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ISSN 1387-3547, Volume 12, Number 6 ISSN 1387-3547, Volume 12, Number 6 This article was published in the above mentioned Springer issue. The material, including all portions thereof, is protected by copyright; all rights are held exclusively by Springer Science + Business Media. The material is for personal use only; commercial use is not permitted. Unauthorized reproduction, transfer and/or use may be a violation of criminal as well as civil law. Biol Invasions (2010) 12:1839–1846 Author's personal copy DOI 10.1007/s10530-009-9594-1 ORIGINAL PAPER North American arthropods at risk due to widespread Fraxinus mortality caused by the Alien Emerald ash borer Kamal J. K. Gandhi • Daniel A. Herms Received: 21 January 2009 / Accepted: 26 September 2009 / Published online: 16 October 2009 Ó Springer Science+Business Media B.V. 2009 Abstract Emerald ash borer (Agrilus planipennis Another 30 arthropod species are associated with 1–2 Fairmaire) (EAB), an alien invasive wood-boring host plants in addition to ash, and herbivory on these buprestid beetle, is causing large-scale decline and hosts may increase as these arthropods shift from mortality of the most widely distributed species of declining ash trees. Extirpation of arthropods depen- ash (Fraxinus spp.) trees endemic to eastern North dent upon ash may unleash multiple extinctions of America. We determined which arthropod species affiliated species with which they may be inextricably that are associated with ash may become threatened, linked. The demise of North American ash species endangered, and co-extinct with the demise of ash as due to EAB is expected to lead to biotic loss with a dominant tree species. A literature survey revealed cascading ecological impacts and altered processes that 43 native arthropod species in six taxonomic within forested ecosystems. groups (Arachnida: Acari; Hexapoda: Coleoptera, Diptera, Hemiptera, Hymenoptera, and Lepidoptera) Keywords Agrilus planipennis Á are known to be associated only with ash trees for Arthropods Á Ash Á Biodiversity Á Emerald ash borer Á either feeding or breeding purposes, and thus face Extirpation Á Extinction Á Fraxinus Á high risk of endangerment. Most of these species are Invasive species Á North America gall-formers followed by folivores, subcortical phloem/xylem feeders, sap feeders, and seed predators. Introduction Electronic supplementary material The online version of this article (doi:10.1007/s10530-009-9594-1) contains During the last two centuries, anthropogenic distur- supplementary material, which is available to authorized users. bances have resulted in large-scale alterations to North K. J. K. Gandhi (&) American forests, leading to widespread decline in Daniel B. Warnell School of Forestry and Natural forest biodiversity (Lovett et al. 2006). Species Resources, The University of Georgia, Athens, extinction rates have increased 1,000 fold since pre- GA 30602, USA e-mail: [email protected] settlement times, with up to 20% of native species becoming extinct in many taxonomic groups (Chapin D. A. Herms et al. 2000). Major disturbances include loss and Department of Entomology, Ohio Agricultural and changes in habitat, fragmentation, climatic changes, Research Development Center, The Ohio State University, 1680 Madison Avenue, Wooster, and establishment of alien species (Gandhi and Herms OH 44691, USA 2009). In particular, invasion by exotic species is 123 1840 Author's personal copy K. J. K. Gandhi, D. A. Herms among the most insidious cause of decline and The wide-scale decimation of an important over- extirpation of native species diversity within forested story tree species within a short-time could unleash a landscapes (Vitousek et al. 1997; Lovett et al. 2006). staggering cascade of direct and indirect effects on The number of exotic insects and other species that are forest ecosystems (Mattson 1997; Gandhi and Herms introduced and established in North America is 2009). Fraxinus ranks among the most abundant tree predicted to continue climbing concurrently with genera in forests of northeastern US. Ash species rank international trade (Liebhold et al. 1995; McCullough among the most widely distributed tree species in et al. 2006). eastern North America, and are a component of more Emerald ash borer (Agrilus planipennis Fairmaire) than 26 forest cover types (Burns and Honkala 1990; (EAB) is a phloem-feeding wood-boring beetle Cappaert et al. 2005). In communities in which they (Coleoptera: Buprestidae) indigenous to eastern Asia occur, ash can also rank among the most abundant (Cappaert et al. 2005). It was first detected in North tree species. For example, a survey estimated 3.8 America in 2002 in Michigan near Detroit (Haack billion white ash (F. americana L.) trees in Ohio, et al. 2002; Cappaert et al. 