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

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High temperature tolerance and thermal plasticity in emerald ash borer Agrilus planipennis

• 1 The emerald ash borer Agrilus planipennis (Coleoptera: Buprestidae) (EAB), an invasive wood‐boring beetle, has recently caused significant losses of native ash (Fraxinus spp.) trees in North America. Movement of wood products has facilitated EAB spread, and heat sanitation of wooden materials according to International Standards for Phytosanitary Measures No. 15 (ISPM 15) is used to prevent this.
• 2 In the present study, we assessed the thermal conditions experienced during a typical heat‐treatment at a facility using protocols for pallet wood treatment under policy PI‐07, as implemented in Canada. The basal high temperature tolerance of EAB larvae and pupae was determined, and the observed heating rates were used to investigate whether the heat shock response and expression of heat shock proteins occurred in fourth‐instar larvae.
• 3 The temperature regime during heat treatment greatly exceeded the ISPM 15 requirements of 56 °C for 30 min. Emerald ash borer larvae were highly tolerant of elevated temperatures, with some instars surviving exposure to 53 °C without any heat pre‐treatments. High temperature survival was increased by either slow warming or pre‐exposure to elevated temperatures and a recovery regime that was accompanied by up‐regulated hsp70 expression under some of these conditions.
• 4 Because EAB is highly heat tolerant and exhibits a fully functional heat shock response, we conclude that greater survival than measured in vitro is possible under industry treatment conditions (with the larvae still embedded in the wood). We propose that the phenotypic plasticity of EAB may lead to high temperature tolerance very close to conditions experienced in an ISPM 15 standard treatment.

     

Optimizing early detection strategies: defining the effective attraction radius of attractants for emerald ash borer Agrilus planipennis Fairmaire

1. Adult emerald ash borers are attracted to green prism traps baited with the ash host volatile (3Z)-hexenol and the sex pheromone of emerald ash borer (3Z)-dodecen-12-olide [(3Z)-lactone]. Quantifying the heretofore unknown range of attraction of such traps would help optimize deployment strategies for early detection.
2. Examining trap captures of traps deployed in pairs at variable distances offers insight into the range of attraction. Recent work has shown the range of attraction can be estimated as half the intertrap distance at which trap catch begins to decrease, which should occur when proximate traps overlap their respective attractive ranges.
3. We estimated these traps' attractive range for emerald ash borer using 98 baited dark green prism traps deployed in pairs, one trap per tree, in an urban park in Saint Paul, Minnesota, USA in summer 2020.
4. We estimate attractive range by fitting a logistic model to trap catch data using Bayesian inferential methods and describe advantages thereof.
5. The attractive range of these baited traps was estimated to be between 16 and 73 m, with a median of 28 m. We recommend that dark green prism traps baited with these semiochemicals be placed 25–35 m apart near high-risk entry points.

     

The persistence of blue ash in the aftermath of emerald ash borer may be due to adult oviposition preferences and reduced larval performance

1. We examined the health of mature blue ash, Fraxinus quadrangulata, in two forests in southwestern Ohio in relation to that of mature white ash, F. americana, and examined the potential importance of oviposition preferences and larval resistance in the persistence of blue ash.
2. Both blue ash and white ash were largely unaffected by emerald ash borer in 2012. By 2018, nearly 90% of the blue ash trees observed in these forests had full or nearly full canopies, as opposed to less than 20% of the white ash encountered in our studies. In 2021, blue ash maintained a similar degree of canopy health as in 2018, but no standing live mature white ashes remained.
3. Bark removals revealed no current or past larval feeding attempts in blue ash in 2018 or 2021, except for one attacked and killed tree in 2018. All white ash trees examined were attacked. In a laboratory bioassay with cut stems, emerald ash borer larvae fed less and grew significantly more slowly on blue ash than on white ash.
4. Both reduced larval performance and reduced adult oviposition likely contribute to the persistence of blue ash in forests devastated by emerald ash borer.

     

Effects of the emerald ash borer invasion on the community composition of arthropods associated with ash tree boles in Maryland,U.S.A.

