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RMD-13-08: Pest Risk Management Document – Hymenoscyphus fraxineus (ash dieback pathogen)

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November 24, 2014

Preface

As described by the International Plant Protection Convention (IPPC), Pest Risk Analysis (PRA) includes three stages: initiation, pest risk assessment and pest risk management. Initiating the PRA process involves identifying pests and pathways of concern and defining the PRA area. Pest risk assessment provides the scientific basis for the overall management of risk. Pest risk management is the process of identifying and evaluating potential mitigation measures which may be applied to reduce the identified pest risk to acceptable levels and selecting appropriate measures.

This Risk Management Document (RMD) includes a summary of the findings of a pest risk assessment and records the pest risk management process for the identified issue. It is consistent with the principles, terminology and guidelines provided in the IPPC standards for pest risk analysis.

Table of Contents

1.0 Executive Summary

Hymenoscyphus fraxineus (T. Kowalski) Baral, Queloz, Hosoya, comb. nov. (ash dieback) is a harmful pathogen affecting ash trees in Europe. The severity and the rapid spread of the disease, and recent data demonstrating the susceptibility of North American ash (Fraxinus spp.) species to the disease make it a pest of concern to Canada.

The risk posed by H. fraxineus to Canada was evaluated through a Canadian Food Inspection Agency (CFIA) Pest Categorisation (November, 2012). The categorisation concluded that H. fraxineus meets the definition of a quarantine pest and that its introduction into Canada could cause significant negative economic and environmental impacts. It is expected that the introduction of H. fraxineus could result in the death or decline of large numbers of ash trees in forests, parks and urban landscapes, as well as in nurseries.

Due to the significant threat posed by H. fraxineus, the CFIA had implemented interim phytosanitary measures to mitigate the risk of introducing this pest to Canada. Since January 30, 2013, importation of ash (Fraxinus spp.) nursery stock, branches and seeds that were previously permitted entry into Canada from infested countries have been prohibited. These measures were temporary pending determination of the regulatory status of H. fraxineus in Canada. The CFIA then consulted on two risk management options for H. fraxineus. The first option proposed maintenance of the status quo, i.e. to not regulate H. fraxineus. The second option, the CFIA's preferred approach, proposed regulation of H. fraxineus and consequently, to maintain the implementation of interim measures for ash plant material. Following the consultation held in early 2014, the decision has been made to regulate H. fraxineus and maintain phytosanitary requirements for ash plant material. However, the prohibition on in vitro plants from Germany and the Netherlands implemented as part of the interim measures in January 30, 2013 will not be maintained.

2.0 Purpose

The purpose of this document is to communicate the CFIA risk management decision for the ash dieback pathogen, H. fraxineus.

3.0 Scope

This RMD examines the risk associated with the introduction of the ash dieback pathogen, H. fraxineus, into Canada, and outlines the risk decision for this disease.

Information pertaining to current import requirements for specific plants or plant products may be obtained from the CFIA's Automated Import Reference System (AIRS).

4.0 Definitions, Abbreviations and Acronyms

Definitions for phytosanitary terms used in this document can be found in the Plant Health Glossary of Terms or the IPPC Glossary of Phytosanitary Terms.

5.0 Background

Ash dieback, caused by H. fraxineus, is a serious emerging plant pest attacking ash trees in Europe. Since its detection in Poland and Lithuania in the early 1990s, this pathogen has spread across Europe, where it causes mortality of European ash trees. The disease is characterised by a rapid dieback of the crown, associated with the presence of cankers or lesions girdling the affected plant parts, which usually leads to plant death.

H. fraxineus, previously referred to as Chalara fraxinea or Hymenoscyphus pseudoalbidus, was recently found to be affecting some native North American ash tree species planted in Europe. The new host range for the pathogen now includes the native North American species Fraxinus nigra, F. pennsylvanica and F. americana, as well as F. mandschurica, native to Asia. This expanded host range has added to the concern that if the pathogen were to be introduced and become established in North America, it might cause significant harm to North American Fraxinus species.

