56 Chapter 8

Columbia, General Technical Report NE-277. US Department of Agriculture, Forest Service, Northeastern Research Station, Newtown Square, Pennsylvania, pp. 65–73. Lyons, D.B., Kenis, M. and Bourchier, R.S. (2002) Acantholyda erythrocephala (L.), pine false webworm (Hymenoptera: Pamphiliidae). In: Mason, P. and Huber, J. (eds) Biological Control Programmes against and Weeds in 1981-2000. CAB International, , pp. 22–28. Mayfi eld III, A.E., Allen, D.C. and Briggs, R.D. (2005) Radial growth impact of pine false webworm defoliation on eastern white pine. Canadian Journal of Forest Research 35, 1071–1086. Mayfi eld III, A.E., Allen, D.C. and Briggs, R.D. (2007) Site and stand conditions associated with pine false webworm populations and damage in mature eastern white pine plantations. Northern Journal of Applied Forestry 24, 168–176. Moreau, G. and Lucarotti, C.J. (2007) A brief review of the past use of baculoviruses for the management of eruptive forest defoliators and recent developments on a sawfl y virus in Canada. The Forestry Chronicle 83, 105–112. Staples, J.K., Bartelt, R.J. and Cossé, A.A. (2009) Sex pheromone of the pine false webworm Acantholyda erythrocephala. Journal of Chemical Ecology 35, 1448–1460. Zahner, V., Lucarotti, C.J. and McIntosh, D. (2008) Application of 16S rDNA-DGGE and plate culture to characterization of bacterial communities associated with the sawfl y, Acantholyda erythrocephala (Hymenoptera, Pamphiliidae). Current Microbiology 57, 564–569.

8 assectella (Zeller), (: )

Peter G. Mason,1 Wade H. Jenner,2,3 Andrea Brauner1, Ulrich Kuhlmann2 and Naomi Cappuccino3 1Agriculture and Agri-Food Canada, , ; 2CABI, Delémont, Switzerland; 3Carleton University, Ottawa, Ontario

8.1 Pest Status and is predicted to establish widely in eastern , Acrolepiopsis assectella (Mason et al., 2011). Cultivated (Zeller) (Lepidoptera: Acrolepiidae), native spp., particularly , A. sativum L., to , is an invasive alien pest of leek, A. porrum L. and , A. cepa L., Allium spp. (Amaryllidaceae) in North are the preferred hosts. However, nodding America. First reported in the Ottawa area onion, A. cernuum Roth, and prairie onion, in 1993 (Landry, 2007), A. assectella has A. stellatum Nutt. ex Ker Gawl., native to since spread throughout eastern Ontario North America, can support development and southern , is found in upper of A. assectella (Allison et al., 2007) and New York State, New Brunswick and are therefore potentially at risk of attack

