Policy paper

Annexes: Evidence summaries

Published 6 June 2019

© Crown copyright 2019

This publication is licensed under the terms of the Open Government Licence v3.0 except where otherwise stated. To view this licence, visit nationalarchives.gov.uk/doc/open-government-licence/version/3 or write to the Information Policy Team, The National Archives, Kew, London TW9 4DU, or email: psi@nationalarchives.gov.uk.

Where we have identified any third party copyright information you will need to obtain permission from the copyright holders concerned.

This publication is available at https://www.gov.uk/government/publications/ash-tree-research-strategy-2019/annexes-evidence-summaries

Annexes: Evidence summaries

Confidence ratings

Data in this paper has been sourced from different organisations/publications. In order to help the reader understand the data presented a confidence rating has been applied where appropriate.

  1. CR High: Based on significant evidence (e.g. recent survey, statistically sound using up to date methods, HMRC data, current industry practices; published in peer reviewed papers; recent qualitative research (interviews, focus groups etc.) with sound methodology that includes results from a number of studies in different locations with different types of people that report similar findings).

  2. CR Medium: Based on incomplete or dated evidence (e.g. an estimate based on old survey data, trade association estimates, a survey result which may not be entirely representative of the whole; qualitative research from one or two case studies; published in only one or two peer reviewed papers; published in grey literature).

  3. CR Low: Based on speculative or incomplete evidence (e.g. rough estimate from a single expert, or industry body lacking supporting analysis, or early result based on fast developing situation on ground, not published in peer reviewed papers, qualitative research that involves a single case or does not provide details of the sample studied or method used.

Evidence summary: ash

  • Fraxinus excelsior is a large tree, native to the UK and found across much of mainland Europe. In Britain ash is the second most abundant tree species in small woodland patches after the native oak species, and the third most abundant in larger areas of forest. Outside of woodlands ash grows, or is planted, in hedgerows, next to roads and railways and in urban environments [1].(CR Medium)
  • 12% of broadleaf woodland in Great Britain is ash [2]. (CR High)
  • It is estimated that there are 125 million ash trees in woodlands and between 27-60 million ash trees outside of woodlands in the UK, plus potentially 2 billion saplings and seedlings in woodlands and non-woodland situations. [3, 4] (CR Medium)
  • 9,500 ancient, veteran and notable ash trees have been recorded in the Ancient Tree Inventory [5]. (CR High)
  • The social and environmental value of ash woodlands in Great Britain have been estimated at over £230 million per year reflecting recreation, landscape, carbon sequestration, air pollution absorption and elements of biodiversity value. [6] (CR Medium)
  • The population structure of British common ash shows that the majority of the population belongs to the same population as mainland western and central Europe. With a few exceptions found in eastern Scotland and north Wales. [7] [8] (CR Medium)
  • The UK National Tree Seed Project has conserved over 59 seed collections from 659 mother trees and as a result captured >90% of all British ash alleles. [9] (CR Medium)
  • 955 species have been identified as having all or part of their lifecycle associated with ash woodlands in the UK, for example as a habitat, food source or hunting ground. Of these 44 are only recorded on ash and are considered obligate, a further 62 are highly associated but have also been recorded on other species. [10-12] (CR High)
  • No single tree species will be able to fill the niche provided by ash trees in terms of both its ecosystem function (e.g. nutrient cycling and light penetration properties that influence other ground cover) and biodiversity contribution. The most appropriate strategy for managing the biodiversity impacts of loss of ash will vary from site to site. [13, 14] (CR Medium)
  • Ash wood is highly valued for specialist uses such as tool handles and furniture, as well as for firewood, making ash timber one of the most valuable native hardwoods.[15] (CR High)

References

  1. Thomas, P.A., (2016) Biological Flora of the British Isles: Fraxinus excelsior. Journal of Ecology. 104(4), 1158-1209.
  2. Forestry Commission. (2018) Forestry Statistics 2018. [Online]. Available: https://www.forestresearch.gov.uk/tools-and-resources/statistics/forestry-statistics/forestry-statistics-2018/. Accessed: 1 December 2018.
  3. Department of Food Environment and Rural Affairs. (2015) Chalara in Non-Woodland Situations TH0148. [Online]. Available: http://randd.defra.gov.uk/Default.aspx?Menu=Menu&Module=More&Location=None&ProjectID=19770. Accessed: 6 January 2019.
  4. Forestry Commission. (2013) NFI preliminary estimates of quantities of broadleaved species in British woodlands, with special focus on ash. [Online]. Available: https://www.forestry.gov.uk/pdf/NFI_Prelim_BL_Ash_Estimates.pdf/$FILE/NFI_Prelim_BL_Ash_Estimates.pdf. Accessed: 7 Feb 2019.
  5. Woodland Trust. (2019) Ancient Tree Inventory. [Online]. Available: https://ati.woodlandtrust.org.uk/. Accessed: 3/3/2019.
  6. Department of Food Environment and Rural Affairs. (2016) Tree Health Resilience Strategy. [Online]. Available: https://www.gov.uk/government/publications/tree-health-resilience-strategy-2018. Accessed: 1/3/2019.
  7. Sutherland, B.G., Belaj, A., Nier, S., Cottrell, J.E., S, P.V., Hubert, J., and Russell, K., (2010) Molecular biodiversity and population structure in common ash (Fraxinus excelsior L.) in Britain: implications for conservation. Mol Ecol. 19(11), 2196-211.
  8. Heuertz, M., Hausman, J.F., Hardy, O.J., Vendramin, G.G., Frascaria-Lacoste, N., and Vekemans, X., (2004) Nuclear microsatellites reveal contrasting patterns of genetic structure between western and southeastern European populations of the common ash (Fraxinus excelsior L.). Evolution. 58(5), 976-988.
  9. Hoban, S., Kallow, S., and Trivedi, C., (2018) Implementing a new approach to effective conservation of genetic diversity, with ash (Fraxinus excelsior) in the UK as a case study. Biological Conservation. 225, 10-21.
  10. Mitchell, R.J., Bailey, S., Beaton, J.K., Bellamy, P.E., Brooker, R.W., Broome, A., Chetcuti, J., Eaton, S., Ellis, C.J., Farren, J., Gimona, A., Goldberg, E., Hall, J., Harmer, R., Hester, A.J., Hewison, R.L., Hodgetts, N.G., Hooper, R.J., Howe, L., Iason, G.R., Kerr, G., Littlewood, N.A., Morgan, V., Newey, S., Potts, J.M., Pozsgai, G., Ray, D., Sim, D.A., Stockan, J.A., Taylor, A.F.S., and Woodward, S. (2014) The potential ecological impact of ash dieback in the UK (phase 1). [Online]. Available: http://jncc.defra.gov.uk/pdf/JNCC483_web.pdf. Accessed: 1/3/2019.
  11. Mitchell, R.J., Bailey, S., Beaton, J.K., Bellamy, P.E., Brooker, R.W., Broome, A., Chetcuti, J., Eaton, S., Ellis, C.J., Farren, J., Gimona, A., Goldberg, E., Hall, J., Harmer, R., Hester, A.J., Hewison, R.L., Hodgetts, N.G., Hooper, R.J., Howe, L., Iason, G.R., Kerr, G., Littlewood, N.A., Morgan, V., Newey, S., Potts, J.M., Pozsgai, G., Ray, D., Sim, D.A., Stockan, J.A., Taylor, A.F.S., and Woodward, S. (2014) Assessing and addressing the impacts of ash dieback on UK woodlands and trees of conservation importance (Phase 2). [Online]. Available: http://publications.naturalengland.org.uk/publication/5273931279761408. Accessed: 1/3/2019.
  12. Mitchell, R.J., Beaton, J.K., Bellamy, P.E., Broome, A., Chetcuti, J., Eaton, S., Ellis, C.J., Gimona, A., Harmer, R., Hester, A.J., Hewison, R.L., Hodgetts, N.G., Iason, G.R., Kerr, G., Littlewood, N.A., Newey, S., Potts, J.M., Pozsgai, G., Ray, D., Sim, D.A., Stockan, J.A., Taylor, A.F.S., and Woodward, S., (2014) Ash dieback in the UK: A review of the ecological and conservation implications and potential management options. Biological Conservation. 175, 95-109.
  13. Mitchell, R.J., Pakeman, R.J., Broome, A., Beaton, J.K., Bellamy, P.E., Brooker, R.W., Ellis, C.J., Hester, A.J., Hodgetts, N.G., Iason, G.R., Littlewood, N.A., Pozsgai, G., Ramsay, S., Riach, D., Stockan, J.A., Taylor, A.F.S., and Woodward, S., (2016) How to Replicate the Functions and Biodiversity of a Threatened Tree Species? The Case of Fraxinus excelsior in Britain. Ecosystems. 19(4), 573-586.
  14. Hill, L., Hemery, G.E., Hector, A., and Brown, A., (2018) Maintaining ecosystem properties after loss of ash in Great Britain. Journal of Applied Ecology. 56(2), 1-12.
  15. Pautasso, M., Aas, G., Queloz, V., and Holdenrieder, O., (2013) European ash (Fraxinus excelsior) dieback - A conservation biology challenge. Biological Conservation. 158, 37-49.

