Biological Control 28 (2003) 332–345 www.elsevier.com/locate/ybcon

Introduction and establishment of for the biological control of the ermine , malinellus (: Yponomeutidae), in the Pacific Northwest

Thomas Unruh,a,* Richard Short,a Franck Herard,b Kim Chen,b Keith Hopper,b,d Robert Pemberton,c,1 Jang Hoon Lee,c,2 Lawrence Ertle,d Kenneth Swan,d Roger Fuester,d and Eric LaGasae

a Yakima Agricultural Research Laboratory, 5230 Konnowac Pass Rd., Wapato, WA 98902, USA b European Biological Control Laboratory, Campus International de Baillarguet, CS90013 Montferrier sur Lez, 34989 St. Gely du Fesc, France c Asian Parasite Laboratory, Seoul, Republic of Korea d Beneficial Research Laboratory, Newark, DE 19713, USA e Washington Department of Agriculture, P.O. Box 42560, Olympia, WA 98504, USA

Received 13 September 2002; accepted 13 April 2003

Abstract

Four parasitoids were imported from five countries in Eurasia and released in northwestern Washington, US, to control the apple (AEM), Zeller, which colonized the Northwest around 1981. From 1988 to 1991, 95,474 in- dividuals of Ageniaspis fuscicollis (Dalman) from France, China, Korea, and Russia were released in Washington. Parasitism of AEM increased 4- to 5-fold over that produced by preexisting natural enemies between 1989 and 1994 at 22 monitored sites. Subsequently, the wasp dispersed up to 20 km from release sites. A. fuscicollis also parasitized the cherry ermine moth, Yponomeuta padellus (L.), which was discovered in the Pacific Northwest in 1993. A total of 1813 individuals of Herpestomus brunnicornis (Gravenhorst) from France, Korea, and Japan were released in 1989–1991, and 26 wasps were recovered in 1994–1995. From 1989 to 1991, 2647 Diadegma armillata (Gravenhorst) individuals from France were released. D. armillata was recovered at one site in 1991 two months following release, but no other recoveries have been made. A total of 8274 Eurystheae scutellaris (Robineau- Desvoidy) individuals were released in 1989 to 1991. However, this tachinid has not been recovered. A consistent decline of AEM populations occurred in 1989–1995, including at sites where A. fuscicollis was not recovered, suggesting other factors also contributed to this pestÕs decline. Now well established in western Washington, A. fuscicollis may help suppress future outbreaks of Y. malinellus and its congener, Y. padellus. Published by Elsevier Science (USA).

Keywords: Yponomeuta malinellus; Ageniaspis fuscicollis; Herpestomus brunnicornis; Apple ermine moth; Biological control; Northwestern USA

1. Introduction temperate regions of the Palaearctic. It is one member of a complex of host-differentiated defoliators known as The apple ermine moth (AEM), Yponomeuta ma- the small ermine (Menken et al., 1992). AEM was linellus Zeller (Lepidoptera: Yponomeutidae), is a uni- first seen in nursery plantings on Vancouver Island, voltine defoliator of found throughout the British Columbia, Canada, in 1981 and 1982. In 1985, it was broadly established and causing significant tree * Corresponding author. defoliation in the lower Fraser River Valley east of E-mail address: [email protected] (T. Unruh). Vancouver and in northwestern Whatcom Co., Wash- 1 Present address: Invasive Plant Research Laboratory, USDA- ARS, Ft. Lauderdale, FL 33314, USA. ington, US (Anonymous, 1985). By 1990 the species was 2 Present address: Research Institute for Natural Science, Dongguk trapped throughout Washington State and was found in University, Seoul 100-715, Republic of Korea. Oregon in 1991 (Unruh et al., 1993).

1049-9644/$ - see front matter. Published by Elsevier Science (USA). doi:10.1016/S1049-9644(03)00101-4 T. Unruh et al. / Biological Control 28 (2003) 332–345 333