2005). This invasive insect ranking it among the five most common tree species aggressively colonizes and kills all major North in the state (Griffith et al. 1993). Ash species American species of ash (Fraxinus spp.) that it has contribute significantly to nutrient cycling within encountered (Cappaert et al. 2005; Poland and hardwood forests (Reiners and Reiners 1970), and are McCullough 2006). Millions of ash trees have died important sources of food and habitat for numerous within urban and forested areas in Michigan, and bird and mammal species (Martin et al. 1951; Faanes billions of ash trees throughout the continent are 1984). Thus, the ecological impacts of widespread threatened as EAB continues to spread (Herms et al. ash mortality may rival or even exceed resulting from 2004; Cappaert et al. 2005). In southeastern Michi- decline of American elm (Ulmus americana L.) and gan, ash mortality due to EAB increased to more than chestnut [Castanea dentata (Marshall) Borkh.] 50% within 3 years from 2004 to 2006 (Smith 2006; caused by Dutch elm disease [fungal agents: Ophi- Gandhi et al. 2007), and now approaches nearly ostoma novo-ulmi Brasier and O. ulmi (Buisman)] 100% in all forest stands near the epicenter of the and chestnut blight [fungal agent: Cryphonectria invasion (Gandhi et al. 2008). We anticipate similar parasitica (Murrill) Barr], respectively (Dunn 1986; trends in other forested landscapes as EAB continues Smock and MacGregor 1988). Ironically, large-scale to spread. As of September 2009, EAB has been mortality of American elm led to an increase in the detected in 13 US states including Illinois, Indiana, abundance and dominance of white ash trees in Kentucky, Maryland, Michigan, Minnesota, Mis- eastern forests (Barnes 1976). souri, New York, Ohio, Pennsylvania, Virginia, West While the loss of biodiversity due to habitat Virginia, and Wisconsin, as well as Ontario and alteration and destruction are well documented (e.g., Quebec in Canada (http://www.emeraldashborer.info), Brook et al. 2003), there is relatively little informa- and may well exist elsewhere. tion about the impacts on native biodiversity of wide- Unlike most other wood-borers, EAB colonizes scale mortality and extinction of an entire tree genus healthy as well as stressed trees in North America, caused by an alien species. Widespread ash mortality thus creating a wood-borer epidemic of unprece- will have direct effects on the fauna dependent upon dented intensity (Cappaert et al. 2005). Asian ashes ash for food, shelter, and reproduction during some appear to be much more resistant, perhaps by virtue part of their life-cycle. Indirect effects of ash of their coevolutionary history with EAB (Rebek mortality will occur at other trophic levels, impacting, et al. 2008). Because of the current lack of effective for example, parasites and predators that are depen- containment and eradication tactics (United States dent upon the faunal communities associated with ash Government Accountability Office 2006), EAB is trees (Koh et al. 2004). The objective of this paper is expected to continue to spread creating the possibility to catalog the native arthropod fauna of ash, and that the entire genus Fraxinus will be functionally assess their relative risk of endangerment and perhaps extirpated from North America within the next few extirpation, should EAB decimate ash throughout decades. North America. 123 North American arthropods at risk Author's personal copy 1841 Methodology specificity reflecting greater risk of endangerment: (1) high risk—monophagous arthropods associated only To identify arthropods associated with ash, exhaus- with ash trees; (2) high-moderate risk—biphagous tive information searches were conducted on 16 arthropods associated with one host species other than North American (north of Mexico) ash species ash; (3) moderate risk—triphagous arthropods associ- including F. americana L. (white ash), F. anomala ated with two host species other than ash; and (4) low Torr. ex S. Wats. (singleleaf ash), F. berlandieriana risk—polyphagous arthropods associated with C three DC (Mexican ash), F. caroliniana P. Mill. (Carolina host species other than ash. To better understand how ash), F. cuspidata Torr. (fragrant ash), F. dipetala each trophic level may respond to ash decline, high risk Hook. and Arn. (two-petal ash), F. gooddingii Little arthropods were further categorized on their feeding (Goodding’s ash), F. greggii A. Gray (Gregg’s ash), and breeding habits as foliage feeders, gall formers, F. latifolia Benth. (Oregon ash), F. nigra Marsh. phloem/xylem feeders, sap feeders, and seed predators. (black ash), F. papillosa Lingelsh. (Chihuahuan ash), F. pennsylvanica Marsh. (green ash), F. profunda Bush (Bush) (pumpkin ash), F. quadrangulata Michx. (blue ash),
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