021. PHYTO-THREATS: Addressing Threats to UK Forests and Woodlands from Phytophthora; Identifying Risks of Spread in Trade and Methods for Mitigation. Forests 2021, 12, 1617 https://doi.org/10.3390/f12121617ý

O’Hanlon, R., Ryan, C., Choiseul, J., Murchie, A.K. and Williams, C. D. 2021 Catalogue of P&P of trees on the island of Ireland. Biology and Enviro

Proceedings of the Royal Irish Academy 2021. Vol. 121, No. 1.12-45 DOI: 10.3318/ BIOE.2021.02

Posted by Faith Campbell

Forest Pests: What’s Improved, What’s Still to Do

sassafras – vulnerable to the rapidly spreading laurel wilt disease; photo by F.T. Campbell

In summer 2019 I posted several blogs summarizing my analysis of forest pest issues after 30 years’ engagement. I reported the continuing introductions of tree-killing insects and pathogens; their relentless spread and exacerbated impacts. I noted the continued low priority given these issues in agencies tasked with preventing and solving these problems. Also, Congress provides not only insufficiently protective policies but also way too little funding. I decried the impediments created by several Administrations; anti-regulatory ideology and USDA’s emphasis on “collaborating” with “clients” rather than imposing requirements.

In my blogs, I called for renewed effort to find more effective strategies – as I had earlier advocated in my “Fading Forests” reports (link provided at the end of this blog), previous blogs, and Lovett et al. 2016

Areas of Progress

Now two years have passed. I see five areas of progress – which give me some hope.

1) Important Activities Are Better Funded than I had realized

a) The US Forest Service is putting significant effort into breeding trees resistant to the relevant pests, more than I had realized. Examples include elms and several conifer species in the West – here and here.

b) USDA has provided at least $110 million since FY2009 to fund forest pest research, control, and outreach under the auspices of the Plant Pest and Disease Disaster Prevention Program (§10201 of the Farm Bill). This total does not include additional funding for the spotted lanternfly. Funded projects, inter alia: explored biocontrol agents for Asian longhorned beetle and emerald ash borer; supported research at NORS-DUC on sudden oak death; monitored and managed red palm weevil and coconut rhinoceros beetle; and detected Asian defoliators. Clearly, many of these projects have increased scientific understanding and promoted public compliance and assistance in pest detection and management.

This section of the Farm Bill also provided $3.9 million to counter cactus pests – $2.7 million over 10 years targetting the Cactoblastis moth & here and $1.2 million over four years targetting the Harissia cactus mealybug and here.

flat-padded *Opuntia* cactus – vulnerable to the *Cactoblastis* moth; National Park Service photo

2) Additional publications have documented pests’ impacts – although I remain doubtful that they have increased decision-makers’ willingness to prioritize forest pests. Among these publications are the huge overview of invasive species published last spring (Poland et al.) and the regional overview of pests and invasive plants in the West (Barrett et al.).

3) There have been new efforts to improve prediction of various pests’ probable virulence (see recent blogs and here.

4) Attention is growing to the importance of protecting forest health as a vital tool in combatting climate change — see Fei et al., Quirion et al., and IUCN. We will have to wait to see whether this approach will succeed in raising the priority given to non-native pests by decision-makers and influential stakeholders.

5) Some politicians are responding to forest pest crises – In the US House, Peter Welch (D-VT) is the lead sponsor of H.R. 1389. He has been joined – so far – by eight cosponsors — Rep. Kuster (D-NH), Pappas (D-NH), Stefanik (R-NY), Fitzpatrick (R-PA), Thompson (D-CA), Ross (D-NC), Pingree (D-ME), and Delgado (D-NY). This bill would fund research into, and application of, host resistance! Also, it would make APHIS’ access to emergency funds easier. Furthermore, it calls for a study of ways to raise forest pests’ priority – thus partially responding to the proposal by me and others (Bonello et al. 2020; full reference at end of blog) to create federal Centers for Forest Pest Control and Prevention.

This year the Congress will begin work on the next Farm Bill – might these ideas be incorporated into that legislation?

What Else Must Be Done

My work is guided by three premises:

1) Robust federal leadership is crucial:

The Constitution gives primacy to federal agencies in managing imports and interstate trade.
Only a consistent approach can protect trees (and other plants) from non-native pests that spread across state lines.
Federal agencies have more resources than state agencies individually or in likely collective efforts – even after decades of budget and staffing cuts.