Throughout Europe, AEM occurs at low, sub-eco- weeks, but remain beneath the egg mass covering (hi- nomic levels punctuated by sporadic outbreaks that can bernaculum) through winter. Larval stages of ermine cause significant damage to apple orchards. Applica- moths are found in colony-like aggregations usually tions of synthetic insecticides or Bacillus thuringiensis composed of siblings from the same egg mass. With Berliner to control codling moth, Cydia pomonella (L.), bud-break in early spring, first-instar larvae collectively and various leaf rollers usually preclude damage by leave the hibernaculum and mine a single leaf. They are AEM in commercial apple orchards in western Europe. defoliators in the second through fifth-instars, produc- However, in areas where fewer insecticides are used, ing a loose silken tent around their aggregations and one AEM remains an important apple (e.g., USSR, or more leaf clusters. Mature larvae aggregate even Nosyreva, 1981). Specialized parasitoids in Eurasia of- more tightly and spin their cocoons together in a tight ten cause parasitism of ermine moths in excess of 50% cluster, often under undamaged leaves. Pupation in (Affolter and Carl, 1986) whereas, in Washington, par- early summer is followed by adult emergence in one to asitoids cause less than 5% parasitism of AEM (Unruh two weeks (Junnikkala, 1960). Moth flight continues et al., 1993). In the absence of effective natural enemies, from early July into early September in northwestern AEM was perceived as an impediment to the develop- Washington (Unruh et al., 1993). ment of an integrated pest management program for Yponomeuta padellus, the cherry or hawthorn ermine apples based on pheromone disruption of the codling moth, is nearly indistinguishable morphologically, both moth, then being developed in Central Washington as larvae and adults, from Y. malinellus (Arduino and (Calkins, 1998; Howell et al., 1992). In late 1987, we Bullini, 1985; Herrebout and Menken, 1990; Menken et began a program to collect, import, and establish al., 1992; Povel, 1984). However, they are distinct as promising parasitoids of AEM from its native range. pupae (Povel, 1984) and in mitochondrial DNA se- Herein we summarize information on collection, quar- quence (Sperling et al., 1995). The species-pair was re- antine, and release of four species, subsequent recover- ferred to as host races of a single species (padellus)in ies, and parasitism rates for the years 1988–1995. This earlier literature (Friese, 1963; Thorpe, 1928). The major study complements and expands on a recent report of host plants of Y. padellus in Europe are Crataegus spp. the parallel program for introductions against AEM in and Prunus spp. (Menken et al., 1992). The species was British Columbia (Cossentine and Kuhlmann, 2000). detected in southwestern British Columbia in 1993, in The parasitoids of the small ermine moths of Europe Whatcom Co., Washington, in 1994, and in six addi- and the Soviet Union have been extensively studied tional counties in 1995 (Sperling et al., 1995, E.L. un- (Affolter and Carl, 1986; Beirne, 1943; Dijkerman et al., published). In contrast to Y. malinellus, Y. padellus 1986; Friese, 1963; Junnikkala, 1960; Kuhlmann, 1996), populations in the Northwest have remained at low while those in Korea, Japan, and China are more poorly densities since their detection (E.L. and T.U., unpub- known (see Friese, 1963). More than 50 species of par- lished observations). Parasites of Y. padellus and Y. asitoids or hyperparasitoids have been associated with malinellus broadly overlap, but host-associated differ- the small ermine moths in Europe, but only a few of ences in encapsulation rates of D. armillata have been these are common (Affolter and Carl, 1986). Several observed (Dijkerman, 1990; Heerard and Preevost, 1997). authors implicate parasitoids as regulating ermine Ageniaspis fuscicollis is a polyembryonic, endopha- moths in Eurasia (Affolter and Carl, 1986; Kuhlmann gous, egg-larval of Yponomeuta spp. and a few et al., 1998; Pyornila and Pyornila, 1979; Vaclav, 1958). other Yponomeutidae species (Blackman, 1965). The We selected four species to import: Ageniaspis fusci- female wasp mates immediately after emergence, dis- collis (Dalman) (Hymenoptera: Encyrtidae), Herpesto- covers a host egg-mass and lays one or two eggs into each mus brunnicornis (Gravenhorst), Diadegma armillata of several host eggs in the mass (Kuhlmann, 1994). The (Gravenhorst) (Hymenoptera: Ichneumonidae), and parasitoid spends the winter as an egg within the diap- Eurystheae scutellaris (Robineau-Desvoidy) (Diptera: ausing first-instar larvae of the host. Multiple embryos Tachinidae). Parasitoids were selected using two criteria: develop from the egg during the middle instars of the (1) they produced significant parasitism (>40%) in more host in early summer, and they finish consuming internal than one study in Europe; and (2) published host re- host tissues after it spins its cocoon, but before pupation. cords were predominately from Yponomeuta spp. (see The host larval exoskeleton becomes mummified and also Hopper, 1995). takes on the shape of the 25–150 wasp pupae that it encloses. Adults emerge from this mummy about two 1.1. Biologies weeks after moth emergence and are thus highly syn- chronized with the availability of host eggs (Junnikkala, Yponomeuta malinellus is a monophagous, univoltine 1960; Neenon, 1978). A. fuscicollis is widely distributed in defoliator of apples. A female lays eggs in masses (about the Palaearctic and is consistently the dominant parasite 50 eggs/mass) on 1–3-year-old branches from mid to late of the ermine moths (Affolter and Carl, 1986). Parasitism summer. Larvae hatch from the eggs in about three rates range from 5 to 98% in Eurasia and often have been 334 T. Unruh et al. / Biological Control 28 (2003) 332–345 reported to exceed 20% (Affolter and Carl, 1986; in France (1988–1991), Korea (1989–1991), Japan Blackman, 1965; Friese, 1963; Kuhlmann, 1994). (1989–1990), China (1990–1991), and Russia, S.S.R. Herpestomus brunnicornis is a solitary, endophagous, (1991) by USDA-ARS European Parasite Laboratory, late-larval or pupal parasite of Yponomeuta spp. It is Behoust, France (EPL), and Asian Parasite Laboratory univoltine, passing the fall, winter, and spring as an (APL), Seoul, Korea. passed through quarantine adult (Affolter and Carl, 1986; Kuhlmann, 1996; at the USDA-ARS Beneficial Insect Research Labora- Thorpe, 1930). Upon emergence, just after AEM in mid tory (BIRL), Newark, DE, and were released into in- to late summer, the wasps mate. Eventually, females find fested sites in western Washington by the USDA-ARS overwintering sites, and males die before winter (Kuhl- Yakima Agricultural Research Laboratory (YARL), mann, 1996). Early the following summer, females find Yakima, WA, and the Washington Department of Ag- and parasitize fifth-instars, prepupae, or pupal hosts. riculture (WSDA), Olympia, WA. Because AEM is Rearing records of H. brunnicornis are entirely Ypo- univoltine and difficult to rear in the laboratory and the nomeuta species (Kuhlmann, 1996) and it is thus the parasitoids are substantially or wholly dependent on this most host-specific parasite of those introduced. Para- host, we proceeded with a direct collect, ship, quaran- sitism of 50% has been reported, but in most studies it is tine, and release effort. No rearing through one or more less than 10% (Affolter and Carl, 1986). The wasp also generations were conducted in quarantine. kills a significant number of hosts through host feeding (Kuhlmann, 1996). 2.1. Foreign collections and shipments Diadegma armillata is a solitary, endophagous, par- asitoid of mid-stage larvae. It attacks Yponomeuta spe- Unless otherwise noted, all larvae were collected from cies in the early summer and emerges from host pupae in feral apple trees or abandoned or unsprayed apple or- midsummer. It has also been recorded from various chards of various varieties (Malus domestica Borkh.). Yponomeutidae, Torticidae, , and Coleo- Egg-larval, larval, and pupal parasitoids all emerge from phoridae (Affolter and Carl, 1986; Friese, 1963; Jun- the cocooned host larvae or pupae, hence, collections nikkala, 1960 and references therein). In northern usually consisted of cocoon-clusters. When mid to late- Europe, D. armillata may be univoltine (Thorpe, 1930). stage larvae were collected, they were reared to the co- In southern Europe it is bivoltine and in the second cooned pupae in the laboratory on bouquets of apple generation it may attack late-developing univoltine Yp- foliage. Shipments from foreign laboratories to quar- onomeuta spp. (Pyornila and Pyornila, 1979) and the antine were of three types: Ageniaspis-mummified host bivoltine Yponomeuta virginopuntatis Retzius (Dijker- larvae removed from the host cocoons; adults of the man, 1987). Various authors have speculated that it may solitary parasitoids; and host cocoon-clusters. For adult overwinter on other, unknown, hosts as well (Dijker- parasitoid shipments from EPL or APL, individual co- man, 1987; Junnikkala, 1960). The species is heavily coon-clusters or cocoons were isolated into cages or hyperparasitized in Europe, and Affolter and Carl vials, respectively, adults allowed to emerge, and tar- (1986) suggested that, in the absence of this high hy- geted species were shipped once or more per week. All perparasitism, D. armillata may be a valuable natural living insects were shipped in secure, insulated contain- enemy in North America. It is the most abundant and ers to quarantine at BIRL, via Philadelphia, by air- geographically widespread larval parasitoid of Ypo- freight. nomeuta (Affolter and Carl, 1986; Junnikkala, 1960) and France. In 1988, shipments from France consisted generally second in parasitism rate after A. fuscicollis. exclusively of AEM larvae mummified by A. fuscicollis. Eurystheae scutellaris is a solitary, endophagous In 1989 and 1990, ermine moth cocoon-clusters were parasite of mid–late instar larvae. This tachinid may be shipped. In 1990 and 1991, Yponomueta cagnagellus bivoltine; Yponomeuta spp. and some are its (Hubner) was also collected from spindle tree (Euony- major hosts in Europe, at least for the first generation mus europaeus [L.]). This moth flies earlier in the season (Affolter and Carl, 1986; Silvestri, 1923). The range of than Y. malinellus and was collected to allow earlier hosts for the second generation and how it spends the release of D. armillata in Washington. D. armillata that winters are substantially unknown. It is similar to D. emerged from Y. cagnagellus in France in 1990 and 1991 armillata and A. fuscicollis in abundance and geographic were sent to the USA as adults in 1991. Most wasps range, and tends to rank third among the four target collected in 1990 were reared for three generations in the parasitoids in parasitism rates reported in the literature. laboratory in France on Y. cagnagellus feeding on bouquets of spindle tree foliage and F3 wasps were shipped to the USA together with the 1991 field collec- 2. Materials and methods tion. Additional collections of Y. malinellus and Y. ca- gnagellus were made in France, Germany, and The organization of this project consisted of foreign Switzerland in 1993 to obtain larger numbers of exploration and collection of parasitized ermine moths H. brunnicornis. Adults of this species, together with T. Unruh et al. / Biological Control 28 (2003) 332–345 335

