BIOLOGICAL CONTROL albicans (Diptera: ) Does Not Prevent the Outbreak of (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, (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 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 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 Ͼ160 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 Ϸ5% 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 ᭧ 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 Ϸ1Ð2 cm below the soil surface where a cocoon is spun. Pupae remain in the soil for Ϸ6 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 Ϸ4 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, Ϸ1,000Ð 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 Ϸ8 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 Ϸ10 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 Ͼ90% 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. 1 ha of mixed forest vegetation. Studies were carried out method (Varley and Gradwell 1968). Throughout pu- at the western side of the park where birch woodland pation, late April until early June, 20 plastic bedding predominates. Birch trees (Betula papyrifera variety trays Þlled with sifted peat were placed along the communata Marshall) of a variety of ages occurred at transects beneath the host plants at each site. After the site. Some sumac (Rhus glabra L.) and hemlock pupation had ceased, the trays were sifted to Þnd the [Tsuga heterophylla (RaÞnesque-Schmaltz) Sargent] cocoons. grew among the birch. The undergrowth consisted In 1991 and 1992, densities of emerging adults were largely of salal (Gaultheria shallon Pursh) and high- estimated at birch sites using sticky traps. Estimates bush blueberry. The Edwards site (125 by 50 m) had were made only in 1992 at blueberry sites. Ten trees habitat very similar to the site at Richmond Nature or bushes were arbitrarily chosen from each site. The Park. In 1992, an area (Ϸ25 by 50 m) at the western canopy area of each tree and bush was estimated. edge of this stand, where the study had previously Sticky traps, bands of masking tape tightly wrapped been concentrated, was cut down. about the tree or bush trunk and coated with tangle- Downloaded from https://academic.oup.com/ee/article/28/1/96/502294 by guest on 29 September 2021 The other 2 sites, Watanabe Farm and Schultz Farm, foot (Tanglefoot, Grand Rapids, MI), were placed at were neglected blueberry plots on agricultural land a height of Ϸ1m on each of the ten trees and 50 cm on (Fig. 1, sites 3 and 4, respectively). Blueberry plots (50 the blueberry bushes. Trapping was carried out from by 20 m) were not commercially harvested. Pesticides early October until February. were not used at the sites. Both sites had a number of Mortality Estimates. Larvae were collected at each different varieties of highbush blueberry with consid- site as described above, from the middle of April until erable variation in size among the bushes. In general, early May in 1991, and from early March until early bushes at the Watanabe site were smaller with a lower May in 1992. The larvae were kept in individual plastic planting density. Some young birch were interspersed containers in an outside shed and reared through to among the blueberry bushes at both sites. pupation. Larvae were fed ample supplies of birch or Population Density Estimates. Larval densities blueberry foliage from uninfested areas. Leaves were were estimated between 1989 and 1993 at the blue- changed every 2Ð4 d. A number of the larvae were berry sites, and between 1991 and 1993 at the birch frozen immediately after collection and examined for sites. The sampling unit for larvae was the leaf cluster. viral or microsporidian disease. All larvae that died A leaf cluster consists of all the leaves that develop during rearing were also examined for pathogens. from a single bud. Clusters were collected in late Smears were made from dead larvae and stained with March or early April when larval eclosion was com- Naphthalene black in 1991 and with both Naphthalene plete. Clusters that had developed from apical buds black and Giemsa in 1992. Dead larvae were not dis- were collected from 4 transects at each of the blue- sected or otherwise examined for parasitoids. Exam- berry sites and from 3 transects at each birch site. Five inations for microsporidia were carried out at every bushes or trees were arbitrarily selected from each stage of the life cycle, except eggs in 1991. In 1992, eggs transect. A single cluster was taken from each of the were teased apart, Þxed in methanol and stained in cardinal points. Clusters were collected from birch Giemsa. Larvae were stained as above. For adults, the trees with telescopic pruners that reached a height of abdomens were severed, the contents were then Ϸ15 m. In total, 80 clusters were collected on each moistened, Þxed, and stained with Giemsa (BDH sampling date from blueberry sites and 60 from birch Chemicals, Toronto, Ontario). sites. In 1992, larval densities on undergrowth blue- Mortality of prepupae caused by C. albicans para- berry bushes at the birch sites were recorded and sitism was estimated by examination of pupae col- larval densities were estimated from 6 top (20 m) and lected in the pupal drop trays. Mortality of pupae as a 6 lower branches (3 m) of 5 felled birch at the Edwards result of unidentiÞed causes, henceforth referred to as site. In 1991 and 1992, defoliation was estimated visu- “death due to unknown causes” was also scored on ally at the birch sites. examination of the pupae. In 1989, estimates were Levels of damage at the blueberry sites were not made from all the collected pupae taken together; estimated. In 1992, the occurrence and developmental whereas from 1990 to1992, estimates were on a per tray stage of larvae on either leaf or ßower buds in blue- basis. In 1993, late instars were collected from the berry was noted from among the clusters collected. To birch sites and maintained through to pupation. These investigate preferences for clusters, laboratory reared were also examined for the incidence of parasitism and neonates were set out on blueberry branches at the death due to unknown causes. Because densities were Watanabe farm. Branches with 4 apical ßower buds very low in 1993, late instars were not found at the were chosen and a band of tanglefoot was placed blueberry sites. below the 4th bud