BioControl https://doi.org/10.1007/s10526-019-09986-6 (0123456789().,-volV)( 0123456789().,-volV) Augmentation of native North American natural enemies for the biological control of the introduced emerald ash borer in central Canada Justin M. Gaudon . Sandy M. Smith Received: 22 July 2019 / Accepted: 28 November 2019 Ó International Organization for Biological Control (IOBC) 2019 Abstract Agrilus planipennis Fairmaire (Col: Chalcididae) (16.67 ± 16.67%) and Atanycolus spp. Buprestidae) (EAB) has been spreading rapidly Foerster (Hym: Braconidae) (48.18 ± 4.29 %) was throughout North America, killing millions of ash observed in all plots over three years after native trees, Fraxinus spp. L. (Oleaceae). Eradication is not parasitoids were released. However, no reduction was viable, so biological control using natural enemies is seen in EAB density between the treatment and control now the leading management strategy. Little infor- plots or over time. There was no significant relation- mation is available on whether native parasitoids and ship found between predation by woodpeckers and predators can be manipulated to increase EAB mor- year or between control and parasitoid-release plots. tality. We moved freshly cut ash logs infested with However, woodpecker predation increased signifi- EAB parasitoids to field sites where there was no cantly with EAB density. Movement of ash logs record of EAB mortality by native North American containing native parasitoids to sites newly infested by natural enemies. Changes in EAB parasitism, EAB EAB, but with low native natural enemy populations, density, and woodpecker predation were monitored can increase long-term EAB mortality as an added over the following three years. Higher parasitism of component in management strategies to slow its EAB by Phasgonophora sulcata Westwood (Hym: spread. Keywords Augmentative biological control Á Handling Editor: Dirk Babendreier Biocontrol Á Agrilus planipennis Á Atanycolus spp. Á Phasgonophora sulcata Á Woodpeckers J. M. Gaudon (&) Á S. M. Smith Faculty of Forestry, University of Toronto, 33 Willcocks Street, Toronto, ON M5S 3B3, Canada e-mail: [email protected] Introduction Present Address: J. M. Gaudon The emerald ash borer (EAB), Agrilus planipennis School of Environment, Resources and Sustainability, University of Waterloo, 200 University Avenue West, Water- Fairmaire (Col: Buprestidae), is an invasive jewel loo, ON N2L 3G1, Canada beetle introduced into North America from Asia during the 1990s (Haack et al. 2002; Siegert et al. Present Address: 2014). Since then, it has shown a continued pattern of J. M. Gaudon rare Charitable Research Reserve, 1679 Blair Road, Cam- spread in all directions from intial invasion and is now bridge, ON N34R8, Canada 123 J. M. Gaudon, S. M. Smith present in five Canadian provinces and 35 US states. all with the potential to switch from native Agrilus EAB is considered one of the most damaging and Curtis (Col: Buprestidae) hosts to EAB, a closely- costly insects to invade North American forests related, introduced species. Native avian predators, because of its ability to kill healthy ash trees, Fraxinus especially woodpeckers (Picidae) such as the hairy spp. L. (Oleaceae), with up to 99% tree mortality woodpecker [Picoides villosus (L.)], downy wood- observed within a few years of arrival (Knight et al. pecker [Picoides pubescens (L.)], and red-bellied 2013). Early management efforts involved quarantine woodpecker [Melanerpes carolinus (L.)], are known strategies to isolate and eradicate known EAB popu- to increase in abundance after outbreaks of saproxylic lations, thereby limiting the spread of infested ash beetles [i.e., mountain pine beetle, Dendroctonus material (Cappaert et al. 2005). However, these were ponderosae Hopkins (Col: Curculionidae)] and Asian discontinued due to the beetle’s rapid spread, lack of longhorned beetle, Anoplophora glabripennis funding, and the cryptic nature of the wood-boring Motschulsky (Col: Cerambycidae) (Jiao et al. 2008; larvae (Liu et al. 2003; Herms and McCullough 2014). Edworthy et al. 2011). These three species have also Now, short-term management tools (e.g., quarantine been shown to attack EAB in North America with up of EAB-infested material, chemical treatment, tree to 95% mortality (Cappaert et al. 2005; Lindell et al. removal, girdled ‘‘trap trees’’) and long-term 2008; Jennings et al. 2013). Similarly, high rates of approaches such as biological control are being used EAB parasitism by native wasps [i.e., up to 71% to combat EAB in North America (Herms and mortality by Atanycolus cappaerti Marsh and Straza- McCullough 2014). nac (Hym: Braconidae) (Cappaert and McCullough Although many abiotic and biotic mortality factors 2009) and 40% mortality by Phasgonophora sulcata affect EAB populations, including natural host tree Westwood (Hym: Chalcididae) (Lyons 2010)] suggest resistance (Anulewicz et al. 2007; Tannis and McCul- that they could be augmented for biological control. lough 2012), extreme cold (Crosthwaite et al. 2011), This latter approach for managing EAB has received cold-warm-cold