In light of the severity and rapid spread of the disease, and reports of the sensitivity of North American Fraxinus species, a Pest Categorisation was completed by the CFIA to evaluate the risk posed by H. fraxineus to Canada. The Pest Categorisation concluded that H. fraxineus meets the definition of a quarantine pest, and its introduction into Canada could cause significant negative economic and environmental impacts.

6.0 Pest Categorisation Summary

The CFIA's Pest Categorisation for H. fraxineus was completed in November 2012 (CFIA, 2012). The following sections present the highlights of the categorisation.

6.1 Nomenclature

The asexual (anomorphic) stage of the fungus was initially referred to as Chalara fraxinea, while Hymenoscyphus pseudoalbidus was considered to be the sexual (teleomorph) stage of the disease. Previously, the teleomorph was reported to be H. albidus, which was considered to be non-pathogenic, saprotrophic, native and widespread in Europe. Further molecular analysis revealed that the sexual stage was actually a new species which was named Hymenoscyphus pseudoalbidus. At the time when the asexual morph name Chalara fraxinea, and the sexual morph name Hymenoscyphus pseudoalbidus, were described, separate scientific names for the different morphs were permitted. However, according to the "one fungus, one name" principle adopted by the International Code of Nomenclature for algae, fungi and plants, the ash dieback disease should be referred to as Hymenoscyphus fraxineus.

6.2 Pest Biology

6.2.1 Life History

The biology of the fungus is not yet fully understood. Observations in Europe, however, have suggested that the pathogen may enter ash trees through the leaves, in particular, the leaf petioles, which may enable the pathogen to subsequently grow into the vascular system of shoots (McKinney et al., 2011; Timmermann et al., 2011). Reproductive structures of the sexual state, H. fraxineus, usually appear on previous year's leaf litter, but occasionally develop on dead shoots of young ash seedlings in nurseries, as well as on dead, broken shoots and twigs in contact with the ground (Timmermann et al., 2011).

6.2.2 Host Range

Fraxinus is the only genus known to be affected by H. fraxineus. Fraxinus spp. originating from North America, Europe and Asia have been found to be susceptible to the pathogen (Table 1).

Table 1. Ash species (Fraxinus spp.) known to be host of H. fraxineus
Origin Scientific name Common name
North America Fraxinus americana White ash
North America F. nigra Black ash
North America F. pennsylvanica Green or red ash
Europe F. angustifolia Narrow-leaf ash
Europe F. excelsior European ash, common ash
Europe F. ornus Flowering ash
Asia F. mandschurica Manchurian ash

6.2.3 Symptoms

H. fraxineus is characterised by a rapid dieback of the crown, associated with the presence of cankers or lesions girdling the affected plant parts, usually leading to tree death (Kowalski and Holdenrieder, 2009; DEFRA, 2012). Symptoms of the disease occur in the bark and vascular system of shoots, twigs, branches and stems, as well as on leaves of ash trees (Timmermann et al., 2011). The most obvious disease characteristics are: wilting, discoloration and premature shedding of leaves; dieback of shoots, twigs and branches; necrosis of bark, leaves and buds; necrotic cankers in the bark, shoots and branches; a brown to grey discolouration of the inner bark; and discoloration of the wood (Bakys et al., 2009; Goudet et al., 2012; Timmermann et al., 2011). The appearance of small necrotic lesions on leaf petioles and leaflet veins are the first indication of infection (Timmermann et al., 2011). The fungus has been occasionally detected in roots, but only when the stem was also infected (Schumacher et al., 2010). Diseased trees react with prolific formation of epicormic shoots (Kirisits et al., 2008). The fungus has also been linked to basal stem necrosis (Langer and Werres, 2013).

6.3 Distribution

Since its emergence in Poland, the disease has progressed rapidly across Europe, where, to date, the disease has been observed in, or reported from, the following countries: Austria, Belgium, Belarus, Croatia, Czech Republic, Denmark, Estonia, Finland, France, Germany, Hungary, Ireland, Italy, Latvia, Lithuania, Netherlands, Norway, Poland, Romania, Russia, Slovakia, Slovenia, Sweden, Switzerland, Ukraine and the United Kingdom (Timmermann et al., 2011).