Evidence summary: ash dieback

Pathogen

  • Ash dieback is a disease caused by the fungus Hymenoscyphus fraxineus (formerly Chalara fraxinea and Hymenoscyphus pseudoalbidus). [16, 17] (CR High)
  • H. fraxineus is native to Asia where it is a weak pathogen of the Asian species of ash (Fraxinus mandshurica and F. rhynchophylla) [18]. It was first identified in Poland in 2006 but is thought to have established in Europe as early as 1992. [16] The disease has now been recorded in most European countries [19]. (CR High)
  • The first recorded incidence of H. fraxineus in the wider environment in England was 2012, new research has demonstrated that the fungus had already been present in some locations since at least 2004. [20] (CR High)
  • Genetic analysis has demonstrated that the European population of H. fraxineus is very similar, indicating a single or small number of introductions into Europe. [21, 22] (CR High)
  • H. fraxineus arrived in the UK both through airborne spores and through infected planting material, the mode of arrival has not influenced the genetic diversity of the pathogen. [23] (CR Medium)
  • Research into the dynamics and genetic structure of H. fraxineus suggests that there is a high fitness cost to pathogenicity. In addition, the large population size and frequent mating of H. fraxineus has generated a high genotypic diversity which natural selection can act on. Coevolutionary theory predicts that in this scenario natural selection will act to make the pathogen less pathogenic. It is likely that this will take several hundred years. [23] (CR Medium/Low)

Lifecycle

  • H. fraxineus undergoes both sexual and asexual reproduction. Sexual reproduction happens on the fallen ash petioles in the leaf litter, this results in fruit body production. Asexual reproduction takes place in autumn and winter, the role these conidia have in the lifecycle of H. fraxineus is not yet clear. [24-26] (CR High)
  • Infection is via air-borne spores produced from fruit bodies on leaf litter. The fruit bodies occur on infected fallen leaves and shoot material in the growing season (June – August) after infection for up to 5 years [27]; trees are likely to need a high dose of spores to become infected. Spore density is highest close to the ground. [28, 29] (CR High)
  • Spores germinate soon after they are released in the presence of water, a small proportion can survive dry conditions for 7 days. [30] (CR Low)
  • Moist conditions favour the production of fruit bodies. In addition, occasionally fruit bodies can be produced on dead shoots, stems and root collars of recently dead young trees. [20, 31] (CR High)
  • Natural spread occurs with wind-blown spores (ascospores) from the fruiting bodies. [16, 32]. Spread can also occur via the movement of infected trees in leaf through trade or through movement of fallen leaves. Data from Europe has shown that the disease is capable of dispersing 50-75km per year. [24, 33, 34] (CR High)
  • H. fraxineus infection starts primarily on leaves and is progressive over time with dieback and stem lesions becoming pronounced over the next growing season. Stem lesions are considered to be a reproductive dead end for the fungus. [24] (CR High).
  • On susceptible hosts the disease causes loss of leaves, dieback of the crown of the tree, basal lesions and often leads to tree death. [24, 35] (CR High)
  • Basal lesions can be caused primarily by H. fraxineus and also in conjunction with secondary pathogens, such as honey fungus (Armillaria spp.). Basal lesions drive mortality in larger trees and trees can become structurally unstable. Basal lesions are more likely to be found on sites which are wet and already suffering from crown dieback. [36-39] (CR High)
  • Basal lesions correlate with crown dieback [38], however in some cases basal lesions have been observed on trees with minimal crown damage. [40] (CR Medium)

Host

  • H. fraxineus has infected many species of Fraxinus, but with differing intensities [18, 41] . Common ash (Fraxinus excelsior) is one of the most severely affected species and is the only native species of ash in the UK. F. angustifolia, F. quadrangulata and F. nigra are also considered to be highly susceptible. [18, 42] (CR High)
  • Recently H. fraxineus has been found to infect other species in the Oleaceae; Philyrea latifolia, P. angustifolia and Chionanthus virginicus, it is not yet known if H. fraxineus can complete its lifecycle on these hosts. (CR Low)
  • Other species in the Oleaceae family have been tested including Forsythia x intermedia and Ligustrum vulgare and these were found not to be susceptible to H. fraxineus.[43] (CR Medium)
  • The disease progresses quickly in young trees (as their stem diameter is quickly girdled), trees growing in stressed conditions (for example on sites with and extreme excess of or lack of moisture) and in ash dominated woodlands with higher levels of leaf litter and consequently spore loads. [36, 44] (CR High)
  • Fewer symptoms have been observed in ash trees growing on well managed sites in open spaces, such as parklands. It is thought that trees are escaping the disease and at these sites, trees can survive for years without many observed symptoms [36, 44]. (CR High)

Tolerance

Definition: In this summary we use the word tolerance to refer to all terms used in the scientific literature where ash trees have low susceptibility to ash dieback; this includes tolerance, resistance, partial resistance, low susceptibility and disease avoidance.