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Genetic analysis of emerald ash borer (<Emphasis Type="Italic">Agrilus planipennis</Emphasis> Fairmaire) populations in Asia and North America

Emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), is an invasive pest of North American ash (Fraxinus spp.) trees first discovered outside of its native range of northeastern Asia in 2002. EAB spread from its initial zone of discovery in the Detroit, Michigan and Windsor, Ontario metropolitan areas, in large part, from inadvertent human-assisted movement of infested ash materials. EAB infestations are now known in 15 US states and two Canadian provinces. The primary goal of this study was to use molecular markers to characterize the population genetic structure of EAB in its native and introduced range. This information may provide valuable insights on the geographic origin, potential host range, invasion potential, and additional biological control agents for ongoing management efforts of this destructive wood-boring beetle. EAB were collected from 17 localities in its native Asian range and from 7 localities in North America, and population structure analyzed using mtDNA gene sequences, AFLP fingerprints, and alleles at 2 microsatellite loci. Analysis of mtDNA cytochrome oxidase subunit I gene (COI; 439 bp) sequences revealed all North American individuals carry a common mtDNA haplotype also found in China and South Korea. Additional mtDNA haplotypes observed in China and South Korea differed from the common haplotype by 1–2 nucleotide substitutions and a single individual from Japan differed by 21 nucleotide changes (4.8%). Analysis using AFLP fingerprints (108 loci) indicated Asian populations were more highly variable, yet had less overall population structure, than the North American populations. North American populations appear most closely related to populations in our sample from the Chinese provinces of Hebei and Tianjin City. Further, population assignment tests assigned 88% of the individual beetles from North America to either Hebei or Tianjin City.     

Differential utilization of ash phloem by emerald ash borer larvae: ash species and larval stage effects

• 1 Two experiments were performed to determine the extent to which ash species (black, green and white) and larval developmental stage (second, third and fourth instar) affect the efficiency of phloem amino acid utilization by emerald ash borer (EAB) Agrilus planipennis Fairmaire (Coleoptera: Buprestidae) larvae.
• 2 EAB larvae generally utilized green ash amino acids more efficiently than those of the other two species. For example, the concentrations of only six (two essential) and seven (two essential) amino acids were lower in frass from EAB that fed upon black and white ash than in the corresponding phloem, respectively. By contrast, concentrations of 16 (eight essential) amino acids were lower in the frass from EAB that fed upon green ash than in the phloem. In addition, in green ash, the frass : phloem ratios of 13 amino acids were lower than their counterparts in black and white ash.
• 3 The concentrations of non‐essential amino acids glycine and hydroxylproline were greater in frass than in phloem when EAB fed on black ash, although not when EAB fed on green or white ash.
• 4 The concentration of total phenolics (a group of putative defensive compounds to EAB, expressed as antioxidant activity of acetone extraction) was high in EAB frass but even higher in the phloem samples when the data were pooled across ash species and EAB larval stages. This suggests EAB larvae may eliminate phenolics through a combination of direct excretion and enzymatic conversion of phenolics to nonphenolics before excretion. Because the ratio of frass total phenolics to phloem total phenolics in white ash was lower than the ratios in black and green ash, the ability to destroy phenolics or convert them to nonphenolics was greater when EAB larvae fed on white ash.
• 5 Fourth‐instar EAB extracted phloem amino acids, including threonine, more efficiently than third‐instar EAB. The different larval developmental stages of EAB did not differ in their apparent ability to destroy phenolics or convert them to nonphenolics.

     

A decade of emerald ash borer effects on regional woodpecker and nuthatch populations

The emerald ash borer (EAB) Agrilus planipennis, first detected in 2002 in the vicinity of Detroit, Michigan, USA, has spread throughout much of eastern and midwestern North America as of 2016, resulting in widespread mortality of ash trees in the genus Fraxinus. We investigated the effects of this newly available, exotic food source on populations of six species of largely resident insectivorous birds, including five species of woodpeckers and white-breasted nuthatch (Sitta canadensis), using North American Breeding Bird Survey data for breeding season estimates and Audubon Christmas Bird Counts for winter season estimates. We found evidence for relatively modest and variable effects of EAB invasion on the populations of these birds during the breeding season, but highly significant numerical increases during the winter that in several cases appeared to be increasing as the EAB invasion has progressed. Our results confirm that the EAB invasion is resulting in increased populations of several insectivorous birds, primarily during the winter. They also suggest that the numerical response of woodpeckers to EAB may be such that avian predation, which represents a significant, and possibly the largest, morality factor affecting some EAB populations, may continue to increase and help control the EAB epidemic as the invasion continues.     