The disease has also been reported outside of Europe. A recent publication describes the Japanese fungus Lambertella albida as conspecific with H. fraxineus, suggesting that the correct name of L. albida, which had previously been reported from the petioles of the Asian ash species Fraxinus mandshurica in Japan, is actually H. fraxineus (Zhao et al., 2012). Similarly, H. fraxineus was reported from decomposing leaves of F. mandschurica in China in 2013 (Zheng et al., 2013). No symptoms of disease were observed on the ash trees in China, strengthening the earlier belief that the pathogen was introduced into Europe from Asia as some Asian ash species such as Manchurian ash, planted as ornamental species in Europe, appeared immune to the disease (Coghlan, 2012).

6.4 Means of Introduction and Spread

The pathogen can be carried through trade via Fraxinus spp. bark, leaves, roots, stems, branches, seeds and wood. Movement of infected host material, such as Fraxinus spp. nursery stock, appears to be primary pathway for long-distance spread of the disease. The recent discovery in England of nursery plants infected with H. fraxineus, which were imported directly from other nurseries in continental Europe (the Netherlands), indicates that the pathogen is spread long-distances via the plants for planting pathway (DEFRA, 2012). As well, the pathogen was shown to be able to produce conidia from infected wood (Husson et al., 2012), suggesting that untreated ash logs or related wood products, such as firewood and woodchips, may be able to carry the pathogen over long distances and act as pathways of introduction into disease-free areas.

In Europe, the pathogen is also thought to also be spreading naturally over long distances via wind-borne sexual spores (ascospores) (Wingen et al. 2013; Timmermann et al., 2011). Sexual spores may also disperse via the movement of soil, water, or insect vectors, although no insect vectors have been identified to date (Prokrym and Neeley, 2009; Timmermann et al., 2011). Seeds of declining F. excelsior trees have also been shown to carry the pathogen at low levels, although the effect of H. fraxineus on seed germination and seedling emergence is currently unknown (Cleary et al., 2013). International trade of Fraxinus seed collected from areas known to be infested may therefore serve as a potential pathway for the introduction of this pathogen (Cleary et al., 2013).

6.5 Potential for Establishment and Spread

Host species suitable for establishment and spread of H. fraxineus are present in Canada. These include F. nigra (black ash), F. pennsylvanica (green or red ash) and F. americana (white ash) (Drenkhan and Hanso, 2010), all of which are known to be susceptible to the fungus.

In Europe, the North American black ash species, F. nigra, was severely affected by H. fraxineus. F. nigra commonly occurs in Canada in northern swampy woodlands from eastern Manitoba into the Atlantic Provinces including Newfoundland (Farrar, 1995). Fraxinus pennsylvanica was moderately affected in Europe, with symptoms similar to F. nigra, but with less evidence of dead shoots within the canopy. It is the most widely distributed ash in Canada, ranging from Saskatchewan to Nova Scotia. Fraxinus americana, white ash, was the least affected by the fungus in Europe, showing signs of wilting leaves but only minor dieback of shoots and twigs and bark necrosis (Drenkhan and Hanso, 2010). F. americana is an eastern species and the most common native ash in Canada (Farrar, 1995). Fraxinus excelsior is considered to be highly susceptible to the fungus. It was introduced in North America but it has a relatively limited distribution in the Eastern U.S. and Canada (Prokrym and Neeley, 2009).

Other species of ash in Canada include F. quandrangulata (blue ash), F. latifolia (Oregon ash) and F. profunda (pumpkin ash). There is currently no data available on their susceptibility to H. fraxineus.

The known distribution of the fungus includes parts of southern, central, northern and north-eastern Europe which lie within plant hardiness zones 3 to 10 (NAPPFAST, 2012). The geographic range of the host Fraxinus species growing in Canada lie predominantly within NAPPFAST climate Zones 3 to 8, well within the climatic range of the countries in which the pathogen is known to occur. Southern and central areas of Saskatchewan, Manitoba, Ontario, Quebec, New Brunswick, Nova Scotia and Prince Edward Island, where either native F. americana, F. nigra or F. pennsylvanica trees grow, would be expected to have current climatic conditions conducive to disease development, should the pathogen be introduced into Canada.