2) Success depends on a continuing, long-term effort founded on institutional and financial commitments commensurate with the scale of the threat. This requires stable funding; guidance by research and expert staff; and engagement by non-governmental players and stakeholders. Unfortunately, as I discuss below, funding has been neither adequate nor stable.

3) Programs’ effectiveness needs to be measured. Measurement must focus on outcomes, not just effort (see National Environmental Coalition on Invasive Species’ vision document).

Preventing New Introductions – Challenges and Solutions

We cannot prevent damaging new introductions without addressing two specific challenges.

1) Wood packaging continues to pose a threat despite past international and national efforts. As documented in my recent blogs, the numbers of shipping containers – presumably with wood packaging – are rising. Since 2010, CBP has detected nearly 33,000 shipments in violation of ISPM#15. The numbers of violations are down in the most recent years. However, a high proportion of pest-infested wood continues to bear the ISPM#15 mark. So, ISPM#15 is not as effective as it needs to be.

We at CISP hope that by mid-2022, a new analysis of the current proportion of wood packaging harboring pests will be available. Plus there are at least two collaborative efforts aimed at increasing industry efforts to find solutions – The Nature Conservancy with the National Wooden Pallet and Container Association; and the Cary Institute with an informal consortium of importers using wooden dunnage.

2) Imports of living plants (“plants for planting”) are less well studied so the situation is difficult to assess. However, we know this is a pathway that has often spread pests into and within the US. There have been significant declines in overall numbers of incoming shipments, but available information doesn’t tell us which types of plants – woody vs. herbaceous, plant vs. tissue culture, etc. – have decreased.

APHIS said, in a report to Congress (reference at end of blog), that introductions have been curbed – but neither that report nor other data shows me that is true.

Scientists are making efforts to improve risk assessments by reducing the number of organisms for which no information is available on their probable impacts (the “unknown unknowns”).

Solving Issues of Prevention

While I have repeatedly proposed radical revisions to the international phytosanitary agreements (WTO SPS & IPPC) that preclude prevention of unknown unknowns (see Fading Forests II and blog), I have also endorsed measures aimed at achieving incremental improvements in preventing introductions, curtailing spread, and promoting recovery of the affected host species.

citrus longhorned beetle exit hole in bonsai tree; USDA APHIS photo

The more radical suggestions focus on: 1) revising the US Plant Protection Act to give higher priority to preventing pests introductions than to facilitating free trade (FF II Chapter 3); 2) APHIS explicitly stating that its goal is to achieve a specific, high level of protection (FF II Chapter 3); 3) APHIS using its authority under the NAPPRA program to prohibit imports of all plants belonging to the 150 genera of “woody” plants that North America shares with Europe or Asia; 4) APHIS prohibiting use of packaging made from solid wood by countries and exporters that have a record of frequent violations of ISPM#15 in the 16 years since its implementation.

Another action leading to stronger programs would be for APHIS to facilitate outside analysis of its programs and policies to ensure the agency is applying the most effective strategies (Lovett et al. 2016). The pending Haack report is an encouraging example.

I have also suggested that APHIS broaden its risk assessments so that they cover wider categories of risk, such as all pests that might be associated with bare-root woody plants from a particular region. Such an approach could speed up analyses of the many pathways of introduction and prompt their regulation.

Also, APHIS could use certain existing programs more aggressively. I have in mind pre-clearance partnerships and Critical Control Point integrated pest management programs. APHIS should also clarify the extent to which these programs are being applied to the shipments most likely to transport pests that threaten our mainland forests, i.e. imports of woody plants belonging to genera from temperate climates. APHIS should promote more sentinel plant programs. Regarding wood packaging, APHIS could follow the lead of CBP by penalizing importers for each shipment containing noncompliant SWPM.

Getting APHIS to prioritize pest prevention over free trade in general, or in current trade agreements, is a heavy lift. At the very least, the agency should ensure that the U.S. prioritize invasive species prevention in negotiations with trading partners and in developing international trade-related agreements. I borrow here from the recent report on Canadian invasive species efforts. (I complained about APHIS’ failure to even raise invasive species issues during negotiation of a recent agricultural trade agreement with China.)

