European study buttresses case for revolutionary changes to phytosanitary system


rhododendron in Europe sickened by P. ramorum; photo from EPPO website


A recently published study by European researchers [Jung, T. et al. 2015] documents the failure of current European and global phytosanitary programs and calls for “a new holistic and integrated systems approach”.  The authors specifically criticize Article VI.2 of the International Plant Protection Convention  because it requires that a plant pest be identified and its risks assessed before a country may adopt a phytosanitary measures.  The authors call this requirement “paradoxical” given the large number of potentially damaging plant pests that remain unknown to science.


The study focuses on the genus Phytophthora, which contains about 150 identified species and perhaps 500 species not yet identified by scientists.  The identified species include plant pathogens which are responsible for more than 66% of all fine root diseases & more than 90% of all collar rots of woody plant species.  Examples include the pathogens responsible for the Irish potato famine, sudden oak death, Port-Orford-cedar root disease, the die-off of many endemic plant species in Western Australia and damage to many other species in Europe and North America, and mortality and decline of oaks and alders across Europe.


The authors note that

  • Most of the ~150 currently known species and designated taxa of Phytophthora were unknown to science before they turned up in new environments on other continents as invasive aggressive pathogens of native plants.
  • Forty-four of the 64 Phytophthora taxa detected in the present study were unknown to science before 1990.
  • None of the 59 putatively exotic Phytophthora taxa detected in the present study had been intercepted at European ports of entry. (Some of these introductions are known to be recent; see UK reports on the 4th P. ramorum lineage ) and P. lawsonii detections in the U.K., France and the Netherlands in 2010.)
  • In many cases, had a Phytophthora been detected, the detection would not have resulted in rejection of the shipment because only 5 Phytophthora species are regulated under European regulations.
  • Spread of the quarantine organism ramorum was not halted despite the presence of strict quarantine regulations.


I have written several times about the threat to U.S. trees and forests from insects and – especially – pathogens introduced via the trade in live plants; see Fading Forests II and III .  Fading Forests II discusses the threat from unknown pests and the roadblocks to managing that threat raised by the World Trade Organization’s Agreement on the Application of Sanitary and Phytosanitary Measures and the implementing procedures adopted by the International Plant Protection Convention.  Fading Forests III discusses USDA APHIS efforts to adopt more effective regulatory approaches through adoption of both international and regional standards (ISPM#36 and RSPM#24) and revision of its own Q-37 regulations.

Jung and his 65 (!) coauthors present some frightening facts about the situation in European nurseries and forest, landscape, and ornamental plantings:

  • They found a total of 68 Phytophthora taxa (species, informally designated taxa, and previously unknown taxa). 49 taxa were found in nurseries, 56 in forest and landscape plantings.
  • 91% of the 732 nurseries analyzed had at least 1 Phytophthora taxon present; in the 101 infested nurseries in which more than 5 stands were tested, an average of 3.6 Phytophthora taxa per nursery were detected
  • 66% of forest & landscape plantings had at least 1 Phytophthora taxon present
  • The majority of infested plants in nurseries did not display symptoms; the sampling methods for plantings relied to a large extent on symptoms, so the presence of symptomless plants could not be evaluated.
  • Hundreds of previously unknown Phytophthora–host associations were observed.
  • One or more of 19 Phytophthora which can attack native European or widely-planted trees and shubs were isolated from 84% of ornamental planted stands. Two such pathogens were detected in 11.8% of those stands.
  • In a single British ornamental and amenity planting, 15 different Phytophthora taxa were isolated from 33 different species and varieties of plants. Smaller numbers were isolated from smaller numbers of sampled plants in other countries.
  • The infestation rate for various types of plantings ranged from 94% for riparian plantings through 83.1% for horticultural plantings to 79.3% for forest plantings. About half of amenity and ornamental plantings had one or more infestations.
  • 64% of oak plantings were infested by at least one Phytophthora species associated with decline of mature oak stands. Eight of the 9 plantings of Laurus nobilis in Spain and the UK hosted Phytophthora. Rates varied for other types of trees.
  • In total, 755 ornamental plantings of 281 broadleaved woody and herbaceous species were sampled in 8 countries. 45% had at least one of the 21 Phytophthora taxa known to damage a wide range of European and widely planted exotic tree and shrub species. About 10% of the tested stands had more than one.