Drought stress increased survival and development of emerald ash borer larvae on coevolved Manchurian ash and implicates phloem‐based traits in resistance

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Interspecific variation in resistance to emerald ash borer (Coleoptera: Buprestidae) among North American and Asian ash (Fraxinus spp.)

We conducted a 3-yr study to compare the susceptibility of selected North American ash and an Asian ash species to emerald ash borer, Agrilus planipennis Fairmaire, an invasive wood-boring beetle introduced to North America from Asia. Because of a coevolutionary relationship between Asian ashes and emerald ash borer, we hypothesized an Asian ash species, Manchurian ash, is more resistant to the beetle than its North American congeners. Consistent with our hypothesis, Manchurian ash experienced far less mortality and yielded far fewer adult beetles than several cultivars of North American green and white ash. Surprisingly, a black ash (North American) x Manchurian ash hybrid was highly susceptible to emerald ash borer, indicating this cultivar did not inherit emerald ash borer resistance from its Asian parent. A corollary study investigated the efficacy of soil-applied imidacloprid, a systemic, neonicotinoid insecticide, for controlling emerald ash borer in each of the five cultivars. Imidacloprid had no effect on emerald ash borer colonization of Manchurian ash, which was low in untreated and treated trees. In contrast, imidacloprid did enhance survival of the North American and hybrid cultivars and significantly reduced the number of emerald ash borer adults emerging from green and white ash cultivars. We identify a possible mechanism of resistance of Manchurian ash to emerald ash borer, which may prove useful for screening, selecting, and breeding emerald ash borer-resistant ash trees.     

Decreased emergence of emerald ash borer from ash treated with methyl jasmonate is associated with induction of general defense traits and the toxic phenolic compound verbascoside

The emerald ash borer (EAB; Agrilus planipennis Fairmaire) is causing widespread mortality of ash (Fraxinus spp.) in North America. To date, no mechanisms of host resistance have been identified against this pest. Methyl jasmonate was applied to susceptible North American and resistant Asian ash species to determine if it can elicit induced responses in bark that enhance resistance to EAB. In particular, phenolic compounds, lignin, and defense-related proteins were quantified, and compounds associated with resistance were subsequently tested directly against EAB larvae in bioassays with artificial diet. MeJA application decreased adult emergence in susceptible ash species, comparable to levels achieved by insecticide application. Concentration of the phenolic compound verbascoside sharply increased after MeJA application to green and white ash. When incorporated in an artificial diet, verbascoside decreased survival and growth of EAB neonates in a dose-dependent fashion. Lignin and trypsin inhibitors were also induced by MeJA, and analogs of both compounds reduced growth of EAB larvae in artificial diets. We conclude that the application of MeJA prior to EAB attack has the ability to enhance resistance of susceptible ash trees by inducing endogenous plant defenses, and report evidence that induction of verbascoside is a mechanism of resistance to EAB.     

Temporal dynamics of woodpecker predation on emerald ash borer (Agrilus planipennis) in the northeastern U.S.A.

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Girdling increases survival and growth of emerald ash borer larvae on Manchurian ash

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Visual and chemical cues affecting the detection rate of the emerald ash borer in sticky traps