  • Observations from young planted trials in the UK and Europe have demonstrated that between 1-5% of the population may be tolerant to H. fraxineus. This tolerance varies between genotypes demonstrating that tolerance has a genetic component. [45-49] (CR High)
  • Different experimental approaches have been used to quantify tolerance of individual ash trees to the H.fraxineus pathogen. Most use direct exposure to the pathogen but recently spectroscopy has been suggested as a means of phenotyping individuals. [35, 50-52] (CR Medium)
  • Basal lesions represent a different infection pathway to crown dieback but their incidence also has a host genetic component. [53] (CR Medium)
  • The climate and site factors play a large role in how trees succumb to H. fraxineus, this includes soil type, soil moisture, air humidity, temperature, stand age and stocking density. [36] (CR Medium)
  • In Europe, narrow sense heritability for tolerance has been calculated at between 0.3-0.5 which offers hope for a future breeding programme. [46, 47, 54] (CR High)
  • Variation in tolerance exists in all populations of ash rather than in specific regions. This natural tolerance within all populations provides an opportunity to maintain ash as a species. [36, 46] (CR High)
  • In a trial in Denmark, tolerant female trees have been found to produce more seed when compared to very susceptible trees, demonstrating that ash forests could recover in time. [55] (CR Medium)
  • The F. excelsior genome has been sequenced and 38,852 protein-coding genes have been annotated .[56] (CR Medium)
  • Transcriptomic markers have been developed which predicted 25% of the observed variation seen in a Danish panel of trees. [56, 57] (CR Medium)
  • A small survey of forest managers in the UK identified that this sector have a strong interest in the concept of tolerant ash if this ash has similar characteristics, retains genetic diversity and withstands future pest and disease threats. [58] (CR Low)
  • A metabolomics study using a small sample of Danish trees demonstrated that trees tolerant to ash dieback may have less iridoid glycosides, well known anti herbivory chemicals. This suggests that low susceptibility to ash dieback may result in increased susceptibility to insect pests such as emerald ash borer (Agrilus planipennis). [59] (CR Low)
  • A genome wide association study of 1250 ash trees has identified genomic markers associated with ash dieback damage scores. The markers can distinguish between trees with high and low ash dieback damage with 69% accuracy. The identified markers could speed up any breeding programme for ash dieback tolerance.[60] (CR Low)
  • A survey of the public acceptability to tree breeding solutions in response to ash dieback showed the majority of respondents were concerned about the loss of ash from the British countryside and were looking for an active response. Breeding native ash through conventional means was preferable but accelerated breeding with the assistance of markers was also acceptable. . [61, 62] (CR Medium/Low)

Management

  • Managing H. fraxineus in forest stands depends on the management objective, stand condition, age, type, site conditions and the extent of H. fraxineus. Disease progression is generally faster in young, pure ash stands. Other tree species can influence the amount of ash crown dieback by changing the conditions for sporulation of H. fraxineus. [63] (CR High)
  • Hypovirulence involves the infection of a fungal pathogen with a virus and can reduce the pathogenicity of the fungus. Success depends on low vegetative compatibility group diversity of the fungus. Populations of H. fraxineus in the UK have shown a wide variation in vegetative compatibility groups. This makes the introduction of hypovirulence as a form of control very unlikely. [23] (CR High)
  • Some evidence suggests that clear felling areas of pure ash will result in less natural regeneration of ash. Healthy seed trees should be maintained for as long as possible to ensure regeneration from tolerant mother trees. Promoting ash regeneration will encourage the process of natural selection. Regeneration should be promoted as a mix of species to avoid a more susceptible pure ash stand. [36, 64] (CR Medium)
  • Some fungicides can be used as preventative treatment and could be used in forest nurseries. [36, 65] (CR Medium)
  • Removal of leaf litter is an effective way to reduce the level of inoculum in certain conditions i.e. urban environments. [36] (CR Medium/Low)
  • Data from Europe has demonstrated that coppice regrowth becomes severely infected, it is thought this could be to do with the proximity of the regrowth to the high spore load. [64] (CR Low)

Impacts

  • The impact of H. fraxineus infection depends on tree age, provenance or genotype, location, weather and microclimate conditions, and presence of honey fungus (Armillaria) or opportunistic secondary pathogens. Trees in forests are more likely to be more affected because of the greater prevalence of honey fungus and favourable microclimates for spore production and infection. Trees cannot recover from infection, but larger trees can survive infection for a considerable time and some might not die. [36] (CR Medium)
  • Reported mortality rates from ash dieback vary. Predicting mortality in mature trees is difficult as the disease progresses slowly. One recent analysis of data across Europe found that the maximum mortality recorded so far was~85% in plantations , ~70% in woodlands and ~82% in naturally regenerated saplings.[66] (CR Medium)
  • It is difficult to relate the European experience with ash dieback to what might happen in the UK as it is estimated ash comprises less than 1% of the total wooded area in Europe, although locally it can occupy a higher proportion. [67] (CR Medium)
  • The European experience with H. fraxineus has demonstrated that foresters have proactively felled the healthiest and therefore removed the most tolerant trees to achieve the greatest returns. In addition, some countries have reported mass felling for health and safety reasons because of basal lesions making trees liable to fall over. [36, 37, 68] (CR High)
  • The total cost of ash dieback to the UK has been estimated at £14.6 billion, based on the cost of dealing with the impacts of the disease (e.g. felling), replanting and loss of ecosystem services. [69] (CR Low)

