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

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Effects of the emerald ash borer invasion on four species of birds

The emerald ash borer (EAB) Agrilus planipennis, first detected in 2002 in the vicinity of Detroit, Michigan, USA, is one of the most recent in a long list of introduced insect pests that have caused serious damage to North American forest trees, in this case ash trees in the genus Fraxinus. We used data from Project FeederWatch, a citizen science program focused on winter bird populations, to quantify the effects of EAB invasion on four species of resident, insectivorous birds known or likely to be EAB predators: three woodpecker species and the white-breasted nuthatch (Sitta canadensis). We compared relative numbers of birds within 50 km of the epicenter of the region where EAB was first detected, an area known to have suffered high ash tree mortality by 2008, to numbers 50–100 km from the epicenter and to control sites within 50 km of five comparable Midwestern cities where damage due to EAB has yet to be severe. We found evidence for significant effects on all four of the species in response to the EAB invasion in the highly impacted region, with red-bellied woodpeckers (Melanerpes carolinus) and white-breasted nuthatches showing numerical increases while downy woodpeckers (Picoides pubescens) and hairy woodpeckers (Picoides villosus) initially declined but exhibited at least temporary increases several years later. Temporal correlation analyses failed to provide support for immigration being a major cause of the elevated numbers in the highly impacted area, and thus these results are consistent with the hypothesis that increases were due to enhanced survival and/or reproduction associated with the EAB invasion within the highly impacted area. Results suggest that the continuing invasion of EAB into new areas is likely to significantly alter avian communities, although not always in ways that will be easy to predict.     

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.     

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.     

Do increases in the availability of standing dead trees affect the abundance,nest-site use,and niche partitioning of great spotted and middle spotted woodpeckers in riverine forests?

Standing dead trees may be a limited resource for woodpeckers in managed forests, especially for species that rely on dead wood for their nest or roost cavity, and as foraging sites. Effective conservation strategies for woodpeckers require a detailed knowledge of species’ responses to dead wood availability. To investigate the importance of standing dead wood (snags) for the abundance and nest-site use of the great spotted woodpecker Dendrocopos major and middle spotted woodpecker Leiopicus medius in mature riverine forests, we compared the responses of birds between two periods—before mass mortality, and during a pulse in standing dead trees. The density of standing dead trees available for cavity excavation by the great spotted woodpecker and the middle spotted woodpecker increased significantly during the study period: 37-fold and 4-fold, respectively. Temporal trends in the abundance of both woodpecker species from 2000 to 2015 were not significant. Great spotted woodpeckers were significantly more likely to use dead trees and places with wounds in species other than oak and ash during the outbreak period than in the pre-outbreak period. Middle spotted woodpeckers were significantly less likely to excavate cavities in tree species other than oak and ash in the outbreak period, but dead trees were more likely selected. An interspecific comparison suggests that the probability of a nest-hole having been excavated by a middle spotted woodpecker increased with a nest-hole sited in ash, in a dead tree, in a limb/branch, and decreased with a nest-hole in a closed forest. These findings suggest that woodpecker species, especially weak excavators, may benefit from an increase in dead wood availability leading to nest niche shifts into more favorable substrates for cavity excavation. However, a strong increase in dead wood availability does not modify the general pattern of niche partitioning between great spotted and middle spotted woodpeckers. Conservation plans for the specialized middle spotted woodpecker must consider the preference for dead and decaying trees. The decreasing number of large ashes and oaks, and the lack of natural regeneration of the latter species, may negatively affect the middle spotted woodpecker in the future.     

白蜡窄吉丁幼虫及其天敌在空间格局上的关系

调查了白蜡窄吉丁幼虫与其寄生性天敌白蜡吉丁柄腹茧蜂和捕食性天敌啄木鸟啄食白蜡窄吉丁的啄痕在空间格局上的规律.结果表明,在林间水平方向上,白蜡窄吉丁幼虫呈聚集分布,白蜡吉丁柄腹茧蜂和啄木鸟的啄痕也表现为聚集分布;在垂直方向上,白蜡窄吉丁幼虫分布于地面至3.37m以下的树干,主要集中于1.0m左右的主干,天敌也集中在此范围内活动.     

