Ashes in Europe are in danger: the invasive range of Agrilus planipennis in European Russia is expanding

The emerald ash borer, Agrilus planipennis (Coleoptera, Buprestidae), is a pest of ash native to Asia. This major stem borer has killed millions of ash trees in North America. It was first found in Europe in 2003 in the city of Moscow. Now it is rapidly spreading in European Russia. In 2012 A. planipennis was found in the Tula, Kaluga, and Smolensk regions. A survey of green plantations in 22 localities in 2013 has revealed that A. planipennis occurs also in the Tver, Orel, Voronezh, Tambov, and Yaroslavl regions. It occurs 230 km northeast, 350 km southeast, and 460 km south from Moscow. Most ashes in the Moscow region, both alien American Fraxinus pennsylvanica and the indiginous European ash Fraxinus excelsior, are dying or already dead. Thousands of trees in other regions are seriously damaged. The pest will cross the western border of Russia soon. It represents a serious threat for ashes in other European countries.     

Biology and damage traits of emerald ash borer planipennis Fairmaire）in China

Emerald ash borer （Agrilus planipennis Fairmaire） （Coleoptera： Buprestidae） is a major stem borer of ash （Fraxinus spp.）. It is univoltine in Tianjin, while it is semivoltine in Heilongjiang Province, and both univoltine and semivoltine in Changchun, Jilin Province, where the majority is univoltine. The longevity of emerald ash borer adults is 17.2 ± 4.6 days （n = 45）, eggs 9.0 5：1.1 days （n = 103）, univoltine larvae 308 days, semivoltine larvae 673 days, and pupae 61.2 ± 1.6 days （n = 45）. It takes about 100 days from the time larvae bore into the phloem to when they complete the pupal cell. In a 10-year-old velvet ash （Fraxinus velutina Tort.） plantation in Tianjin, emerald ash borer preferred to oviposit on the regions of boles from 50-150 cm above ground, accounting for 76.7% of the total girdling. Girdling on the south side of the tree boles accounted for 43.40% of the total girdling. The emerald ash borer population density is higher at the edge of the plantation compared with the center.     

The overwintering physiology of the emerald ash borer, Agrilus planipennis fairmaire (coleoptera: buprestidae)

Ability to survive cold is an important factor in determining northern range limits of insects. The emerald ash borer (Agrilus planipennis) is an invasive beetle introduced from Asia that is causing extensive damage to ash trees in North America, but little is known about its cold tolerance. Herein, the cold tolerance strategy and mechanisms involved in the cold tolerance of the emerald ash borer were investigated, and seasonal changes in these mechanisms monitored. The majority of emerald ash borers survive winter as freeze-intolerant prepupae. In winter, A. planipennis prepupae have low supercooling points (∼−30 °C), which they achieve by accumulating high concentrations of glycerol (∼4 M) in their body fluids and by the synthesis of antifreeze agents. Cuticular waxes reduce inoculation from external ice. This is the first comprehensive study of seasonal changes in cold tolerance in a buprestid beetle.     

Regional assessment of emerald ash borer, <Emphasis Type="Italic">Agrilus planipennis</Emphasis>, impacts in forests of the Eastern United States

Native to Asia, the emerald ash borer (Agrilus planipennis Fairmaire) has caused extensive mortality of ash tree species (Fraxinus spp.) in the eastern United States. As of 2013, the pest was documented in 18 % of counties within the natural range of ash in the eastern United States. Regional forest inventory data from the U.S. Forest Service Forest Inventory and Analysis program were used to quantify trends in ash mortality rate and volume per hectare relative to the year of initial emerald ash borer detection. Results indicate that the annual ash mortality rate increases by as much as 2.7 % per year after initial detection of the pest in a county. Corresponding decreases in ash volume (as much as 1.8 m³ per hectare per year) continue for several more years until most live ash is killed. These results, while not necessarily representative of the effects on ash in urban ecosystems, document the severe impact this invading herbivore is having on forests as it expands its range in North America.     