6.6 Potential Economic and Environmental Consequences

If introduced into Canada, it is expected that H. fraxineus could result in the death or decline of large numbers of ash trees in forests, parks and urban landscapes, as well as in nurseries. This could lead to significant negative economic and environmental impacts.

H. fraxineus symptoms would be highly undesirable aesthetically, if the pathogen were to infect urban ash tree populations. In urban environments, symptoms of the disease may lead to the removal and replacement of affected ash trees at considerable costs; the average monetary value of urban trees has been estimated at $700 per tree (Kenney and Idziak, 2000). This value represents only the replacement costs and does not reflect the benefit to society provided by trees in urban environments. In addition, trees in urban environments provide a number of environmental benefits such as helping to remove gaseous air pollution, energy conservation (heating and cooling costs), storm-water attenuation, noise buffering, providing wildlife habitats, increasing property values, enhancing aesthetics, protection from wind and psychological well-being (Rosen and Kenney, 2003). These benefits could be negatively impacted due to a loss of trees in urban environments (Kenney and Idziak, 2000; Rosen and Kenney, 2003).

Fraxinus americana is the most common native ash in Canada and also the most commercially valuable species, used in the manufacture of wood products such as handles, sporting goods such as hockey sticks and baseball bats, furniture, baskets and kitchen cabinets (Farrar, 1995; Panshin and de Zeeuw, 1970). White ash is also used for veneer and hardwood flooring products. Dead or dying trees are not used in the manufacture of wood products for which ash wood is favoured (Panshin and de Zeeuw, 1970). Furthermore, the discoloration of the wood caused by the fungus would make wood from affected ash trees undesirable and unmarketable for manufactured wood products. Canada's ash wood export market would be negatively impacted as this pathogen could pose a risk in the more extensive and diverse deciduous forests of the U.S., Canada's largest trading partner (Shore, 1992). H. fraxineus is considered a reportable (quarantine) pest in the U.S. (USDA-APHIS, personal communication, 2012).

A change in forest biodiversity may also occur due to a change in forest composition as a result of a large decline in ash trees (USDA-APHIS/ARS/FS, 2010). Ash trees often fill gaps in the forest, providing shade for the forest floor; ash is one of the few native trees able to out-compete weeds that prevent other species from becoming established (USDA-APHIS/ARS/FS, 2010).

7.0 Risk Management Considerations

7.1 Phytosanitary Requirements Prior to the Implementation of Interim Measures

The introduction of H. fraxineus to Canada would most likely occur through the importation of ash wood products, nursery stock, branches and seeds. Phytosanitary requirements for the importation of ash plant material had previously been put in place to mitigate the risk posed by other quarantine pests. Phytosanitary requirements in place prior to the implementation of the interim phytosanitary measures for areas other than continental U.S. are described below.

Ash wood products from foreign sources have been subject to phytosanitary requirement to mitigate the entry of various quarantine pests as outlined in D-02-12, Import requirements for non-processed wood and other non-propagative wood products, except solid wood packaging material, from all areas other than the continental United States (CFIA, 2011). In general, ash wood products must be free from bark and heat treated or fumigated with methyl bromide as per requirements described in the D-02-12, or prior approval is required.

Ash plants and plant parts for planting have been Not Approved Pending Pest Risk Analysis (NAPPRA) as per directive D-08-04, Plant protection import requirements for plants and plant parts for planting, from all countries except the U.S., Germany and the Netherlands (CFIA, 2013). Ash plants and plant parts from Germany and the Netherlands had been required to be accompanied by an Import Permit and a Phytosanitary Certificate. As of January 2013, prior to the implementation of the interim phytosanitary measures, there were a very limited number of valid Import Permits for the import of rooted ash plants, and only for a diameter equal to or less than 10 mm.