References

  1. Kowalski, T., (2006) Chalara fraxinea sp. nov. associated with dieback of ash (Fraxinus excelsior) in Poland. Forest Pathology. 36(4), 264-270.
  2. Baral, H.O. and Bemmann, M., (2014) Hymenoscyphus fraxineus vs. Hymenoscyphus albidus – A comparative light microscopic study on the causal agent of European ash dieback and related foliicolous, stroma-forming species. Mycology. 5(4), 228-290.
  3. Nielsen, L.R., Mckinney, L.V., Hietala, A.M., and Kjær, E.D., (2017) The susceptibility of Asian, European and North American Fraxinus species to the ash dieback pathogen Hymenoscyphus fraxineus reflects their phylogenetic history. European Journal of Forest Research. 136(1), 59-73.
  4. Eppo. (2018) EPPO Global Database - Hymenoscyphus fraxineus (CHAAFR) Distribution [Online]. Available: https://gd.eppo.int/taxon/CHAAFR/distribution. Accessed: 2 January 2019.
  5. Wylder, B., Biddle, M., King, K., Baden, R., and Webber, J., (2018) Mortality dating of Fraxinus excelsior to assess when ash dieback (Hymenoscyphus fraxineus) arrived in England. Forestry 00, 1-10.
  6. Mcmullan, M., Rafiqi, M., Kaithakottil, G., Clavijo, B.J., Bilham, L., Orton, E., Percival-Alwyn, L., Ward, B.J., Edwards, A., Saunders, D.G.O., Garcia Accinelli, G., Wright, J., Verweij, W., Koutsovoulos, G., Yoshida, K., Hosoya, T., Williamson, L., Jennings, P., Ioos, R., Husson, C., Hietala, A.M., Vivian-Smith, A., Solheim, H., Maclean, D., Fosker, C., Hall, N., Brown, J.K.M., Swarbreck, D., Blaxter, M., Downie, J.A., and Clark, M.D., (2018) The ash dieback invasion of Europe was founded by two genetically divergent individuals. Nature Ecology and Evolution. 2(6), 1000-1008.
  7. Downie, J.A., (2017) Ash dieback epidemic in Europe: How can molecular technologies help? PLoS Pathogens. 13(7), 1-6.
  8. Brown, J. and Webber, J., ((in press) 2019) Population structure and natural selection in the ash dieback fungus, Hymenoscyphus fraxineus (THAPBI report). Department of Food Environment and Rural Affairs.
  9. Gross, A., Holdenrieder, O., Pautasso, M., Queloz, V., and Sieber, T.N., (2014) Hymenoscyphus pseudoalbidus, the causal agent of European ash dieback. Molecular Plant Pathology. 15(1), 5-21.
  10. Fones, H.N., Mardon, C., and Gurr, S.J., (2016) A role for the asexual spores in infection of Fraxinus excelsior by the ash-dieback fungus Hymenoscyphus fraxineus. Scientific Reports. 6, 1-10.
  11. Orton, E.S., Brasier, C.M., Bilham, L.J., Bansal, A., Webber, J.F., and Brown, J.K.M., (2018) Population structure of the ash dieback pathogen, Hymenoscyphus fraxineus, in relation to its mode of arrival in the UK. Plant Pathology. 67(2), 255-264.
  12. Kirisits, T., (2015) Ascocarp formation of Hymenoscyphus fraxineus on several-year-old pseudosclerotial leaf rachises of Fraxinus excelsior. Forest Pathology. 45(3), 254-257.
  13. Timmermann, V., Børja, I., Hietala, A.M., Kirisits, T., and Solheim, H., (2011) Ash dieback: Pathogen spread and diurnal patterns of ascospore dispersal, with special emphasis on Norway. EPPO Bulletin. 41(1), 14-20.
  14. Hietala, A.M., Timmermann, V., Børja, I., and Solheim, H., (2013) The invasive ash dieback pathogen Hymenoscyphus pseudoalbidus exerts maximal infection pressure prior to the onset of host leaf senescence. Fungal Ecology. 6(4), 302-308.
  15. Mansfield, J.W., Galambos, N., and Saville, R., (2018) The use of ascospores of the dieback fungus Hymenoscyphus fraxineus for infection assays reveals a significant period of biotrophic interaction in penetrated ash cells. Plant Pathology. 67(6), 1354-1361.
  16. Kirisits, T. and Freinschlang, C., (2011) Ash dieback caused by Hymenoscyphus pseudoalbidus in a seed plantation of Fraxinus excelsior in Austria. Journal of Agricultural Extension and Rural Development. 4(9), 184-191.
  17. Queloz, V., Grünig, C.R., Berndt, R., Kowalski, T., Sieber, T.N., and Holdenrieder, O., (2011) Cryptic speciation in Hymenoscyphus albidus. Forest Pathology. 41(2), 133-142.
  18. Solheim, H. and Hietala, A.M., (2017) Spread of ash dieback in Norway. Baltic Forestry. 23(1), 144-149.
  19. Grosdidier, M., Ioos, R., Husson, C., Cael, O., Scordia, T., and Marçais, B., (2018 in press) Tracking the invasion: dispersal of Hymenoscyphus fraxineus airborne inoculum at different scales. FEMS Microbiology Ecology.
  20. Kowalski, T. and Holdenrieder, O., (2009) Pathogenicity of Chalara fraxinea. Forest Pathology. 39(1), 1-7.
  21. Skovsgaard, J.P., Wilhelm, G.J., Thomsen, I.M., Metzler, B., Kirisits, T., Havrdová, L., Enderle, R., Dobrowolska, D., Cleary, M., and Clark, J., (2017) Silvicultural strategies for Fraxinus excelsior in response to dieback caused by Hymenoscyphus fraxineus. Forestry. 90(4), 455-472.
  22. Enderle, R., Sander, F., and Metzler, B., (2017) Temporal development of collar necroses and butt rot in association with ash dieback. IForest. 10(3), 529-536.
  23. Chandelier, A., Gerarts, F., San Martin, G., Herman, M., and Delahaye, L., (2016) Temporal evolution of collar lesions associated with ash dieback and the occurrence of Armillaria in Belgian forests. Forest Pathology. 46(4), 289-297.
  24. Marçais, B., Husson, C., Godart, L., and Caël, O., (2016) Influence of site and stand factors on Hymenoscyphus fraxineus-induced basal lesions. Plant Pathology. 65(9), 1452-1461.
  25. Enderle, R., Peters, F., Nakou, A., and Metzler, B., (2013) Temporal development of ash dieback symptoms and spatial distribution of collar rots in a provenance trial of Fraxinus excelsior. European Journal of Forest Research. 132(5-6), 865-876.
  26. Kowalski, T., Bilanski, P., and Holdenrieder, O., (2015) Virulence of Hymenoscyphus albidus and H.fraxineus on Fraxinus excelsior and F.pennsylvanica. PLoS ONE. 10(10), 1-15.
  27. Kräutler, K. and Kirisits, T., (2011) The ash dieback pathogen Hymenoscyphus pseudoalbidus is associated with leaf symptoms on ash species (Fraxinus spp.). Journal of Agricultural Extension and Rural Development. 4(9), 261-265.
  28. Madigan, A., Bełka, M., Taylor, A.F.S., Kirisits, T., Cleary, M., Nguyen, D., Elfstrand, M., and Woodward, S., (2015) Can Hymenoscyphus fraxineus infect hardy members of the Oleaceae other than ash species? Forest Pathology. 45(5), 426-429.
  29. Heinze, B., Tiefenbacher, H., Litschauer, R., and Kirisits, T., (2017) Ash dieback in Austria - history, current situation and outlook in Dieback of European Ash (Fraxinus spp.) - Consequences and Guidelines for Sustainable Management, R. Vasaitis and R. Enderle, Editors., Uppsala, Sweden: Swedish University of Agricultural Sciences. 33-53.