The effect of bark thickness on host partitioning between Tetrastichus planipennisi (Hymen: Eulophidae) and Atanycolus spp. (Hymen: Braconidae), two parasitoids of emerald ash borer (Coleop: Buprestidae)

Parasitoids have recently been introduced from Asia to aid in biological control in the United States of the invasive, highly damaging, emerald ash borer, Agrilus planipennis. Three introduced parasitoids have established and field biological studies are underway to improve our understanding of niche partitioning among them. Here we report one such investigation, a field experiment conducted to determine how outer bark thickness of ash trees might affect parasitism by one introduced (Tetrastichus planipennisi) and one native parasitoid (Atanycolus spp.). We found that T. planipennisi was unable to parasitize EAB larvae in trees with outer bark thicker than 3.2 mm (>11.2-cm DBH) whereas Atanycolus spp. parasitized EAB larvae in ash trees with outer bark up to 8.8 mm thick (>57.4-cm DBH). These results suggest that establishment of, and control by T. planipennisi at release sites with only large diameter trees is less likely, and that T. planipennisi will be more effective in stands with younger trees (<12-cm DBH). Releasing T. planipennisi near the leading edge of EAB invasion may have little impact on EAB populations if many ash trees are too large. We recommend releasing T. planipennisi in stands dominated by small, early successional or regenerating ash trees. This may maximize the establishment and effectiveness of this species. This limitation of T. planipennisi for biological control of emerald ash borer suggests that other EAB parasitoids from its native range with longer ovipositors, such as Spathius galinae (Hymenoptera: Braconidae), should be sought and evaluated for possible use as EAB biocontrol agents in the US. The results of this study also suggest the importance of parasitoid guild introduction for biological control in general, and hint at possible broader implications relating to resource partitioning among native and introduced parasitoids.     

Interactions between Spathius agrili (Hymenoptera: Braconidae) and Tetrastichus planipennisi (Hymenoptera: Eulophidae), larval parasitoids of Agrilus planipennis (Coleoptera: Buprestidae)

Three hymenopteran parasitoids native to China are being released in the United States as biological control agents for the emerald ash borer (EAB), Agrilus planipennis Fairmaire, an Asian buprestid species responsible for mortality of ash trees (Fraxinus spp.) in North America. Two of these hymenopterans, Spathius agrili Yang (Braconidae), a larval ectoparasitoid, and Tetrastichus planipennisi Yang (Eulophidae), a larval endoparasitoid, prefer late-instar EAB larvae. This overlapping host preference raises concerns that interspecific competition following field releases may compromise establishment of one or both species. In a series of laboratory and field experiments, we found S. agrili and T. planipennisi exhibited similar parasitism rates when presented alone with EAB larvae for 12–14 days. However, S. agrili was more efficient at locating and parasitizing hosts within the first 27 h, possibly explaining why S. agrili excluded T. planipennisi in the laboratory trials and nearly excluded T. planipennisi in field trials when the two species were presented together with EAB larvae. We found that S. agrili parasitized larvae previously parasitized by T. planipennisi but not the reverse. However, S. agrili offspring failed to complete development on hosts that were previously parasitized by T. planipennisi. We recommend releasing these species separately in time or space to avoid the antagonistic interactions observed in this study.     

Development of methods for the field evaluation of Oobius agrili (Hymenoptera: Encyrtidae) in North America,a newly introduced egg parasitoid of the emerald ash borer (Coleoptera: Buprestidae)

A field study was conducted in forested plots near Lansing, Michigan in 2008 and 2009 to evaluate the newly introduced egg parasitoid Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae) for control of the invasive emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae). To measure parasitism by O. agrili, laboratory-reared “sentinel EAB eggs” were deployed under bark flaps on trunks of selected ash trees in both parasitoid-release and non-release control plots. In addition, naturally occurring EAB eggs were collected in both parasitoid-release and control plots to measure parasitism. While no parasitism was detected with either sentinel or naturally occurring EAB eggs in control plots in either 2008 or 2009, a low level of parasitism by O. agrili was detected in the parasitoid-release plots in both artificially deployed sentinel eggs (?1%) and field-collected, naturally occurring eggs (1.1–4.2%) in both years. In addition to losses due to parasitism by O. agrili, a large proportion (37–52%) of the field-deployed sentinel eggs disappeared, possibly due to predators such as ants, in both parasitoid-release and control plots. While no statistical differences in parasitism by O. agrili were detected between parasitoid release and control plots, other sources of egg mortality such as disappearance due to predation on eggs, varied significantly across study sites in both 2008 and 2009. The relevance of these findings to future release and evaluation strategies for O. agrili for biological control of the invasive emerald ash borer in the US is discussed.     