Solving Issues of Spreading Pests

The absence of an effective system to prevent a pest’s spread within the U.S. is the most glaring gap in the so-called federal “safeguarding system”. Yet this gap is rarely discussed by anyone – officials or stakeholders. APHIS quarantines are the best answer – although they are not always as efficacious as needed – witness the spread of EAB and persistence of nursery outbreaks of the SOD pathogen.

APHIS and the states continue to avoid establishing official programs targetting bioinvaders expected to be difficult to control or that don’t affect agricultural interests. Example include laurel wilt, and two boring beetles in southern California – goldspotted oak borer, Kuroshio shot hole borer and polyphagous shot hole borer and their associated fungi.

One step toward limiting pests’ spread would come from strengthening APHIS’ mandate in legislation, as suggested above. A second, complementary action would be for states to adopt quarantines and regulations more aggressively. For this to happen, APHIS would need to revise its policies on the “special needs exemption” [7 U.S.C. 7756]. Then states could adopt more stringent regulations to prevent introduction of APHIS-designated quarantine pests (Fading Forests III Chapt 3).

Finally, APHIS should not drop regulating difficult-to-control species – e.g., EAB. There are repercussions.

APHIS’ dropping EAB has not only reduced efforts to prevent the beetle’s spread to vulnerable parts of the West. It has also left states to come up with a coherent approach to regulating firewood; they are struggling to do so.

Considering interstate movement of pests via the nursery trade, the Systems Approach to Nursery Certification (SANC) program) is voluntary and was never intended to include all nurseries. Twenty-five nurseries were listed on the program’s website as of March 2020. It is not clear how many nurseries are participating now. The program ended its “pilot” phase and “went live” in January 2021. Furthermore, the program has been more than 20 years in development, so it cannot be considered a rapid response to a pressing problem.

Solving Issues of Recovery and Restoration via Resistance Breeding

I endorse the findings of two USFS scientists, Sniezko and Koch citations. They have documented the success of breeding programs when they are supported by expert staff and reliable funding, and have access to appropriate facilities. The principle example of such a facility is the Dorena Genetic Resource Center in Oregon. Regional consortia, e.g., Great Lakes Basin Forest Health Collaborative and Whitebark Pine Ecosystem Foundation are trying to overcome gaps in the system. I applaud the growing engagement of stakeholders, academic experts, and consortia. Questions remain, though, about how to ensure that these programs’ approaches and results are integrated into government programs.

resistant and vulnerable ash seedlings; photo courtesy of Jennifer Koch, USFS

In Bonello et al., I and others call for initiating resistance breeding programs early in an invasion. Often other management approaches, e.g., targetting the damaging pest or manipulating the environment, will not succeed. Therefore the most promising point of intervention is often with by breeding new or better resistance in the host. This proposal differs slightly from my suggestion in the “30 years – solutions” blog, when I suggested that USFS convene a workshop to develop consensus on breeding program’s priorities and structure early after a pest’s introduction.

Funding Shortfalls

I have complained regularly in my publications (Fading Forests reports) and blogs about inadequate funding for APHIS Plant Protection program and USFS Forest Health Protection and Research programs. Clearly the USDA Plant Pest and Disease Management and Disaster Program has supported much useful work. However, its short-term grants cannot substitute for stable, long-term funding. In recent years, APHIS has held back $14 – $15 million each year from this program to respond to plant health emergencies. (See APHIS program reports for FYs 20 and 21.) This decision might be the best solution we are likely to get to resolve APHIS’ need for emergency funds. If we think it is, we might drop §2 of H.R. 1389.

Expanding Engagement of Stakeholders

Americans expect a broad set of actors to protect our forests. However, these groups have not pressed decision-makers to fix the widely acknowledged problems: inadequate resources – especially for long-term solutions — and weak and tardy phytosanitary measures. Employees of federal and state agencies understand these issues but are restricted from outright advocacy. Where are the professional and scientific associations, representatives of the wood products industry, forest landowners, environmental NGOs and their funders, plus urban tree advocates – who could each play an important role? The Entomological Society’s new “Challenge” is a welcome development and one that others could copy.

