Biological Control 28 (2003) 332–345 www.elsevier.com/locate/ybcon Introduction and establishment of parasitoids for the biological control of the apple ermine moth, Yponomeuta malinellus (Lepidoptera: 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 Insect 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 ermine moth (AEM), Yponomeuta malinellus 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 moths (Menken et al., 1992). AEM was linellus Zeller (Lepidoptera: Yponomeutidae), is a uni- first seen in nursery plantings on Vancouver Island, voltine defoliator of apples 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 pest (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 parasitoid 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