D. armillata, and E. scutellaris, were shipped. These years were enumerated, but often only identified to importations were used for an additional release of or superfamily. D. armillata earlier in the season, to support laboratory breeding of H. brunnicornis, or frozen for genetic 2.3. Release studies. Russia. A single collection of AEM cocoons was Parasitoids were liberated into tree canopies directly made in mid-July 1991 in Pyatigorsk in the north Cau- from the paper cartons in which they had been shipped casus (Russia S.S.R.). These were carried to Switzerland to Washington. Numbers released were based on the and shipped to the USA as cocoon-clusters. Emerged A. counts made in quarantine corrected for the dead ob- fuscicollis adults were the only insects utilized from these served in the containers after release. No correction was cocoons. made for differential mortality of the sexes. All releases Asia. Tents and cocoon-clusters were collected at all were made in Whatcom, Skagit, Snohomish, King, and sites in Asia and carried or shipped to APL for pro- San Juan Counties, west of the Cascade Mountains in cessing. H. brunnicornis were allowed to emerge in Ko- Washington State. rea and were shipped to the USA as adults while A. Release sites consisted of a group of AEM-infested fuscicollis mummies were isolated and shipped prior to apple or crab apple trees in suburban and rural settings wasp emergence. In Korea, AEM were collected in that were isolated by at least 100 m from one another. 1989–1990 from feral Malus (probably baccata [L.]). Tree numbers, age, variety, and condition were highly Also, Yponomeuta evonymelus (L.) were collected from variable both within and among sites. Releases of most Prunus padus (L.). In China, AEM were collected in Chinese (1990, 1991) and Russian (1991) A. fuscicollis 1990 and 1992 in Shanxi Province from cultivated apple. were made several kilometers distant from sites where Only Ageniaspis mummies were shipped to the USA French wasps (1988, 1989) were released. Korean A. from China. In Japan, AEM were collected from Malus fuscicollis were released with a small number of French sieboldii (Regel) Rehd. and Malus baccata at high alti- wasps at one site (1989, 1990) and with larger numbers tudes (600–850 m) and from abandoned apple trees at of Russian and Chinese wasps (1991) at a second site. A moderate altitudes (200 m) in Honshu in 1989. A small similar approach was used with H. brunnicornis release collection was made on M. sieboldii in Hokkaido in sites. Exact addresses of release sites are maintained as 1990. permanent records of release data which are maintained at BIRL and in the ROBO database (Coulson, 1992). In 2.2. Quarantine 1994 and in 1995, several thousand adult A. fuscicollis that emerged from our collections in Washington (see Adult parasites were allowed to emerge from either below) were provided to the Oregon Department of isolated mummies or host cocoon-clusters at 22 °C un- Agriculture for release on Sauve Island, Oregon (Bai, der long photophase (16:8 (L:D) h) and 50 10% RH. 2000). Similarly, in 1995, emerged A. fuscicollis were When many hundreds of mummies or cocoon-clusters released near Renton and Olympia Washington, after were received in quarantine, some were placed in a cool our final collections there. room (15 °C) to delay development and to allow careful In 1993, we tried to artificially synchronize host and processing of emerging specimens. As time permitted, parasitoids by infesting apple seedlings in screen cages collections were moved to emergence cages. Parasitoids with AEM larvae whose development had been slowed were identified individually (solitary parasitoids) or in in the laboratory. A cage (2 2 2 m) of tan nylon small groups (5 wasps/vial; A. fuscicollis), were pack- screen cloth (mesh ¼ 8 6 fibers/cm) was placed over aged in USDA shipping containers (Fisher and Andres, plantings of 50, 2-year-old, apple seedlings planted in 1999), and shipped overnight to Washington within 1–5 spring. AEM egg-masses on branches were collected in days of parasitoid emergence. mid-winter and kept in cold storage until second instar Hyperparasitoids, inquilines, and other insects reared AEM larvae were observed in the field. The egg-bearing from cocoon-clusters were retained in quarantine and branch pieces were tied to seedlings in the cages and subsequently identified. Insect identifications were pro- allowed to infest them. D. armillata were released into vided by R.W. Carlson (Ichneumonidae), E.E. Grissell the cage when it contained abundant second–fourth in- (Pteromalidae), and N.E. Woodley (Tachinidae) of the star in AEM larvae. Systematic Entomology Laboratory, USDA, ARS, To increase the probability of establishment of H. Beltsville, Maryland. Voucher specimens of released brunnicornis, we tried to maintain wasps in the labora- species are maintained there and at BIRL. Hyperpar- tory over the winter. Several wasps from Japan, Korea, asitoids that emerged in 1988 from shipments of mum- and France in 1989, and from Germany and Switzerland mies from France were exhaustively enumerated and in 1991, and virtually all wasps from Europe in 1993 identified. Nontarget primary parasitoids, hyperparasi- were kept in cages under cool (10 °C), short day (8:16 toids, predators, and inquilines emerging in subsequent (L:D) h) regimes with honey, water, and shredded paper. 336 T. Unruh et al. / Biological Control 28 (2003) 332–345

AEM egg-masses were collected in mid-winter and in- parasitoid of interest had emerged (or were mummified duced to develop under long-day conditions in the lab- by Ageniaspis) divided by the number of cocoons from oratory on greenhouse grown apple seedlings in early which all parasitoids and the host had emerged. How- February. Fifth-instar larvae spinning cocoons became ever, we did consider host pupae that contained dead, available in mid–late March. Bouquets of apple foliage but fully formed ermine moth adults as living adults that containing one or more clusters of cocooning ermine presumably died from handling. Similarly, tachinidae moth were confined with nominally mated H. brunni- that successfully pupated, but that never emerged, were cornis females in glass-topped sleeve cages (Fisher and scored as living. Total parasitism by tachinidae included Andres, 1999). Several host cocoon-clusters were ex- these unemerged, presumably diapausing, tachinid pu- posed in succession to the same wasp. Subsequently paria. All other unemerged individuals, where cause of cocoon clusters were incubated at 22–24 °C with long- mortality was unidentifiable, were grouped as unknown day conditions (16:8 (L:D) h) and checked daily for mortality, and were excluded from the estimation of moth and wasp emergence. parasitism. Most of the unknown mortality occurred in the larval stage and often appeared to be predation 2.4. Recovery and parasitism (Unruh et al., 1993), but was not critically classified in this study. Recovery and parasitism samples from Washington (1988–1996) consisted of Y. malinellus and Y. padellus 2.5. Ermine moth abundance (1994–1995 only) cocoon-clusters. These were placed individually into re-sealable plastic bags in the field, kept AEM population abundance has been estimated us- cool, and transferred into 40 dram (125 ml) plastic vials ing egg mass, larval, or pupal abundance (e.g., number with screen-ventilated lids within 2 days of collection. of larvae per 100 leaf clusters; Kuhlmann, 1996), but Subsets of the cocoon-clusters each year were carefully such approaches proved unreliable for the highly diverse teased apart and individual cocoons were isolated in 4- tree ages, varieties, and conditions encountered for feral dram glass vials with cork stoppers. Samples were reared and dooryard trees in western Washington. Hence, we to emergence at 20–25 °C with long photophase (16:8 used pheromone trap data to provide a crude measure of (L:D) h) and 50 10% RH. The number of sites sampled regional population trends of AEM across years. A varied each year, beginning in 1988 with five sites prior synthetic lure based on the AEM male sex pheromone to the release of parasitoids (Unruh et al., 1993), and (McDonough et al., 1990; see also Lofstedt et al., 1986) reaching a maximum of 133 sites in 1994. Collection was used to monitor populations at 8–11 study sites in sites were in Whatcom, Skagit, and San Juan Counties 1988–1996. Pherocon 1-C traps were baited with grey of northwestern Washington in 1988–1993. In 1994– rubber septa impregnated with a two component lure 1995, Snohomish and King Counties were also included (200 lg of Z11-14:OH and Z9-12:Ac in a ratio of 200:3; in the collection survey. We attempted to collect 30 McDonough et al., 1990) and three traps were placed at cocoon-clusters from each site. Only collections with each site beginning when cocooning was observed. four or more clusters and 20 or more host cocoons have Traps were serviced every 14 days and septa were re- been used in our summaries of parasitism rate. All col- placed every 28 days. The peak trap catch for each bi- lections, regardless of size, were utilized to document weekly interval was calculated and the number of males/ natural spread of parasitoids. trap/day was used as an index of population density in Depending on year, collections occurred over a 7–21 the vicinity of the study site (Unruh et al., 1993). The day period and were timed for when most ermine moth mean over all sites of these peak trap catch indices was larvae had spun their cocoons, but before extensive calculated to provide a trend of the regional population moth flight. Each year a modest percentage (1–10%) of over 8 years. the hosts had eclosed, leaving exuviae in the cocoons as evidence. This timing was optimal to give total genera- tional parasitism because all parasitoids emerge from 3. Results and discussion the cocoons, exposure of larvae and pupae in the field was maximized, and parasitoids emerge after the moths 3.1. Collections in Eurasia (Dijkerman et al., 1986; Kuhlmann, 1996; Unruh et al., 1993). The earliest emerging parasitoid is A. fuscicollis, In 1988, 1894 cocoon-clusters of AEM were collected and it leaves behind a distinctive mummified host. No A. in France, and from these 2702 A. fuscicollis mummies fuscicollis had emerged before cocoon collections. were isolated and shipped (Table 1). In 1989–1991, 5755 After parasitoid emergence ceased in the laboratory, AEM cocoon-clusters were collected and shipped from cocoon-clusters were teased apart and evaluated. Para- five French Departments. Also in 1991, 260 laboratory- sitism rates for each species were calculated (Unruh reared F3 D. armillata adults and 791 adult D. armillata et al., 1993) as the number of cocoons from which the collected in 1991 and emerged in France were shipped. T. Unruh et al. / Biological Control 28 (2003) 332–345 337