Factors affecting the survival of ash (Fraxinus spp.) trees infested by emerald ash borer (Agrilus planipennis)

Emerald ash borer (Agrilus planipennis) (EAB), an Asian woodboring beetle accidentally introduced in North America, has killed millions of ash (Fraxinus spp.) trees and is spreading rapidly. This study examined the effects of tree- and site-level factors on the mortality of ash trees in stands infested by EAB in OH, USA. Our data show that ash populations in forested sites can progress from healthy to almost complete mortality of mature trees within 6 years. Although the end result of nearly complete mortality does not vary, survival analysis with 5 years of data showed that some factors affected the rate of mortality. We found more rapid mortality in stands with lower densities of ash trees. This finding supports an extension of the resource dilution hypothesis whereby concentration of EAB on few trees in low ash density areas leads to rapid decline of these trees. This contradicts an extension of the resource concentration theory that greater host density increases relative pest abundance and host mortality. Although reductions in ash density via diversification may be desirable for other silvicultural, conservation, and management objectives in preparation for EAB, our study shows that the management strategy of reducing ash density is unlikely to protect the remaining ash trees. Survival analysis also showed that mortality was more rapid for trees shaded by other trees and for trees initially exhibiting dieback. In management scenarios where hazard tree removal must be spread over several years due to budget constraints, focusing initial tree removal on stressed trees is recommended.     

Effects of learning experience on behaviour of the generalist parasitoid Sclerodermus pupariae to novel hosts

Massicus raddei Blessig (Coleoptera: Cerambycidae), also referred to as the oak long‐horned beetle (OLB), is a non‐natural host for the generalist parasitoid Sclerodermus pupariae Yang et Yao (Hymenoptera: Bethylidae). To determine whether this generalist parasitoid might be a suitable agent for the control of OLB, the adaptive learning experience of adult female parasitoids to OLB larvae was investigated in the laboratory. A Y‐tube olfactometer bioassay was used to examine the effects of adaptive learning experience on the foraging ability of parasitoids for OLB larvae. The results indicated that parasitoids were significantly attracted by the volatiles of ash bark, Fraxinus velutina, with emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae) larvae and larval frass, after exposure to ash bark mixed with EAB larval frass (learning condition A). In contrast, after exposure to oak bark, Quercus liaotungensis, mixed with OLB larval frass (learning condition C), parasitoids showed significant preference for the volatiles of oak bark with OLB larvae and larval frass. On the basis of the results of no‐choice tests, we found that parasitoids exposed to learning condition C had greater paralysis efficiency and higher OLB larvae parasitism rates than those exposed to learning condition A or no experience. Furthermore, parasitoids fed on OLB larvae in learning condition C had significantly greater paralysis efficiency and higher OLB larvae parasitism rates than other parasitoids tested. Parasitoids fed on EAB larvae in learning condition A had the lowest paralysis efficiency and OLB larvae parasitism rates among the parasitoids tested. These findings suggested that adaptive learning significantly enhanced the ability of a generalist parasitoid to utilize a novel host. This may provide a new approach to controlling non‐natural hosts using generalist parasitoids.     

