INTRODUCTION

Biological invasions are occurring at unprecedented spatial and temporal scales (Ricciardi, 2007) and are considered major drivers of global change (Vitousek et al., 1996). The establishment and spread of non-native species have caused ecological impacts worldwide, threatening native biodiversity and ecosystem services (Boyd et al., 2013; Liebhold et al., 1995; Wilcove et al., 1998). Understanding the direct and indirect impacts of invasive species on native ecosystems is a research priority and will help inform the management of natural habitat and conservation of biodiversity (Byers et al., 2002; Parker et al., 1999).

Wood-boring insects, including emerald ash borer (EAB; Agrilus planipennis Fairmaire), are causing significant ecological and economic impacts in urban and natural forests of North America (Aukema et al., 2011; Hauer & Peterson, 2017; Klooster et al., 2018). Since its accidental introduction, EAB has killed hundreds of millions of ash trees (Fraxinus spp.) (Herms & McCullough, 2014; Ward et al., 2021), causing a cascade of direct and indirect ecological impacts on forest structure and function (Gandhi & Herms, 2010a; Klooster et al., 2018; Perry et al., 2018; Smith et al., 2015) that pose a significant threat to native biodiversity (Gandhi & Herms, 2010b; Wagner, 2007; Wagner & Todd, 2015). Native herbivores that utilize ash during some part of their lifecycle will be directly impacted by widespread ash loss, while cascading indirect effects will impact species at other trophic levels such as predators and parasitoids (Koh et al., 2004). Arthropods at high risk of habitat loss include native ash specialist herbivores in the taxa Acari, Lepidoptera, Hemiptera, Diptera, Coleoptera, and Hymenoptera (Gandhi & Herms, 2010b). Within these taxa, gall former and leaf miner guilds contain the highest proportion of at-risk specialists (Gandhi & Herms, 2010b; Wagner & Todd, 2015).

As EAB continues to spread across North America, the functional extirpation of native ash from urban and natural forests is a growing ecological concern (Jerome et al., 2017a, 2017b; Westwood et al., 2017a, 2017b), with implications for the community of associated fauna. For example, green ash (F. pennsylvanica Marsh.), white ash (F. americana L.), and black ash (F. nigra Marsh.) experienced greater than 99% mortality in southeast Michigan forests near the epicentre of the invasion (Klooster et al., 2014). Conversely, the Asian species Manchurian ash (F. mandshurica Fubr.), which shares a coevolutionary history with EAB, is inherently resistant (Rebek et al., 2008; Villari et al., 2016) and is colonized successfully primarily when stressed (Herms, 2015; Liu et al., 2007; Showalter et al., 2018; Wei et al., 2004).

As native ash populations decline, conservation of ash specialists in North America will be dependent in part on their ability to shift to alternative hosts (Gandhi & Herms, 2010b; Wagner, 2007), which could include EAB-resistant ash species, hybrids, as well as selections of native genotypes with resistance to EAB. Although Asian ash species are resistant to EAB, they may not be a viable conservation resource capable of supporting native biodiversity in the absence of native ash. Many non-native plant species are not preferred by and/or are unpalatable to native specialist herbivores, which limits their ability to support native herbivore communities, and thus food resources for affiliated species at higher trophic levels (Tallamy, 2004). For example, non-native early successional plant species supported lower arthropod abundance, species richness, and biomass than native plants (Ballard et al., 2013). Fewer larvae of generalist and specialist Lepidoptera species were reported on non-native plants, and non-native plant congeners supported only a subset of the diverse Lepidoptera species found on native plants (Burghardt et al., 2010). Moreover, generalist Lepidoptera larvae experienced reduced growth and survival when fed foliage from non-native plants (Tallamy et al., 2010).

Conversely, there also is evidence that some generalist herbivores prefer non-native over native plants (Agrawal & Kotanen, 2003; Maron & Vila, 2001; Parker & Hay, 2005). This pattern is predicted when a non-native plant species is introduced into plant communities that already contain a native congener, whereas non-native plants that are phylogenetically distant from native plants within the community may be less preferred by native herbivores (Agrawal & Kotanen, 2003). Therefore, native generalists may be more likely to accept Asian ash species as hosts than are specialist herbivores that have coevolved with native North American ash species.

