INTRODUCTION

Persistence of a plant species in the face of rapidly-spreading invasive insects is associated with the degree to which it attracts or deters oviposition by adults, as well as resists and tolerates attack should adults choose to oviposit on it. Emerald ash borer (Agrilus planipennis Fairmaire, EAB) (Coleoptera: Buprestidae) is an Asian wood-boring beetle that is invasive in North America that has killed hundreds of millions of ash trees (Fraxinus spp.) (Herms & McCullough, 2014). Relative to its primary Asian host species, Manchurian ash (Fraxinus mandshurica), EAB shows increased adult and larval performance on North American ash species and is consequently more damaging to them (e.g., Rebek et al., 2008). Adult feeding rates and survival on foliage and their oviposition preferences generally correlate with larval performance of this beetle in the phloem across species. The order of oviposition preference and adult and larval feeding performance for major eastern Fraxinus species by EAB (from best to worst) appears to be green ash (F. pennsylvanica Marshall) and black ash (F. nigra Marshall), white ash (F. americana L.), and, finally, blue ash (F. quadrangulata Michx.) (Anulewicz et al., 2006, 2008; Tanis & McCullough, 2012, 2015).

Blue ash appears to be surviving in the aftermath of EAB throughout the Midwestern United States at a much higher rate than other ash species. In Michigan, survival and health of blue and white ash trees were examined over several years throughout an EAB infestation. Significantly fewer white ash survived the infestation over the course of 3 years than did blue ash, and 60% of surviving blue ash trees were considered ‘healthy’ (Tanis & McCullough, 2012). Another study in Michigan found that blue ash trees had higher survival rates, fuller canopies, and were larger and older, on average, than the white ash in the study because most of the older and larger white ash trees succumbed to attack (Spei & Kashian, 2017).

The persistence of blue ash in the face of EAB attack could be due to several factors, including being less attractive to adults for oviposition, being a poorer substrate for adult foliar feeding, possessing increased larval resistance in the phloem, and exhibiting a higher tolerance of damage after attack. In the only study to address adult attraction to blue ash, blue ash bolts received fewer EAB eggs in the field than bolts of other more susceptible ash species in early host range tests in North America (Anulewicz et al., 2008). In terms of larval performance, Anulewicz et al. (2006) found that EAB larvae established a similar density of feeding galleries on blue ash as on black, white, and green ash in no-choice bioassays using adults caged on stems. Peterson et al. (2015) found that a similar proportion of EAB larvae from inoculated eggs developed and reached the prepupal stage on cut blue ash stems as on cut green ash stems, but they took much longer to do so. This indicates that blue ash is a poorer substrate for larvae although significant damage can still be accumulated across a season. In a similar vein, Olson and Rieske (2019) found that EAB larvae survived at a lower rate and fed slightly less on cut stems of blue ash than on cut stems of white ash. In the same study, field-grown blue ash trees produced a much higher level of callous tissue around artificial wounds than field-grown white ash, which suggests a heightened ability to repair phloem damage by this species. Finally, Tanis and McCullough (2015) found that young blue ash trees exposed to wild EAB in a plantation in Michigan harboured substantially fewer feeding galleries and live larvae than that observed in black, green, or white ash of similar age, which may have resulted from either oviposition preferences, host resistance, or both.

In this study, we sought to determine if there would be similar patterns in the persistence of blue and white ash trees in two ‘EAB aftermath’ forests in Ohio as has been observed in Michigan, and to assess the potential for adult oviposition preferences and larval resistance to be possible explanations for the persistence of blue ash. We first compared the canopy health ratings of mature white and blue ash trees in Glen Helen Nature Preserve in Yellow Springs, OH in 2018 and again in 2021. Ash trees in this preserve were first infested by EAB in ~2011 (Cipollini, 2015), and a survey in 2012 at this site indicated that most of the mature white and blue ash trees present in this preserve were healthy at that time on the basis of a standard ash tree canopy rating system (e.g., Knight et al., 2014; D. Cipollini, personal observation). We hypothesized that by 2018 and persisting in 2021, blue ash trees would continue to survive and maintain their health better than white ash trees, in accordance with other studies. We conducted a similar study of tree health of mature blue versus white ash trees in the Wright State University Woods in 2018 and again in 2021 and also examined larval feeding gallery densities as a proxy for comparative attack rates. We expected to observe greater persistence of blue ash and less historical evidence of feeding galleries in blue ash than in white ash. Lastly, we compared EAB larval performance on blue and white ash trees in cut stem bioassays using stems cut from trees in the Wright State University Woods. We predicted that performance of EAB larvae on cut stems would be poorer on blue ash than on white ash.