  30. Mckinney, L.V., Nielsen, L.R., Hansen, J.K., and Kjaer, E.D., (2011) Presence of natural genetic resistance in Fraxinus excelsior (Oleraceae) to Chalara fraxinea (Ascomycota): an emerging infectious disease. Heredity (Edinb). 106(5), 788-97.
  31. Mckinney, L.V., Nielsen, L.R., Collinge, D.B., Thomsen, I.M., Hansen, J.K., and Kjær, E.D., (2014) The ash dieback crisis: Genetic variation in resistance can prove a long-term solution. Plant Pathology. 63(3), 485-499.
  32. Kjaer, E.D., Mckinney, L.V., Nielsen, L.R., Hansen, L.N., and Hansen, J.K., (2012) Adaptive potential of ash (Fraxinus excelsior) populations against the novel emerging pathogen Hymenoscyphus pseudoalbidus. Evol Appl. 5(3), 219-28.
  33. Enderle, R., Nakou, A., Thomas, K., and Metzler, B., (2015) Susceptibility of autochthonous German Fraxinus excelsior clones to Hymenoscyphus pseudoalbidus is genetically determined. Annals of Forest Science. 72(2), 183-193.
  34. Stocks, J.J., Buggs, R.J.A., and Lee, S.J., (2017) A first assessment of Fraxinus excelsior (common ash) susceptibility to Hymenoscyphus fraxineus (ash dieback) throughout the British Isles. Sci Rep. 7(1), 16546.
  35. Villari, C., Dowkiw, A., Enderle, R., Ghasemkhani, M., Kirisits, T., Kjaer, E.D., Marciulyniene, D., Mckinney, L.V., Metzler, B., Munõz, F., Nielsen, L.R., Pilura, A., Sterner, L., Schockas, V., Rodriguez-Saona, L., Bonello, P., and Cleary, M., (2018) Advanced spectroscopy-based phenotyping offers a potential solution to the ash dieback epidemic. Scientific Reports. 8, 1-9.
  36. Orton, E., Clarke, M., Brasier, C., Webber, J., and Brown, J., (2018) A versatile method for assessing pathogenicity of Hymenoscyphus fraxineus to ash foliage. Forest Pathology. 49(2), 1-5.
  37. Schwanda, K. and Kirisits, T., (2016) Pathogenicity of Hymenoscyphus fraxineus towards leaves of three European ash species: Fraxinus excelsior, F. angustifolia and F. ornus. Plant Pathology. 65(7), 1071-1083.
  38. Munõz, F., Marçais, B., Dufour, J., and Dowkiw, A., (2016) Rising out of the Ashes: Additive genetic variation for crown and collar resistance to hymenoscyphus fraxineus in fraxinus excelsior. Phytopathology. 106(12), 1535-1543.
  39. Plumb, W.J., Coker, T.L.R., Stocks, J.J., Woodcock, P., Quine, C.P., Nemesio-Gorriz, M., Douglas, G.C., Kelly, L.J., and Buggs, R.J., ((in press)) The viability of a breeding programme for ash in the British Isles in the face of ash dieback. Plants People Planet.
  40. Semizer-Cuming, D., Finkeldey, R., Nielsen, L.R., and Kjaer, E.D., (2019) Negative correlation between ash dieback susceptibility and reproductive success: good news for European ash forests. Annals of Forest Science. 76(16).
  41. Sollars, E.S., Harper, A.L., Kelly, L.J., Sambles, C.M., Ramirez-Gonzalez, R.H., Swarbreck, D., Kaithakottil, G., Cooper, E.D., Uauy, C., Havlickova, L., Worswick, G., Studholme, D.J., Zohren, J., Salmon, D.L., Clavijo, B.J., Li, Y., He, Z., Fellgett, A., Mckinney, L.V., Nielsen, L.R., Douglas, G.C., Kjaer, E.D., Downie, J.A., Boshier, D., Lee, S., Clark, J., Grant, M., Bancroft, I., Caccamo, M., and Buggs, R.J., (2017) Genome sequence and genetic diversity of European ash trees. Nature. 541(7636), 212-216.
  42. Harper, A.L., Mckinney, L.V., Nielsen, L.R., Havlickova, L., Li, Y., Trick, M., Fraser, F., Wang, L., Fellgett, A., Sollars, E.S.A., Janacek, S.H., Downie, J.A., Buggs, R.J.A., Kjær, E.D., and Bancroft, I., (2016) Molecular markers for tolerance of European ash (Fraxinus excelsior) to dieback disease identified using Associative Transcriptomics. Scientific Reports. 6.
  43. Marzano, M., Woodcock, P., and Quine, C.P., (in press) “Bring me an [resistant] ash tree and make it snappy”: Forest manager attitudes towards resistant ash trees in the United Kingdom Biological Conservation.
  44. Sambles, C.M., Salmon, D.L., Florance, H., Howard, T.P., Smirnoff, N., Nielsen, L.R., Mckinney, L.V., Kjaer, E.D., Buggs, R.J.A., Studholme, D.J., and Grant, M., (2017) Ash leaf metabolomes reveal differences between trees tolerant and susceptible to ash dieback disease. Sci Data. 4, 170190.
  45. Stocks, J.J., Metheringham, C.L., Plumb, W.J., Lee, S.J., and Buggs, R.J., (2019 in press) Genomic basis of European ash tree resistance to ash dieback fungus.
  46. Jepson, P. and Arakelyan, I., (2017) Exploring public perceptions of solutions to tree diseases in the UK: Implications for policy-makers. Environ Sci Policy. 76, 70-77.
  47. Jepson, P.R. and Arakelyan, I., (2017) Developing publicly acceptable tree health policy: public perceptions of tree-breeding solutions to ash dieback among interested publics in the UK. Forest Policy and Economics. 80, 167-177.
  48. Havrdová, L., Zahradník, D., Romportl, D., Pešková, V., and Černý, K., (2017) Environmental and silvicultural characteristics influencing the extent of ash dieback in forest stands. Baltic Forestry. 23(1), 168-182.
  49. Lygis, V., Bakys, R., Gustiene, A., Burokiene, D., Matelis, A., and Vasaitis, R., (2014) Forest self-regeneration following clear-felling of dieback-affected Fraxinus excelsior: Focus on ash. European Journal of Forest Research. 133(3), 501-510.
  50. Department of Food Environment and Rural Affairs. (2016) Mitigation of impacts of on ash dieback in the UK – an investigation of the epidemiology and pathogenicity of Hymenoscyphus pseudoalbidus (anamorph: Chalara fraxinea) and development of methods for detection and containment of disease spread - TH0119. [Online]. Available: http://randd.defra.gov.uk/Default.aspx?Menu=Menu&Module=More&Location=None&ProjectID=18683. Accessed: 6 January 2019.
  51. Coker, T.L.R., Rozsypalek, J., Edwards, A., Harwood, T.P., Butfoy, L., and Buggs, R.J., (2019) Estimating mortality rates of European ash (Fraxinus excelsior) under the ash dieback (Hymenoscyphus fraxineus) epidemic. Plants People Planet. 1, 48-58.
  52. Hemery, G.E., (2008) Forest management and silvicultural responses to projected climate change impacts on European broadleaved trees and forests. International Forestry Review. 10(4), 591-607.
  53. Husson, C., Cael, O., Grandjean, J.P., Nageleisen, L.M., and Marçais, B., (2012) Occurrence of Hymenoscyphus pseudoalbidus on infected ash logs. Plant Pathology. 61, 889-895.
  54. Hill, L., Jones, G., Atkinson, A., Hector, A., Hemery, G.E., and Brown, N., (2019 ) Ash dieback in Britain may cost £15 billion. Current Biology. 29(9), 315-316.