Core RNAi machinery and gene knockdown in the emerald ash borer (Agrilus planipennis)

The RNA interference (RNAi) technology has been widely used in insect functional genomics research and provides an alternative approach for insect pest management. To understand whether the emerald ash borer (Agrilus planipennis), an invasive and destructive coleopteran insect pest of ash tree (Fraxinus spp.), possesses a strong RNAi machinery that is capable of degrading target mRNA as a response to exogenous double-stranded RNA (dsRNA) induction, we identified three RNAi pathway core component genes, Dicer-2, Argonaute-2 and R2D2, from the A. planipennis genome sequence. Characterization of these core components revealed that they contain conserved domains essential for the proteins to function in the RNAi pathway. Phylogenetic analyses showed that they are closely related to homologs derived from other coleopteran species. We also delivered the dsRNA fragment of AplaScrB-2, a β-fructofuranosidase-encoding gene horizontally acquired by A. planipennis as we reported previously, into A. planipennis adults through microinjection. Quantitative real-time PCR analysis on the dsRNA-treated beetles demonstrated a significantly decreased gene expression level of AplaScrB-2 appearing on day 2 and lasting until at least day 6. This study is the first record of RNAi applied in A. planipennis.     

Occurrence of emerald ash borer (Coleoptera: Buprestidae) and biotic factors affecting its immature stages in the Russian Far East

Field surveys were conducted from 2008 to 2011 in the Khabarovsk and Vladivostok regions of Russia to investigate the occurrence of emerald ash borer, Agrilus planipennis Fairmaire, and mortality factors affecting its immature stages. We found emerald ash borer infesting both introduced North American green ash (Fraxinus pennsylvanica Marshall) and native oriental ashes (F. mandshurica Rupr. and F. rhynchophylla Hance) in both regions. Emerald ash borer densities (larvae/m(2) of phloem area) were markedly higher on green ash (11.3-76.7 in the Khabarovsk area and 77-245 in the Vladivostok area) than on artificially stressed Manchurian ash (2.2) or Oriental ash (10-59). Mortality of emerald ash borer larvae caused by different biotic factors (woodpecker predation, host plant resistance and/or undetermined diseases, and parasitism) varied with date, site, and ash species. In general, predation of emerald ash borer larvae by woodpeckers was low. While low rates (3-27%) of emerald ash borer larval mortality were caused by undetermined biotic factors on green ash between 2009 and 2011, higher rates (26-95%) of emerald ash borer larval mortality were caused by putative plant resistance in Oriental ash species in both regions. Little (<1%) parasitism of emerald ash borer larvae was observed in Khabarovsk; however, three hymenopteran parasitoids (Spathius sp., Atanycolus nigriventris Vojnovskaja-Krieger, and Tetrastichus planipennisi Yang) were observed attacking third - fourth instars of emerald ash borer in the Vladivostok area, parasitizing 0-8.3% of emerald ash borer larvae infesting Oriental ash trees and 7.3-62.7% of those on green ash trees (primarily by Spathius sp.) in two of the three study sites. Relevance of these findings to the classical biological control of emerald ash borer in newly invaded regions is discussed.     

The life cycle of the emerald ash borer Agrilus planipennis in European Russia and comparisons with its life cycles in Asia and North America

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Long-term monitoring of the introduced emerald ash borer (Coleoptera: Buprestidae) egg parasitoid,Oobius agrili (Hymenoptera: Encyrtidae), in Michigan,USA and evaluation of a newly developed monitoring technique

Emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), is a serious invasive pest of ash trees (Fraxinus spp.) in North America from China. The egg parasitoid Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae) was introduced from China as a biological control agent for this pest in Michigan and throughout the infested area of the United States. A critical component of any biological control program is post-release monitoring and evaluation; however, because of the small size and cryptic nature of O. agrili, evaluation of its impact is difficult. We compared two methods for measuring parasitism of emerald ash borer eggs: (1) timed visual searches of bark on standing ash trees and (2) bark collection, sifting, and sorting. Both methods were carried out in paired parasitoid-release and control plots, the visual search method over a six-year period (2008–2013) and the more recently developed bark-collection and sifting method for 2 years (2012–2013). The visual search method found parasitism in release plots remained low (0.7–4.2%) in samples taken from 2008 to 2012 and reached 10.6% in 2013. In comparison, the bark-sifting method found that rates of egg parasitism were considerably higher in release plots, 21.8% and 18.9% for samples taken in 2012 and 2013, respectively. These findings indicate that the population-level impact of O. agrili is increasing and may be an important source of mortality for EAB populations. We recommend the bark-collection and sifting method as the more effective method to recover parasitoids and estimate parasitism rates of O. agrili.     

Rail transport as a vector of emerald ash borer

1. The emerald ash borer (EAB) Agrilus planipennis Fairmaire (Coleoptera: Buprestidae) is an invasive woodboring beetle native to northeastern Asia that continues to expand its range within North America and European Russia. The insect reproduces within and kills most North American species of ash Fraxinus spp.
2. Because both the adult and larval life stages of EAB are difficult to detect prior to development of tree symptoms, much work has focused on quantifying spread and clarifying the potential movement pathways to improve early detection and monitoring strategies.
3. In the present study, we retrospectively analyzed county‐level infestations of emerald ash borer in the state of Iowa, U.S.A., subsequent to the initial detection of EAB in 2010. Visual data analysis had suggested that new infestations were not in accordance with the expected patterns of establishment along roads, near campgrounds or by large population centres.
4. We found a positive correlation between the establishment and detection of EAB in Iowa counties and the length of railroads in each county. To our knowledge, this is the first statistically significant association between rail pathways and the spread of EAB on the North American continent.

     

Patterns in the within-tree distribution of the emerald ash borer Agrilus planipennis (Fairmaire) in young, green-ash plantations of south-western Ontario, Canada

1 The emerald ash borer Agrilus planipennis Fairmaire (Coleoptera: Buprestidae) is a serious exotic pest of ash trees (Fraxinus spp.) in North America, and is responsible for the deaths of millions of trees in Ontario and Michigan. One of the greatest challenges facing the successful management of the pest is the ability to accurately detect its presence in a tree. 2 Observations were made on A. planipennis larval feeding galleries found within 65 young, green‐ash trees cut from plantations in Essex County, Ontario, Canada. The within‐tree distributions of feeding galleries were described in relation to height‐above‐ground, stem diameter, bark thickness and stem aspect. 3 Galleries were not distributed randomly or evenly; minimum boundaries of stem diameter and bark thickness and a maximum boundary of height‐above‐ground were detected. Indications of maximum boundaries for stem diameter and bark thickness were also observed. Galleries were found most often on the south‐west side of the tree. 4 Using the technique of upper boundary regression, we were able to identify significant quadratic relationships between A. planipennis gallery density and stem diameter and bark thickness, as well as a significant negative linear relationship between gallery density and height‐above‐ground. 5 Agrilus planipennis gallery density in newly‐infested trees was lower than in previously‐infested trees, and was observed to peak at smaller stem diameters and bark thicknesses than in previously‐infested trees. 6 Survey teams would increase their probability of detecting new A. planipennis infestations by initiating searches for exit holes and feeding galleries in trunk sections and branches of approximately 7 cm in diameter.     

Effects of grafting on host plant resistance in ash (Fraxinus spp.) to emerald ash borer (Agrilus planipennis Fairmaire)

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Genome‐wide SNP identification in Fraxinus linking genetic characteristics to tolerance of Agrilus planipennis