As the authors state, their results clearly demonstrate that the vast preponderance of nursery stands across Europe are infested by a large array of Phytophthora species.  Nurseries and other plantings relied on as sources of plants for afforestation and other outplantings are routinely infected by the most aggressive Phytophthora pathogens that attack the respective tree or crop species. The result is continuous high-frequency spread of these aggressive pathogens to planted forests and horticultural systems — and will inevitably result in their introduction to the wider environment.


They estimate that 4.8 million ha of the 6 million ha of new forests planted in Europe over the past 20 years are potentially infested by Phytophthora pathogens.  Another 17.6 million ha of forests replanted after harvesting or fire were possibly established with Phytophthora-infested nursery stock.


Why has this happened? The authors note that under current nursery growing practices, individual plants often flow largely unregulated through several nurseries both within and between countries before being sold to a consumer. In addition, such common nursery practices as reusing containers, irrigating with unfiltered surface water or recirculated water, poor drainage and failure to remove dead plants and debris all contribute to establishment and spread of Phythothora.  These same criticisms have been made by U.S. scientists – and incorporated into APHIS’ revised regulations for management of sudden oak death and the nursery-regulatory SANC program now being tested.


Is the situation equally bad in North America?  Jung et al. cite several publications that cumulatively demonstrate high infestation rates of U.S. ornamental nurseries with at least 31 Phytophthora species.  They say that the situation in forest nurseries is largely unknown.

Certainly both continents are at high risk of additional introductions.  U.S. plant imports reached 3.2 billion in 2007 (Liebhold et al. 2012). I am unaware of a more recent calculation … In 2010, ten European countries cumulatively imported 4.3 billion living plants from overseas; almost all were imported first to the Netherlands.  The principal source was Africa (3.6 billion). Asia shipped 456 million plants; North America 181 million; South America 81 million; Oceania only 2.4 million plants. Between 2007 and 2010, the volume of imported woody plants increased by 44%, and in 2010, the proportion of woody plants reached 20.8% of all imported plants.  Only 3% of the imported consignments are subject to phytosanitary inspections.


As Jung et al. note, their study joins an ever-longer list of analyses that have concluded that current international plant health protocols based on random visual inspections for symptoms of listed quarantine organisms have failed and must be changed fundamentally.  (See, for example, the writing of Clive Brasier  and the Montesclaros Declaration.


Jung et al. call for adoption of a pathway regulation approach based on pathway risk analyses, and risk-based inspection regimes performed by an adequate number of skilled staff using molecular high-throughput detection tools. Nurseries wishing to ship plants internationally would have to comply with mandatory best practices. The requirements must be supported by rigorous enforcement and bold outreach campaigns. This approach would minimize the risks of further introductions and dissemination of both known and, even more importantly, unknown potential pathogens.




Revising the international phytosanitary regime will be difficult, requiring 170 countries to agree to amend both the World Trade Organization’s SPS Agreement and the International Plant Protection Convention. The difficulties will be not only political. Allowing countries to regulate unknown organisms that are potential pests will open a door to protectionist restrictions.  The countries that wrote these agreements have long sought to block protectionist restrictions by requiring that phytosanitary measures be based on scientific analyses of specific risks.


However, as Jung et al. – and before them many others, especially Clive Brasier  – have demonstrated, the current requirement that each pathogen be identified and its risk analyzed before  regulations are adopted is counter to the scientific fact that most pathogens and arthropods are not known to science.  The knowledge gap is many times greater when the question is how those microorganisms and arthropods will interact with millions of plant species if introduced to novel habitats.


Meanwhile, USDA APHIS has begun trying to close some of the regulatory gaps.  In 2011 APHIS adopted regulations creating a temporary holding category, called “Not Authorized (for importation) Pending Pest Risk Analysis,” or NAPPRA. Now, APHIS has authority to temporarily prohibit import of certain types of plants, from specific countries of origin, that it considers to pose a particular pest risk. The temporary ban gives APHIS time to complete a pest risk analysis and then enact appropriate safeguards to ensure that imported plants will be as pest-free as possible.  However, APHIS has been unable to utilize this new power.  The agency proposed a second round of “NAPPRA” species in May 2013, but nearly 3 years later it has not finalized that action. Even if fully implemented, NAPPRA does not address the problem of unknown pests and pathogens.