to restrict larval movement. Neo- Estimates of pupal predation were made through nates were placed between the 2nd and 3rd bud at Þeld deployment of pupae. Tethers consisted of densities of 5, 10, and 20 per twig with 6 replicates of groups of 4 pupae attached by ßower wire to a central each density. Twigs were clipped after 24 h and larval wooden skewer. Pupae were spaced at Ϸ10-cm inter- distribution examined. The 4 apical buds of each twig vals along the wire. Skewers were placed along were also measured with further bud samples mea- transects at intervals of Ϸ5 m. The pupae, complete sured at the Schultz Farm. with cocoons, were covered with a layer of humus Ϸ3 Pupal densities were estimated from 1989 to 1992. cm deep. In total, 80 pupae were deployed at each site Estimates were made using the pupal drop tray in each year from 1989 to 1992, with tethers set out February 1999 HORGAN ET AL.: NEW INTRODUCTION OF WINTER MOTH AND PARASITOID 99 after pupation was complete in late June. Tethers were Data Analysis. Data for larvae on blueberry and collected before the 2nd wk of October, about a month birch were analyzed separately because of differences before adult winter moth emergence. in size, leaf area, and number of leaves in clusters from Fecundity. The suitability of 3 host plants for winter the 2 hosts. All data were tested against the normal moth was examined in 1991. Larvae were collected as distribution using the Bartlett test (P Ͻ 0.05) (Wilkin- early instars and reared on diets of birch and blueberry son et al. 1992). Larval data were log transformed in plastic containers in an outside shed. A 3rd group of before analysis to reduce heterogeneity of variance. larvae were reared on apple (Malus domestica L.), However, the data for larvae at the blueberry sites on which is another important host on the lower main- different sampling dates could not be adequately land. Leaves were changed every 2 d. After pupation transformed and so were analyzed using the nonpara- all pupae were weighed. Also in 1991, prepupae were metric MannÐWhitney U test (Wilkinson et al. 1992). collected from the 3 hosts in the wild and held until Differences between top and lower branches of felled pupation in the laboratory. The pupae were then birch were determined using a t-test. Differences in Downloaded from https://academic.oup.com/ee/article/28/1/96/502294 by guest on 29 September 2021 weighed. In 1991 and 1992, pupae collected in the the densities of larvae between years and between pupal drop trays were weighed. Female fecundity was blueberry sites were determined using 2-way analysis estimated using a relationship in Roland and Myers of variance (ANOVA). Larval data from Richmond (1987) for pupal weight versus fecundity on oak-fed Nature Park were analyzed by 1-way ANOVA. Larval individuals. The validity of this was tested by dissect- densities at the Edwards site were not included be- ing adult females collected at the sites during the cause of interference at that site in 1992. The chi- winter of 1991. squared test was used to analyze the distribution of Pupal Predators. In 1991 and 1992, pitfall trapping larvae in buds on blueberry branches (Zar 1984), was carried out at all sites from the 2nd wk of June until whereas differences in bud volume were determined the 1st wk of September. Each site had 20 traps laid out using 1-way ANOVA. in 2 transects of 10 and spaced at Ϸ15-m intervals. Differences in pupal densities at the sites were an- Traps consisted of 0.5-liter plastic goblets with small alyzed using 2-way ANOVA with a Tukey test applied slits made at the sides to drain water. In 1991, trap for postvariate analysis (Wilkinson et al. 1992). Adult catches were removed every 2 wk. In 1992, wire grids densities at the blueberry sites were compared using a t-test. Data on adult densities from 1992 could not be were placed over the traps to prevent the capture of adequately transformed so a nonparametric KruskalÐ small mammals, and trap catches were removed Wallis test was applied to determine differences be- weekly. Medium to large sized predatory beetles and tween sites (Wilkinson et al. 1992). Differences in the ants were recorded. weights of pupae reared in the laboratory and taken Spread of the Winter Moth and C. albicans. Surveys from the Þeld were determined using 1-way ANOVA, of the spread of the winter moth and C. albicans were whereas weight differences between pupae collected carried out in April and early May of 1992 and 1993. in the drop trays at the sites and in different years were Host plants from stands or as ornamentals were sam- determined using 2-way ANOVA. All percentage data pled at 23 sites in the western Fraser Valley. Trees (parasitism and death due to unknown causes) were were sampled in a roughly north to south transect arcsine transformed and differences in these mortal- from the north shore of Vancouver to Delta and in an ities between sites and years were determined by east to west transect from the University of British 2-way ANOVA. Regression analyses were performed Columbia to Simon Fraser University in Burnaby (Fig. using the GLM procedure (Wilkinson et al. 1992) for 1.). Host trees included apple, crabapple (Malus sil- (Y) within site pupal density per meter squared versus vestris L.), blueberry, and birch. A leaf-cluster was (X) percentage parasitism or percentage death due to collected from each of the cardinal points of 3Ð10 unknown causes according to individual trays. Data arbitrarily chosen trees or bushes at each site, depend- for 1989 were not included in any analysis of these ing on the number of plants available at each location. mortalities because estimates were made per site and Clusters were collected from birch using telescopic not per tray in that year. Differences in the abundance pruners and by hand from blueberry, apple, and of small mammals at the sites were analyzed using crabapple. All prepupae were returned to the labora- 1-way ANOVA while 2-way ANOVA was applied to tory and reared through to pupation to estimate inci- test for differences in beetle abundance between the dence of parasitism. In 1992, both larval densities and sites and between 2 yr. levels of parasitism by C. albicans were estimated; The magnitude and trends in mortality were dem- whereas in 1993, only parasitism was estimated. onstrated using k values (Varley et al. 1973). The