From areas other than the continental U.S., fresh ash decorative branches have been allowed entry only from Germany and the Netherlands if accompanied by a Phytosanitary Certificate and an Import Permit. However, there were no valid Import Permits in the CFIA's records as of January 2013.

Dried ash branches larger than 1.5 cm imported from all areas other than the continental U.S. have been required to be fumigated with methyl bromide (CFIA, 2011). Dried branches smaller than 1.5 cm have not been subject to any specific phytosanitary requirements.

The importation of ash seeds previously required an Import Permit. Again, there were very few valid Import Permits for ash seeds in the CFIA's records as of January 2013.

7.2 Interim Phytosanitary Measures

On January 30, 2013, due to the important threat posed by H. fraxineus, the CFIA implemented interim phytosanitary measures prohibiting the importation of ash (Fraxinus spp.) nursery stock and fresh branches from the Netherlands and Germany as well as seeds, in vitro plants and dried branches from all countries infested with H. fraxineus. AIRS was updated to reflect this and, where applicable, Import Permits were amended or cancelled. A World Trade Organisation (WTO) Notification of Emergency Measures was published on January 23, 2013. The decision outlined in this RMD maintains most of the interim phytosanitary measures implemented on January 30, 2013. However, the prohibition of in vitro plants from Germany and the Netherlands implemented with the interim measures on January 30, 2013 will not be maintained.

7.3 Treatment and Control Options

There are currently no pesticide products registered for H. fraxineus in Canada, and limited or no pesticides are registered in other countries (PMRA, personal communication, 2013).

Research into naturally resistant trees has been carried out on the European species F. excelsior (Kjaer et al., 2012; McKinney et al., 2011). A very limited number of trees in the population have been found to show a partial resistance to the pathogen. We can hypothesize that some level of resistance may be present in North American species.

8.0 Risk Management Decision: Regulate Hymenoscyphus fraxineus and Implement Phytosanitary Import Requirements for Ash Plant Material

After critical evaluation of H. fraxineus (ash dieback pathogen), along with the risks associated with its potential introduction into Canada, and feedback from the consultative process, the CFIA has decided to regulate H. fraxineus and implement phytosanitary import requirements for ash plant material.

Phytosanitary requirements for host material have been modified to take into account the risk posed by H. fraxineus. The following import conditions have been applied to Fraxinus spp. plant material:

The countries currently infested with H. fraxineus are listed in section 6.3 of this RMD. In addition to those countries, CFIA also considers all other countries from the European Union to be potentially infested in view of the wide distribution of this disease in Europe.

The CFIA believes that the scientific data currently available does not support the development of phytosanitary measures for ash plants and plant parts for planting (i.e. rooted and unrooted plants, fresh and dried branches and seeds) that would mitigate the risk associated with H. fraxineus to an acceptable level. As more information on the disease becomes available, the CFIA may be able to consider pest-free areas and systems approaches as satisfactory mitigation measures for countries from which import was previously approved i.e. the Netherlands and Germany. All other infested countries (currently NAPPRA) are still subject to a full Pest Risk Analysis to determine if they would be admissible. For the U.S., phytosanitary requirements remain unchanged as H. fraxineus is not known to occur in the U.S.

Phytosanitary requirements for ash wood products (e.g. sawn wood) continue to require a Phytosanitary Certificate attesting that the wood has been either heat-treated or fumigated with methyl bromide. It is currently believed that these two treatments adequately mitigate the risk of introducing H. fraxineus into Canada via these wooden products and no further action is required. Prior approval is still required for any other ash wood products.

The decision to regulate this pest, and the formal implementation of interim measures (excluding the initial prohibition of in vitro plantlets from the Netherlands and Germany) for host material of H. fraxineus mitigates the risk of introducing this pathogen to Canada and helps preserve our ash wood and plant export market. By regulating H. fraxineus, the CFIA has the authority to require phytosanitary measures for host material and to respond to incursions by applying official control measures, and also prevents the entry into Canada of a potentially ineradicable pest. Furthermore, as this pest is not known to occur in North America, the decision to regulate strengthens our cooperation with the U.S. as the U.S. regulates H. fraxineus.