SOURCES

Bonello, P., Campbell, F.T., Cipollini, D., Conrad, A.O., Farinas, C., Gandhi, K.J.K., Hain, F.P., Parry, D., Showalter, D.N, Villari, C. and Wallin, K.F. (2020) Invasive Tree Pests Devastate Ecosystems—A Proposed New Response Framework. Front. For. Glob. Change 3:2. doi: 10.3389/ffgc.2020.00002

Krishnankutty, S., H. Nadel, A.M. Taylor, M.C. Wiemann, Y. Wu, S.W. Lingafelter, S.W. Myers, and A.M. Ray. 2020. 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. Journal of Economic Entomology 2020, 1 – 12

Liebhold, A.M., E.G. Brockerhoff, L.J. Garrett, J.L. Parke, and K.O. Britton. 2012. Live plant imports: the major pathway for forest insect and pathogen invasions of the US. Front. Ecol. Environ. 2012; 10(3):135-143

Lovett, G.M., M. Weiss, A.M. Liebhold, T.P. Holmes, B. Leung, K.F. Lambert, D.A. Orwig, F.T. Campbell, J. Rosenthal, D.G. McCullough, R. Wildova, M.P. Ayres, C.D. Canham, D.R. Foster, SL. Ladeau, and T. Weldy. 2016. NIS forest insects and pathogens in the US: Impacts and policy options. Ecological Applications, 26(5), 2016, pp. 1437–1455

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.

Poland, T.M., Patel-Weynand, T., Finch, D., Miniat, C. F., and Lopez, V. (Eds) (2019), Invasive Spp in Forests and Grasslands of the US: A Comprehensive Science Synthesis for the US Forest Sector. Springer Verlag. (in press).

Roy, B.A., H.M Alexander, J. Davidson, F.T Campbell, J.J Burdon, R. Sniezko, and C. Brasier. 2014. Increasing forest loss worldwide from invasive pests requires new trade regulations. Front Ecol Environ 2014; 12(8): 457–465

Schulz, A.N., A.M. Mech, M.P. Ayres, K. J. K. Gandhi, N.P. Havill, D.A. Herms, A.M. Hoover, R.A. Hufbauer, A.M. Liebhold, T.D. Marsico, K.F. Raffa, P.C. Tobin, D.R. Uden, K.A. Thomas. 2021. Predicting non-native insect impact: focusing on the trees to see the forest. Biological Invasions.

United States Department of Agriculture Animal and Plant Health Inspection Service. Report on the Arrival in the US of Forest Pests Through Restrictions on the Importation of Certain Plants for Planting. https://www.caryinstitute.org/sites/default/files/public/downloads/usda_forest_pest_report_2021.pdf

Posted by Faith Campbell

New Study on Forest Carbon and Pests: The Picture is Ugly

lodgepole pines killed by mountain pine beetle in British Columbia; photo courtesy of Wikipedia

Natural systems, especially forests, could provide as much as 37% of the near-term mitigation necessary to meet Paris global climate goals. In the US, conservation, restoration, and improved land management could provide carbon sequestration equivalent to an estimated 21% of current net annual emissions.

However, the current U.S. forest carbon sink, which includes soils and standing and downed wood as well as live trees, might be in jeopardy due to increasing levels of disturbance, conversion, and/or declining sequestration rates in old growth stands.

Insects and plant diseases are one such disturbance agent. Acting alone or in combination with other forest stressors, they can damage or kill large numbers of trees in short periods of time, thereby reducing carbon sequestration and increasing emissions of stored carbon through decomposition of wood in dead or injured trees.

Historically, native and introduced insects and diseases have impacted an estimated 15% of the total U.S. forest cover annually. This impact is likely to increase. One study (Fei et al., 2019) found that an estimated 41% of the live forest biomass in the contiguous U.S. could be impacted by the 15 most damaging introduced pests already established in the U.S. Continuing introductions of new pests and exacerbated effects of native pests associated with climate change portend worsening losses of live trees. These rising impact of pests, combined with more frequent and severe fires and other forest disturbances, are likely to negate efforts to improve forests’ carbon sequestration capacity.

Sources of information about introduced pests’ impacts is available from, inter alia Campbell and Schlarbaum Fading Forests II and III, Lovett et al 2016, Poland et al. 2021, many blogs on this site, and pests’ profiles posed here under “invasive species” tab. Chapter 4 of Poland et al. (2021) provides a summary of what is known about interactions between invasive species and climate change – both climate impacts on bioinvaders and bioinvaders’ effect on carbon sequestration.