In 1992, a tree banding program was initiated in mortality of eggs and larvae (klarval) was estimated as southern Vancouver in response to severe defoliation the difference between the log of the estimated egg of maple (Acer spp.) and birch by winter moth larvae. potential each year and the log mean density of pre- The areas that were suitable for winter moth pupation pupae entering the soil each year. The egg potential under the banded birch trees were calculated (i.e., each year was estimated by multiplying the number of excluding roads and concrete pathways). The bands adult females per square meter that year by the av- were examined periodically and adult densities esti- erage fecundity of females in the same year. The value mated from 3 to 4 trees at each of 4 sites (Fig. 1, sites for 1990 was estimated by multiplying an estimate of 7, 8, 10, and 11). adults per square meter (derived from pupal densities 100 ENVIRONMENTAL ENTOMOLOGY Vol. 28, no. 1 and pupal mortality estimates) by 150, an average fecundity for the species (Embree 1965b).

Mortality caused by parasitism (kparasitism) was es- timated as the difference between the log of the mean density of prepupae and the log of the density of healthy pupae. An important mortality factor, termed kunknown, was observed each year. This was the dif- ference between the log density of unparasitized pre- pupae dropping to the soil and the log density of healthy pupae in the soil (i.e., death due to unknown causes). In 1993, the values for kparasitism and kunknown at the birch sites were estimated from collections of late instars which were maintained through pupation Downloaded from https://academic.oup.com/ee/article/28/1/96/502294 by guest on 29 September 2021 in the laboratory.

Pupal predation (kpredation) was estimated as the difference between the log density of healthy pupae Fig. 2. Incidence of winter moth larvae on ßower (shad- in the soil and the log of the estimated density of adults ed) and leaf (solid) clusters at 2 blueberry sites in Richmond that emerge from pupae having survived predation. in 1992. Bars indicate standard errors. Asterisks indicate sig- Estimates of the numbers of adults emerging were niÞcantly higher larval densities on ßower buds in March at derived from predation estimates using the tether the Schultz site (U ϭ 918, df ϭ 99, P Ͻ 0.01) and signiÞcantly method. Examination of the pupal condition for evi- higher densities on leaf buds in April at the same site (U ϭ dence of predation means that this mortality factor 264, df ϭ 61, P Ͻ 0.05). accounts speciÞcally for predation and thus differs from mortality in the soil which generally includes the developing ßower buds earlier in the season and death of prepupae, death of pupae due to factors other later moved to feed on the blueberry leaves (Fig. 2). than predation, and death of adults after emergence On blueberry, larvae at different densities concen- but before trapping in sticky traps. trated on apical buds (Table 1); this behavior was not inßuenced by larval density (␹2 ϭ 7.96, df ϭ 6, P Ͼ 0.05). The apical buds are signiÞcantly larger than the Results subapicals (F ϭ 16.881; df ϭ 3, 232; P ϭ 0.001). Larval Defoliation. In 1989 and 1990, birch in the Rich- densities peaked in late March when all eggs had mond area had been moderately to severely defoliated hatched (very few 1st instars were present at that (Wood and van Sickle 1990). In 1991, we estimated time) and 5th instars had not yet appeared. that Ϸ50% of leaves were damaged at the Edwards site Population Densities at Richmond. Winter moth and 30% at the site in Richmond Nature Park. Out- populations at Richmond reached the peak of the break areas were very localized. At Richmond Nature outbreak in 1990. Population densities were constantly Park, defoliation was greatest on the western side of higher at the birch sites (Fig. 3). Larval densities were the park in an area of Ϸ5ha. At the Edwards site, an very similar at the 2 blueberry sites (F ϭ 1.244; df ϭ area of 50 by 50 m at the northern edge of the stand 1, 170; P ϭ 0.2664); densities increased signiÞcantly was heavily defoliated with the majority of birch at the between 1989 and 1990 and underwent a general de- rest of the site having only 10Ð20% of their leaves cline from 1990 until 1992 when populations collapsed damaged. In 1992, similar patterns were observed with (F ϭ 26.164; df ϭ 3, 168; P Ͻ 0.001). There was no average damage of Ϸ30% at the Edwards site and 10% signiÞcant interaction between sites and years (F ϭ at Richmond Nature Park. Within trees, lower 2.420; df ϭ 3, 168; P ϭ 0.0681). Larval densities on birch branches generally had the most damage, presumably in 1989 and 1990 are not known. Evidence from dam- because of the distribution of larvae within the trees age suggests that between 1990 and 1991 the popula- and through downward larval migration throughout tions declined. Between 1991 and 1992, a decrease in the season. In 1992, signiÞcantly fewer 1st instars were larval densities was apparent at Richmond Nature found on top branches of felled birch compared with Park (t ϭ 5.144, df ϭ 88, P Ͻ 0.001), whereas at the lower branches soon after eclosion was complete (t ϭ Edwards site there appears to be a slight increase. Data Ϫ3.224, df ϭ 57, P ϭ 0.0021). Young birch trees were were collected at the western side of the Edwards site particularly damaged, presumably because of their in 1991. In 1992, trees on this side of the site were felled low size, rather than through any differential foliage and so sampling in 1992 and 1993 was carried out at a quality. Undergrowth was often completely defoli- new area within the site. Observations of defoliation ated. patterns in 1991 indicate that the western edge had At the Watanabe Farm, larval distribution was uni- received considerably less defoliation (10% damage to form among bushes, whereas the population at the leaves) than the eastern side (60% damage to leaves), Schultz farm was denser at the southern edge. The which probably explains the increase in density ob- northern edge was immediately adjacent to a com- served at that site in subsequent years. Pupal densities mercial plot. Damage to blueberry is manifested to a differed between sites (F ϭ 79.085; df ϭ 3, 317; P Ͻ large degree in the reduction of fruit yield, which was 0.001) and years (F ϭ 27.695; df ϭ 3, 317; P Ͻ 0.01). not examined in this study. Larvae generally attacked However, there was a signiÞcant interaction between February 1999 HORGAN ET AL.: NEW INTRODUCTION OF WINTER MOTH AND PARASITOID 101