APHIS has also proposed a major revision of its plant import regulations (called “Q-37”).  This change would implement the IPPC standard on living plants (ISPM#36) and authorize APHIS to require foreign suppliers of plants to apply hazard identification and mitigation practices to ensure plants are pest-free. APHIS proposed this rule change 3 years ago, in 2013.  Again, the change has not yet been finalized.


What You Can Do

Write to your member of Congress and Senators and ask them to urge the Secretary of Agriculture to finalize the two pending regulations – to add the second round of species to the NAPPRA list and to update the Q-37 regulations.



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

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.



Posted by Faith Campbell

Time to view “Trees in Trouble”!

ash & sky

Andrea Torrice’s film “Trees in Trouble: Saving America’s Urban Forests” depicts the impact of non-native tree-killing insects and diseases.

The film is being broadcast in April as part of Earth Day and Arbor Day programming on the PBS World Channel. Check your local public television station website for their schedule or visit the filmmaker’s site for more information.

Andrea’s film focuses on emerald ash borer in Cincinnati. It explores our connections to the trees and forests in our communities – and the threats to those trees. Featured experts and speakers include Prof. Dan Herms of Ohio State, Jenny Gulcik, a community forestry consultant, and Cincinnati Council member Wendell Young.

Because of the high value of urban trees, these pests’ greatest economic damage is in urban and suburban areas.  [See my earlier blogs about the wood packaging pathway and this study: Aukema, J.E., B. Leung, K. Kovacs, C. Chivers, K. O. Britton, J. Englin, S.J. Frankel, R. G. Haight, T. P. Holmes, A. Liebhold, D.G. McCullough, B. Von Holle.. 2011. Economic Impacts of Non-Native Forest Insects in the Continental United States PLoS One September 2011 (Volume 6 Issue 9)]

Nor is this damage limited to southern Ohio – or even the Northeast broadly. Such pests are usually introduced first in cities – not necessarily ports! – because that is where crates and pallets, imported ornamental plants, and other articles to which pests attach arrive.  Furthermore, trees along streets and in yards and parks are often more vulnerable than forest trees to such introduced pests because they are often subject to other stresses such as soil compaction, air pollution, elevated temperatures, and salt exposure.  Finally, city trees are often planted as multiple individuals of the same species; when a pest that attacks that species arrives, entire neighborhoods can lose their tree canopy – and the real values that canopy provides.

See the film. Ask your friends to watch it!  Be inspired by the film to contact members of Congress to ask that they support programs aimed at preventing tree pest introductions.  (These programs are operated by APHIS; see my blog about APHIS’ funding needs posted in March.)

If you want to do more – visit the “resources” page of the filmmaker’s website to obtain toolkits for outreach and hosting an event.


Posted by Faith Campbell

Threats to America’s Magnificent Oaks

Oak trees are immensely symbolic to many people and many are magnificent. Congress even designated the red oak as America’s “national tree”.


Photo of Q. rubra leaves by Becca MacDonald, Sault College;


Of course, there are many kinds – from those that span many states to those that grow in just some special areas. USDA’s Plants database lists more than 300 native species for the U.S. alone.  Many provide substantial ecosystem services and all parts of the country would be poorer without them.

Despite our oaks’ importance, we are doing far too little to protect them from the full range of non-native insects and diseases that pose threats.


In the East (from the Atlantic to the Great Plains), oaks are under attack from at least four non-native pests:

  • One of these, the European gypsy moth (Lymantria dispar), is the target of major containment and suppression programs operated by USDA Animal and Plant Health Inspection Service (APHIS), the US Forest Service and the states. In fact, the US Forest Service spends half of its entire budget for studying and managing non-native pests on the European gypsy moth. In part, this is because the European gypsy moth is so widespread, with outbreaks from Nova Scotia to Wisconsin and south across eastern Ohio to Virginia. (See the map of EGM range here). It also attacks a wide range of tree and shrub species.