9.0 Stakeholder Communications

The following trading partners and stakeholders will be notified of changes in import requirements resulting from the risk management decision:

10.0 References

Bakys R, R Vasaitis, P Barklund, IM Thomsen, J Stenlid. 2009. Occurrence and pathogenicity of fungi in necrotic and non-symptomatic shoots of declining common ash (Fraxinus excelsior) in Sweden. European Journal of Forest Research 128(1): 51-60.

Baral, H-O, Queloz, V, Hosoya, T. 2014. Hymenoscyphus fraxineus, the correct scientific name for the fungus causing ash dieback in Europe. IMA Fungus: The Global Mycological Journal 5(1): 79–80.

Cleary, MR, N Arhipova, T Gaitnieks, J Stenlid, and R Vasaitis. 2013. Natural infection of Fraxinus excelsior seeds by Chalara fraxinea. Forest Pathology 43(1): 83-85.

Canadian Food Inspection Agency (CFIA). 2011. Directive D-02-12: Import requirements for non-processed wood and other non-propagative wood products, except solid wood packaging material, from all areas other than the continental United States (July 18th, 2011 (6th Revision))

Canadian Food Inspection Agency (CFIA). 2012. Pest Categorisation: Chalara fraxinea (Hymenoscyphus fraxineus) (Ash Dieback Pathogen). Plant Health Risk Assessment Unit, Plant Health Science Division. Ottawa, Ontario. April 16 2012, Revised November 16, 2012.

Canadian Food Inspection Agency (CFIA). 2013. Directive: D-08-04: Plant Protection Import Requirements for Plants and Plant Parts for Planting (November 25th, 2013 (2nd Revision))

Coghlan, A. 2012. Are Europe's ash trees finished? New Scientist. 31 October 2012. Online publication [http://www.newscientist.com/article/dn22449-are-europes-ash-trees-finished.html]

Department for Environment, Food & Rural Affairs (DEFRA). 2012. Rapid Risk Assessment: Rapid assessment of the need for a detailed Pest Risk Analysis for Chalara fraxinea. Online publication. [http://www.fera.defra.gov.uk/plants/plantHealth/pestsDiseases/documents/chalaraFraxinea.pdf] Accessed November 6th, 2012.

Drenkhan R and M Hanso. 2010. New host species for Chalara fraxinea. New Disease Reports 22, 16.

Farrar, JL 1995. Trees in Canada. Fitzhenry & Whiteside Limited and the Canadian Forest Service Natural Resources Group. 502 pp.

Forestry Commission (Great Britain). 2012. Chalara dieback of ash (Chalara fraxinea). Online publication. [http://www.forestry.gov.uk/chalara]. Accessed November 13th, 2012.

Goudet, M and D Piou. 2012. Ash dieback or chalarose- what do we know? Revue Forestiere Francaise. Vol. 64(1): 27-40.

Husson, C, O Cael, JP Grandjean, LM Nageleisen and B Marcais, 2012. Occurrence of Hymenoscyphus fraxineus on infected ash logs. Plant Pathology 61(5): 889-895.

Kenney, WA and C Idziak. 2000. The State of Canada's Municipal Forests - 1996 to 1998. Forestry Chronicle 76(2): 231-234.

Kirisits T, M Matlakova, S Mottinger-Kroupa, and E Halmschlager. 2008. Involvement of Chalara fraxinea in Ash Dieback in Austria. Forstschutz Akuell 44.

Kjaer, ED, LV Mckinney, LR Nielsen, LN Hansen and JK Hansen. 2012. Adaptive potential of ash (Fraxinus excelsior) populations against the novel emerging pathogen Hymenoscyphus fraxineus. Evolutionary Applications 5(3): 219-228.

Kowalski, T and O Holdenrieder. 2009. The teleomorph of Chalara fraxinea, the causal agent of ash dieback. Forest Pathology 39: 304-308.

