252 Review of the emerald ash borer (Coleoptera: Buprestidae), life history, mating behaviours, host plant selection, and host resistance Therese M. Poland,1 Yigen Chen, Jennifer Koch, Deepa Pureswaran Abstract—As of summer 2014, the invasive emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), has become established in 24 states in the United States of America and has killed tens of millions of ash trees since its introduction into Michigan in the 1990s. Considerable research has been conducted on many aspects of EAB life history, natural history, ecology, and management strategies in an attempt to contain this devastating pest. In this article, we review the life history, mating behaviours, and host plant selection by EAB in North America as well as host resistance to EAB attack. Introduction 99% within a number of years of EAB infestation (Knight et al. 2013). Forest inventories report The emerald ash borer (EAB), Agrilus planipennis almost 8 billion ash trees on United States of Fairmaire (Coleoptera: Buprestidae) is an Asian (i.e., America timberlands valued at US$282.25 billion China, Japan, Korea, Mongolia, Eastern Russian) (United States Department of Agriculture, Forest flat-headed borer that is primarily a pest of ash, Service 2008). Ash is also one of the most pre- Fraxinus Linnaeus (Oleaceae), species. It was valent trees in agricultural lands, shelterbelts, and discovered near Detroit, Michigan, United States of urban areas. The projected costs to communities America and Windsor, Ontario, Canada in 2002 and landowners for treatment, removal, and (Haack et al. 2002) and is infesting and killing replacement of urban ash trees within a 25-state native North American ash at unprecedented levels. area from 2009 to 2019 was estimated at US$10.7 Based on dendrochronological evidence, EAB billion (Kovacs et al. 2010). In response to the was likely introduced to North America in the threat posed by EAB, federal, state and provincial 1990s (Siegert et al. 2014) and has been spreading agencies imposed quarantines to restrict movement rapidly through natural dispersal and human- of ash from known infested areas, implemented assisted movement of infested logs, firewood, large-scale surveys to detect new infestations, and and nursery material. As of summer 2014, it has have supported extensive research to understand become established in 24 states in the United EAB natural history, behaviour, and host interac- States of America (http://www.emeraldashborer. tions in order to develop effective management info). It has the potential to spread and kill ash strategies. trees throughout North America. Ash mortality in In this paper, we review the life history, mating some infested forested areas could reach up to behaviours, and host plant selection by EAB. Received 8 September 2014. Accepted 15 December 2014. T. M. Poland,1 United States Department of Agriculture, Forest Service, Northern Research Station, 3101 Technology Blvd., Suite F, Lansing, Michigan 48910, United States of America Y. Chen, Department of Entomology and Nematology, University of California, One Shields Avenue, Davis, California 95616, United States of America J. Koch, USDA Forest Service, Northern Research Station, 359 Main Rd. Delaware, Ohio 43015, United States of America D. Pureswaran, Canadian Forest Service, Laurentian Forestry Centre, 1055 rue du PEPS, Québec, Québec, Canada G1V 4C7 1Corresponding author (e-mail: [email protected]). Subject editor: Krista Ryall doi:10.4039/tce.2015.4 Can. Entomol. 147: 252–262 (2015) © The Entomological Society of Canada 2015. Parts of this work are that of the US Government and therefore such parts are not subject to copyright protection in the United States. Parts of this work are that of the Canadian Government and therefore such parts are subject to Canadian Crown Copyright. Poland et al. 253 Other aspects of natural history, ecology, and and continues into May, followed by adult emer- management strategies have been reviewed else- gence approximately three weeks later (Bauer where (Crook and Mastro 2010; Herms and et al. 2004). Some EAB overwinter as young McCullough 2014). larvae in their galleries and then require a second year of development before emerging as adults Life history (Cappaert et al. 2005; Tluczek et al. 2011). Emerald ash borer generally has a one-year life Mating behaviours cycle, but may require two years to complete development in cooler climates, when attack Emerald ash borer adults become sexually densities are low, hosts are vigorous, or when mature ~10–14 days after feeding on host plants oviposition occurs in late summer (Cappaert et al. (Lelito et al. 2007; Rodriguez-Saona et al. 2007). 