Evidence summary: emerald ash borer

Pest and distribution

  • Emerald ash borer is a xylophagous buprestid beetle, Agrilus planipennis, which is native to countries of eastern Asia, including China, eastern Russia, Democratic People’s Republic of Korea, Republic of Korea, and Japan [1] (CR High)
  • The beetle has also been recorded in Mongolia, but these records are uncertain, as several authors have not reported emerald ash borer from this country, and there is also a near absence of the genus Fraxinus in Mongolia [1, 4, 47] (CR Low)
  • Emerald ash borer was first recorded outside of Asia in Michigan, USA, in September 2002, and shortly after in Ontario, Canada [1, 2] (CR High)
  • Genetic analysis indicates that this was a result of a single introduction, possibly from the Tianjin/Hebei region of China [49] (CR Medium)
  • The beetle has since spread to 34 states of the USA and 5 provinces of Canada [1] (CR High)
  • Emerald ash borer was first confirmed in Europe in Moscow, Russia, in 2005, and has now been reported within 6 km of Ukraine and 50 km of Belarus, and is likely to be present in Ukraine [3] (Forest Research personal communication, CR Medium)

Hosts

  • Emerald ash borer feeds on ash trees (Fraxinus spp.) [4] (CR High)
  • In China, the beetle is a minor and relatively rare pest of Manchurian ash (F. manchuria) and Chinese ash (F. chinensis), and mainly attacks stressed trees [4] (CR High)
  • Ash species in the USA, including Fraxinus americana, F. nigra, and F. pennsylvanica, on the other hand, are particularly susceptible [4, 5] (CR High)
  • The outbreak in and around Moscow has been mainly on F. pennsylvanica (planted as an amenity and landscaping tree). The beetle has also been found on Fraxinus excelsior (European ash) in Moscow, where it is planted in low numbers, but also in mixed-broadleaf woodland to the south where it is a co-dominant tree species [50] (CR High).
  • European ash is considered to be less susceptible than F. americana, F. nigra and F. pennsylvanica [6] (CR Medium)
  • The susceptibility of European ash infected with Hymenoscyphus fraxineus (ash dieback) is unknown (CR Low)
  • Juglans ailantifolia, J. mandshurica, Ulmus davidiana and Pterocarya rhoifolia have been reported as further hosts of the beetle in Japan, but these reports may refer to a different species of beetle, and there is no evidence that emerald ash borer can complete its lifecycle on these hosts [4, 47] (CR Low)
  • Chionanthus virginicus (white fringetree) has been recorded as a host in North America [7, 8] (CR Medium)
  • Experimental work suggests that Olea europaea (olive) is a host [9] (CR Low)