Table 1 Living parasitoid material shipped to BIRL from the collections in France by year and Department for 1988–1993 Year Shipment Nos.a French Department Species and stage No. shipped 1988 4, 14, 16, 23 Gard A. fuscicollis mummies 502 15, 26 Puy-du Dome A. fuscicollis mummies 127 17, 20, 21, 25 Aveyron A. fuscicollis mummies 1032b 18, 19, 22, 24, 27, 28 Lozere A. fuscicollis mummies 1032b 1989 19–21, 29, 30, Gard Y. malinellus cocoons 337 24–28 Puy-du Dome Y. malinellus cocoons 300 14–18, 33, 34 Aveyron Y. malinellus cocoons 405 9–13, 23, 31, 32, 35–38, 46 Lozere Y. malinellus cocoons 714 43–45, 47 Haute-Loire Y. malinellus cocoons 303 1990 12–15, 19–26, 34 Gard Y. malinellus cocoons 1233 27–33, 35, 62, 74, 80–83 Aveyron Y. malinellus cocoons 1356 75–79, 84 Haute-Loire Y. malinellus cocoons 375 1991 34–46 Gard Y. malinellus cocoons 732 19 Gard D. armillata adultsc 260 20–22 Cevennnes D. armillata adults 791 1993d 53, 62, 63 Gard D. armillata adults 342 The host or parasitoid life stage shipped to Newark (BIRL) is also enumerated. a By addition of the prefix EBCL-yr- to this number allows cross-referencing these collections to detailed records maintained in the ROBO data base. b Coincidentally identical. c F3 generation; parents collected from Y. cagnagellus in 1990 and reared in laboratory. d Not included here are additional D. armillata, H. brunnicornis, and E. scutellaris imported from France, Germany, and Switzerland for lab propagation and genetic studies.

In 1993, additional adult D. armillata from field col- 1991. Finally, approximately five super-aggregations of lected Y. cagnagellus were reared in France and shipped. AEM cocoons were collected in Pyatygorsk, Russia, and Additional collections from Germany and Switzerland shipped to BIRL from Switzerland. in 1993 to support laboratory overwintering of H. brunnicaornis are not reported, but discussed below. 3.2. Quarantine From Korean collections, 229 A. fuscicollis mummies and 301 H. brunnicornis adults were shipped in 1989– Hyperparasitism of A. fuscicollis pupae from France 1990 (Table 2). Of the four species targeted for release in 1988 was about 2%, although hyperparasitized against AEM, only H. brunnicornis was collected in Ja- mummies also produced A. fuscicollis indicating the pan; 215 adults were shipped in 1989 and 18 adults in proportion of hyperparasitized mummies was higher. 1991. Collections from China produced 2011 mummies BIRL staff isolated 44,248 A. fuscicollis,703Pachyneu- isolated from AEM cocoons and shipped from 1990 to ron spp., and 140 Tetrastichus spp., the latter two being

Table 2 Summary of the collections in China, Korea, Japan, and Russia and the hosts stages shipped to Newark from 1989 to 1991 Year Shipment No.a Country Species and stage No. shipped Location 1989 5 Korea H. brunnicornis adults 106 Hongchon, Gangwon Prov.; Mt. Yongmoon, Kyonggi Prov. 5 Korea A. fuscicollis mummies 79 As above 7, 8 Japan H. brunnicornis adults 232 Tohoku area, Honshu 1990 8, 9, 13, 15 China A. fuscicollis mummies 1409 Huan Yuanm, Yang Gao, and Huai Ren Counties, Shanxi 5, 6 Korea A. fuscicollis mummies 150 As in 1989 5, 6 Korea H. brunnicornis adults 173 As in 1989