The United States and other major polluting countries have certain advantages. Their strong economies have the scientific and financial resources needed to implement effective invasive species prevention and forest management strategies. At the same time, many of them receive the most new forest pests – because they are major importers. These introduced pests pose the most serious and urgent near-term ecological threat to their forests and all the ecosystem services forests provide.

So, reducing insect and disease impacts to forests can simultaneously serve several goals—carbon sequestration, biodiversity conservation, and protecting the myriad economic and societal benefits of forests. See the recent IUCN report on threatened tree species.

A Major New Study

A new study by Quirion et al. (2021) takes another step in quantifying the threat to U.S. forests’ ability to sequester carbon by analyzing data from National Forest Inventory plots. Unfortunately, the re-measurement data for the period 2001 – 2019 are not available in the NFI for the Rocky Mountain states, which represents a critical data gap in the NFI program. This gap might not have had a significant impact on the national findings, however, because while the insect damage level (measured by an earlier inventory round) was quite severe in the Rocky Mountain States, the relatively slow growth of trees in that region means carbon sequestration rates are low.

Forest stand productivity – and carbon sequestration — will typically decline immediately after pest outbreaks, then recover or even increase beyond pre-outbreak levels depending on the productivity and maximum achieved biomass of replacement plant species and related soil characteristics. However, when prevalence of the disturbance increases, by, for example, more frequent pest outbreaks, carbon stocks in standing trees and sequestration rates can be reduced for extended periods.

Findings

Nationally, insects and diseases have decreased carbon sequestration by live trees on forest land by 12.83 teragrams carbon per year. This equals ~ 9% of the contiguous states’ total annual forest carbon sequestration and equivalent to the CO₂ emissions from over 10 million passenger vehicles driven for one year.
This estimate includes the impacts of both native and introduced insects and diseases, because the NFI database does not distinguish between them.
Insect-caused mortality had a larger impact than disease-caused mortality (see below). Forest plots recently impacted by insect disturbance sequestered on average 69% less carbon in live trees than plots with no recent disturbance. Plots recently impacted by disease disturbance sequestered on average 28% less carbon in live trees than plots with no recent disturbance.
Ecoprovinces in which the greatest annual reductions in live tree carbon sequestration due to pests were the Southern Rocky Mountain Steppe, Cascade Mixed Forest, Midwest Broadleaf Forest, and Laurentian Mixed Forest. (Ecoprovinces are outlined – but not named – in Quirion et al. 2021; more complete information is provided in the supplementary material.)

If this study had been carried out in the 1920’s, when chestnut blight and white pine blister rust were spreading across vast areas and killing large trees, the impact of diseases would have been much higher. Today, the most widespread impacts of diseases are on either small trees (e.g., redbay succumbing to laurel wilt) or slow-growing, high-elevation trees (e.g., whitebark and limber pine to white pine blister rust). As long as no equivalents of those earlier diseases are introduced, insects will probably continue to have the larger impacts.

western white pine killed by blister rust; photo from National Archives

Quirion et al. 2021 note that their estimates should be considered conservative. The USFS’s inventory records only major disturbances. That is, when mortality or damage is equal to or exceeds 25% of trees or 50% of an individual tree species’ count on an area of at least 0.4 ha. This criterion largely excludes less severe pest disturbances, including those from which trees recover but which might have temporary negative effects on carbon sequestration.

The study’s authors note that their work has important limitations. The dearth of data from the Rocky Mountain states is one. Other factors not considered include transfers of carbon from live biomass to dead organic matter, soils, and salvaged or preemptively harvested wood products. As trees die from pests or diseases, their carbon becomes dead wood and decays slowly, producing a lag in the carbon emissions to the atmosphere. A small fraction of the carbon in dead wood might be incorporated into soil organic matter, further delaying the emissions. A full accounting of the carbon consequences of pests and diseases would require assessment of these lags, probably through a modeling study.

affects of mountan pine beetle on lodgepole pine in Rocky Mountain National Park, Colorado photo from Wikimedia

Actions to Maintain Carbon Sequestration

Quirion et al. (2021) outline several actions that would help protect the ability of America’s forests to sequester carbon. These suggestions address both native and introduced pests, since both contribute to the threatened reduction in capacity.

Concerning native pests, the authors call for improved forest management, but warn that measures must be tailored to species and environmental context.