Table 1. Chi-squared analysis of larval distribution on blueberry buds at three different densities

a Bud position b Density n ␹2 df 1234 20 23 18 10 8 59 9.9** 3 102312244126.6*** 3 5 1011212413.7** 3 Pooled 56 41 14 13 124 52.4*** 3

** P Ͻ 0.005; *** P Ͻ 0.001. Bud position refers to the position of the buds on individual twigs, where 1 is the apical bud and 2 the subapical, ecetera. these factors (F ϭ 6.305; df ϭ 9, 311; P Ͻ 0.001). taken from different hosts in the Þeld and who com- Postvariate analysis indicates that densities were sim- pleted pupation in the laboratory. Also, differences Downloaded from https://academic.oup.com/ee/article/28/1/96/502294 by guest on 29 September 2021 ilar at the 2 blueberry sites but were signiÞcantly between the weights of pupae taken from pupal drop different between the birch sites (P ϭ 0.03) and be- trays at the 4 sites during 2 yr (1991 and 1992) were tween the birch and the blueberry sites (P Ͻ 0.001 for not signiÞcant. The lighter weights of pupae reared all comparisons). SigniÞcant population declines were from blueberry in the laboratory compared with wild noted only in 1992 (P Ͻ 0.05 for all comparisons of 1992 individuals may be caused by their leaf diet rather than densities with previous years). There was no signiÞ- a diet of the preferred ßower buds. cant change in adult densities between 1991 and 1992 Disease. Of 628 larvae reared in 1991 and 1,021 in at the birch sites. In 1992, there were signiÞcantly 1992, there was no indication of viral disease. All larvae more adults per meter squared at the birch sites than that had died in the rearing facility and a number of at the blueberry sites (H ϭ 26.60, df ϭ 3, P Ͻ 0.001). extra larvae taken from the Þeld (56 in 1991 and 339 Populations on both blueberry and birch changed in 1992) were examined for incidence of disease. At little after the 1992 decline. the Watanabe site in early May of 1991, 14 5th instars Fecundity. Host plants had a signiÞcant effect on (7% of those collected) had dark staining ovoid bodies the size of pupae reared in the laboratory (F ϭ 18.92; of 2Ð4 ␮m, which appeared to be microsporidia. It is df ϭ 2, 257; P Ͻ 0.001). We assume a 1:1 sex ratio. possible that the larger bodies may have been cyto- Pupae on blueberry were signiÞcantly smaller, plasmic polyhedrosis virus (CPV). In 1991, 69 adults whereas pupae reared on apple and birch were similar were examined; and in 1992, 120 eggs, 27 adults, and (Fig. 4). There was no difference between prepupae 28 pupae were examined for microsporidia. No further

Fig. 3. Densities of winter moth larvae per leaf or ßower cluster (circles) and densities of pupae (triangles) and adults (squares) per meter squared at (A) 2 blueberry sites (open symbols, Watanabe site; solid symbols, Schultz site) and (B) at 2 birch sites (open symbols, Edwards site; solid symbols, Richmond Nature Park) in Richmond. 102 ENVIRONMENTAL ENTOMOLOGY Vol. 28, no. 1

and microsporidial disease have had little effect on the lower mainland populations. Parasitism. Three parasitoid species were recov- ered from the Richmond populations. C. albicans was the most common species and has been present at all 4 sites at least since 1989. Agrypon sp. was also present in small numbers at birch sites. This species was found among pupae at levels below 0.5% from 1989 to 1990. In 1991, a 3rd species, morphologically and behavior- ally similar to Ephialtes spp. (Wylie 1960), was recov- ered from prepupae at the Edwards site only. Levels of parasitism were below 0.1%. Species of ephialtine ichneumonids have been noted in killing larvae with- Downloaded from https://academic.oup.com/ee/article/28/1/96/502294 by guest on 29 September 2021 out yielding a parasite (Campbell 1963); and parasit- ized prepupae often result in deformed pupae (Met- terhouse 1981) and may have contributed to some of the deformities noted among the pupae at the sites. However, only C. albicans appears to have played any important role in the dynamics of the winter moth at the sites during the study period. Parasitism by C. albicans ßuctuated between years at all sites (F ϭ 11.552; df ϭ 2, 159; P Ͻ 0.001), but was Fig. 4. Mean weights of winter moth pupae individually not signiÞcantly different between sites (F ϭ 1.556; reared on apple, blueberry or birch in an outside shed (shad- df ϭ 3, 158; P ϭ 0.2027); this is reßected in the trends ed) with a comparison of pupal weights from individuals for kparasitism (Fig. 5). There was no signiÞcant inter- collected as prepupae feeding on the 3 hosts in the wild ϭ ϭ (nonshaded). Bars indicate standard errors and numbers action between these factors (F 1.557; df 6, 155; indicate sample sizes. P ϭ 0.1638). Regression analysis of levels of parasitism against pupal densities per tray (i.e., prepupae per square meter) failed to indicate density dependent evidence of microsporidial disease was encountered. parasitism at either blueberry or birch sites in any year. There was no evidence of nuclear polyhedrosis virus The highest levels of parasitism occurred in 1991, with (NPV) in either year. It appears therefore, that viral 60.90 Ϯ 4.86% (mean Ϯ SE) of the pupae at the birch