1991 5 China A. fuscicollis mummies 602 Tai Gu County, Shanxi CIBCES-91-1 Russia Y. malinellus cocoons 5 Pyatigorsk 11 Japan H. brunnicornis adults 18 Hokkaido 7 Korea H. brunnicornis adults 22 As in 1989 a By addition of the prefix APL-yr- to this number allows cross-referencing these collections to detailed records maintained in the ROBO database. 338 T. Unruh et al. / Biological Control 28 (2003) 332–345 hyperparasitoids. Processing these collections to ensure survival for the larval parasitoids were recorded in that hyperparasites were excluded was time-consuming Washington. In 1988, relatively low numbers (375 fe- and required that collections be kept in cold storage males/site) of A. fuscicollis were released at many sites (15 °C) to control emergence. If each mummified host (57). In 1989 and 1990 more individuals of A. fuscicollis received by BIRL in 1988 had produced 50 A. fuscicollis, were released at fewer sites (770 and 4283 females/site at then 287,750 wasps would have emerged. Only 16% of 18 and 4 sites, respectively). that estimate was processed. Both the time required to We attempted to time releases of parasitoids when identify each specimen prior to release and variable suitable host stages were present in the field. All A. emergence rates of A. fuscicollis among collections fuscicollis releases were made between mid-July and contributed to reduced utilization of emergence. Dura- mid-August in 1988–1991 and fell well within the range tion of cold storage accounted for little of the variation of available host stages (Table 5). Synchronizing / in emergence from the collections ðF1;14 ¼ 1:07; P ¼ pupal parasitoid releases with suitable host stages was 0:32; data not shown), although, collections kept in cold more difficult to achieve. Both D. armillata and E. storage for more than three weeks had emergence rates scutellaris attack mid-stage larvae (D. armillata: instars below 40 wasps. More significant, collections from some 2–4; E. scutellaris: instars 3–5; Affolter and Carl, 1986; French localities produced low emergence (Les Vignes, Dijkerman, 1987; Junnikkala, 1960). These stages were Lozeere) while others yielded high emergence rates (Arre, substantially past by the time parasitoids were released Gard; Le Buisson, Lozeere). in 1989. But large larvae (fourth to fifth instars) were The parasitic insects that emerged in quarantine from observed in the field for at least the first week of the AEM cocoons collected in 1989–1991 are enumerated in parasitoidsÕ release intervals in 1990 and for two weeks Table 3. Hyperparasitism rates were not calculated be- in 1991. The latter was a cool spring in northwestern cause some hyperparasitoids are gregarious (e.g., Di- Washington and host development was later (Table 5). brachys, Tetrastichus) and host associations remain In 1993, second and third instar AEM was abundant provisional because cocoons were not reared individu- in the field cage when D. armillata was released. The ally and other hosts may have occasionally contami- cage approach failed; soon after parasitoids were re- nated these cocoon-clusters. leased into the cages, populations of spiders exploded, virtually destroying ermine moth larvae and the par- 3.3. Releases in Washington asitoids. Herpestomus brunnicornis attacks fifth instar larvae to Over 95,000 adult A. fuscicollis from France, China, pupae of Yponomeuta (Kuhlmann, 1996; F.H., K.C. and Russia were released in 1988–1991 (Table 4). Via- unpublished data). These stages were abundant during bility of wasps shipped from BIRL was high; greater the release interval, especially in 1991 (Table 5). How- than 90% survival for A. fuscicollis and greater than 95% ever, the H. brunnicornis imported to Washington in

Table 3 Species reared in quarantine from cocoon-clusters shipped from western Eurasia or as adult parasitoids and mummies shipped from Asia in 1989– 1993a Parasitoids Type Family France Switzerland Asiab Ageniaspis fuscicollis (Dalman) Primary Encyrtidae 23,736 29 50,220 Coccygomimus disparis (Viereck) Primary Ichneumonidae 0 0 1540 Diadegma armillata (Gravenhorst) Primary Ichneumonidae 1822 33 0 Herpestomus brunnicornis Gravenhorst Primary Ichneumonidae 1998 58 447 Itoplectis spp. Primary Ichneumonidae 14 1 0 Agria mamillata Pand. Primary Sarcophagidae 4 0 0 Eurystheae scutellaris (Robineau) Primary Tachinidae 13,683 314 0 Bactromyia aurulenta (Meigen) Primary Tachinidae 36 2 1 Bessa parallela (Meigen) Primary Tachinidae 140 0 14 Elasmus sp. Hyper Elasmidae 15 0 0 Baryscapus sp. (prob. pospielovi) Hyper Eulophidae 101 0 0 Tetrastichus spp. Hyper Eulophidae 1388 0 483 Eupelmus sp. Hyper Eupelmidae 4 0 0 Mesochorus spp. Hyper Ichneumonidae 899 3 0 Mesochorus vitiator Zett. Hyper Ichneumonidae 17 0 0 Dibrachys spp. Hyper Pteromalidae 2619 0 0 All specimens were not released. a Unidentified specimens included 3390 Chalcidoidea, 954 Pteromalidae, 80 Ichneumonidae, and 21 Tachinidae (not shown in the table). b Only A. fuscicollis (2593 individuals) were enumerated from the emergence from Y. malinellus cocoon-clusters from USSR (Pyatigorsk) in 1991. T. Unruh et al. / Biological Control 28 (2003) 332–345 339

Table 4 Parasitoids released in Washington by country of origin Origin Year Speciesa Total No. Sex No. of Females (SD) No. released frozen ratiob sites per site releases France 1988 A.f. 36,655 3457 60.2 57 375.3 362.4 103 1989 A.f. 19,259 509 69.9 18 770.3 635.5 31 D.a. 369 0 76.7 6 47.2 36.8 9 E.s. 852 56 68.5 6 97.7 88.4 11 H.b. 927 50 30.5 10 47.6 33.7 19 1990 D.a. 802 0 64.1 4 128.5 48.1 10 E.s. 5091 0 48.9 4 622.8 253.6 19 H.b. 475 0 34.7 5 49.4 21.3 7 1991 D.a. 1134 0 55.1 3 208.3 276.2 4 E.s. 2331 183 51.3 4 393.0 291.7 6 1993 D.a. 342 – 69.3 1 237.0 – 1 China 1990 A.f. 28,654 1762 59.8 4 4283.0 1978.0 26 1991 A.f. 1964 0 48.8 2 480.0 170.0 3 Korea 1989 A.f. 135 0 81.5 1 110.0 – 1 H.b. 104 2 92.3 2 48.0 0.0 2 1990 A.f. 6688 250 50.4 2 1660.0 505.0 5 H.b. 148 25 55.4 1 30.0 – 1 Japan 1989 H.b. 159 56 69.3 2 51.5 1.5 2 Russia 1991 A.f. 2119 240 50.1 3 353.3 250.8 6 Also shown are number of release sites, mean number of females released per site, and specimens frozen for future studies. a A.f.—Ageniaspis fuscicollis; D.a.—Diadegma armillata; H.b.—Herpestomus brunnicornis; E.s.—Eurysthaea scutellaris. b Sex ratio (% female) was derived from all specimens including those frozen for enzymatic analyses.

Table 5 Range of release dates for parasitoids in Washington by species and year and major flight period of Y. malinellus assessed by biweekly pheromone traps Species 1988 1989 1990 1991 1993 Ageniaspis fuscicollis 7/9–8/23 7/13–8/9 7/17–8/17 7/16–8/28 – Diadegma armillata – 7/13–8/3 6/21–7/24 6/21–7/19 6/14 Eurysthaea scutellaris – 7/13–8/9 6/21–7/24 7/10–8/29 – Herpestomus brunnicornis – 7/13–8/9 6/28–7/26 – – Yponomeuta malinellusa 7/26–8/9 7/7–7/13 7/10–7/24 7/23–8/7 7/7–7/21 a Based on pheromone traps changed weekly (1989) or biweekly. The 1988 interval was the first interval trapped in that year and may incorrectly identify this fortnight as the period of peak flight; data from subsequent years suggest the peak was earlier in 1988.