Using sticky traps, we compared the efficacy of chemical and visual lures, both alone and in combination, for improving the detection of populations of the emerald ash borer (EAB), Agrilus planipennis. Ash leaflets to which EAB visual decoys were pinned and coated with sticky material were able to trap EAB with as high a rate of detection as large sticky visually unbaited ‘prism traps’ currently used in wide‐scale EAB surveillance programs in North America, in a high‐density area. Both the sticky leaf traps and prism traps captured more EAB when a point source of plant odours, either manuka or phoebe oil, was deployed with the trap. For the sticky leaf traps, the shape of the EAB visual decoy lure was found to be important in optimizing the detection rate. Either an entire dead beetle or else two elytra placed side by side to mimic a resting beetle resulted in optimal trap performance. When two elytra were placed end to end or else other body parts were deployed, the traps lost their efficacy. Small green plastic surfaces to which EAB visual decoys were pinned were found to be fairly good substitutes for live ash leaflets, but the rate of beetle detection was reduced significantly from that of the ash leaflet plus EAB decoy. Throughout all experiments, a clear male bias occurred in sticky leaf traps when EAB visual decoys were placed on the traps. The implications of these findings for developing new trapping designs for EAB and other forest buprestids are discussed.     

Temperature responses of carbon dioxide fluxes from coarse dead wood in a black ash wetland

Wetlands Ecology and Management - The invasive emerald ash borer (EAB, Agrilus planipennis Fairmaire) causes widespread ash tree mortality in North America, and the CO2 efflux (respiration, F) from...     

Visually Mediated ‘Paratrooper Copulations’ in the Mating Behavior of <Emphasis Type="Italic">Agrilus planipennis</Emphasis> (Coleoptera: Buprestidae), a Highly Destructive Invasive Pest of North American Ash Trees

The emerald ash borer, Agrilus planipennis, is a serious invasive pest of North American ash (Fraxinus) trees. In captivity, mating is initiated by beetles at least 10 days old, and appears to be based simply on random contact with a member of the opposite sex. In the field, male A. planipennis search the tree during flight, and attempt to copulate with dead beetles of both sexes pinned to leaves, after descending rapidly straight down onto the pinned beetles from a height of from 30 to 100 cm. All evidence suggests that males find potential mates using visual cues. Equal numbers of feral males approach all ‘dummy’ beetles; however, considerably more time is spent attempting copulation with dead females rather than males, suggesting a contact chemical cue. Sticky traps prepared from dead, pinned EAB capture crawling insects as well as male A. planipennis, at a rate similar to that at which small purple sticky traps of similar overall area capture crawling insects and both sexes of feral EAB.     

Effects of water availability on emerald ash borer larval performance and phloem phenolics of Manchurian and black ash

The invasive emerald ash borer (EAB) beetle is a significant threat to the survival of North American ash. In previous work, we identified putative biochemical and molecular markers of constitutive EAB resistance in Manchurian ash, an Asian species co‐evolved with EAB. Here, we employed high‐throughput high‐performance liquid chromatography with photodiode array detection and mass spectrometry (HPLC‐PDA‐MS) to characterize the induced response of soluble phloem phenolics to EAB attack in resistant Manchurian and susceptible black ash under conditions of either normal or low water availability, and the effects of water availability on larval performance. Total larval mass per tree was lower in Manchurian than in black ash. Low water increased larval numbers and mean larval mass overall, but more so in Manchurian ash. Low water did not affect levels of phenolics in either host species, but six phenolics decreased in response to EAB. In both ashes, pinoresinol A was induced by EAB, especially in Manchurian ash. Pinoresinol A and pinoresinol B were negatively correlated with each other in both species. The higher accumulation of pinoresinol A in Manchurian ash after attack may help explain the resistance of this species to EAB, but none of the responses measured here could explain increased larval performance in trees subjected to low water availability.     

Moisture content and nutrition as selection forces for emerald ash borer larval feeding behaviour