Fig. 5. Mortality of winter moth in Richmond at (A) 2 blueberry sites between 1989 and 1992 and (B) 2 birch sites between 1989 and 1993. Solid squares, ktotal; solid circles, kpredation; open circles), kparasitism, solid triangles, klarval; and open triangles, kunknown. February 1999 HORGAN ET AL.: NEW INTRODUCTION OF WINTER MOTH AND PARASITOID 103

Table 2. Comparison of soil mortality and pupal predation at the 2 Richmond birch sites in 1991 and 1992 and at the blueberry sites in 1992

Edwardsa Richmond Nature Parka Watanabea Schultza Site 1991 1992 1991 1992 1992 1992 % pupal predation 90.28 Ϯ 17.45 67.50 Ϯ 24.08 92.11 Ϯ 11.94 80.00 Ϯ 21.53 95.45 Ϯ 10.72 63.63 Ϯ 23.33 % soil mortalityb 90.41 Ñ 78.57 Ñ 91.86 Ñ 84.29 Ñ 95.38 Ñ 98.09 Ñ

a Variance in pupal predation estimates are indicated (n ϭ 20). b Soil mortality is estimated as the difference between the density of healthy pupae in the soil in June and the density of adults emerging the following Winter. Variance estimates are not included for the soil mortality since these were absolute estimates each year.

sites parasitized and 38.25 Ϯ 9.92% (mean Ϯ SE) at at the Edwards site, which was rare at this site in 1991 Downloaded from https://academic.oup.com/ee/article/28/1/96/502294 by guest on 29 September 2021 blueberry sites. For some reason, parasitism was low in but increased considerably in 1992 (18% increase). A 1990 with levels at all sites between 13 and 20%. De- large number of small mammals were accidentally spite the decline in populations in 1993, parasitism at trapped in 1991 before grids were placed over the birch sites remained high with 53% of prepupae par- pitfall traps (Fig. 6B). SigniÞcantly more small mam- asitized. mals, mainly unidentiÞed shrews and Þeld mice were Mortality in the Soil. Adult densities as estimated captured at the Edwards site than at the other sites from sticky bands suggest a high mortality of winter (F ϭ 10.644; df ϭ 3, 73; P Ͻ 0.001). Furthermore, large moth between pupal drop and adult female capture. numbers of ants (Myrmica sp. and Formica sp.) were Tethered pupae only allow estimates of the levels of captured only at the Watanabe site in both years. pupal predation. Estimates for both soil mortality and During the 4 yr of study, the levels and trends in pupal predation were generally very similar at birch predation were remarkably similar among sites (Fig. sites in 1991 and 1992 and at blueberry sites in 1992 5). Between 1989 and 1990, predation increased mark- (Table 2), indicating that most of the mortality in the edly at all sites. By 1990, Ͼ90% of the pupae at all sites soil is attributable to predation of pupae by generalist were predated. Levels of predation changed little be- predators. This mortality factor did not appear to be tween 1990 and 1991, except at the Edwards site where dependent on prepupal densities in any year. it decreased by almost 10%, resulting in a 0.89 decrease

Many of the pupae collected in the pupal drop trays in ktotal that year. In 1992, pupal densities were lower were found to be either deformed or dead (Fig. 5). at all sites and predation dropped considerably with This death due to unknown causes differed signiÞ- the exception of the Watanabe site where it increased cantly among 3 yr, with the highest levels occurring in slightly. 1992 at each site (F ϭ 7.24; df ϭ 2, 176; P Ͻ 0.005) and a marked increase at the blueberry sites in that year (birch 31.04%, blueberry 45.00%). There was no sig- niÞcant difference in the incidence of death due to unknown causes between sites (F ϭ 1.36; df ϭ 3, 175; P Ͼ 0.05). There was no signiÞcant interaction be- tween the 2 factors (F ϭ 0.0690; df ϭ 6, 172; P Ͼ 0.05). Pupal Predators and Predation. The predator as- semblages at each site differed considerably. At the birch sites, Pterostichus herculaneus Mannerheim was the most abundant species, accounting for Ͼ90% of the catches at Richmond Nature Park in both years and 90 and 75% at the Edwards site in 1991 and 1992, respectively. The Watanabe site was dominated by Amara aurata Dejean, Amara littoralis Mannerhiem, and Harpalus affinus (Schrank), which were very rare or absent at the other sites. Pterostichus melanarius (Illiger) was also present at the Watanabe site and was the most important species at the Schultz Farm. Cara- bus nemoralis Mu¨ ller and Carabus granulatus Linne´ were present at both blueberry sites. Abundance of beetles at the sites differed signiÞcantly (F ϭ 58.57; df ϭ 3, 171; P Ͻ 0.001) and did not change in the 2 yr (F ϭ 0.8; df ϭ 1, 173; P ϭ 0.32) this is reßected in Fig. 6A. There was no signiÞcant interaction between the factors (F ϭ 2.1177; df ϭ 3, 171; P ϭ 0.0910). The slight Fig. 6. (A) Abundance of predatory beetles trapped increases in numbers of predators at 3 of the sites in from June until September 1991 (open) and 1992 (shaded) 1992 can mainly be attributed to predatory staphylin- with (B) the number of small mammals accidentally trapped ids that had lower numbers in 1991 and to C. granulatus in 1991 at 4 sites in Richmond. Bars indicate standard errors. 104 ENVIRONMENTAL ENTOMOLOGY Vol. 28, no. 1