1989 to 1991 appeared to be in reproductive diapause. over the winter. These attempts failed; female wasps Dissections of several females following their receipt in became sluggish and began dying in March and April each year showed that their ovaries were undeveloped each year. A few offspring were produced in early spring and no offspring were produced when hosts were ex- of 1992 by exposing ermine moth larvae (cocooning fifth posed to the wasps in the laboratory, despite observa- instar), prepupae, and pupae whose development had tions of probing and host feeding behavior. Also, males been forced in the laboratory. Host exposures in the confined in the laboratory died within a month. We laboratory in spring produced fewer wasp offspring than inferred that adult female wasps mate in late summer the number of parental females employed in the effort. and pass the winter as adults, an inference confirmed by After a similar failure in 1993, all efforts to produce KuhlmannÕs (1996) studies. Thus, wasps have about 10 parasites during the winter were abandoned. Kuhlmann months when they could disperse from the release sites (1996) encountered similar difficulties. A reliable method and survive the challenges of their new habitat in to overwinter and condition H. brunnicornis in the Washington. This further suggests that an Allee effect laboratory would be highly desirable for future intro- may be an especially important consideration in at- ductions. An alternative strategy may be to collect post- tempts to establish this promising parasitoid (Hopper diapause females from the field in Eurasia when they are and Roush, 1993). To circumvent the difficulties posed parasitizing hosts and ship them with due speed through by reproductive diapause, we attempted to keep wasps quarantine to direct release. 340 T. Unruh et al. / Biological Control 28 (2003) 332–345

3.4. Parasitoid recoveries Korean and Chinese (1989, 1990) release sites, and re- coveries there may be partially or wholly French in Three of the four parasitoid species released in 1988– origin. Overall, sequential recoveries and increasing 1993 to control AEM were recovered from the 7 years parasitism (see below) at multiple sites demonstrates of post-release collections: A. fuscicollis, H. brunnicor- that A. fuscicollis is established. At present, we have no nis,andD. armillata. Of these, only A. fuscicollis is evidence of biological differences between the geo- likely to represent a permanent establishment. A. fusci- graphical races of A. fuscicollis. collis has been found each year since 1989, the year The release and recovery sites for H. brunnicornis are following its first release in Washington. From 1989 to depicted in Fig. 2. It was recovered for the first time in 1994, A. fuscicollis was recovered from 8 of 28, 7 of 17, 1994, 3 years after its last release in 1991. Although only 17 of 31, 16 of 18, 19 of 22, and 20 of 21 release sites 22 wasps were recovered in 1994, these issued from hosts sampled in the Bellingham area of Whatcom Co., at five sites in two areas of Bellingham, one of which was Washington. Fig. 1 (inset) depicts recoveries of A. over a kilometer from the nearest release site. None of fuscicollis in relation to release sites (pooled over 1988– the H. brunnicornis were collected at a release site, 1995) in the Bellingham area. The different geographic supporting our concerns that substantial dispersal may races of A. fuscicollis are shown as well. Recovery and occur during the 10 months that adult females live. persistence at release sites suggest establishment by Recoveries from two additional sites in 1995 support the French, Chinese, and Russian races. However, because conclusion that this species established, but the small French populations were released first (1988, 1989), it is numbers recovered suggest that the permanence of this possible that they spread to both Russian (1991) and establishment is tenuous.

Fig. 1. Release and recovery sites of A. fuscicollis in western Washington from 1988 to 1995. Inset shows detail around Bellingham, Washington including geographic origin of released wasps where C—China, F—France (or unlabelled), K—Korea, and R—Russia. T. Unruh et al. / Biological Control 28 (2003) 332–345 341

Fig. 2. Release and recovery sites of H. brunnicornis near Bellingham, Whatcom County, Washington, with geographic origins of released wasps indicated.

Diadegma armillata (2 females, 5 males) was recov- Washington in relation to release sites. All release sites ered at one site in 1991. Earlier that summer large re- are not shown, but those nearest to recovery sites are leases of the parasite were made when third to fifth depicted. It is evident that the parasite has spread over instar larvae were present. We infer that the recoveries 20 km from the nearest release site in some instances. in 1991 were the progeny of wasps released earlier that This dispersal is cumulative from 1988 to 1994 or 1995 summer, and we have no evidence that wasps success- and corresponds to about 3 km/year. This reinforces the fully overwintered. No other recoveries of D. armillata caveat raised above, that putative recoveries of Russian were made through 1995 suggesting that it has not es- and Chinese wasps could also be offspring of French tablished in northwestern Washington. E. scutellaris has wasps that dispersed. Regardless of racial origin, para- not been recovered in any collection even though it was sitism rates exceeding 10% at these sites quite distant abundantly released when host were in suitable stages from release foci suggest both that A. fuscicollis is firmly in 1990 and 1991 (Table 5). It remains possible that established and likely to disperse southward following both D. armillata and E. scutellaris have established, the spread AEM. Releases of emerged individuals to but are still too rare to have been seen in recovery Sauve Island, Oregon, resulted in establishment there samples. (Bai, 2000). In 1994 and 1995, a few cocoon-clusters of Y. 3.5. Spread of A. fuscicollis padellus were collected from Crataegus tridenta in southern Bellingham, Whatcom Co. These Y. padellus In 1994 and 1995, sampling of hosts for parasite re- were parasitized by A. fuscicollis (less than 10% in covery expanded beyond the primary release areas of both years). No other parasitoids were reared. As of western Whatcom and San Juan Counties. Fig. 1 depicts 2002, Y. padellus remains uncommon in northwestern the distribution of recoveries of A. fuscicollis in western Washington. 342 T. Unruh et al. / Biological Control 28 (2003) 332–345

3.6. Parasitism rates by Ageniaspis and resident parasi- through 1995 (Fig. 4, panels 2 and 3). Resident tachinid toids parasitoids included, in roughly equal numbers, the endemic Hemisturmia parva (Bigot) and the exotic spe- Parasitism of AEM by A. fuscicollis significantly in- cies Compsilura concinnata (Meigen), the latter previ- creased during 1989–1994 at 22 sites near Bellingham, ously introduced for gypsy moth (Boettner et al., 2000). WA, where A. fuscicollis from France (20 sites) and The resident hymenopteran parasitoids were virtually all from China and Korea (2 sites) were released (Fig. 3). Itoplectis quadricingulata (Provencher) (Ichneumoni- Site-specific parasitism reached a maximum of 64%. The dae). Parasitism by flies was usually less than 2% per parasitism rate by A. fuscicollis, calculated by tent or year and parasitism by wasps was usually less than 1%. larval aggregation of AEM, was inversely related to C. concinnata, H. parva, and I. quadricingulata ac- aggregation size as observed in Germany (Kuhlmann, counted for more than 97% of all endemic parasitoids 1996; data not shown). High parasitism at many original reared with the remainder consisting of several uniden- release sites was contrasted by collections from many tified Ichneumonidae and hyperparasitism by Dibrachys other sites that displayed little or no parasitism, espe- cavus (Walker) (Pteromalidae) of unidentified solitary cially in 1994 where many non-release sites were sam- wasps. pled. Unweighted, mean parasitism by A. fuscicollis increased from 1989 to 1993, but declined slightly in 3.7. Ermine moth population trends 1994 (Fig. 4, panel 1). Parasitism by endemic parasitoids was about 5% prior to A. fuscicollis establishment Impact of A. fuscicollis on AEM populations is dif- (Unruh et al., 1993) and continued at roughly that level ficult to assess. Planned comparisons between release

Fig. 3. Parasitism rates of Y. malinellus at 22 study sites where collections were made for at least three years. Dashed line indicates samples are not from consecutive years. The site with highest parasitism in the figure received no A. fuscicollis, but it was within 250 m of a parasite release site. All other curves represent release sites and are provided with different symbols and grouped only to facilitate presentation. T. Unruh et al. / Biological Control 28 (2003) 332–345 343

onstrate that the decline of AEM was caused by A. fuscicollis. We conclude that moth populations declined from the combined effect of parasitism, abiotic factors, and generalist predators. The latter may remain the most important (Chang and Kareiva, 1999) and includes , aculeate wasps, ants, and predatory mites (Unruh et al., 1993).