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 8 57

from this pest. Damage is caused by the approach such as organic growers face larval stages, which feed on the aerial greater challenges. Biologically based growing tissues (Noyes, 1974). In eastern insecticides such as Bacillus thuringiensis Canada, damage is most severe in organic Berliner (Bacillaceae) and Spinosad® are production systems. In garlic, the scapes lethal to leek moth larvae (Mason et al., are destroyed early in the season and the 2006a; Allen et al., 2007; Allen and bulbs can be destroyed after harvest when Appleby, 2008), although to be effective, the crop is hung and larvae move down the they must be applied when 1st instar leek plant as it dries. Damage to can be so moth are present on plant surfaces. Float- severe that plants are unmarketable and ing row covers provide the best protection, entire crops destroyed. particularly in organic production systems, Adult A. assectella overwinter and by preventing leek moth from ovipositing become active in spring when temperatures on the crop (Mason et al., 2006b). rise above 15°C (Abo-Ghalia and Thibout, Pino and Morton (2008) investigated the 1983). Females lay eggs singly on the leaf use of Steinernema feltiae (Filipjev) surfaces, and each female lays an average (Rhabditida: Steinernematidae) against A. of 100 eggs in fi eld conditions. Soon after assectella in leeks. They observed larval hatching, 1st instar larvae mine into the mortalities of 71.1–87.7% in experimental leaf tissue where they feed, completing 5 fi eld plots and concluded that S. feltiae instars. Mature larvae exit from the inner was effective because of the moist micro- plant tissues, spin a loosely woven cocoon habitat provided by the overlapping plant on external surfaces and develop through leaves and the tunnelling habit of A. prepupal and pupal stages. Adults emerge, assectella larvae. and, depending on the time of year, In the area of origin in Europe, a number produce a new generation or enter repro- of are reported in the literature ductive to overwinter. Repro- to attack A. assectella (Table 8.1). The ductive diapause (Thibout, 1981) is complex varies from generation to gener- induced when developing larvae are ation (Plaskota and Dabrowski, 1986) and exposed to daylengths shorter than 15 h many of the species have a broad host (Abo-Ghalia and Thibout, 1982). In eastern range (Jenner and Kuhlmann, 2004). Canada, development above a threshold of Although several predators have been 7°C takes 441.7 degree-days (DD) from egg reported, no comprehensive studies have to adult (Mason et al., 2010), similar to been conducted to provide information on requirements (450 DD above 6°C) in central incidence and impact. Europe (Bouchet, 1973) but signifi cantly Jenner (2008) studied A. assectella less than the 630 DD above 6°C required in populations in Switzerland. Four Hymen- (Åsman, 2001). In eastern Ontario, optera species were reared from A. three generations can occur, marked by assectella larval hosts: two Ichneu monidae, fl ight periods in early spring, mid- to late- Diadegma chrysostictos (Gmelin) and D. June and mid-July (Mason et al., 2010). A fenestrale Holmgren; and two Eulophidae, fourth generation is probable in south- Pnigalio soemius (Walker) and P. pectini- western Ontario (Mason et al., 2011) where cornis (L.). Acrolepiopsis assectella pupae A. assectella will likely invade. were parasitized by two Ichneumonidae: Diadromus pulchellus Wesmael and Itoplectis maculator (Fabricius). Among 8.2 Background these, D. pulchellus was the only species that appeared to be host-specifi c. There are Chemical insecticides such as Matador®/ no known records of this emerg- Warrior® may provide some protection ing from hosts other than A. assectella in against A. assectella (Allen et al., 2007; the fi eld, whereas the other fi ve species Allen and Appleby, 2008). However, those have been associated with between 29 and using a reduced risk pest management 124 host species (Yu et al., 2009). 58 Chapter 8

Table 8.1. Parasitoids associated with Acrolepiopsis assectella in the European literature.