Lifecycle

  • Adults of emerald ash borer emerge in spring and summer, live for about 2-3 weeks, and feed on the foliage of ash trees [4] (CR High)
  • Adults mate, and females subsequently lay eggs (~ 68-90 per female) on the bark of ash trees, usually within crevices and cracks [4] (CR High)
  • Larvae hatch from the eggs and bore into the inner bark and outer sapwood, where they feed through the summer and autumn and produce long sinuous galleries of 10-50 cm in length, before overwintering in the fourth larval stage or prepupae [4] (CR High)
  • Pupation occurs in pupal cells in the outer sapwood or bark in the spring of the following year [4] (CR High)
  • Emerald ash borer generally has one generation per year, though some individuals may require two years, in which case the larvae continue to feed until winter of the second year, and pupation occurs in the third year [4] (CR High)
  • Studies have found the average lethal temperatures for prepupae and larvae to be -25°C and -30°C, respectively, and have found adults to be active in strong sunlight and temperatures of > 25°C. These studies suggest that climatic conditions in Europe and the UK are suitable for establishment [4, 57, 58, 59] (CR High).
  • Symptoms include D-shaped exit holes, larval galleries, discolouration of foliage, thinning, longitudinal bark splits, epicormic growth, dying branches, woodpecker damage, and dead trees [4] (CR High)

Dispersal pathways

  • Emerald ash borer is a strong flyer and typically flies in 8-12 m bursts, though longer-distance flights of over 1 km are possible [51] (CR High)
  • In flight-mills experiments, the average flight was > 3 km, with 20% of mated females able to fly > 10 km in 24 h, and 1% > 20 km [52] (CR Medium)
  • When ash trees are available in the immediate surroundings, dispersal distances tend to be lower and most emerging adults fly < 100 m [53] (CR Medium)
  • In North America, human-assisted spread has also played a significant role in spread, especially via the movement of infested firewood for camping trips [4] (CR High)
  • Ash commodities and pathways that are likely to introduce and spread the pest include ash wood (including round, sawn and fire wood, with and without bark), ash plants for planting, waste wood and scrap wood containing ash, hardwood woodchips, wood packaging material made from ash, bark products, furniture and finished wood products made from untreated ash wood, cut branches, and hitch-hiking on vehicles [4] (CR Medium).
  • It is likely that the pest will spread naturally across Europe from its centre of introduction in Moscow and, potentially rapidly and over long distances, by human-assisted transport of infested ash [4] (CR Medium).
  • The probability of detecting the beetle in Belarus, Ukraine, Estonia, Latvia, and Lithuania as a result of spread from Russia by 2022 is 15%–40% [56] (CR Medium)

Impacts

  • Trees are generally killed within 4 years of infestation, and within 1-2 years in some cases [4] (CR High)
  • Tens of millions of trees have been killed in North America [4] (CR High)
  • Timber and other forestry products have been lost, ecosystem services, such as water regulation, have been impoverished, and social benefits like shading, recreation and cultural traditions have been affected [4] (CR High)
  • In 2010, the cost of treating, removing, and replacing 17 million ash trees across 25 states of the USA was estimated to be €7.9 billion, while a study in 2012 estimated the cost of removing and replacing ash in Canada would be €332-1476 million over a 30 year period [54, 55] (CR Medium)
  • Impacts are also likely to be high in the UK [10] (CR Medium)

Prevention

  • Emerald ash borer is a IAI EU listed pest, which means that it is banned from being introduced, and spread within, all EU member states [11] (CR High)
  • Wood (of certain types), wood chips, particles, sawdust, shavings, wood waste and scrap, isolated bark and objects made of bark, plants including cut branches, and furniture and other objects made of untreated wood, of Fraxinus spp., Juglans ailantifolia, Juglans mandshurica, Ulmus davidiana and Pterocarya rhoifolia, originating in Canada, China, Democratic People’s Republic of Korea, Japan, Mongolia, Republic of Korea, Russia, Taiwan and USA, must come from a Pest Free Area [11] (CR High)
  • Wood (of certain types) may also be treated by removing the bark and outer sapwood or using ionizing radiation, as an alternative to a Pest Free Area [11] (CR High)
  • Wood packaging material from third countries must be debarked, treated and marked in line with the International Standard of Phytosanitary Measures No. 15 [11] (CR High)
  • Inspections are required in the exporting country for all plants for planting from third countries, as well as wood (of certain types), bark, and cut branches, of Fraxinus spp., Juglans ailantifolia, Juglans mandshurica, Ulmus davidiana and Pterocarya rhoifolia, originating in Canada, China, Democratic People’s Republic of Korea, Japan, Mongolia, Republic of Korea, Russia, Taiwan and USA [11] (CR High)
  • Importation of Fraxinus plants intended for planting into Britain from any third country or member state must come from an area free from Hymenoscyphus fraxineus (ash dieback) [12] (CR High)

Detection and surveillance

  • Because of the cryptic lifecycle of the beetle and the delay in observable symptoms, visual surveillance from the ground or by air is not likely to be effective for early detection [4, 13] (CR High)
  • The use of girdled trees is a very sensitive method of detection, but is also invasive. Girdled trees are used regularly in the USA [14, 15, 16] (CR High).
  • Subsampling, either by branch sampling or trunk windows, is also a sensitive method of detection, but less sensitive than girdling. Branch sampling is regularly used in Canada [13, 17] (CR High).
  • In the USA, purple prism traps baited with (3Z)-hexanol, and to a lesser extent Manuka oil and Phoebe oil, are used, while in Canada, green prism traps baited with (3Z)-hexenol are preferred [16, 18, 19, 20, 21] (CR High)
  • Double decker traps may be more effective at detecting emerald ash borer at lower levels of infestation than prism traps [19, 22] (CR Medium)
  • Biosurveillance using hymenopteran wasps could be used [16, 17, 23] (CR Medium)
  • Sniffer dogs have potential for use in a surveillance programme [4, 24] (CR Medium)

Management

  • Eradication of emerald ash borer is only likely to be possible for localised outbreaks where the beetle has not had time to spread [4] (CR High)
  • Despite intensive management and attempts to restrict long-distance spread, it has not been possible to eradicate the pest after its introduction to North America (both the USA and Canada) [4] (CR High)
  • The principle method of controlling emerald ash borer in an eradication programme is through the felling of ash trees and restricting the movement of susceptible material, as instructed in EPPO standard 9/14 [25] (CR High)
  • Injecting the tree with the insecticide emamectin benzoate (Tree-Äge and Arborjet) provides 2-3 years of protection for an ash tree from one application, and is used regularly in the USA [26, 27] (CR High)
  • Treating a small proportion of ash trees with emamectin benzoate in a woodland has been shown to reduce the progression of ash decline across the woodland [48] (CR Medium)
  • Injecting the tree with the insecticide azadirachtin (Treeazin) provides 1-2 years of protection for an ash tree from one application, and is used regularly in Canada [21, 28] (CR High)
  • Neither emamectin benzoate or azadirachtin are approved for use as a tree injection in the UK [29] (CR High)
  • Because of the cost, chemical treatments are generally limited for use on high value trees, such as those in urban areas or those of historical interest [4] (CR High)
  • Biopesticides have been investigated, but do not provide good coverage as sprays and need to be regularly reapplied, and are therefore not used in the USA or Canada [17] (CR High)
  • Two native parasitoids in the USA, Atanycolus cappaerti and Phasgonophora sulcata, have exhibited high parasitism of emerald ash borer and show potential for use in a control programme [30, 31] (CR Medium)
  • Four non-native parasitoids from Asia have been released in the USA, including the larval parasitoids Tetrastichus planipennisi, Spathius agrili and S. galinae, and the egg parastioid Oobius agrili, and are potentially having a positive impact on ash recovery [17, 32, 33, 34, 35, 36, 37] (CR High)
  • Spathius polonicus, a European parasitoid of emerald ash borer identified in Russia, may also be of value [38] (CR Medium)
  • Movement restrictions of ash trees, branches, logs and firewood, have been accompanied by a public awareness campaign in the USA and have shown value in reducing spread [39, 40] (CR Medium)
  • A multiagency project in North America called SLow Ash Mortality (SLAM) incorporates a number of different control techniques to slow the progression of ash loss in recent infestation and outlier sites [41, 42] (CR High)
  • Resistance/tolerance to emerald ash borer varies between ash species, and F. mandshurica, F. platypoda, F. chinensis, F. baroniana, and F. floribunda are able to kill emerald ash borer larvae that enter their trunks [6] (CR Medium)
  • Candidate alleles for resistance/tolerance have been identified in F. mandshurica, F. platypoda, F. baroniana, and F. floribunda, including those in the phenylpropanoid and flavonoid synthesis pathways. These could be searched for in the UK’s ash population, assisting a breeding programme [6] (CR Medium)
  • In the USA, ecosystem structure of some ash dominated forests is likely to be lost [43] (CR Medium)
  • Ecosystem structure can be preserved to a degree by encouraging natural regeneration of non-ash species using appropriate silvicultural techniques and/or by additional planting of non-ash species [44, 45, 46] (CR High)