Concerning introduced insects and pathogens, Quirion et al. (2021) call for strengthening international trade policies and phytosanitary standards, as well as their enforcement. The focus should be on the principal pathways: wood packaging (click on “wood packaging” category for on this blog site) and imported plants (click on “plants as vectors” category for on this blog site). Specific steps to reduce the rate of introduction of wood-boring insects include enforcement to increase compliance with the international treatment standard (ISPM#15), requiring trade partners – especially those which have repeatedly shipped infested packaging – to switch to packaging made from alternative materials. Introductions via the plant trade could be reduced by requiring foreign shippers to employ integrated management and critical control point systems (per criteria set by the U.S.) and using emergency powers (e.g., NAPPRA) to further restrict imports of the plants associated with the highest pest risk, especially plant species that are congeneric with native woody plants in North America. See Lovett et al 2016; Fading Forests II & III

As backup, since even the most stringent prevention and enforcement will not eliminate all risk, the authors urge increased funding for and research into improved inspection, early detection of new outbreaks, and strategic rapid response to newly detected incursions.

To reduce impacts of pests established on the continent – both recently and years ago – they recommend increasing and stabilizing dedicated funding for classical biocontrol, research into technologies such as sterile-insect release and gene drive, and host resistance breeding.

Thinning is useful in reducing damage by native bark beetles to conifers. However, it has not been successful in controlling introduced pests for which trees do not have an evolved resistance. Indeed, preemptive harvesting of susceptible species can harm forest ecosystems directly through impacts of the harvesting operation and indirectly as individual trees that may exhibit resistance are removed, reducing the species’ ability to develop resistance over time.

Further research is needed to clarify several more issues, including whether introduced pests’ impacts are additive to, or interact with, those of native species and/or other forest stressors.

SOURCE

Quirion BR, Domke GM, Walters BF, Lovett GM, Fargione JE, Greenwood L, Serbesoff-King K, Randall JM & Fei S (2021) P&P Disturbances Correlate With Reduced Carbon Sequestration in Forests of the Contiguous US. Front. For. Glob. Change 4:716582. [Volume 4 | Article 716582] doi: 10.3389/ffgc.2021.716582

SOURCES of additional information

Campbell, F.T. and S.E. Schlarbaum. Fading Forest reports at http://treeimprovement.utk.edu/FadingForests.htm

Lovett, G.M., M. Weiss, A.M. Liebhold, T.P. Holmes, B. Leung, K.F. Lambert, D.A. Orwig, F.T. Campbell, J. Rosenthal, D.G. McCullough, R. Wildova, M.P. Ayres, C.D. Canham, D.R. Foster, S.L. Ladeau, and T. Weldy. 2016. Nonnative forest insects and pathogens in the United States: Impacts and policy options. Ecological Applications, 26(5), 2016, pp. 1437-1455

Poland, T.M., Patel-Weynand, T., Finch, D., Miniat, C. F., and Lopez, V. (Eds) (2019), Invasive Species in Forests and Grasslands of the United States: A Comprehensive Science Synthesis for the United States Forest Sector. Springer Verlag. Available for download at no cost at https://www.fs.usda.gov/treesearch/pubs/61982

Posted by Faith Campbell

Tuning in to the News – Mostly Depressing

In late July I participated in the annual meeting of the National Plant Board (NPB) – the organization representing the states’ phytosanitary agencies. USDA’s APHIS, DHS’ Bureau of Customs and Border Protection (CBP), and various industry associations also participated in the meeting. As usual, I learned lots of depressing developments.

A. Old problems continue to vex:

rhododendron plant infested by P. ramorum; photo by Jennifer Parke, Oregon State University

1) Sudden Oak Death in the Nursery Trade – Again!!!

As you might remember, spring 2019 saw an alarming number of plants infested by the sudden oak death pathogen (Phytophthora ramorum) shipped from west coast nurseries to nurseries in 18 states. Another major incident occurred in 2021. The California Oak Mortality Task Force (COMTF) newsletter for June 2021 reports that one nursery in Oregon shipped plants exposed to P. ramorum to big-box stores in 36 states — twice the number of states that received pathogen-exposed plants in 2019.