Host stage European countriesa where Parasitoid species attacked found Reference Hymenoptera: Braconidae Apanteles impurus (Nees) ? AT, BE, BG, CZ, FR, DE, HU, Plaskota and Dabrowski IE, IT, LV, LT, MN, PL, RU, (1986); Yu et al. (2009) SE, CH, GB Aphaereta brevis Tobias ? BG, CZ, HU, RU, ES, RSPL Plaskota and Dabrowski (1986); Jenner and Kuhlmann (2004); Yu et al. (2009) Microchelonus blackburni ? Jenner and Kuhlmann (2004); (Cameron) Yu et al. (2009) Microgaster globata (L.) larva AL, AM, AT, AZ, BE, BG, CZ, Jenner and Kuhlmann (2004); FI, FR, GE, DE, GR, HU, IE, Yu et al. (2009) IT, KZ, LV, LT, MD, MN, NL, NO, PL, RO, RU, SK, SI, ES, SE, CH, TR, TM, UA, GB, RS Microgaster hospes Marshallb larva BG, CZ, FI, GE, DE, HU, IE, IT, Plaskota and Dabrowski LT, MD, MN, NL, PL, RU, (1986); Jenner and SK, CH, TR Kuhlmann (2004); Yu et al. (2009) Hymenoptera: Ichneumonidae Campoletis annulata ? AT, BE, BG, CZ, DK, FI, FR, DE, Yu et al. (2009) (Gravenhorst) HU, IE, IL, IT, LV, NL, PL, RO, RU, ES, SE, GB Diadegma fenestrale larva AT, AZ, BE, BG, CZ, DK, FI, FR, Plaskota and Dabrowski (Holmgren) DE, HU, IS, IE, IT, KZ, LV, LT, (1986); Jenner and MD, NL, NO, PL, PT, RO, Kuhlmann (2004) ; Yu et al. RU, ES, SE, CH, TR, TM, UA, (2009) GB, RS Diadromus collaris AT, AZ, BE, BG, CZ, FR, DE, Jenner and Kuhlmann (2004); (Gravenhorst) GR, IT, MD, NL, PL, PT, RO, Yu et al. (2009) ES, SE, TR, TM, UA, GB, RS Diadromus pulchellus pupa BE, FI, DE, FR, PL, SE, GB Jenner and Kuhlmann (2004); Wesmael Yu et al. (2009) Diadromus varicolor ? AT, AZ, BE, BG, FI, FR, DE, HU, Jenner and Kuhlmann (2004); Wesmael NL, RO, RU, ES, SE, CH, GB Yu et al. (2009) Endromopoda nigricoxis ? PL Plaskota and Dabrowski (Ulbricht) (1986) Itoplectis europeator Aubert larva FR, HU, RO, CH, TR Yu et al. (2009) Itoplectis tunetana pupa AM, AT, AZ, BG, FR, GR, HU, Jenner and Kuhlmann (2004); (Schmiedeknecht) IT, KZ, KG, MK, MD, MN, Yu et al. (2009) PL, RO, RU, ES, CH, TR, TM, UA, UZ, RS, ME Tycherus impiger (Wesmael) pupa AT, BE, BG, CZ, FI, FR, DE, Plaskota and Dabrowski HU, IT, LI, NL, NO, PL, RO, (1986); Jenner and RU, SE, GB Kuhlmann (2004) Zaglyptus varipes larva AT, AZ, BY, CZ, DE, FI, FR, DE, Jenner and Kuhlmann (2004); (Gravenhorst)c HU, IT, LV, LT, MD, NL, NO, Yu et al. (2009) PL, RO, RU, ES, SE, TR, GB aISO 3166-1 Encoding list of countries (http://www.iso.org/iso/iso-3166-1_decoding_table); balso in USA; calso in Canada, USA; ?, no data available. Chapter 8 59

Furthermore, D. pulchellus was the most (2008) and Jenner et al. (2012) conducted abundant parasitoid on A. assectella, it was host specifi city testing and showed that in the only species found attacking A. the laboratory D. pulchellus would suc- assectella in all three generations and it cessfully develop in non-target species that was the sole species obtained from A. were taxonomically closely related to A. assectella in the fi nal generation. assectella. Experimental fi eld releases in In Canada, only a few individuals of the the area of origin demonstrated that in the following parasitoid species, Itoplectis wild D. pulchellus only attacked the target, conquisitor (Say), Scambus pterophori A. assectella (Jenner, 2008). This fi nding (Ashmead), Scambus hispae (Harris) confi rmed earlier work by Thibout (1988) (Hymenoptera: Ichneumonidae), Bracon and others that complex chemical cues are furtivus Fyles (Hymenoptera: Braconidae) involved in host location and acceptance. and Conura albifrons (Walsh) (Hymen- Thus, D. pulchellus can be considered to optera: Chalcididae) have been reared from be host specifi c. A. assectella (Mason et al., 2010). Among Jenner et al. (2010b) assessed the effi cacy these C. albifrons is the most common. of D. pulchellus in fi eld trials in its native According to Yu et al. (2009), C. albifrons range in central Europe by simulating is an endoparasitoid/facultative hyper- introductory releases. In a 2-year study, parasitoid with a very broad host range in experimental leek plots were artifi cially several orders; B. furtivus is an infested with A. assectella larvae to mimic ectoparasitoid of Gelechiidae and Noctui- the higher pest densities common in dae; I. conquisitor is a prepupal-pupal Canada. Diadromus pulchellus adults were parasitoid of Lepidoptera, Coleoptera and mass-released into the fi eld plots when the Hymenoptera (171 recorded hosts); S. fi rst A. assectella cocoons were observed. pterophori is a larval parasitoid of Lepi- The laboratory-reared agents reproduced doptera and Coleoptera; and S. hispae is a successfully in all trials and signifi cantly larval, prepupal/pupal endo- or ecto- reduced A. assectella survival. Accounting parasitoid of Lepidoptera and Coleoptera for background parasitism by naturally (103 recorded hosts). occurring D. pulchellus, the released individuals parasitized at least 15.8%, 43.9%, 48.1% and 58.8% of the available 8.3 Biological Control Agents hosts in the four release trials, respectively. When this signifi cant mortality is combined 8.3.1 Pathogens with other mortality factors reported by Jenner et al. (2010a), the total pupal Bacillus thuringiensis Berliner serovar. mortality increased from 60.1% to 76.7%. kurstaki (Btk) was lethal to A. assectella in Jenner et al. (2010c) conducted labora- laboratory bioassays, however, fi eld trials tory and fi eld experiments on the over- have shown no signifi cant differences in A. wintering capacity of immature and mature assectella larval numbers between Btk D. pulchellus. They concluded that D. treated plants and untreated plants (Mason pulchellus overwinters primarily, if not et al., 2006a). Since larvae must consume a exclusively, in the adult stage. Results lethal dose, their habit of boring into plant indicated that among adults, females tissues in the 1st larval instar likely protects demon strated greater cold hardiness than them from surface application of Btk. males. Their results suggested that D. pul- chellus should survive winters in the tar- geted release areas of Ontario and Quebec. 8.3.2 Parasitoids A petition for release of D. pulchellus in Canada (Mason et al., 2009) was approved Diadromus pulchellus is the only natural and releases were made in 2010, 2011 and enemy so far investigated as a potential 2012 (Table 8.2). Progeny of D. pulchellus classical biological control agent. Jenner collected from the Seeland region of west- 60 Chapter 8