fluctuations (Sobek-Swant et al. 2012), little attention in North America to date. predators (Rutledge et al. 2013; Jennings et al. 2015), Successful augmentative biological control parasitoids (Duan et al. 2009, 2012), and pathogens requires key information on the most effective method (Bauer et al. 2004; Kyei-Poku and Johny 2013), none to distribute large quantities of natural enemies, have yet provided sufficient mortality to naturally optimal timing, and location for release, as well as suppress EAB. Thus, classical biological control has factors affecting subsequent dispersal and monitoring. been proposed involving the introduction of non-native In forestry, augmentation of natural enemies has been parasitoids from Asia where EAB is native, namely, explored only in a few forest systems. Notable exam- Tetrastichus planipennisi Yang (Hym: Eulophidae), ples include (1) mass release of the native egg Oobius agrili Zhang and Huang (Hym: Encyrtidae), parasitoid, Trichogramma minutum Riley (Hym: Tri- Spathius agrili Yang (Hym: Braconidae), and Spathius chogrammatidae), against outbreak populations of galinae Belokobylskij and Strazanac (Hym: Bra- native spruce budworm, Choristoneura fumiferana conidae). Recent studies show that the introduction of (Clemens) (Lep: Tortricidae) in Canada (Smith 1996), several parasitoids, especially T. planipennisi, can and (2) mass release of native parasitoids against non- cause significant EAB mortality (Duan et al. 2017). native Sirex woodwasps (Hym: Siricidae) in Australia However, these co-evolved parasitoids alone have not (Haugen and Underdown 1990). The life-history traits yet suppressed EAB populations below damaging of native parasitoids attacking EAB in North America thresholds. There remains a need to explore additional are generally unfavourable for mass rearing and biocontrol options for managing EAB spread through- release, i.e., P. sulcata has a 1:1 parasitoid:host ratio out its introduced range in North America. (i.e., solitary) and is univoltine with a long generation Augmenting native natural enemy populations time (Roscoe 2014). Thus, despite clearly showing where they are absent or in low numbers to combat promise, the only feasible way for native parasitoids to introduced species such as EAB have been used be augmented against EAB would be to move plant against at least 32 species in Canada (MacQuarrie material containing parasitoids from the field to target et al. 2013, 2016). North America is home to a rich sites with high EAB populations, similar to that used complex of native natural enemies of Agrilus beetles, against Sirex (Hauden and Underdown 1990). 123 Augmentation of native North American natural enemies for the biological control of the… To date, proof of concept and criteria for long-term Ash trees were sampled in 2013 before parasitoid- introduction, establishment, and spread of native infested logs were transported to the sites, as well as parasitoids on EAB remains to be shown. Here, we one and three years after the initial transport. In 2013, assess the relative rate of increase in parasitism and its we removed one to three logs per sample tree from two relationship to EAB density following augmentative or three trees in each plot to quantify the number of biological control of native North American natural native EAB parasitoids, number of EAB, and number enemies. Specifically, we ask: (1) does EAB para- of woodpecker holes in the log linked directly to EAB. sitism increase over time following augmentation?; In the following year (2014), we sampled fewer trees (2) do all native parasitoids respond similarly?; (3) (i.e., one or two) per plot, removing more logs (i.e., does EAB parasitism reduce EAB density?; and (4) two to four logs per tree) to conserve the number of how does predation by native woodpeckers impact living trees remaining in each plot. Due to the EAB density or parasitism over the same time? destructive nature of sampling and rapid decline of ash trees in these EAB-infested plots, a complete sample of trees in the parasitoid release and non- Materials and methods release control plots was not done in 2015, but rather all plots were examined to ensure that sufficient living Experimental design ash and viable phloem was available for EAB and its parasitoids to reinfest. In the final sampling year In 2013, woodlots near the epicentre of the initial EAB (2016) two to four logs per tree were sampled from invasion in southwestern Ontario, Canada were sur- two to seven trees per plot. Upon removal from the veyed for a source of native parasitoids attacking EAB field, logs were fully enclosed in emergence netting and suitable collection sites were identified using data and hung on hooks in a rearing chamber at a mean on EAB ash-infested logs obtained by the Canadian temperature of 22.8 ± 0.5 °C and RH of Forest Service in 2012. Three collection sites were 51.4 ± 2.9%. The length and diameter of both ends identified, two in Middlesex County, Ontario and of all logs were measured, and a mean surface area another in Elgin County, Ontario, all which had calculated for each log.