Table 3. Winter moth larval densities per cluster at sites surveyed in the Lower Fraser Valley in 1992 with percentage parasitism by C. albicans in 1992 and 1993

Larval Host Parasitism Site no.a Site n density Plant mϪ2 1992 1993 1 Richmond Nature Park Birch 60 0.25 Ϯ 0.28 55 53 Blueberry 159 0.48 Ϯ 0.69 Ñ Ñ 2 Edwards birch site Birch 55 0.43 Ϯ 0.32 54 53 Blueberry 141 0.54 Ϯ 0.70 Ñ Ñ 3 Watanabe farm Blueberry 120 0.11 Ϯ 0.33 36 Ñ 4 Schultz farm Blueberry 120 0.07 Ϯ 0.26 14 Ñ 5 PeterÕs Commercial Blueberry Blueberry 36 0.17 Ϯ 0.38 0 Ñ 6 Department of National Defense Birch 28 0.01 Ϯ 0.07 0 Ñ

Blueberry 70 0.01 Ϯ 0.11 0 Ñ Downloaded from https://academic.oup.com/ee/article/28/1/96/502294 by guest on 29 September 2021 7 West 61 & Granville Birch 22 0.38 Ϯ 0.43 2 5 8 Elm & 39th Birch 18 Ñ Ñ 22 9 Granville & 35th Birch 24 Ñ Ñ 11 10 Granville & 45th Birch 18 Ñ 14 17 11 Adera & 54th Birch 20 Ñ Ñ 24 12 Jerico beach Birch 16 0.02 Ϯ 0.05 0 Ñ 13 Locarno beach Birch 16 0.01 Ϯ 0.05 0 Ñ 14 Spanish banks Birch 16 0.01 Ϯ 0.07 0 0 Apple 49 0.06 Ϯ 0.24 0 Ñ 15 West 13 & Trimble Birch 23 0.01 Ϯ 0.05 0 Ñ 16 West 9 & Alma Birch 22 0 Ñ Ñ 17 University of British Columbia Birch 16 0.01 Ϯ 0.05 0 0 18 Burnaby Lake Birch 12 0 Ñ Ñ 19 Simon Fraser University Birch 16 0 Ñ Ñ 20 Vancouver International Airport Birch 22 0 Ñ Ñ 21 Westham Island Birch 13 0.04 Ϯ 0.14 0 Ñ Crabapple 16 0.07 Ϯ 0.23 0 Ñ 22 Deas Island Birch 16 0.01 Ϯ 0.07 0 Ñ 23 112 Street North Birch 12 0 Ñ Ñ

a Site numbers correspond with sites shown in Fig. 1. b Variance estimates are indicated for each value.

k Factor Analysis. k Factors indicate that pupal lowest values occurring in 1991 after the initial pop- predation (kpredation) has been a source of high mor- ulation decline. tality throughout the 4 yr for which data are available Spread of the Winter Moth and C. albicans. Winter (Fig. 5), increasing markedly between 1989 and 1990 moth was common in Richmond and southern Van- at a time when the winter moth population was also couver in 1992 and 1993 (Table 3). Winter moth larvae increasing. High levels of predation in 1990 greatly and damage were not identiÞed from sites at Burnaby, contributed to the population decline noted in 1991 and larval densities were very low on the northern and helped maintain the populations at low densities shore of Vancouver and on Westham, Deas, and Sea that year despite low levels of larval mortality. High Islands. There appear to be 3 localized outbreaks larval mortality in 1992 meant that there were much where the moth had built up numbers to cause severe fewer pupae in the soil that year, which may have defoliation with a subsequent increase in parasitism by caused a subsequent reduction in predation at 3 of the C. albicans (see Fig. 1). In 1990, very severe defoliation sites. Although predation was lower in 1992, larval (90%) had been noted on isolated oak trees (Quercus densities did not increase at the sites in 1993. Mortality sp.) in Ladner and on apple in Tsawwassen where caused by predation was greater than mortality caused parasitism reached levels of up to 80% (apple) and by C. albicans (kparasitism) at each site and each year populations subsequently collapsed. Severe defolia- and was highest when larval mortality and mortality tion of birch and high levels of parasitism had also due to unknown causes were low. Larval mortality occurred in Delta in that year (R.v.M., unpublished

(klarval) increased in 1992 at each site though to a lesser data). In this survey, densities were high at Richmond extent at the Schultz Farm. The klarval, which includes on both blueberry and birch where the outbreak had all mortality of eggs, neonates, and larvae until the peaked in 1990. New outbreaks began on ornamentals prepupal stage, was responsible for the population in south Vancouver in 1991 (J.H.M., unpublished decrease noted from both larval and pupal counts in data) and 1992. Adult densities recorded from banded