Table 8.2. Releases and recoveries of Diadromus pulchellus in Ontario during 2010–2012. Location Geographic coordinates Release date Number Recoveries and notes Ottawa 45.3886°, −75.7127° June 2010 648Ƃ, 185ƃ 18 D. pulchellus recovered from sentinel A. assectella in 2010; 1 D. pulchellus recovered from wild A. assectella in 2011 (year after release) June 2012 171Ƃ, 138ƃ July 2012 144Ƃ, 126ƃ August 2012 607Ƃ 641ƃ no recoveries to date Union Hall 45.1441°, −76.2936° September 2010 254Ƃ, 250ƃ no recoveries July 2012 22Ƃ, 131ƃ no recoveries to date August 2012 250Ƃ, 279ƃ Arklan 45.0845°, −76.3407° June 2011 573Ƃ, 478ƃ 5 D. pulchellus recovered from July 2011 287Ƃ, 165ƃ sentinel A. assectella in 2011; 3 D. pulchellus recovered from sentinel A. assectella in 2012 (year after release) June 2012 331Ƃ, 259ƃ 5 D. pulchellus recovered from July 2012 280Ƃ, 212ƃ sentinel A. assectella in year of August 2012 531Ƃ, 586ƃ release Lloyd 45.1438°, −76.3193° July 2011 202Ƃ, 45ƃ no recoveries June 2012 100Ƃ, 53ƃ no recoveries to date July 2012 40Ƃ, 33ƃ August 2012 76Ƃ, 73ƃ central Switzerland (46.9883°, 7.1222°) and 3. Development of a molecular toolkit to Delémont, Switzerland (47.3564°, 7.3267°) identify and quantify parasitism by D. pul- were the source of individuals released. chellus in fi eld samples; 4. Continued monitoring of non-target spe- cies, such as Plutella xylostella (L.) 8.4 Evaluation of Biological Control (Lepidoptera: ), to validate host specifi city predictions and impact on local It is too soon to determine if D. pulchellus ; has established. Recovery of individuals 5. Assess additional parasitoids, e.g. the from sentinel A. assectella pupae during larval parasitoids Aphaereta brevis Tobias the years of release indicates that D. (Hymenoptera: Braconidae) and Diadegma pulchellus females are fi nding and fenestrale (Holmgren) (Hymenoptera: ovipositing in hosts in the fi eld. The Ichneu monidae), and the pupal parasitoids recoveries in the years following release Diadromus collaris (Gravenhorst), Dia- confi rms that adult D. pulchellus can dromus varicolor Wesmael, Dolichogenidea survive winter conditions. impura (Nees) and Phaeogenes impiger Wesmael (Hymenoptera: Ichneumonidae); 8.5 Future Needs 6. Evaluation of nematodes for inundative biological control of A. assectella. Further work should include: 1. Additional releases of D. pulchellus to Acknowledgements ensure that a population establishes; 2. Developing methods for mass produc- Ana Maria Farmakis, Louis Gagnon, tion of D. pulchellus to provide the needed Llewellyn Haines, Melanie Lacroix, Jake numbers for rapid establishment and dis- Miall, Kathryn Makela, Tom Parlee, Warren persal; Pringle, Michael Sarazin and Michael Chapter 8 61