Ash (Fraxinus spp.) is one of the most widely distributed tree genera in North America. Populations of ash in the United States and Canada have been decimated by the introduced pest Agrilus planipennis (Coleoptera: Buprestidae; emerald ash borer), having negative impacts on both forest ecosystems and economic interests. The majority of trees succumb to attack by A. planipennis, but some trees have been found to be tolerant to infestation despite years of exposure. Restriction site‐associated DNA (RAD) sequencing was used to sequence ash individuals, both tolerant and susceptible to A. planipennis attack, in order to identify single nucleotide polymorphism (SNP) patterns related to tolerance and health declines. de novo SNPs were called using SAMtools and, after filtering criteria were implemented, a set of 17,807 SNPs were generated. Principal component analysis (PCA) of SNPs aligned individual trees into clusters related to geography; however, five tolerant trees clustered together despite geographic location. A subset of 32 outlier SNPs identified within this group, as well as a subset of 17 SNPs identified based on vigor rating, are potential candidates for the selection of host tolerance. Understanding the mechanisms of host tolerance through genome‐wide association has the potential to restore populations with cultivars that are able to withstand A. planipennis infestation. This study was successful in using RAD‐sequencing in order to identify SNPs that could contribute to tolerance of A. planipennis. This was a first step toward uncovering the genetic basis for host tolerance to A. planipennis. Future studies are needed to identify the functionality of the loci where these SNPs occur and how they may be related to tolerance of A. planipennis attack.     

Developing a non-sticky trap design for monitoring jewel beetles

There is an urgent need in Europe to prepare resources for the arrival of the emerald ash borer, Agrilus planipennis (Buprestidae, Coleoptera) from European Russia, and possibly other invasive jewel beetles. A lightweight, easy to handle, non-sticky trap could facilitate monitoring and detection to derive information about emerald ash borer and other jewel beetle populations. In two experiments carried out over two consecutive years in an oak forest, a new non-sticky multi-funnel trap design with a light-green (sometimes described as fluorescent yellow) visual cue was developed. Altogether, there were 238 (2018) and 194 (2019) specimens captured often (2018) and eight (2019) Agrilus species, eight of which are oak-related and one (A. convexicollis) was linked to ash. The new light-green multi-funnel trap performed similarly to the sticky design with a similar coloured surface. Our results suggest that the new trap design may be suitable for catching a wide range of buprestid species. It may also have the potential to be further optimized with respect to visual and olfactory cues, which would provide an even more useful tool for monitoring both invasive and indigenous buprestids.     

Ash (Fraxinus spp.) mortality,regeneration, and seed bank dynamics in mixed hardwood forests following invasion by emerald ash borer (Agrilus planipennis)

Emerald ash borer (EAB; Agrilus planipennis) has killed millions of ash trees and threatens ash throughout North America, and long-term persistence of ash will depend on the potential for regeneration. We quantified ash demography, including mortality and regeneration, of Fraxinus americana (white ash), Fraxinus pennsylvanica (green ash), and Fraxinus nigra (black ash) in mixed hardwood forests near the epicenter of the EAB invasion in southeastern Michigan and throughout Ohio. Plots were established across a gradient of ash densities. Ash was the most important species in hydric sites, and ranked second among all species in mesic and xeric sites. In sites nearest the epicenter in Michigan, ash mortality exceeded 99 % by 2009, and few or no newly germinated ash seedlings were observed, leaving only an “orphaned cohort” of established ash seedlings and saplings. As ash mortality increased, the number of viable ash seeds in soil samples decreased sharply, and no viable seeds were collected in 2007 or 2008. In Ohio sites farther from the epicenter, densities of new ash seedlings were much higher in plots with healthy ash trees compared to plots where trees had died. EAB was still present in low densities in Michigan and Ohio stands in 2012 where average mortality of ash was nearly 100 %. The future of ash at these sites will depend on the outcome of the dynamic interaction between the orphaned cohort of previously established ash seedlings and saplings and low density EAB populations.     