4. Conclusions

Ageniaspis fuscicollis has established in northwestern Washington State following the release of over 95,000 adult wasps from France, Russia, Korea, and China. Field collections at release sites demonstrate striking increases in parasitism rates by this polyembryonic en- cyrtid. Additionally, collections at various distances away from release areas show that the parasitoid is spreading in Washington. Small collections of Y. padellus showed that it was also attacked by A. fusci- collis in northwestern Washington. Cossentine and Kuhlmann (2000) reported similar establishment data for the parallel program in British Columbia, Canada, that began in 1987 (see also Frazer, 1989; Smith, 1989). The ichneumonid H. brunnicornis may also have es- tablished following our release of over 1600 wasps from France, Korea, and Japan. However, H. brunnicornis was only recovered at a few sites in 1994 and 1995 and parasitism rates by this wasp were extremely low. We think permanent establishment is questionable. Populations of AEM declined significantly from 1989 Fig. 4. Average trends of total parasitism of Y. malinellus (open bars) to 1995 in the original outbreak areas in Whatcom and that by A. fuscicollis (filled bars; panel 1), by endemic wasps (panel County, followed by significant increases in parasitism 2), and by the endemic or adventitious tachinid flies (panel 3). Panel 4 shows the trend of the Y. malinellus meta-population in Whatcom by Ageniaspis. High rates of parasitism suggest it will County based on peak trap catch of male moths at 8 (1989–1991), and contribute to ermine moth suppression in the future, but 11 (1992–1995) study sites. only long-term studies will show the role it plays along with resident natural enemies in the suppression of er- mine moth. From a practical perspective, long-term and control (no release) sites were abandoned in 1990 studies are currently difficult to justify because of the because host cocoons could not be reliably found from low abundance of AEM in western Washington since one year to the next at many sites, including most con- 1993. If, as observed in Europe, AEM displays sporadic trol sites. We often observed that high AEM popula- outbreaks, then additional studies should be conducted tions were extirpated by generalist predators or by to determine the role played by parasitoids in sup- pesticide applications or tree removal by property pressing the outbreaks. Renewed efforts, especially re- owners. Local population trends of the moth, assessed distribution of A. fuscicollis, would be justified if AEM by peak flight catch at 11 sites in Whatcom Co., declined became abundant in the apple production areas of from 1989 to 1995 (Fig. 4, panel 4). This decline cannot Washington and Oregon or it spread and became be attributed exclusively to parasitism because it begins abundant in California. before significant parasitism by A. fuscicollis was re- corded (i.e., in 1991). Furthermore, decline at 2 of the 11 4.1. Hindsight trap locations occurred in the absence of recorded par- asitism by A. fuscicollis at those sites (data not shown). The AEM program began 3 years before HowarthÕs However, areas surrounding trap sites may have had (1991) highly visible review of non-target effects of bio- moth production reduced from parasitism by Agenia- logical control introductions, and before there was spis, thereby contributing to reductions in trap catch. In widespread evidence for the adoption of non-target the absence of isolated control sites, we cannot dem- hosts by many insect biological control agents (Boettner 344 T. Unruh et al. / Biological Control 28 (2003) 332–345 et al., 2000; Hawkins and Marino, 1997; Hennenman Blackman, D.L., 1965. A review of the literature on Ageniaspis and Memmott, 2001). The program also took place fuscicollis. CAB International Institute of Biological Control, before the vigorous debate that still continues on bio- Deleemont, Switzerland, December 1965, 10pp. Boettner, G.H., Elkinton, J.S., Boettner, C.A., 2000. Impact of an logical control safety (Follett and Duan, 1999; Howarth, introduced biological control on three species of native Saturniids. 1991; Michaud, 2000; Simberloff and Stiling, 1996; Conservation Biology 14, 1798–1806. Strong and Pemberton, 2000, 2001; Thomas and Willis, Calkins, C.O., 1998. Review of the codling moth areawide suppression 1998; Wajnberg et al., 2001), a debate that has resulted program in the Western United States. J. Agric. Entomol. 15, 327– in reforms in our practices. We introduced two special- 333. Chang, G.C., Kareiva, P., 1999. The case for indigenous generalists in ized parasitoids (A. fuscicollis and H. brunnicornis) and biological control. In: Hawkins, B.A., Cornell, H.V. (Eds.), two narrowly generalist parasitoids (D. armillata and E. Theoretical Approaches to Biological Control. Cambridge Univer- scutellaris). All would be less likely to be released today, sity Press, Cambridge, pp. 103–115. especially the more generalist species. If AEM reemerges Cossentine, J.E., Kuhlmann, U., 2000. Status of Ageniaspis fuscicollis as a significant threat in the U. S. A., we would critically (Hymenoptera: Encyrtidae), an introduced parasitoid of the apple ermine moth (Lepidoptera: Yponomeutidae). Canad. Entomol. address the risks of unintended effects posed by any of 132, 685–689. the species prior to reintroduction. This is more than Coulson, J.R., 1992. Documentation of classical biological control hindsight being better than foresight; it is applied science introductions. Crop Protect. 11, 195–205. evolving with changing standards for the safe conduct of Dijkerman, H.J., 1987. Parasitoid complexes and patterns of parasit- biological control. ization in the genus Yponomeuta Latreille (Lepidoptera, Yponom- eutidae). J. Appl. Ent. 104, 390402. Dijkerman, H.J., 1990. Suitability of eight Yponomeuta-species as hosts of Diadegma armillata. Entomol. Exp. Appl. 54, 173–180. Acknowledgments Dijkerman, H.J., De Groot, J.M.B., Herrebout, W.M., 1986. The parasitoids of the genus Yponomeuta Latreille (Lepidoptera, Yponomeutidae) in the Netherlands. Proc. Kon. Ned. Akad. van Technical assistance provided by Mike Haskett and Wetensch. C89, 379–398. JohnWraspir (WSDA, Yakima and Bellingham), Brad Fisher, T.W., Andres, L.A., 1999. Quarantine: concepts, facilities, and Higbee (USDA, Yakima), and Goen Hyoung Lee procedures. In: Bellows, T.S., Fisher, T.W. (Eds.), Handbook of (USDA, Seoul) was critical. Ren Wang (Sino-American Biological Control. Academic Press, San Diego, pp. 103–123. Biological Control Laboratory, Beijing) facilitated and Follett, P., Duan, J., 1999. Nontarget Effects of Biological Control. Kluwer Academic Publishers, Dortrecht. participated in collections in China. Klaus Carl (CABI- Frazer, B.D., 1989. Ageniaspis fuscicollis (Dalman) a parasite of the Delemont, Switzerland) assisted in collection made in apple ermine moth. Biocontrol News 2, 24. USSR. Early planning efforts by JamesKrysan (USDA, Friese, G., 1963. Die parasiten der palaaarktischen€ Yponomeutidae Yakima) are also acknowledged. VicMaestro (USDA- (Lepidoptera, Hymenoptera, Diptera). Beitr. z. Ent. 13, 311–326. APHIS, OTIS Development Center) and LesMcDon- Hawkins, B.A., Marino, P.C., 1997. The colonization of native phytophagous insects in North America by exotic parasitoids. ough and C. Smithhisler (USDA, Yakima) supplied Oecologia 112, 566–571. pheromone for survey and monitoring traps. Reviews of Henneman, M.L., Memmott, J., 2001. Infiltration of a Hawaiian various versions of the manuscript by D.R. Horton community by introduced biological control agents. Science 293, (USDA-ARS, Wapato), Barry Bai (Oregon Department 1314–1316. Yponomeuta malinellus of Agriculture), and Vincent Jones (Washington State Heerard, F., Preevost, G., 1997. Suitability of and Y. cagnagellus (Lepidoptera: Yponomeutidae) as hosts of University, Wenatchee) are gratefully acknowledged. Diadegma armillata (Hymenoptera: Ichneumonidae). Environ. Entomol. 26, 932–938. Herrebout, W.M., Menken, S.B.J., 1990. Preliminary data on the References origin of small ermine moths introduced into North America. Proc. Exp. Appl. Entomol. 1, 146–151. Affolter, F., Carl, K.P., 1986. The natural enemies of the apple ermine Hopper, K.R., 1995. Potential impacts on threatened and endangered moth Yponomeuta malinellus in Europe: a literature review. CAB insect species in the United States from introductions of parasitic International Institute of Biological Control, Delemont, Switzer- Hymenoptera for the control of insect pests. In: Hokkanen, land, November 1986, 30pp. H.M.T., Lynch, J.M. (Eds.), Biological Control: Benefits and Anonymous, 1985. Apple ermine moth new to the United States. Risks. Cambridge University Press, Cambridge, pp. 64–74. USDA APHIS PPQ Plant Pest Updates 1–2. Hopper, K.R., Roush, R.T., 1993. Mate, dispersal, number released, Arduino, P., Bullini, L., 1985. Reproductive isolation and genetic and the success of biological control introductions. Ecol. Entomol. divergence between the small ermine moths Yponomeuta padellus 18, 321–331. and Y. malinellus (Lepidoptera: Yponomeutidae). Atti Acc. Lincein Howell, J.F., Knight, A.L., Unruh, T.R., Brown, D.F., Krysan, J.L., Mem. Fis. XVIII 2, 33–61. Sell, C.R., Kirsch, P.A., 1992. Control of codling moth in apple Bai, B.B., 2000. Apple ermine moth and its biological control in and pear with sex pheromone-mediated mating disruption. J. Econ. Oregon. In: Shenk, M., Kogan, M. (Eds.), IPM in Oregon: Entomol. 85, 918–925. Achievements and Future Direction. Oregon State University Howarth, F.G., 1991. Environmental impacts of classical biological Extension Service, Corvalis, OR, pp. 78–82. control. Annu. Rev. Entomol. 36, 485–509. Beirne, B.P., 1943. The biology and control of the small ermine moths Junnikkala, E., 1960. Life history and insect enemies of Hyponomeuta (Hyponomeuta spp.) in Ireland. Econ. Proc. R. Dublin Soc. 3 (15– malinellus Zell. (Lepidoptera: Hyponomeutidae) in Finland. Ann. 16), 191–220. Zool. Soc. ‘‘Vanamo’’ 21, 1–44. T. Unruh et al. / Biological Control 28 (2003) 332–345 345