1. The exotic phloem‐feeding emerald ash borer (EAB), Agrilus planipennis, has killed tens of millions of North American ash trees (Fraxinus) since its first detection in the U.S.A. in 2002. Ash trees are killed by larval feeding in the cambial region, which disrupts translocation of photosynthates and nutrients. 2. We observed that EAB larvae feed predominantly downwards in naturally grown green ash trees, a behaviour confirmed in greenhouse‐grown black ash seedlings. Furthermore, biomass of larvae feeding downwards was greater than that for larvae feeding upwards. 3. We sought to determine the relative importance of four selection forces (i.e. gravity, moisture content, plant defence, and nutrition) in driving this downward feeding behaviour in this study. The gravity and plant defence (i.e. polyphenols) hypotheses were ruled out because even when seedlings were grown upside down, more EAB larvae moved upwards (towards the root area), and phloem tissue below the feeding site contained higher concentrations of defensive compounds than that above the feeding site. 4. The moisture content hypothesis was supported as phloem moisture above the feeding site decreased to levels reducing survivorship and biomass but was unaffected below. The nutrition hypothesis was also supported as the levels of 11 amino acids (mostly essential amino acids) below the feeding site were greater than those above. Furthermore, growth of larvae reared on an artificial diet deficient in protein and amino acids was worse than larvae reared in diet with complete ingredient or diet deficient in either protein or amino acids. 5. We conclude that moisture content and nutrients are two selective forces for the downward feeding behaviour of EAB larvae.     

Interspecific proteomic comparisons reveal ash phloem genes potentially involved in constitutive resistance to the emerald ash borer

The emerald ash borer (Agrilus planipennis) is an invasive wood-boring beetle that has killed millions of ash trees since its accidental introduction to North America. All North American ash species (Fraxinus spp.) that emerald ash borer has encountered so far are susceptible, while an Asian species, Manchurian ash (F. mandshurica), which shares an evolutionary history with emerald ash borer, is resistant. Phylogenetic evidence places North American black ash (F. nigra) and Manchurian ash in the same clade and section, yet black ash is highly susceptible to the emerald ash borer. This contrast provides an opportunity to compare the genetic traits of the two species and identify those with a potential role in defense/resistance. We used Difference Gel Electrophoresis (DIGE) to compare the phloem proteomes of resistant Manchurian to susceptible black, green, and white ash. Differentially expressed proteins associated with the resistant Manchurian ash when compared to the susceptible ash species were identified using nano-LC-MS/MS and putative identities assigned. Proteomic differences were strongly associated with the phylogenetic relationships among the four species. Proteins identified in Manchurian ash potentially associated with its resistance to emerald ash borer include a PR-10 protein, an aspartic protease, a phenylcoumaran benzylic ether reductase (PCBER), and a thylakoid-bound ascorbate peroxidase. Discovery of resistance-related proteins in Asian species will inform approaches in which resistance genes can be introgressed into North American ash species. The generation of resistant North American ash genotypes can be used in forest ecosystem restoration and urban plantings following the wake of the emerald ash borer invasion.     

Feeding by emerald ash borer larvae induces systemic changes in black ash foliar chemistry

The exotic wood-boring pest, emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), has been threatening North American ash (Fraxinus spp.) resources, this being recognized since its first detection in Michigan, USA and Ontario, Canada in 2002. Ash trees are killed by larval feeding in the cambial region, which results in disruption of photosynthate and nutrient translocation. In this study, changes in volatile and non-volatile foliar phytochemicals of potted 2-yr-old black ash, Fraxinus nigra Marshall, seedlings were observed in response to EAB larval feeding in the main stem. EAB larval feeding affected levels of six compounds [hexanal, (E)-2-hexenal, (Z)-3-hexenyl acetate, (E)-β-ocimene, methyl salicylate, and (Z,E)-α-farnesene] with patterns of interaction depending upon compounds of interest and time of observation. Increased methyl salicylate emission suggests similarity in responses induced by EAB larval feeding and other phloem-feeding herbivores. Overall, EAB larval feeding suppressed (Z)-3-hexenyl acetate emission, elevated (E)-β-ocimene emission in the first 30 days, but emissions leveled off thereafter, and generally increased the emission of (Z,E)-α-farnesene. Levels of carbohydrates and phenolics increased overall, while levels of proteins and most amino acids decreased in response to larval feeding. Twenty-three amino acids were consistently detected in the foliage of black ash. The three most abundant amino acids were aspartic acid, glutamic acid, glutamine, while the four least abundant were α-aminobutyric acid, β-aminoisobutyric acid, methionine, and sarcosine. Most (16) foliar free amino acids and 6 of the 9 detected essential amino acids decreased with EAB larval feeding. The ecological consequences of these dynamic phytochemical changes on herbivores harbored by ash trees and potential natural enemies of these herbivores are discussed.