白蜡吉丁柄腹茧蜂的羽化和产卵与寄主之间的关系

白蜡窄吉丁是危害白蜡属树木的一种重要蛀干害虫,因其幼虫期高度的隐蔽性生活而极难检测和防治.白蜡吉丁柄腹茧蜂是新发现外寄生于白蜡窄吉丁幼虫的优势天敌种,对寄主害虫的控制作用较强,具有良好的生物防治利用前景.研究调查了白蜡吉丁柄腹茧蜂及其寄主白蜡窄吉丁越冬代成虫羽化的时序差异、不同时期林间的寄生率、寄主密度与寄生率的关系以及寄主幼虫大小与茧蜂产卵量的关系.结果表明,越冬后白蜡吉丁柄腹茧蜂的羽化时间比其寄主害虫白蜡窄吉丁的羽化要晚1个多月.2003年白蜡吉丁柄腹茧蜂越冬代成虫的羽化从6月中旬持续到8月中旬,羽化高峰期在7月份;寄主白蜡窄吉丁的羽化期在5月中下旬.2004年白蜡吉丁柄腹茧蜂越冬代成虫的羽化从5月下旬持续到7月下旬,羽化高峰期在6月下旬至7月上旬;寄主羽化期在4月中旬至5月中旬（室内）.越冬后天敌的羽化时间刚好适应最早寄主发育到可供寄生的龄期,这是二者长期协同进化的结果,也表明白蜡吉丁柄腹茧蜂很可能是一种专性寄生蜂.林间白蜡吉丁柄腹茧蜂对白蜡窄吉丁幼虫的自然寄生率随着时间的推移总体上是逐步上升的.自然条件下茧蜂决定是否产卵与寄主幼虫的大小即龄期有关,它仅在前胸宽和体宽1.5 mm、体长12 mm以上,即3～4龄的寄主幼虫体表产卵,但只要接受寄主并产卵,不同龄期寄主幼虫上的产卵量无显著的差异.     

Measuring the impact of biotic factors on populations of immature emerald ash borers (Coleoptera: Buprestidae)

Cohorts of emerald ash borer larvae, Agrilus planipennis Fairmaire, were experimentally established in July of 2008 on healthy green ash (Fraxinus pennsylvanica) trees in two wooded plots at each of three sites near Lansing, MI, by caging gravid emerald ash borer females or placing laboratory-reared eggs on trunks (0.5-2 m above the ground) of selected trees. One plot at each site was randomly chosen for release of two introduced larval parasitoids, Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae) and Spathius agrili Yang (Hymenoptera: Braconidae), whereas the other served as the control. Stage-specific mortality factors and rates were measured for all experimentally established cohorts and for associated wild (i.e., naturally occurring) emerald ash borer immature stages via destructive sampling of 2.5 m (above the ground) trunk sections of cohort-bearing trees in the spring and fall of 2009. Host tree defense was the most important mortality factor, causing 32.0 to 41.1% mortality in the experimental cohorts and 17.5 to 21.5% in wild emerald ash borer stages by spring 2009, and 16.1 to 29% for the remaining experimental cohorts, and 9.9 to 11.8% for wild immature emerald ash borer stages by fall 2009. Woodpecker predation was the second most important factor, inflicting no mortality in the experimental cohorts but causing 5.0 to 5.6% mortality to associated wild emerald ash borer stages by spring 2009 and 9.2 to 12.8% and 3.2 to 17.7%, respectively, for experimental cohorts and wild emerald ash borer stages by fall 2009. Mortality from disease in both the experimental and wild cohorts was low (<3%) in both the spring and fall sample periods. In the fall 2009 samples, ≈ 1.5% of experimental cohorts and 0.8% of the wild emerald ash borer stages were parasitized by T. planipennisi. While there were no significant differences in mortality rates because of parasitism between parasitoid-release and control plots, T. planipennisi was detected in each of the three release sites by the end of the study but was not detected in the experimental cohorts or associated wild larvae in any of the three control plots.     

Impacts of the emerald ash borer (Agrilus planipennis Fairmaire) induced ash (Fraxinus spp.) mortality on forest carbon cycling and successional dynamics in the eastern United States