Langer, G. and S. Werres. 2013. Fungi associated with stem necrosis on ash trees infected with Hymenoscyphus fraxineus in Schleswig-Holstein. (Abstract) COST Action FP1103 FRAXBACK 4th MC Meeting & Workshop "Frontiers in ash dieback research", 4-6th of September 2013, Sankt Gertrud Konferens, Malmö, Sweden

Marčiulynienė D., M. Clear, D. Shabunin, J. Stenlid and R. Vasaitis. 2013. Detection of Hymenoscyphus fraxineus in Primorye region, Far East Russia. (Abstract) COST Action FP1103 FRAXBACK 4th MC Meeting & Workshop "Frontiers in ash dieback research", 4-6th of September 2013, Sankt Gertrud Konferens, Malmö, Sweden

McKinney LV, LR Nielsen, JK Hansen, and ED Kjaer. 2011. Presence of natural genetic resistance in Fraxinus excelsior (Oleraceae) to Chalara fraxinea (Ascomycota): an emerging infectious disease. Heredity 106: 788–797.

NCSU/APHIS Plant Pest Forecast (NAPPFAST). 2012. NAPPFAST Global Plant Hardiness Zones based on CFSR base data. North Carolina State University APHIS Plant Pest Forecasting System. August, 2012. Online publication.

Panshin AJ, C de Zeeuw. 1970. Textbook of wood technology. Vol. 1. Structure, identification, uses, and properties of the commercial woods of the United States and Canada. McGraw-Hill Book Company, Toronto, pp. 705.

Pautasso M, G Aas, V Queloz and O Holdenrieder. 2013. European ash (Fraxinus excelsior) dieback – A conservation biology challenge. Biological Conservation 158: 37-49.

Prokrym, DR and AD Neeley. 2009. New Pest Advisory Group (NPAG) Report: Chalara fraxinea T. Kowalski: Ash dieback. United States Department of Agriculture, Center for Plant Health Science and Technology, Plant Epidemiology and Risk Analysis Laboratory.

Rosen, MR and WA Kenney. 2003. Urban Forestry Trends in Canada. Online publication. [http://www.fao.org/docrep/ARTICLE/WFC/XII/0752-B1.HTM]

Shore TL. 1992. Ambrosia beetles. Forest Pest Leaflet #72, Canada-British Columbia Partnership Agreement on Forest resource Development: FRDA II.

Schumacher J, R Kehr and S Leonhard. 2010. Mycological and histological investigations of Fraxinus excelsior nursery saplings naturally infected by Chalara fraxinea. Forest Pathology 40: 419-429.

Timmermann V, I Borja, AM Hietala, T Kirisits and H Solheim. 2011. Ash dieback: pathogen spread and diurnal patterns of ascospore dispersal, with special emphasis on Norway. EPPO Bulletin, 41: 14–20.

USDAAPHIS/ARS/FS. 2010. Emerald Ash Borer, Agrilus planipennis Fairmaire, Biological Control Release Guidelines. USDAAPHISARS-FS, Riverdale, Maryland. Online publication. [http://na.fs.fed.us/fhp/eab/ar/ar.shtm]. Accessed November 2012.

Wingen LU, MW Shaw and JKM Brown. 2013. Long-distance dispersal and its influence on adaptation to host resistance in a heterogeneous landscape. Plant Pathology 62(1): 9-20.

Zhao Y-J., T Hosoya, H-O Baral, K Hosaka and M Kakishima. 2012. Hymenoscyphus fraxineus, the correct name for Lambertella albida reported from Japan. Mycotaxon. 122: 25-41.

Zheng, H.-D. and W.-Y. Zhuang. 2013. Hymenoscyphus albidoides sp. nov. and H. fraxineus from China. Mycological Progress DOI: 10.1007/s11557-013-0945-z. [http://link.springer.com/article/10.1007%2Fs11557-013-0945-z/fulltext.html]. Accessed January 16, 2014.

11.0 Endorsement

Approved by:

space for the signature of the Chief Plant Health Officer
Chief Plant Health Officer

Signature of the Chief Plant Health Officer is required only on completion of the pest risk management process, to indicate approval of the final decision. This section is included in the RMD after stakeholder consultation has occurred and a final decision is made.

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