The inherent resistance of coevolved Asian ash species to EAB provides an opportunity to develop resistant ash genotypes through hybridization of Asian and North American ash species. Although cases of intentional anthropogenic hybridization often are viewed critically and as undeserving of conservation status, hybrid species have the potential to be ecologically beneficial (Piett et al., 2015; Whitham et al., 1994). Hybrids with resistance to EAB may aid in the preservation of genetic diversity of North American ash species, as well as threatened ash specialists if the hybrids are adopted as hosts by these arthropods that otherwise may not readily colonize the Asian parent. The horticultural ash cultivar Fraxinus × ‘Northern Treasure’, a hybrid between North American black ash and Asian Manchurian ash (Davidson, 1999), was shown to have high EAB resistance in two common garden studies (Herms, 2015; Subburayalu & Sydnor, 2018), and active breeding to develop additional ash hybrids with resistance to EAB is ongoing (Koch et al., 2012, 2015). Therefore, North American × Asian ash hybrids with resistance to EAB may contribute to biodiversity conservation as North American species of ash decline by serving as a refuge for native arthropods that directly or indirectly depend on ash, especially in urban environments.

To investigate whether a North American × Asian hybrid ash could serve as a refuge for North American arthropods, we compared beetle communities and associated herbivory on North American species (green and black ash), an Asian species (Manchurian ash), and the black × Manchurian hybrid ‘Northern Treasure’ ash in a common garden experiment. Beetles (Order Coleoptera) are an abundant and diverse group of insects of which more than 20 North American species have been identified as at risk of habitat loss caused by EAB-induced ash mortality (Gandhi & Herms, 2010b; Wagner & Todd, 2015). If specialist herbivores can utilize the North American × Asian hybrid as a host, then beetle communities and levels of herbivory would be similar among North American species and hybrid ash. Alternatively, the assemblage of beetles acquired by Manchurian ash and the hybrid will represent only a subset of the community found on the North American species and experience less herbivory if specialist herbivores are unable to utilize these species as hosts.

中文翻译：

---

在翡翠灰蛀虫入侵的后期阶段，混合和非原生灰对保护灰专家的价值是有限的

介绍

生物入侵以前所未有的空间和时间尺度发生（Ricciardi，  2007 年），被认为是全球变化的主要驱动力（Vitousek 等人，  1996 年）。非本地物种的建立和传播已在全球范围内造成生态影响，威胁到本地生物多样性和生态系统服务（Boyd 等，  2013；Liebhold 等，  1995；Wilcov 等，  1998）。了解入侵物种对本地生态系统的直接和间接影响是一项研究重点，将有助于为自然栖息地的管理和生物多样性的保护提供信息（Byers 等人，  2002 年；Parker 等人，  1999 年）。

蛀木昆虫，包括翡翠蛀虫（EAB；Agrilus planipennis Fairmaire），正在对北美城市和天然森林造成重大的生态和经济影响（Aukema 等人，  2011 年；Hauer 和彼得森，  2017 年；Klooster 等人。 ,  2018 年）。自意外引入以来，EAB 已经杀死了数亿棵白蜡树（水曲柳属）（Herms & McCullough，  2014 年；Ward 等人，  2021 年），对森林结构和功能造成了直接和间接的生态影响（Gandhi & Herms，  2010a；Klooster 等人，  2018 年；Perry 等人，  2018 年；Smith 等人， 2015 年）对本地生物多样性构成重大威胁（Gandhi & Herms,  2010b ; Wagner,  2007 ; Wagner & Todd,  2015）。在其生命周期的某些部分使用灰烬的本地食草动物将直接受到广泛的灰烬损失的影响，而级联的间接影响将影响其他营养级别的物种，例如捕食者和寄生蜂（Koh 等人，  2004 年）。栖息地丧失高风险的节肢动物包括螨类、鳞翅目、半翅目、双翅目、鞘翅目和膜翅目类群中的本地灰专业食草动物（Gandhi & Herms,  2010b）。在这些分类群中，瘿原和采叶者公会包含最高比例的高危专家（Gandhi & Herms,  2010b; 瓦格纳和托德，  2015 年）。

