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Cyzenis Albicans (Diptera: Tachinidae) Does Not Prevent the Outbreak Of

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Cyzenis Albicans (Diptera: Tachinidae) Does Not Prevent the Outbreak Of BIOLOGICAL CONTROL Cyzenis albicans (Diptera: Tachinidae) Does Not Prevent the Outbreak of Winter Moth (Lepidoptera: Geometridae) in Birch Stands and Blueberry Plots on the Lower Mainland of British Columbia 1 2 FINBARR G. HORGAN, JUDITH H. MYERS, AND ROSE VAN MEEL Departments of Zoology and Plant Science, University of British Columbia, 6270 University Boulevard, Vancouver, BC, V6T 1Z4, Canada Downloaded from https://academic.oup.com/ee/article/28/1/96/502294 by guest on 29 September 2021 Environ. Entomol. 28(1): 96Ð107 (1999) ABSTRACT In the late 1980s, a new outbreak of the introduced winter moth, Operophtera brumata (L.), occurred in Richmond, on the lower mainland of British Columbia. This was accompanied by the introduced parasitoid, Cyzenis albicans (Falle´n). Populations were monitored at 2 birch wood- lands and 2 blueberry plots between 1989 and 1993. Parasitism by C. albicans and predation by generalist predators were important mortality factors during the outbreak. Predation of moth pupae increased at all sites between 1989 and 1990. Parasitism by C. albicans caused signiÞcant mortality each year reaching a maximum in 1991 and remaining high through to 1993 at birch sites. The winter moth populations collapsed simultaneously in 1992 at all study sites, despite different levels of parasitism and 2 very different host plants. As the outbreak collapsed at Richmond, the moth continued to increase in numbers and cause severe defoliation of birch at new sites in southern Vancouver where parasitism remained low. C. albicans is unable to prevent the initial outbreak of winter moth even when the 2 species are introduced simultaneously. The parasitoid requires high density host populations before becoming well established, but may contribute sufÞcient additional mortality to prevent subsequent prolonged outbreaks. The control of high density winter moth populations in North America by C. albicans supports the hypothesis that natural enemies that are rare in their native habitat will be effective control agents when released into exotic habitats without competitors or their own natural enemies. KEY WORDS Operophtera brumata, Cyzenis albicans, simultaneous introduction, winter moth, biological control INTRODUCED INSECTS OFTEN increase to outbreak den- lation (Varley and Gradwell 1968, Hassell 1969a, Var- sities after release from their natural enemies, but they ley et al. 1973). sometimes also decline to lower densities without the Though winter moth larvae are largely monopha- introduction or establishment of biological control gous the species is polyphagous. Feeding has been agents (Beirne 1975, Myers and Iyer 1981). It is im- described from .160 species of primarily deciduous portant to understand if apparently successful biolog- trees and shrubs from 14 different plant families. It is ical control is in fact the result of the introduced generally accepted that oak (Quercus spp.) is the pri- natural enemy. mary host (Varley and Gradwell 1958, Feeny 1970, Reduction of high density winter moth populations, Hunter 1990). Other important hosts include apple, Operophtera brumata (L.), in Canada by the tachinid (Malus spp.), pears (Pyrus spp.), hazel (Corylus avel- Cyzenis albicans (Falle´n) is one of the most important lanae L.), and beech (Fagus sylvatica L.) (Wint 1983). examples of successful classical biological control In North America, important hosts include oak, apple, (Embree 1966, DeBach 1974, Murdoch et al. 1985). birch (Betula spp.), highbush blueberries (Vaccinium This case is particularly interesting because the intro- corymbosum L.), raspberries (Rubus spp.), and com- duction of the parasitoid has been associated with the mercial Þlberts (Corylus spp.) (Embree 1965b, decline of sustained high density host populations Gillespie et al. 1978, AliNiazee 1986, Fitzpatrick et al. even though the parasitoid is generally rare in its 1991). In Scotland, larvae cause substantial damage native habitat in Europe (Varley et al. 1973). Most and distorted growth of sitka spruce (Picea sitchensis European studies were carried out in Britain where C. (Bongard) Carrie´re) (Watt and Macfarlane 1991). albicans normally parasitized only '5% of the popu- Adult winter moth emerge in early November on the lower mainland of British Columbia. Females lay up to 300 eggs (but generally 100Ð200 eggs) either 1 Current address: Escuela de BiologÕa, Facultad de Ciencias Na- turales y Matematica, Universidad de El Salvador, Final 25 Avenida singly or in small groups in cracks on the host bark, and Norte, San Salvador, El Salvador. under lichens. There are 5 instars. The larval stage lasts 2 To whom correspondence should be addressed. from March until the middle of May, the prepupae 0046-225X/99/0096Ð0107$02.00/0 q 1999 Entomological Society of America February 1999 HORGAN ET AL.: NEW INTRODUCTION OF WINTER MOTH AND