Wogin provided technical assistance. Jack Bennett (Ichneumonidae), Henri Goulet Hinton, Glennis Harwig, Mike Gillespie, (Braconidae) and Gary Gibson (Chalci- Jack Fraser, Ron Farmer, John Moore, didae). The Agriculture and Agri-Food David and Inez McCreery and Dave Cornell Canada, Improving Farming Systems and are gratefully acknowledged for their Practices Initiative grant MU03-Ent2 and collaboration and on-site guidance about the Pesticide Risk Reduction Programme the leek moth in their crops. Expert grants PRR03-360 and PRR10-030 provided identifi cations were provided by Drs Andy funding.

References

Abo-Ghalia, A. and Thibout, E. (1982) Fréquence de la diapause reproductrice en fonction de l’évolution de la photopériode à températures constantes et recherche du stade sensible chez une souche d’Acrolepiopsis assectella (Lepidoptera, Hyponomeutoidea). Annales de la Société Entomologique de 18, 173–179. Abo-Ghalia, A. and Thibout, E. (1983) Levée de la diapause imaginale et reprise de l’activité sexuelle chez la teigne du poireau (Acrolepiopsis assectella) Zell. (Lepidoptera). Agronomie 3, 717–722. Allen, J.K. and Appleby, M. (2008) Evaluation of organic and conventional insecticides for control of leek moth on garlic and onion, 2007. Pest Management Research Report 46, 92–94. Allen, J.K., Appleby, M. and Mason, P. (2007) Evaluation of organic and conventional insecticides for control of leek moth on garlic and onion, 2006. Pest Management Research Report 45, 56–59. Allison, J., Jenner, W., Cappuccino, N. and Mason, P.G. (2007) Oviposition and feeding preference of Acrolepiopsis assectella Zell. (Lepidoptera: Acrolepiidae). Journal of Applied Entomology 131, 690–697. Åsman, K. (2001) Effect of temperature on development and activity periods of the leek moth Acrolepiopsis assectella Zell. (Lep., Acrolepiidae). Journal of Applied Entomology 125, 361–364. Bouchet, J. (1973) La prevision des attaques de la teigne du poireau a la station d’avertissements agricoles des pays de la Loire. Phytoma-Défense des Cultures 25, 24–28. Jenner, W.H. (2008) Evaluation of a candidate classical biological control agent and critical assess- ment of suggested host specifi city testing guidelines. PhD thesis, Carleton University, Ottawa. Jenner, W. and Kuhlmann, U. (2004) Biological control of leek moth, Acrolepiopsis assectella. Annual Report 2004/2005, Unpublished Report, CABI Bioscience Switzerland Centre, Delémont, Switzerland. Jenner, W.H., Kuhlmann, U., Mason, P.G. and Cappuccino, N. (2010a) Comparative life tables of leek moth, Acrolepiopsis assectella (Zeller) (Lepidoptera: Acrolepiidae), in its native range. Bulletin of Entomological Research 100, 87–97. Jenner, W.H., Mason, P.G., Cappuccino, N. and Kuhlmann, U. (2010b) Native range assessment of classical biological control agents: impact of inundative releases as pre-introduction evaluation. Bulletin of Entomological Research 100, 387–394. Jenner, W.H., Kuhlmann, U., Cappuccino, N. and Mason, P.G. (2010c) Pre-release analysis of the overwintering capacity of a classical biological control agent supporting prediction of establishment. BioControl 55, 351–362. Jenner, W.H., Cappuccino, N., Kuhlmann, U. and Mason, P.G. (2012) Manipulation of parasitoid state infl uences host exploitation by Diadromus pulchellus Wesmael (Hymenoptera: Ichneumonidae). Biological Control 63, 264–269. Landry, J.-F. (2007) Taxonomic review of the leek moth genus Acrolepiopsis (Lepidoptera: Acrolepiidae) in North America. The Canadian Entomologist 139, 319–353. Mason, P.G., Appleby, M., Callow, K. and Allen, J. (2006a) Effects of Bacillus thuringiensis and Spinosad on leek moth in garlic and onion. Pest Management Research Report 44, 32–40. Mason, P.G., Appleby, M., Callow, K., Allen, J., Fraser, H. and Landry, J.-F. (2006b) Leek Moth Acrolepiopsis assectella (Lepidoptera: Acrolepiidae) a Pest of Allium spp.: Biology and Minor Use Insecticide Registration. Final Project Report to ‘Improving Farming Systems Program’, AAFC Pest Management Centre (15 May 2006). 62 Chapter 9