Kuhlmann, U., 1994. Spatial host use by Ageniaspis fuscicollis of Silvestri, F., 1923. Contribuzioni alla conoscenza dei Tortricidi dell patchily distributed apple ermine moths Yponomeuta malinellus. querce. I.; II. Boll. Lab. Zool. Gen. Agric. 17, 41–102. Nowegian J. Agric. Sci. Suppl. 16, 337–345. Simberloff, D., Stiling, P., 1996. How risky is biological control? Kuhlmann, U., 1996. Biology and ecology of Herpestomus brunnicornis Ecology 77, 1965–1974. (Hymenoptera: Ichneumonidae), a potential biological control Smith, R.B., 1989. Interference of a predator mite with the biological agent of the apple ermine moth (Lepidoptera: Yponomeutidae). control of the apple ermine moth (Abst.). In: International Vedalia Int. J. Pest Manage. 42, 131–138. Symposium on Biological Control: A Century of Success. River- Kuhlmann, U., Carl, K.P., Mills, N.J., 1998. Quantifying the impact of side, CA, March 27–30, 1989. insect predators and parasitoids on the populations of the apple Sperling, F.H.A., Landry, J.F., Hickey, D.A., 1995. DNA-based ermine moth, Yponomeuta malinellus (Lepidoptera: Yponomeuti- identification of introduced ermine moth species in North America dae), in Europe. Bull. Entomol. Res. 88, 165–175. (Lepidoptera: Yponomeutidae). Ann. Entomol. Soc. Am. 88, 155– Lofstedt, C., Herrebout, W.M., Du, J.-W., 1986. Evolution of the 162. ermine moth pheromone tetradecyl acetate. Nature 323, 521–623. Strong, D.R., Pemberton, R.W., 2000. Biological control of invading McDonough, L.M., Davis, H.G., Smithhisler, C.L., Voerman, S., species—risk and reform. Science 288, 169–179. Chapman, P.S., 1990. Apple ermine moth, Yponomeuta malinellus Strong, D.R., Pemberton, R.W., 2001. Food webs, risks of alien Zeller two components of female sex pheromone gland highly enemies and reform of biological control. In: E. Wajnberg, J.K. effective in field trapping tests. J. Chem. Ecol. 16, 477–486. Scott, C.P. Quimby (Eds.), Evaluating Indirect Ecological Effects Menken, S.B.J., Herrebout, W.M., Wiebes, J.T., 1992. Small ermine of Biological Control. CABI Publishing, Wallingford, pp. 57–79. moths (Yponomeuta): their host relations and evolution. Annu. Thomas, M.B., Willis, A.J., 1998. Biocontrol—risky but necessary? Tr. Rev. Entomol. 37, 41–66. Ecol. Evol. 13, 325–329. Michaud, J.P., 2000. Classical biological control: a critical review of Thorpe, W.H., 1928. Biological races in Hyponomeuta padellus.J. recent programs against Citrus pests in Florida. Ann. Entomol. Linn. Soc. (London) 36, 621–636. Soc. Am. 94, 531–540. Thorpe, W.H., 1930. The natural control of Hyponomeuta padellus L. Neenon, J.P., 1978. Synecology Ageniaspis fuscicollis Thoms. (polyem- Proceedings of the Entomological Society of London 5, 28–30. bryonic Hymenoptera, Chalcidoidae) a parasitoid of the Hyponom- Unruh, T.R., Congdon, B., LaGasa, E., 1993. Yponomeuta malinellus euta (Lepidoptera) control. Ann. Zool. Ecol. Anim. 10, 525–544. Zeller (Lepidoptera: Yponomeutidae), a new immigrant pest of Nosyreva, R.D., 1981. Systematic measures for the protection of fruit apples in the Pacific Northwest: phenology and distribution trees from pests and diseases. Zaschita Rastenii 11, 55–57. expansion, with notes on efficacy of natural enemies. Pan. Pacific Povel, D.E.G., 1984. The identification of the European small ermine Entomol. 69, 57–70. moths, with special reference to the Yponomeuta padeus-complex Vaclav, V., 1958. Importance of parasites on reducing numerousness (Lepidoptera, Yponomeutidae). Proc. K. Ned. Akad. Wet. Ser. C of populations of Hyponomeuta malinella Zell. and H. padellus L. in 87, 149–180. Bosnia and Herzegovina. Plant Protect., Beograd. 49/50, 113–119 Pyornila, M., Pyornila, A., 1979. Role of parasitoids in termination of (In Serbian). a mass occurrence of Yponomeuta evonymellus (Lepidoptera, Wajnberg, E., Scott, J.K., Quimby, P.C., 2001. Evaluating Indirect Yponomeutidae) in northern Finland. Notulae Entomologicae Ecological Effects of Biological Control. CABI Publishing, 59, 133–137. Wallingford.