The first such incident was in 2004 – 17 years ago! Officials of the states that receive these infested plants are angry that every few years they must divert their resources from other duties to inspect nurseries in their states that have been exposed to the pathogen. They note that these “trace-forward” projects cost state governments money and prevent their carrying out other duties; they also impose significant costs on the in-state nurseries due to holds on sales. When infested plants are found, all these costs rise substantially.

The plant health official from Alabama noted that a single west coast nursery that had repeatedly been found to have infected plants shipped 29 lots of host plants to her state in spring 2021. As is clear from the COMTF article, other states also received thousands of plants that had been exposed to the pathogen. The Alabama official questioned why APHIS tilts so far toward a regulatory system that makes it possible for the “exporting” nurseries to ship. The result – too often – is that an infection at one small business can (repeatedly) impose high costs on hundreds of receiving nurseries and states. [I wonder whether anyone has considered a lawsuit against the source nurseries claiming damages? Would that be successful if the regulatory agencies approved the shipments because – at that time – their inspections had failed to detect the problem?]

Officials from the three west coast states, however, want to support their own nurseries’ efforts to relax regulations and maintain or open markets in the central and eastern states. They point to their own considerable efforts to inspect and certify the pest-free status of nurseries in their states.

Because of the different points of view among the states, the National Plant Board per se has never taken a position on the issue.

However, many states – and even APHIS Deputy Administrator El-Lissy – agree that something is not working. So APHIS is in the midst of reviewing its program, with input from NPB members. Such program reviews have been undertaken several times over the past 18 years. So far, they have never produced a program that effectively stops sales of pathogen-infested plants.

2) Contaminated Wood Packaging

Kevin Harriger of CBP reported that over the nine-month period October 2020 – June 2021, CBP intercepted 1,563 shipments that were in violation of ISPM#15, the international rule that requires that wood packaging be treated to kill pests. Most, or 1,148 shipments (73%), lacked the required mark certifying treatment. Four hundred fifteen (26%) of the total number of shipments had a live pest present. Nearly three quarters of the non-compliant shipments transported miscellaneous cargo. This is not a surprise: all of these characteristics are in keeping with past experience.

Meanwhile, APHIS Deputy Director El-Lissy said APHIS was working with importers, exporting countries’ departments of agriculture, and others to improve compliance. Apparently there were two high-profile incidents when shipments of car components were rejected because of ISPM#15 issues. I am trying to learn more about these incidents.

I recently blogged about the pest risk associated with incoming shipping containers and dunnage.

3) Asian ~~Gypsy~~ Moths (Tussock moths) Still Infesting Ships

Harriger also said that the period 2019-2020 saw the largest number of ships infested by Asian tussock moth eggs since the program began in 2012. [I am aware that the Entomological Society is searching for a new name for this group of insects.] On average, 12 of 100 approaching vessels was infested. CBP is using sophisticated models to identify regions within Asian ports where conditions exacerbate the risk of moth contamination. CBP can match individual ships’ loading records to this information to pinpoint which are most likely to be infested.

Oregon and Washington continue to find both Asian and European tussock moths in traps along the Columbia River. Such detections prompt eradication programs of varying expense and disruption.

[In April, I blogged about a report evaluating the risk posed by several Asian tussock moths; the report was prepared by experts under the auspices of the North American Plant Protection Organization.]

B. In addition to the arrival of new pests, there is an alarming spread of established ones:

1) Beech leaf disease

State phytosanitary officials reported detections of beech leaf disease (BLD) in Maine and Virginia. The devastating impact of BLD on this hard mast tree species is described here. BLD has now spread through much of southern New England (Connecticut, Rhode Island, Massachusetts) and up the coast to Maine. Connecticut reports that trees of all sizes are affected. Maine reports that the disease is widespread in the central coastal region.

beech trees in Prince William Forest Park

Virginia reported that the disease has been detected in Prince William Forest Park, a forested area south of Washington, D.C., managed by the National Park Service. This detection is too recent to say how widespread it is.

2) Laurel wilt

Kentucky’s plant health officer reported that laurel wilt disease has been detected on sassafras trees in Louisville, at the northern tip of the state and across the river from Ohio. He noted that a second host plant, spice bush, is in the nursery trade. While laurel wilt is not regulated, officials are concerned about its impact in natural forests. Neighboring states are concerned.

sassafras in northern Virginia; photo by F.T. Campbell

I learned by looking at the map that laurel wilt has also been detected in Sullivan County, Tennessee, on the Virginia border.