中文翻译：

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翡翠螟发生后蓝灰的持续存在可能是由于成虫产卵偏好和幼虫性能下降所致

介绍

植物物种在面对快速传播的入侵昆虫时的持久性与它吸引或阻止成虫产卵的程度有关，以及在成虫选择在其上产卵时抵抗和容忍攻击的程度有关。翡翠白蜡虫 ( Agrilus planipennis Fairmaire, EAB)（鞘翅目：Buprestidae）是一种亚洲蛀木甲虫，侵入北美，已杀死数亿棵白蜡树（Fraxinus spp .）（Herms & McCullough，  2014）。相对于其主要的亚洲寄主物种水曲柳 ( Fraxinus mandshurica )，EAB 对北美白蜡树物种的成虫和幼虫表现增强，因此对它们的危害更大（例如，Rebek 等人，2008 年））。成虫的摄食率和在叶子上的存活率及其产卵偏好通常与该甲虫在不同物种韧皮部中的幼虫表现相关。EAB 对主要东部白蜡树物种的产卵偏好以及成虫和幼虫摄食性能的顺序（从最好到最差）似乎是绿蜡树 ( F. pennsylvanica Marshall) 和黑蜡树 ( F. nigra Marshall)、白蜡树( F. nigra Marshall)。 americana L. )，最后是蓝灰 ( F.quadrangulata Michx.) （ Anulewicz 等人，  2006，2008 ； Tanis和 McCullough，  2012，2015）。

在美国中西部地区，EAB 过后，蓝灰的存活率似乎比其他灰烬物种高得多。在密歇根州，我们在 EAB 侵扰期间对蓝白蜡树和白蜡树的生存和健康状况进行了数年的检查。在三年的侵扰过程中，幸存下来的白蜡树数量明显少于蓝白蜡树，并且 60% 的幸存蓝白蜡树被认为是“健康的”（Tanis & McCullough，2012  ）。密歇根州的另一项研究发现，与研究中的白蜡树相比，蓝白蜡树的成活率更高，树冠更饱满，而且平均更大、更老，因为大多数更老、更大的白蜡树都死于攻击（Spei & Kashian ，  2017）。

蓝灰在 EAB 攻击下的持续存在可能是由于多种因素，包括对成虫产卵的吸引力较低、成虫叶面取食的基质较差、韧皮部幼虫的抵抗力增强以及表现出较高的耐受性。攻击后造成伤害。在唯一一项解决成虫对蓝白蜡树吸引力问题的研究中，在北美早期寄主范围测试中，与其他更易受影响的白蜡树物种相比，蓝白蜡树在田间收到的 EAB 卵较少（Anulewicz 等人，2008 年 ）。在幼虫性能方面，Anulewicz 等人。( 2006 ) 发现，在使用笼在茎上的成虫进行的无选择生物测定中，EAB 幼虫在蓝梣木上建立了与黑、白和绿梣木上相似密度的摄食道。彼得森等人。（2015）发现，在切下的蓝白蜡树茎上，接种卵的 EAB 幼虫与在切下的绿白蜡树茎上发育并达到预蛹阶段的比例相似，但它们需要更长的时间才能完成。这表明蓝灰对于幼虫来说是较差的基质，尽管在一个季节中仍然可以积累显着的损害。与此类似，Olson 和 Rieske（2019）发现，EAB 幼虫在蓝白蜡树切茎上的存活率较低，并且在蓝白蜡树切茎上的取食量略少于在白蜡树切茎上的取食量。在同一项研究中，田间种植的蓝白蜡树在人工伤口周围产生的茧组织水平比田间种植的白蜡树高得多，这表明该物种修复韧皮部损伤的能力更强。最后，坦尼斯和麦卡洛（2015）发现，在密歇根州的一个种植园中，暴露于野生 EAB 的年轻蓝白蜡树的取食通道和活幼虫比在相似年龄的黑、绿或白白蜡树中观察到的要少得多，这可能是由于产卵偏好、寄主抗性造成的， 或两者。

在这项研究中，我们试图确定俄亥俄州两个“EAB后果”森林中蓝白蜡树和白蜡树的持久性是否与密歇根州观察到的相似，并评估成虫产卵偏好和幼虫的潜力。抵抗力是蓝灰持续存在的可能解释。我们首先比较了 2018 年和 2021 年俄亥俄州黄泉格伦海伦自然保护区成熟白蜡树和蓝白蜡树的树冠健康评级。该保护区的白蜡树于 2011 年首次受到 EAB 侵染（Cipollini，2015 年 ）， 2012 年对该地点的一项调查表明，根据标准白蜡树冠层评级系统（例如 Knight 等人，2014 年），该保护区中存在的大多数成熟白蜡树和蓝白蜡树当时都是健康的 。; D. Cipollini，个人观察）。根据其他研究，我们假设到 2018 年并持续到 2021 年，蓝白蜡树将继续比白蜡树更好地存活并保持健康。我们于 2018 年和 2021 年在莱特州立大学森林中对成熟的蓝白蜡树和白蜡树的树木健康状况进行了类似的研究，并检查了幼虫取食廊密度作为比较攻击率的代理。我们预计，与白蜡树相比，蓝蜡树的持久性会更强，而蓝蜡树中的进食画廊的历史证据会更少。最后，我们使用从莱特州立大学森林中砍下的树干进行切茎生物测定，比较了蓝白蜡树和白蜡树上的 EAB 幼虫表现。我们预测 EAB 幼虫在切茎上的表现在蓝梣木上比在白梣木上表现要差。