2005; Wei et al. 2007; Tluczek et al. 2011). In Mating behaviours are observed mostly between southern Michigan, EAB adults generally begin 10:00 and 17:00 hours during the day (Rodriguez- emerging from “D”-shaped exit holes in mid-May Saona et al. 2007) and typically take place on the at about 250 growing degree days base 10 °C host trees. Males hover around tree canopies and (DD10) (450 growing degree days base 50 °F may locate potential mates using visual cues as (DD50) (Brown-Rytlewski and Wilson 2004) and they often drop out of the air and land directly emergence continues throughout the summer. on top of females (Lelito et al. 2007). The visual Peak adult activity generally occurs in late June or cues are not sex-specific, however, since EAB early July at 514–556 DD10 (925–1000 DD50) males approach both sexes of pinned dead EAB (McCullough et al. 2009a; Poland et al. 2011) and (Lelito et al. 2007; Rodriguez-Saona et al. 2007). drops off sharply by the end of July at about 833 Olfactory cue(s) from EAB females start playing a DD10 (1500 DD50) as the initial beetles to emerge role after initial physical contact as evidenced by die off and new emergence declines (Brown- arrestment and longer copulation attempts with Rytlewski and Wilson 2004; Poland et al. 2011). females (Lelito et al. 2007) or even at a distance of Adults feed on the margins of ash leaves for up to 5 cm from EAB females (Pureswaran and 10–14 days before becoming sexually mature and Poland 2009a). Mating is prolonged, lasting mating (Rodriguez-Saona et al. 2007). They 50 minutes on average (Pureswaran and Poland continue to feed and mate throughout their life- 2009a). After mating, EAB pairs separate and time, which generally lasts three to six weeks there appears to be no mate guarding. In labora- (Bauer et al. 2004; Lyons et al. 2004). They are tory studies, EAB females mated repeatedly with most active on sunny days with air temperatures multiple males throughout their lifetime (Lyons above 25 °C (Wang et al. 2010) and often rest on et al. 2004). Routledge and Keena (2012) found leaves or in bark crevices on cool days and during that mating with multiple males is likely the best rainy weather (Rodriguez-Saona et al. 2007). strategy for EAB females to maximise fecundity. Emerald ash borer females deposit 60–80 eggs in Two contact pheromones, 3-methyltricosane nature and up to 258 eggs in the laboratory during (Lelito et al. 2009) and 9-methyl-pentacosane their life span (Lyons et al. 2004). Eggs are (Silk et al. 2009), have been isolated and identi- deposited individually or in clusters in bark cracks fied from cuticles of EAB females. Application or crevices (Bauer et al. 2004). of 3-methyltricosane solution to dead and Eggs hatch within two weeks at 25 °C and the dichloromethane-washed EAB females increased larvae feed in the inner phloem, outer xylem, and time male EAB spent in contact with females cambium creating serpentine-shaped galleries that as well as time spent attempting copulation. are packed with frass. Larvae have four develop- However, EAB males spent less time on washed mental instars (Cappaert et al. 2005) and most females and females on which the compound was larvae complete feeding in October or November reapplied compared with unwashed EAB females; in Michigan. Pre-pupae overwinter in cells about therefore, the effects of 3-methyltricosane might 1.25 cm deep in the sapwood of thin-barked trees be synergised by other compounds such as or in the outer bark of thick-barked trees. In 9-methyl-pentacosane (9-Me-C25), which is only southern Michigan, pupation begins in mid-April found in sexually mature females (Silk et al.2009). © The Entomological Society of Canada 2015. Parts of this work are that of the US Government and therefore such parts are not subject to copyright protection in the United States. Parts of this work are that of the Canadian Government and therefore such parts are subject to Canadian Crown Copyright. 254 Can. Entomol. Vol. 147, 2015 Application of 9-Me-C25 to dead and n-hexane- Protection Organization 2013). Ash mortality washed EAB females elicited copulation attempts within stands in North America can reach up to by males similar to those observed for dead and 99% regardless of ash basal area, its relative unwashed EAB females. Furthermore, the number dominance, relative density, overall stand density, of copulation attempts and the length of arrest- stand basal area, or any measure of species ment by EAB males were similar on dead and diversity (Smith et al. 2005; Knight et al. 2013). unwashed females and on dead washed females This suggests that EAB is very efficient at locating with 9-Me-C25 reapplied (Silk et al. 2009). host trees even when they are rare within mixed One volatile pheromone, (3Z)-dodecen-12- species stands. olide [(3Z)-lactone], has been identified from sexually mature EAB adults (Bartelt et al. 2007; Visual orientation Silk et al. 2011). (3Z)-Lactone was detected from EAB preferentially attacks open grown ash both sexes by Bartelt et al.