1992. The klarval greatly inßuenced ktotal in all the years trees in southern Vancouver during 1992 ranged from that it was calculated. The similarities in the trends of 7.2 to 27.8 mϪ2. These densities were higher than those kunknown and klarval at all sites suggest a link between estimated at Richmond birch sites in that year, How- these 2 mortalities. It is likely that this link is through ever, they are almost certainly the result of prepupae foliage quality and thus asynchronies between bud being concentrated into restricted pupation space in burst and egg-hatch. The total generation mortality the urban environment. C. albicans was identiÞed only (k) goes through similar trends at all 4 sites with the at the Richmond and southern Vancouver sites where February 1999 HORGAN ET AL.: NEW INTRODUCTION OF WINTER MOTH AND PARASITOID 105 larval densities were also highest. Parasitism at all this study indicated that pupal predation was respon- urban outbreak sites was generally lower than at the sible for up to 90% of the mortality in the soil at birch Richmond sites, accounting for from 2 to 14% of pre- and blueberry sites in some years in Richmond, pupal mortality in 1992 and from 5 to 24% in 1993. The whereas all other factors (i.e., death of prepupae and southern Vancouver winter moth outbreak declined emerging adults) generally made little contribution to in 1994 and populations have remained low since then. this mortality. Generalist predators were a noted fea- ture in pitfall traps in 1991 and 1992 at all sites. How- ever, the sites had very different abundances of small Discussion mammals, beetles, and ants and had different assem- Despite a wealth of information on winter moth and blages of beetles. Despite this, the levels of predation C. albicans population dynamics in Europe (Varley at all 4 sites were similar and in 1990 and 1991, Ͼ90% and Gradwell 1968; Hassell 1969a, 1969b; Varley et al. of pupae were attacked at each site.