Mason, P.G., Jenner, W.H., Landry, J.-F., Cappuccino, N. and Kuhlmann, U. (2009) Petition to introduce Diadromus pulchellus Wesmael (Hymenoptera: Ichneumonidae) as a classical biological control agent for leek moth, Acrolepiopsis assectella (Zeller) (Lepidoptera: Acrolepiidae), in Canada. Submission to the Canadian Food Inspection Agency, 21 May 2009. Mason, P.G., Appleby, M., Juneja, S., Allen, J. and Landry, J.-F. (2010) Biology and development of Acrolepiopsis assectella (Lepidoptera: Acrolepiidae) in eastern Ontario. The Canadian Entomologist 142, 393–404. Mason, P.G., Weiss, R.M., Olfert, O. and Landry, J.-F. (2011) Actual and potential distribution of an invasive alien Allium spp. pest, Acrolepiopsis assectella (Zeller) (Lepidoptera: Acrolepiidae), in Canada. The Canadian Entomologist 143, 185–196. Noyes, J.S. (1974) The biology of the leek moth. assectella (Zeller). PhD thesis, University of London, UK. Pino, F.G. del, and Morton, A. (2008) Effi cacy of Steinernema feltiae against leek moth Acrolepiopsis assectella in laboratory and fi eld conditions. BioControl 53, 643–650. Plaskota, E. and Dabrowski, Z.T. (1986) Biological principles of leek moth (Acrolepia assectella Zellar, Lepidoptera: Plutellidae) control. II. Biology. Annals of the Warsaw Agricultural University 13, 35–46. Thibout, E. (1981) Observations préliminaires et caractérisation de la diapause reproductrice chez la teigne du poireau, Acrolepiopsis assectella Zell, (Lepidoptera, Hyponomeutoidea). Acta Œcologica/Œcologia Generalis 2, 171–182. Thibout, E. (1988) La spécifi cité de Diadromus pulchellus [Hyménoptère: Ichneumonidae] vis-à-vis de son hôte Acrolepiopsis assectella, la teigne du poireau. Entomophaga 33, 439–452. Yu, D.S., van Achterberg, C. and Horstmann, K. (2009) Taxapad: Scientifi c names for information management. Available at: http://www.taxapad.com/taxapadmain.php (accessed 22 December 2011).

9 Agrilus planipennis Fairmaire, Emerald Ash Borer (Coleoptera: Buprestidae)

D. Barry Lyons Natural Resources Canada, Canadian Forest Service, Sault Ste Marie, Ontario

9.1 Pest Status It probably entered North America in wood-packaging material in a shipping The emerald ash borer, Agrilus planipennis container, probably in the early 1990s Fairmaire (Coleoptera: Buprestidae), is an (Cappaert et al., 2005). As of October 2012, Asian species, fi rst discovered in North A. planipennis has been detected in 18 America in 2002 around Detroit, Michigan states in the USA (Connecticut, Illinois, and Windsor, Ontario (Haack et al., 2002). Indiana, Iowa, Kansas, Kentucky, Maryland, © Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013