But other oak-killing insects and diseases, some with the potential to be at least as damaging, receive far fewer resources.

  • Oak wilt (caused by the fungus Ceratocystis fagacearum) is widespread from central Pennsylvania across Iowa, down the Appalachians in West Virginia and North Carolina-Tennessee border, in northern Arkansas and with large areas affected in central Texas. There is an isolated outbreak in New York State.  (See map here). According to the US Forest Service, oak wilt is one of the most serious tree diseases in the eastern U.S.  It attacks primarily red oaks and live oaks. It is spread by both bark-boring beetles and root grafts.
  • From Long Island along the coast into Nova Scotia and into central Massachusetts, oaks are being killed by the winter moth (Operophtera brumata). Like the gypsy moth, the winter moth has a wide host range. (For more information, see here). A small program led by Joseph Elkington of the University of Massachusetts has focused on biocontrol.  Biocontrol agents have successfully reduced winter moth damage in Nova Scotia and the Pacific Northwest. First results are promising in New England.


In the West, millions of oaks have been killed by several pathogens and insects that are established and spreading; and additional threats loom.

  • Coast live oaks, canyon live oaks, California black oaks, Shreve’s oaks, and tanoaks growing in coastal forests from Monterey County north to southern Oregon that catch fog/rain are being killed by sudden oak death and here. Sudden oak death has killed over one million tanoaks as well as hundreds of thousands of coast live oaks and other trees. In early days of the infestation, Oregon – with considerable help from the US Forest Service – tried to eradicate a small infestation in Curry County. The inherent difficulty in managing a pathogen and interruptions in funding caused that effort to fail. The state is now focused on trying to slow spread of the disease.
  • In California, coast live oaks, black oaks, and canyon oaks in the southern part of the state – primarily in San Diego County, but also parts of San Bernardino, Orange, and Los Angeles counties – are being killed by goldspotted oak borer and here.  At least 100,000 black oaks have been killed in less than 20 years.  Neither the State of California nor USDA APHIS has adopted regulations aimed at preventing spread of the goldspotted oak borer, despite oaks being at risk throughout California.
  • Two more wood-boring beetles threaten oaks in southern California. In five counties in the region, coast live oaks, canyon live oaks, Engelman oaks, and valley oaks – and many other kinds of trees – are being killed by a disease transmitted by the polyphagous and Kuroshio shot hole borers and here.  The polyphagous and Kuroshio shot hole borers attack more than 300 plant species, including tree species that anchor the region’s riparian areas as well as half of the trees planted in urban areas of the region.
  • Also, oaks on the West coast would be attacked by gypsy moths should they reach the area. The risk is two-fold – the Asian gypsy moth continually is carried to the area on ships bearing imports from Asia (as discussed in my blog in March). And the European gypsy moth is sometimes taken across the country on travellers’ vehicles, outdoor furniture, or firewood. Both the West Coast states and USDA search vigilantly for any signs of gypsy moth arrival.

Or course, other non-native pests can also be introduced or spread to new, vulnerable, areas. I have blogged about the risk to the East from sudden-oak-death infested plants moving in the nursery trade (see blogs from July 2015). The polyphagous and Kuroshio shot hole borers might also threaten forests in other warm regions of the country such as the Gulf Coast, where some known and potential host trees grow.


Two apparent threats have come to our attention recently:  fungi in the genus Diplodia and another disease called foamy bark canker.  There is some uncertainty whether the insects or pathogens are non-native. Both are apparently closely linked to drought stress.

  • two Diplodia fungi – Diplodia corticola and quercivora – have been detected in both Florida and California. These fungi were previously known to kill oaks in the Mediterranean region.