Invasive species are widely recognized as altering species and community dynamics, but their impacts on biogeochemical cycling and ecosystem processes are less understood. The emerald ash borer (Agrilus planipennis Fairmaire) is a phloem feeding beetle that was inadvertently introduced to the US in the 1990s and relies solely on ash trees (Fraxinus spp.) to complete its life cycle. Ash trees have a wide geographic distribution and are an important component of many different forest types in the US. The larval feeding behavior of the emerald ash borer (EAB) effectively girdles the tree’s phloem tissue resulting in tree mortality in as little as 2 years and stand mortality in as little as 5 years. Using the forest inventory and analysis database, we found that forest lands in the lower 48 states hold approximately 8.7 billion ash trees and saplings, which represent ~2.5 % of the aboveground forest carbon mass. Furthermore, we measured tree growth in 7 EAB impacted and 5 non-EAB impacted temperate forests in the Midwestern United States to quantify the impacts of EAB induced tree mortality on tree growth. We hypothesized that the initial C lost would be partly compensated for by the enhanced non-ash tree growth in EAB-impacted regions relative to non-EAB impacted regions. The EAB disturbance enhanced growth of non-ash trees in the EAB impacted region relative to the non-EAB impacted region. Results also indicate that in EAB impacted areas, growth of trees from the genera Acer and Ulmus responded most positively. Finally, we quantified annual biometric net primary productivity of the EAB impacted forests and compared these quantities to modeled growth of these forests in the absence of EAB and found that large scale ash tree mortality has reduced short term regional forest productivity. The loss of ash biometric net primary productivity is, in part compensated by enhanced growth of non-ash species. As expected, EAB disturbance severity was greater in forests with higher basal areas of ash. This study illustrates the ecosystem and regional scale impacts of invasive pest-induced disturbance on biogeochemical cycling and forest species composition.     

An improved method for monitoring parasitism and establishment of Oobius agrili (Hymenoptera: Encyrtidae), an egg parasitoid introduced for biological control of the emerald ash borer (Coleoptera: Buprestidae) in North America

Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae) is a solitary egg parasitoid that has been released in the United States since 2007 for biocontrol of the invasive emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae). Field and laboratory trials with ash logs infested with EAB eggs were conducted in Michigan between 2009 and 2010 to improve methods for monitoring the establishment of O. agrili. Naturally occurring EAB eggs were collected in both parasitoid-release and control (non-parasitoid-release) plots to compare with the EAB egg-sentinel log (ESL) technique. In three parasitoid-release plots, >50% of ESLs had O. agrili-parasitized eggs ranging from 3.9% to 48.2% egg parasitism after one week of field exposure. No EAB eggs were attacked by O. agrili on the ESLs deployed in control plots. In the laboratory, 100% of ESLs exposed to O. agrili inside rearing jars for one week had parasitized-eggs (68.5% egg parasitism). Deployment of ESLs detected low levels of parasitism by O. agrili in all three ash stands where O. agrili was released in previous years. In contrast, collection of naturally occurring EAB eggs detected the parasitism in only one of these three parasitoid-release ash stands. No parasitism was detected in control ash stands with either method. These findings indicate that populations of O. agrili released in previous years had successfully overwintered and established in the released ash stands by 2010, but had not yet dispersed to the control stands.     

Natural enemies implicated in the regulation of an invasive pest: a life table analysis of the population dynamics of the emerald ash borer

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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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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.     

Abundance of two threatened woodpecker species in relation to the proportion of spruce plantations in native pine forests of western Norway

In a comparative study we investigated woodpecker abundance in forest landscapes with different proportion of native pine forest and spruce plantations in western Norway. In 100 circular study plots of 100ha each we recorded 38 white-backed –Dendrocopos leucotos, 22 grey-headed –Picus canus, 13 great spotted –Dendrocopos major, 6 green –Picus viridis, and 2 lesser spotted –Dendrocopos minor woodpeckers in the breeding season. The mean number of recorded woodpecker species peaked at 20–40% spruce plantations. The two most common species in the study, the white-backed and the grey-headed woodpeckers are both Red-listed species in Norway and among the rarest woodpeckers in Europe. The white-backed woodpecker preferred plots with higher than average proportions of standing dead trees and deciduous trees, and low proportions of spruce plantations in the plots. The grey-headed woodpecker preferred plots in the western (coastal) parts of the study area with presence of large aspen Populus tremula trees. Logistic regression models did not reveal any clear threshold values with respect to proportion of spruce plantations in plots, although both woodpecker species were extremely rare in plots with >60% spruce plantations. We recommend spruce plantations to be kept at moderate levels to ensure viable populations of woodpeckers in western Norway.     

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.