PARASITOID 97 then spin to the ground to pupate. Pupation occurs '1Ð2 cm below the soil surface where a cocoon is spun. Pupae remain in the soil for '6 mo (unpublished data). The life cycle of C. albicans is synchronized with that of the winter moth. After mating, the adult fe- males feed on ßowers, sap ßuxes, and honey dew for '4 wk (Embree and Sisojevic 1965). By the time the winter moth are in their 5th instar, the parasitoid females have their full complement of eggs, '1,000Ð 2,000 (Hassell 1980). Laying occurs over a period of 8Ð16 d when shiny black microtype eggs are laid on foliage near caterpillar feeding damage (Embree and Downloaded from https://academic.oup.com/ee/article/28/1/96/502294 by guest on 29 September 2021 Sisojevic 1965). The eggs are viable for '8 wk. After ingestion by the host, the larva hatches, penetrates the gut wall, and lodges in the hostÕs salivary gland. After host pupation, this 1st instar feeds with its posterior spiracles inserted in a respiratory funnel, until only the empty pupal case of the host remains. When mature the parasitoid larva forms a puparium inside the hostÕs pupal case. The parasitoid pupa goes into diapause and the adult emerges the following spring, a period of '10 mo (Hassell 1980). Cyzenis albicans was introduced into Canada for biological control purposes on 2 occasions (in the 1960s to Nova Scotia and in the 1980s to Vancouver Fig. 1. Sampling sites in the Fraser Valley (lower main- Island in British Columbia). In both areas the parasi- land of British Columbia). Solid circles indicate the sites toid initiated dramatic crashes in winter moth popu- sampled in 1992 or 1993. Open circles indicate sites for which lations and reached levels of parasitism as high as 80%. observations were made in 1990. Three invasion zones are C. albicans became regulatory soon after its release. identiÞed using points that lie midway between adjacent Furthermore, mortality of winter moth pupae in the sampling sites. (I) In Tsawwassen, high levels of parasitism soil rapidly increased from levels as low as 10% before were recorded in 1990. (II) In Richmond and Delta, out- the parasitoid was released to levels .90% during breaks occurred in 1989 and 1990 and parasitism was highest in 1991. (III) In south Vancouver, high larval densities were collapse of the outbreaks (Embree 1966, Roland 1988). noted in 1991 and 1992, whereas parasitism remained low. All Interestingly, mortality of pupae in the soil became other sampling sites outside these zones had very low winter regulatory in Canada after the biological control in- moth densities and no incidence of parasitism. troductions as it is in regions where the winter moth and C. albicans are native (Roland and Embree 1995). This supported HassellÕs (1980) idea that outbreaks blueberry hosts. We monitored population ßuctua- had originally occurred in Canada because of a lack of tions throughout 5 yr at 4 study sites in Richmond and regulation by predators and the absence of successful recorded the spread of the moth and C. albicans north- parasitoids. ward on the lower mainland. We examined the suit- In 1986, winter moth populations declined in Vic- ability for winter moth of the 2 principal host plants toria on Vancouver Island. However, the moth con- encountered in the Richmond area and investigated tinued to spread north on the Island and east to the predation and parasitism to compare this unusual case lower mainland of British Columbia. In 1985, winter with those of Nova Scotia and Vancouver Island where moth was found in pheromone traps on the lower there had been a time lag between the moth and mainland (Wood and van Sickle 1985, 1986). By 1991, parasitoid introductions and to compare British stud- the moth had spread throughout the Fraser Valley as ies where both species are native. The choice of using far east as Mission. High population densities were life tables facilitates comparisons with previous winter recorded at Richmond, Delta, and Surrey in 1989, moth population studies most of which present data in where birch and blueberry were the most important the form of k values. However, to avoid bias by this hosts (Fitzpatrick et al. 1991). method (Vickery 1991) the original percentage mor- Cyzenis albicans spread with its host to the lower talities are used in statistical analyses. mainland. It was already present among winter moth when this study was initiated in 1989. Despite the Materials and Methods presence of the parasitoid on the lower mainland, an outbreak occurred in Richmond in the late 1980s. This Field Sites. Winter moth populations were studied outbreak offered a rare opportunity to look at the at 4 Þeld sites in Richmond. Two of the sites, Rich- dynamics of the winter moth in a region where it has mond Nature Park and Edwards stand, were predom- been simultaneously introduced with C. albicans. This inantly of birch woodland (Fig. 1, sites 1 and 2, re- study describes winter moth outbreaks on birch and spectively). Richmond Nature Park has an area of 43 98 ENVIRONMENTAL ENTOMOLOGY Vol. 28, no.
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