According to Mullerin and Smith (2015), one or both of these fungi might be native to North America. Diplodia corticola was first identified in the 1980’s in cork oaks (Quercus suber L.) in Mediterranean countries.  It has since been determined to be the cause of mortality in other species of European oaksD. corticola was first reported in California in 1998 in coast live oak trees (Q. agrifolia) that had been colonized by bark and ambrosia beetles. There, it has been an important factor in the deaths of thousands of acres of coast and canyon live oaks (Q. chrysolepis) since 2002 (Mullerin and Smith 2015). In California, periodic diebacks since the late 1970s have been associated with droughts.  Symptoms have mainly shown up in coast live oak (Q. agrifolia), black oak (Q. kelloggii), and valley oak (Q. lobata). Dieback is noticeable in at least 20 California counties, throughout most of the range of coast live oak. (See here.)

The first detection of D. corticola in southern Florida was in 2010; D. quercivora was detected in 2013. In Florida, these fungi attack live oaks (Quercus virginiana).  Almost all the symptomatic trees in Florida grow in cultivated settings where they are exposed to various stresses. In addition, most of the state experienced severe drought in 2010, the year reports of dieback began (Mullerin and Smith 2015).

Host range studies indicate that 33 species of oaks and one species of chestnut that grow in the Southeast are vulnerable, to varying degrees, to D. corticola. Oaks in the red oak group (Section Lobatae) are more vulnerable than are white oaks (Section Quercus) (Mullerin and Smith 2015). In the test, the most vulnerable appear to be the following species native to the Southeast: Q. laurifolia, Q. virginiana, Q. geminata, Q. chapmanni, Q. laevis (turkey oak), Q. phellos, Q. pumila, and Q. incana. (source: poster presented by  Dreaden, Black, Mullerin, Smith at the 2016 USDA Invasive Species Research Forum.)

It is unknown how Diplodia corticola & Diplodia quercivora colonize oaks. However, members of the family (Botryosphaeriaceae) generally enter plants through wounds, including leaf scars, or stomata open for gas exchange. They often live harmlessly as endophytes within the plant, becoming pathogenic when the plant is stressed by environmental factors such as drought, flooding, heat, freezing, herbicide use, or soil compaction (Mullerin and Smith 2015).


  • Foamy bark canker is new disease of oak species caused by a newly discovered species of species of fungus (Geosmithia pallida). The pathogen is vectored by the Western oak bark beetle (Pseudopityophthorus pubipennis). The disease complex has great potential to cause extensive damage to oaks in California.  Still little is known about the disease’ overall distribution, establishment and incidence.

Declining coast live oak trees have been observed since 2012 throughout urban landscapes in Los Angeles, Orange, Riverside, Santa Barbara, Ventura, and Monterey counties in California. Fungal colonies were observed within beetle galleries (Lynch et al. 2014). The Western oak bark beetle is thought to be a native. It commonly attacks trees weakened by other agents; it has not previously been associated with disease. However, the disease vector might be a different, similar beetle; scientists are collecting more, from a larger geographic area, to determine whether it is the native species or something else.  In Europe, the fungus appears to have be associated with a range of bark-boring insects and is widely distributed. There is no previous published record of the fungus occurring in the United States (Lynch et al. 2014).

Symptoms can be viewed here.


Dreaden, T. A. Black, S. Mullerin, and J. Smith risk to oaks from Diplodia cor+cola and D. quercivora, two emergent fungal pathogens (poster at Annapolis 2016) Includes map showing distribution in Florida.

Drill,S. New pest alert for Foamy Canker Disease on Coast Live Oak. 2014.

Lynch, S.C., D.H. Wang,  J.S. Mayorquin, P.F. Rugman-Jones, R. Stouthamer, A. Eskalen. 2014. First Report of Geosmithia pallida Causing Foamy Bark Canker, a New Disease on Coast Live Oak (Quercus agrifolia), in Association with Pseudopityophthorus pubipennis in California. APS Journals Plant DiseaseSeptember 2014, Volume 98, Number 9 Page 1276

Lynch, S., S. Rooney-Latham, A. Eskalen. [DATE?]  Foamy Bark Canker A New Insect-Disease Complex on Coast Live Oak in California Caused by Western Oak Bark Beetle and Geosmithia sp.

Mullerin, S. & J.A. Smith. 2015. Bot Canker of Oak in FL Caused by Diplodia corticola & D. quercivora. Emergent Pathogens on Oak and Grapevine in North America. FOR318


Posted by Faith Campbell