Influence of foraging behavior and host spatial distribution on the localized spread of the emerald ash borer, <Emphasis Type="Italic">Agrilus planipennis</Emphasis>

Management programs for invasive species are often developed at a regional or national level, but physical intervention generally takes place over relatively small areas occupied by newly founded, isolated populations. The ability to predict how local habitat variation affects the expansion of such newly founded populations is essential for efficiently targeting resources to slow the spread of an invasive species. We assembled a coupled map lattice model that simulates the local spread of newly founded colonies of the emerald ash borer (Agrilus planipennis Fairmaire), a devastating forest insect pest of ash (Fraxinus spp.) trees. Using this model, we investigated the spread of A. planipennis in environments with different Fraxinus spp. distributions, and explored the consequences of ovipositional foraging behavior on the local spread of A. planipennis. Simulations indicate that increased larval density, resulting from lower host tree density or higher initial population sizes, can increase the spread rate during the first few years after colonization by increasing a density-dependent developmental rate and via host resource depletion. Both the radial spread rate and population size were greatly influenced by ovipositional foraging behavior. Two known behaviors of ovipositing A. planipennis females, attraction towards areas with high ash tree density and attraction to stressed trees, had opposing effects on spread. Results from this model illustrate the significant influence of resource distribution and foraging behavior on localized spread, and the importance of these factors when formulating strategies to monitor and manage invasive pests.     

Responses of two parasitoids,the exotic Spathius agrili Yang and the native Spathius floridanus Ashmead,to volatile cues associated with the emerald ash borer,Agrilus planipennis Fairmaire

Two parasitoids, the introduced specialist Spathius agrili Yang (Braconidae), and the native generalist Spathius floridanus Ashmead, have been proposed as biological control agents of the emerald ash borer, Agrilus planipennis Fairmaire (Buprestidae). However, little is known about their host-location behaviors. We evaluated responses to their host complex, Fraxinus pennsylvanica stem tissue, F. pennsylvanica foliage, and an A. planipennis larva within a stem. Experiments were conducted in a Y-tube olfactometer, using wasps reared on A. planipennis larvae in F. pennsylvanica stems. Naïve S. agrili were attracted to the entire complex, and to leaf tissue, relative to blanks. S. agrili were also more attracted to stems containing larvae and leaf tissue together than leaf tissue alone. Naïve S. floridanus were attracted to larvae within stems, but nothing else. A further distinction is that S. agrilli moved more, in the presence of foliage. Thus, S. agrili and S. floridanus appear to employ different host-location strategies. The former is attracted to host plant cues, which then elicit increased searching, whereas the latter is only attracted to infested tissue directly. We found no evidence that oviposition influences attraction by S. agrili, suggesting other forms of experience should be evaluated for potential sources of learned cues. Further, S. agrili that declined opportunities to oviposit oriented away from host-associated cues, suggesting distinct behavioral sequences occur by females that are not reproductively ready. Further understanding of host-location behavior may improve biological control by these parasitoids, by suggesting strategies for pre-release conditioning and providing tools for assessing post-release establishment.     

A new forest pest in Europe: a review of Emerald ash borer (Agrilus planipennis) invasion

In this publication, we review the biology, ecology, invasion history, impacts and management options of Emerald ash borer (EAB) Agrilus plannipennis, with a particular focus on its invasion in Europe. Agrilus planipennis (EAB) is a wood‐boring beetle native to East Asia. Having caused massive damages on ash species in North America in the last decades, it was first recorded in Europe in 2003 in Russia (Moscow). All ash (Fraxinus) species native to Europe and North America are known to be susceptible to EAB attacks, which cause high tree mortality even among formerly healthy trees. Recorded expansion rates are between 2.5 and 80 km/year in North America and between 13 and 41 km/year in European Russia. Given current expansion rates, EAB is expected to reach Central Europe within 15–20 years. A combination of mechanical, biological and chemical control and phytosanitary measures may reduce its impact, which nevertheless most likely will be substantial. There is an urgent need to identify native enemies in Europe, to test suitable biocontrol agents and to develop early detection and management measures. Although it is obvious that EAB will become a major pest in Europe, early and dedicated response will likely be able to reduce the level of ash mortality, and thus improve the opportunity for long‐term survival of ash as an important component in European forests.     

Evaluation of tree mortality and parasitoid recoveries on the contiguous western invasion front of emerald ash borer

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