3) Spotted Lanternfly

This pest of grapes, tree fruits, and a wide variety of native trees is spreading in Pennsylvania, Delaware, New Jersey, and Maryland. It has also been found in Ithaca, NY, and in Connecticut. The populations in Virginia and West Virginia also continue to spread; a disjunct outbreak has been detected in Prince William County, VA. (south of D.C.). Most alarming are disjunct populations in Ohio on the West Virginia border and in Indiana on the Ohio River border with northern Kentucky. See map here.

The Indiana population has been present for several years. The affected woodland is close to RV parks and other facilities that make further spread likely.

California has established an external quarantine targetting the spotted lanternfly .

C. Wrestling with Continuing Issues:

1) States try to compensate for APHIS’ end of regulating the emerald ash borer and firewood

The members of the NPB have spent years discussing the pros and cons of continuing to regulate ash wood to contain the emerald ash borer (EAB). As I blogged earlier, APHIS has ended its regulatory program. One state – Minnesota – is seeking to use an APHIS procedure to get APHIS’ continued protection from importation of EAB-infested wood (presumably from Canada). Under the Federally Recognized State Managed Phytosanitary Program (FRSMP), a state petitions APHIS to recognize its program for a specific pest. If APHIS grants that recognition, the agency will support the state by continuing to regulate imports of that pest or commodities that might transport the pest when they are destined for the regulating state.

The states have also tried to formulate a system to maintain regulation of firewood (nearly all states’ firewood regulations were based on the federal regulation of all hardwoods to prevent transport of the EAB). As part of this process, the NPB developed guidelines for adoption of regulations by the individual states (available here). The NPB members are just beginning to explore whether states might set up third-party certification system(s). Among the challenges to any harmonization are states’ differing legal authorities and disagreement on what threat levels should be applied, and for how long.

2) New information about the Asian longhorned beetle in South Carolina

ALB in South Carolina; photo by R. Brad Thompson, APHIS

South Carolina authorities reported that dendrological studies indicated Asian longhorned beetle (ALB) had been present near Charleston, S.C. since 2012, and possibly earlier. The population has the same genetic makeup as the outbreak in Ohio. This might be explained by either transport of infested wood from Clermont County, Ohio, or that wood packaging entering Charleston harbor came from the same part of China. (Charleston is an important port.) In South Carolina, ALB attacks primarily red maple – as is true at the other infestation sites. However, maple densities are much lower in the swamps of South Carolina and scientists don’t know whether the ALB will fly farther or intensify attacks on other host species. Other questions raised by differences between South Carolina and other, more northern, outbreak sites include possible changes in the beetle’s life cycle and flight periods.

Authorities noted the extremely difficult conditions, which impede survey and control efforts – which I described in an earlier blog.

One innovation was sharing of resources: staff from the North Carolina and Tennessee departments of agriculture went to South Carolina to help with surveys. The Resource Sharing Initiative was started a few years ago as a collaborative effort of APHIS and the NPB. This was the first time states tried it. There were several issues that had to be worked out. One issue was the long time it takes to train people to recognize ALB symptoms. All three states’ officials said the project was worthwhile.

black walnut in Fairfax County, VA — in an area where thousand cankers disease has been present for more than a decade; photo by FT Campbell

3) Recinding quarantines of thousand cankers disease of walnut

States which adopted quarantines targetting this insect/pathogen complex a decade ago now think that it poses little risk to black walnut (Juglans nigra) growing in its native range (as distinct from trees planted in the West). Several are in the process of rescinding their quarantines. I think these states have considered the science carefully and are taking the appropriate action.

4) Nursery self-certification – System Set Up; Will Nurseries Participate? Will Customers Support the Process?

Craig Regelbrugge of AmericanHort noted that the SANC program has now been officially launched – it has graduated from being a pilot program. [SANC stands for Systems Approach to Nursery Certification] Participants are exploring incentives to recruit wider participation by nurseries that produce plants and how to get support from plant retailers. SANC is conceived as an elite program for the best nurseries and marketplace leaders. It was never intended to be a remedial program to clean up problem issues such as the P. ramorum debacle. To work, it seems to me, SANC will need to find a way to persuade customers to want to pay more for quality plants. Hence the critical importance of getting retailers involved.

Posted by Faith Campbell