References

  1. EPPO (2018) Agrilus planipennis (AGRLPL) [Online]. Available: https://gd.eppo.int/taxon/AGRLPL/distribution. Accessed: 30/01/2019.
  2. EPPO Reporting Service (2003) Introduction of Agrilus planipennis (Emerald Ash Borer) into North America: addition to the EPPO Alert List [Online]. Available: https://gd.eppo.int/reporting/article-2066. Accessed: 30/01/2019.
  3. EPPO Reporting Service (2007) First report of Agrilus planipennis in the region of Moscow, Russia [Online]. Available: https://gd.eppo.int/reporting/article-1038. Accessed: 30/01/2019.
  4. EPPO (2013a) Pest Risk Analysis for Agrilus planipennis [Online]. Available: https://gd.eppo.int/taxon/AGRLPL/documents. Accessed: 10/01/2019.
  5. Klooster, W. S., Herms, D. A., Knight, K. S., Herms, C. P. and McCullough, D. G. (2014) Ash (Fraxinus spp.) mortality, regeneration, and seed bank dynamics in mixed hardwood forests following invasion by emerald ash borer (Agrilus planipennis). Biological Invasions.16, 859–873.
  6. Kelly, L. J., Plumb, W. J., Carey, D., Mason, M., Cooper, E. D., Crowther, W., Whittemore, A. T., Rossiter, S. J., Koch, J., Buggs, R. J. A. (in prep.) Genes for ash tree resistance to an insect pest identified via comparative genomics.
  7. Cipollini, D. (2015) White fringetree as a novel larval host for emerald ash borer. Journal of Economic Entomology. 108, 370-375.
  8. Cipollini, D. and Rigsby, C. M. (2015) Incidence of infestation and larval success of emerald ash borer (Agrilus planipennis) on white fringetree (Chionanthus virginicus), Chinese fringetree (Chionanthus retusus), and devilwood (Osmanthus americanus). Environmental Entomology. 44, 1375-1383.
  9. Cipollini, D., Rigsby, C. M. and Peterson, D. L. (2017) Feeding and Development of Emerald Ash Borer (Coleoptera: Buprestidae) on Cultivated Olive, Olea europaea. Journal of Economic Entomology. 110, 1935-1937.
  10. Defra (2019) UK Risk Register details for Agrilus planipennis [Online]. Available: https://secure.fera.defra.gov.uk/phiw/riskRegister/viewPestRisks.cfm?cslref=25310. Accessed: 30/01/2019.
  11. EU (2018) Council Directive 2000/29/EC [Online]. Available: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:02000L0029-20180401. Accessed: 30/01/2019.
  12. Plant Health Order (2015) [Online]. Available: http://www.legislation.gov.uk/uksi/2015/610/pdfs/uksi_20150610_en.pdf. Accessed: 30/01/2019.
  13. Ryall, K. L., Fidgen, J. G., Turgeon, J. J. (2010) Detection of emerald ash borer in urban environments using branch sampling. Frontline. Technical Note No. 111.
  14. Cappaert, D., McCullough, D. G., Poland, T. M. and Siegert, N. W. (2005) Emerald ash borer in North America: A research and regulatory challenge. American Entomologist, 51, 152-165.
  15. Mercader, R. J., McCullough, D. G. and Bedford, J. M. (2013) A comparison of girdled ash detection trees and baited artificial traps for Agrilus planipennis (Coleoptera: Buprestidae) detection. Environmental Entomology. 42, 1027-1039.
  16. Ryall, K. (2015) Detection and sampling of emerald ash borer (Coleoptera: Buprestidae) infestations. Canadian Entomologist. 147, 290-299.
  17. Down, R. and Audsley, N. (2017) Review of the Control and Management Strategies for Emerald Ash Borer (Agrilus planipennis). Internal document.
  18. Crook, D. J. and Mastro, V. C. (2010) Chemical ecology of the emerald ash borer Agrilus planipennis. Journal of Chemical Ecology. 36, 101-112.
  19. Poland, T. M. and McCullough, D. G. (2014) Comparison of trap types and colors for capturing emerald ash borer adults at different population densities. Environmental Entomology. 43, 157-170.
  20. Emerald Ash Borer Information Network (2019) Emerald Ash Borer Information Network [Online]. Available: http://www.emeraldashborer.info/. Accessed: 10/01/2019.
  21. Herms, D. A. and McCullough, D. G. (2014) Emerald Ash Borer Invasion of North America: History, Biology, Ecology, Impacts, and Management, Vol. 59: Annual Review of Entomology, Vol 59: 13-30.
  22. Poland, T. M., McCullough, D. G. and Anulewicz, A. C. (2011) Evaluation of double decker traps for emerald ash borer (Coleoptera: Buprestidae). Journal of Economic Entomology. 104, 517-531.
  23. Swink, W. G., Paiero, S. M. and Nalepa, C. A. (2013) Buprestidae collected as prey by the solitary, ground-nesting philanthine wasp Cerceris fumipennis (Hymenoptera: Crabronidae) in North Carolina. Annals of the Entomological Society of America. 106, 111-116.
  24. Hoyer-Tomiczek, U. (2012) Sniffer dogs to find Anoplophora spp. infested plants. In: “Anoplophora chinensis & Anoplophora glabripennis: new tools for predicting, detecting and fighting”. How to save our forests and our urban green spaces. Milan, 9-11 May 2012.
  25. EPPO (2013b) PM 9/14 (1) Agrilus planipennis: procedures for official control. EPPO Bulletin. 43, 499-509.
  26. McCullough, D. G., Poland, T. M., Anulewicz, A. C., Lewis, P. and Cappaert, D. (2011) Evaluation of Agrilus planipennis (Coleoptera: Buprestidae) control provided by emamectin benzoate and two neonicotinoid insecticides, one and two seasons after treatment. Journal of Economic Entomology. 104, 1599-1612.
  27. Poland, T. M., Ciaramitaro, T. M. and McCullough, D. G. (2016) Laboratory evaluation of the toxicity of systemic insecticides to emerald ash borer larvae. Journal of Economic Entomology. 109, 705-716.
  28. McKenzie, N., Helson, B., Thompson, D., Otis, G., McFarlane, J., Buscarini, T. and Meating, J. (2010) Azadirachtin: an effective systemic insecticide for control of Agrilus planipennis (Coleoptera: Buprestidae). Journal of Economic Entomology 103: 708-717.
  29. HSE (2019) Pesticides Register of UK Authorised Products [Online]. Available: https://secure.pesticides.gov.uk/pestreg/. Accessed: 30/01/2019.
  30. Cappaert, D. and McCullough, D. G. (2009) Occurrence and seasonal abundance of Atanycolus cappaerti (Hymenoptera: Braconidae) a native parasitoid of emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae). The Great Lakes Entomologist. 42, 16-29.
  31. Lyons, D. B. (2008) Emerald ash borer: it’s here to stay, let’s learn how to manage it. Forest Health and Biodiversity Newsletter. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario.
  32. Bauer, L. S., Duan, J. J., Lelito, J. P., Liu, H. and Gould, J. R. (2015) Biology of emerald ash borer parasitoids, In: Van Driesche RG, Reardon RC (Eds.) Biology and control of emerald ash borer. USDA-FS FHTET-2014-09. Chapter 4 pp. 97-112.
  33. Gould, J. R., Bauer, L. S., Duan, J. J., Williams, D. and Liu, H. (2015) History of emerald ash borer control. In: Van Driesche RG, Reardon RC (Eds.) Biology and control of emerald ash borer. USDA-FS FHTET-2014-09. Chapter 4 pp. 83-95.
  34. Duan, J. J., Bauer, L. S. and van Driesche, R. G. (2017) Emerald ash borer biocontrol in ash saplings: The potential for early stage recovery of North American ash trees. Forest Ecology and Management. 394, 64-72.
  35. Duan, J. J., Bauer, L. S., van Driesche, R. G. and Gould, J. R. (2018) Progress and Challenges of Protecting North American Ash Trees from the Emerald Ash Borer Using Biological Control. Forests. 9, 142.
  36. Kashian, D. M., Bauer, L. S., Spie, B. A., Duan, J. J. and Gould, J. R. (2018) Potential Impacts of Emerald Ash Borer Biocontrol on Ash Health and Recovery in Southern Michigan. Forests. 9, 296.
  37. Margulies, E., Bauer, L. and Ibáñez, I. (2017) Buying Time: Preliminary Assessment of Biocontrol in the Recovery of Native Forest Vegetation in the Aftermath of the Invasive Emerald Ash Borer. Forests. 8, 369.
  38. Orlova-Bienkowskaja, M. J. (2015) Cascading ecological effects caused by the establishment of the emerald ash borer Agrilus planipennis (Coleoptera: Buprestidae) in European Russia. European Journal of Entomology. 112, 778-789.
  39. Diss-Torrance, A., Peterson, K. and Robinson, C. (2018) Reducing Firewood Movement by the Public: Use of Survey Data to Assess and Improve Efficacy of a Regulatory and Educational Program, 2006–2015. Forests. 9, 90.
  40. Haack, R. A., Jendek, E., Houping, L., Marchant, K. R., Petrice, T. R., Poland, T. M. and Hui, Y. (2002) The emerald ash borer: a new exotic pest in North America. Newsletter of the Michigan Entomological Society. 47, 1– 5.
  41. McCullough, D. G. and Mercader, R. J. (2012) Evaluation of potential strategies to SLow Ash Mortality (SLAM) caused by emerald ash borer (Agrilus planipennis): SLAM in an urban forest. International Journal of Pest Management. 58, 9-23.
  42. Poland, T. M. and McCullough, D. G. (2010) SLAM: A multi-agency pilot project to SL.ow A.sh M.ortality caused by emerald ash borer in outlier sites. Newsletter of the Michigan Entomological Society. 55, 4-8.
  43. Slesak, R. A., Lenhart, C. F., Brooks, K. N., D’Amato, A. W. and Palik, B. J. (2014) Water table response to harvesting and simulated emerald ash borer mortality in black ash wetlands in Minnesota, USA. Canadian Journal of Forest Research. 44, 961–968.
  44. D’Amato, A. W., Palik, B. J., Slesak, R. A., Edge, G., Matula, C. and Bronson, D. R. (2018) Evaluating Adaptive Management Options for Black Ash Forests in the Face of Emerald Ash Borer Invasion. Forests. 9, 348.
  45. Looney, C. E., D’Amato, A. W., Palik, B. J. and Slesak, R. A. (2015) Overstory treatment and planting season affect survival of replacement tree species in emerald ash borer threatened Fraxinus nigra forests in Minnesota, USA. Canadian Journal of Forest Research. 45, 1728–1738.
  46. WDNR (2019) Silviculture trials [Online]. Available: https://dnr.wi.gov/topic/forestmanagement/silviculturetrials.html. Accessed: 11/01/2019.
  47. Orlova-Bienkowskaja, M. J. and Volkovitsh, M. G. (2018) Are native ranges of the most destructive invasive pests well known? A case study of the native range of the emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae). Biological Invasions. 20, 1275-1286.
  48. Mercader, R. J., McCullough, D. G., Storer, A. J., Bedford, J. M., Heyd, R., Poland, T. M. and Katovich, S. (2015) Evaluation of the potential use of a systemic insecticide and girdled trees in area wide management of the emerald ash borer. Forest Ecology and Management. 350, 70-80.
  49. Bray, A. M., Bauer, L. S., Poland, T. M., Haack, R. A., Cognato, A. I., and Smith, J. J. (2011) Genetic analysis of emerald ash borer (Agrilus planipennis Fairmaire) populations in Asia and North America. Biological Invasions. 13, 2869–2887.
  50. Straw, N. A., Williams, D. T., Kulinich, O., and Gninenko, Y. I. (2013) Distribution, impact and rates of spread of emerald ash borer, Agrilus planipennis (Coleoptera; Buprestidae) in the Moscow region of Russia. Forestry. 86, 515–522.
  51. Haack, R. A., Jendek, E., Liu, H., Marchant, K. R., Petrice, T. R., Poland, T. M. and Ye H. (2002) The emerald ash borer: a new exotic pest in North America. Newsletter of the Michigan Entomological Society. 47, 1-5.
  52. Taylor, R. A. J., Bauer, L. S., Poland, T. M. and Windell, K. N. (2010) Flight performance of Agrilus planipennis (Coleoptera: Buprestidae) on a flight mill and in free flight. Journal of Insect Behaviour. 23, 128–148.
  53. Mercader, R. J., Siegert, N. W., Liebhold, A. M. and McCullough, D. G. (2009) Dispersal of the emerald ash borer, Agrilus planipennis, in newly-colonized sites. Agricultural and Forest Entomology. 11, 421–424.
  54. Kovacs, K. F., Haight, R. G., McCullough, D. G., Mercader, R. J., Siegert, N. W. and Liebhold, A. M. (2010) Cost of potential emerald ash borer damage in U.S. communities, 2009–2019. Ecological Economics. 69, 569–578.
  55. McKenney, D. W., Pedlar, J. H., Yemshanov, D., Lyons, D. B., Campbell, K. L., Lawrence, K. (2012) Estimates of the potential cost of emerald ash borer (Agrilus planipennis Fairmaire) in Canadian municipalities. Arboriculture & Urban Forestry Online 38, No. 3.
  56. Orlova-Bienkowskaja, M. J. and Bieńkowski, A. O. (2018) Modeling long‐distance dispersal of emerald ash borer in European Russia and prognosis of spread of this pest to neighboring countries within next 5 years. Ecology and Evolution. 8, 9295-9304.
  57. Crosthwaite, J. C., Sobek, S., Lyons, D. B., Bernards, M. A. and Sinclair, B. J. (2011) The overwintering physiology of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae). Journal of Insect Physiology. 57, 166–173.
  58. Venette, R. C. and Abrahamson, M. (2010) Cold hardiness of emerald ash borer, Agrilus planipennis: a new perspective. In: Black Ash Symposium: Proceedings of the Meeting; May 25-27, 2010. Bemidji, MN. US Department of Agriculture, Forest Service, Chippewa National Forest.
  59. Wang, X. Y., Yang, Z. Q., Gould, J. R., Zhang, Y. N., Liu, G. J. and Liu, E. S. (2010) The biology and ecology of the emerald ash borer, Agrilus planipennis, in China. Journal of Insect Science. 10, 128.
Back to top