随着 EAB 继续在北美蔓延，城市和天然林中原生灰烬的功能性灭绝是一个日益严重的生态问题（Jerome 等人，  2017a，2017b；Westwood 等人，  2017a，2017b），对社区产生影响相关的动物群。例如，绿灰 ( F. pennsylvanica Marsh.)、白灰 ( F. americana L.) 和黑灰 ( F. nigra Marsh.) 在靠近入侵中心的密歇根州东南部森林中的死亡率超过 99%。 Klooster 等人，  2014 年）。相反，亚洲物种满洲灰 ( F. mandshuricaFubr.) 与 EAB 有着共同进化的历史，具有固有的抗性 (Rebek et al.,  2008 ; Villari et al.,  2016 )，并且主要在受到压力时成功定殖 (Herms,  2015 ; Liu et al.,  2007 ; Showalter等人，  2018 年；魏等人，  2004 年）。

随着本土灰烬种群的减少，北美灰烬专家的保护将部分取决于他们转向替代宿主的能力（Gandhi & Herms,  2010b ; Wagner,  2007），其中可能包括抗 EAB 的灰烬物种、杂种，以及以及对 EAB 具有抗性的天然基因型的选择。尽管亚洲灰烬物种对 EAB 具有抗性，但在没有原生灰烬的情况下，它们可能不是能够支持原生生物多样性的可行保护资源。许多非本地植物物种不被本地专业食草动物喜欢和/或不适合本地专业食草动物，这限制了它们支持本地食草动物群落的能力，从而限制了更高营养水平的附属物种的食物资源（Tallamy，  2004）。例如，非本地早期演替植物物种支持的节肢动物丰度、物种丰富度和生物量比本地植物低（Ballard 等人，  2013 年）。据报道，在非本地植物上发现的通才和专业鳞翅目物种的幼虫较少，并且非本地植物同系物仅支持在本地植物上发现的多种鳞翅目物种的一个子集（Burghardt 等，  2010）。此外，当喂食非本地植物的叶子时，多面手鳞翅目幼虫的生长和存活率降低（Tallamy 等人，  2010 年）。

相反，也有证据表明，一些通才食草动物更喜欢非本地植物而不是本地植物（Agrawal 和 Kotanen，  2003 年；Maron 和 Vila，  2001 年；Parker 和 Hay，  2005 年）。当将非本地植物物种引入已经包含本地同源物的植物群落时，可以预测这种模式，而与社区内的本地植物在系统发育上远离本地植物的非本地植物可能不太受本地食草动物的青睐（Agrawal & Kotanen，  2003 年）。因此，与与北美本土灰烬物种共同进化的专业食草动物相比，本土通才可能更可能接受亚洲灰烬物种作为宿主。

共同进化的亚洲灰树种对 EAB 的固有抗性为通过亚洲和北美灰树种的杂交开发抗性灰树种基因型提供了机会。尽管故意人为杂交的案例经常被批评为不值得保护，但杂交物种有可能对生态有益（Piett et al.,  2015 ; Whitham et al.,  1994）。如果杂种被这些节肢动物采用作为宿主，否则这些节肢动物可能不容易在亚洲亲本中定殖，具有 EAB 抗性的杂交种可能有助于保护北美灰种的遗传多样性，以及受威胁的灰种专家。园艺灰品种白蜡树× 'Northern Treasure' 是北美黑灰和亚洲满洲灰的杂交种（戴维森，  1999 年），在两项常见的花园研究（Herms，  2015 年；Subburayalu 和 Sydnor，  2018 年）和积极育种中显示出对 EAB 的高抗性正在开发额外的抗 EAB 的灰烬杂种 (Koch et al.,  2012 , 2015 )。因此，对 EAB 具有抗性的北美×亚洲灰烬杂种可能有助于生物多样性保护，因为北美灰烬物种的减少通过充当直接或间接依赖灰烬的本地节肢动物的避难所，特别是在城市环境中。

为了研究北美 × 亚洲杂交灰是否可以作为北美节肢动物的避难所，我们比较了北美物种（绿色和黑灰）、亚洲物种（满洲灰）和黑色 ×普通花园实验中的满洲杂交“北方宝藏”灰。甲虫（鞘翅目）是一种丰富多样的昆虫群，其中 20 多种北美物种已被确定为因 EAB 引起的灰烬死亡而面临栖息地丧失的风险（Gandhi & Herms,  2010b ; Wagner & Todd,  2015）。如果专业食草动物可以利用北美×亚洲杂交种作为宿主，那么北美物种和杂交灰中的甲虫群落和食草水平将相似。或者，由满洲灰和杂种获得的甲虫组合将仅代表北美物种上发现的群落的一个子集，如果专业食草动物无法利用这些物种作为宿主，它们的食草性就会减少。