1973; Holliday 1977; Kowalski 1977) as well as exten- In 1992, high spring temperatures as a result of the “El Downloaded from https://academic.oup.com/ee/article/28/1/96/502294 by guest on 29 September 2021 sive documentation on control of the moth Ͼ30 yr in Nin˜o” effect caused winter moth to hatch early. Egg Canada (Embree 1965a, 1966; Roland 1988, 1990; hatch was recorded on 25 March in 1991; and in 1992, Pearsall and Walde 1994), we are only just beginning eggs hatched out Ϸ7 March, a time when 20Ð35% of to understand why C. albicans has been such a suc- birch buds and 20% of blueberry buds had not yet cessful control agent (Roland 1994, Roland and Em- opened (F.G.H., unpublished data). This climatic inßu- bree 1995). Currently, it is suggested that the intro- ence may have caused asynchronies between the moth duction of C. albicans causes signiÞcant mortality of and its host plant. Death of pupae due to unknown the moth, reducing population densities to levels low causes, which generally is manifested as deformed pu- enough for pupal predators to become regulatory as pae, increased dramatically at all sites in 1992. Larval they are in Britain (Roland and Embree 1995). mortality also increased at all sites in that year. These The introductions and outbreak reported here of- factors increased the rate of decline of the moth popu- fered a further opportunity to investigate the 2 species lations in 1992 but had not been so important in initiating in a newly invaded region of North America. This the decline that began in 1990. Poor condition of winter study documents a case where the moth and its para- moth in 1992 may have prevented winter moth popula- sitoid have been simultaneously introduced both hav- tions from increasing to any great extent in 1993 even ing likely arrived from Vancouver Island in the early though pupal predation had declined by that year. Dis- 1980s. The Richmond outbreak began before this ease was not an important source of mortality through- study commenced, peaked in 1990, and then went into out the study. Densities of winter moth on blueberry decline as indicated by blueberry larval counts. How- after the 1992 population collapse have remained sufÞ- ever, winter moth pupal densities declined only in ciently low not to cause a problem, whereas light feeding 1992; whereas, at least at the birch sites, adult densities damage continued on birch for some time where den- remained constant that year. Larvae on birch were sities remained obviously higher. concentrated on the lower branches of the trees. This The Richmond outbreak displayed population dy- differed from observations on oak, where the moth namic features more similar to endemic British pop- damage is concentrated on the tops of the trees and ulations and Canadian populations after biological the saplings receive less damage (Embree 1965b, control than to the previous outbreaks in North Amer- Dubrovin 1990, Hunter 1992). On blueberry, larvae ica that had occurred after new introductions of the preferred the larger apical ßower buds. At about the winter moth. Such outbreaks have been well docu- same time as the Richmond outbreak, a ßare-up of mented for Nova Scotia, Vancouver Island, and Ore- winter moth occurred on Vancouver Island (Roland gon (Embree 1965a; Kimberling et al. 1986; Roland and Embree 1995) and localized outbreaks occurred 1990, 1994). Control of the moth in Nova Scotia and on in Ladner and Tsawwassen. Vancouver Island shared a number of similarities in In 1989, high levels of parasitism by C. albicans were the dynamics of the participating species, the timing of already apparent in Richmond and continued events, and in the resulting population trends. In Nova throughout the 5 yr of study. Parasitism reached its Scotia and Vancouver Island, C. albicans was intro- highest level at each site in 1991 after larval densities duced after 10Ð20 yr of sustained high density winter had declined. Levels of parasitism were similar at birch moth populations (Roland and Embree 1995). At each and blueberry sites throughout the study, though the region, there was a time-lag before predation became highest incidence of parasitism was noted from pre- regulatory, during which time both mortality in the pupae at the birch sites. soil and parasitism by C. albicans went through char- k Factors indicate that predation of pupae in the soil acteristic inverse density-dependent phases (Embree was the most important mortality factor during the 1966, Roland 1988). In Richmond, only predation ap- Richmond outbreak. This mortality increased dramat- pears to follow the trends in winter moth pupal den- ically between 1989 and 1990 at the 4 study sites. In sities through 4 yr at some sites. However, 4 yr of data winter moth populations in Britain, and in North are not sufÞcient to draw conclusions on temporal American populations after biological control, mor- density dependence. Similar levels of predation, par- tality in the soil is regulatory (Varley and Gradwell asitism, and death due to unknown causes were noted 1968, Varley et al. 1973, McPhee et al. 1988; Pearsall among sites each year. This may have resulted in the and Walde 1994, Roland 1994). The use of tethers in simultaneous population declines at the sites in spite 106 ENVIRONMENTAL ENTOMOLOGY Vol. 28, no. 1 of different densities of winter moth, different host Cyzenis albicans may increase after high densities of plants and different predator assemblages. the host even in its native habitat. The parasitoid may The parasitoid caused signiÞcant mortality of the moth beneÞt from periods in which the soil predators are during each year of the study having presumably built up swamped by abundant prey, and larval densities are numbers during the increase phase of the outbreak. We not so high as to cause total defoliation, or so low as to failed to indicate spatial or temporal relationships be- make host Þnding inefÞcient. In urban environments tween parasitism and prepupal densities at the sites. as in southern Vancouver, predation may be expected Within site scales are probably important but pupal drop to be lower because of the lack of suitable habitat for trays may not give a good representation of prepupal predators. In such a case, C. albicans might be ex- densities in host plant foliage. The trays are dependent pected to increase rapidly and play a more direct role on overhead canopy characteristics, which may be very in moth population control. The 1994 decline in south- variable, and on movements of the prepupae as they ern Vancouver was probably the result of a successful descend from the canopy. The early presence of C. al- tree-banding program that caused very high mortality Downloaded from https://academic.oup.com/ee/article/28/1/96/502294 by guest on 29 September 2021 bicans may have allowed generalist predators to become of the adult winter moth females. regulatory at all the sites almost immediately after the For some reason, C. albicans continues to parasitize mothÕs introduction, allowing only short (2Ð3 yr) out- a higher proportion of winter moth in some areas of breaks. The sustained outbreaks that were a feature of North America even after the decline in host densities. Nova Scotia and Victoria did not occur on the lower The parasitoid may be released from competitors or mainland. other natural enemies in North America, allowing it to Evidence from larval counts in the western part of reach a higher population equilibrium than it does in the Fraser Valley indicate that as the Richmond out- Europe. However, such high levels of parasitism do break declined the moth built up numbers to the not seem to be necessary for the decline of winter north. In 1991 and 1992, winter moth densities in- moth populations as indicated by Kimberling et al. creased on ornamental birch and maple in southern (1986) in Oregon where parasitism had reached levels Vancouver. Both tree bands and larval counts in south- of only 4% when outbreaks collapsed on Þlberts. ern Vancouver indicated high winter moth densities. Despite this, parasitism remained quite low (from 5 to Acknowledgments 24%) at urban sites. There appears to be a period at which the moth, invading new regions, temporarily We express our appreciation to the land owners and the escapes control by C. albicans as the parasitoid builds staff of Richmond Nature Park for allowing access to Þeld sites throughout this study. We greatly appreciate the help up numbers. Therefore, even with simultaneous in- and interest shown by J. E. OÕHara (Biosystematics Research troductions, an outbreak of the host may be necessary Center) who identiÞed the parasitoid and M. Hunter, B. to allow the parasitoids to become established as was Ryan, and B. Dineen who gave many helpful suggestions for probably the case in Richmond. the manuscript. Thanks to C. Hrymack and A. Lindholm for Outbreaks of winter moth do occur in the presence their help with Þeld work. This research was funded by a of C. albicans in Europe (Tenow 1972, Wigley 1976) grant to J.H.M. from the Blueberry Growers of British Co- and have occurred in Nova Scotia after the initial lumbia, from Agriculture Canada, and from the Natural Sci- ence and Engineering Research Council of Canada. population collapse of the early 1960s (McPhee et al. 1988, Embree 1991). Much of our understanding of native populations of winter moth and C. albicans References Cited comes from studies carried out at Wytham Wood AliNiazee, M. T. 1986. The European winter moth as a pest (Varley and Gradwell 1968). Varley and Gradwell of Þlberts: damage and chemical control. J. Entomol. Soc. began their life-table analysis of the moth in 1950, the BC 83: 6Ð12. year after an outbreak that reached densities never Beirne, B. P. 1975. Biological control attempts by introduc- matched in the next 18 yr of study (see Varley and tions against pest insects in Canada. Can. Entomol. 107: Gradwell 1958). The next major outbreak in the Ox- 225Ð236. ford area was in the early 1970s, just after the Varley Campbell, R. W. 1963. Some ichneumonid-sarcophagid in- and Gradwell study ended (Wigley 1976). During the teractions in the gypsy moth Porthetria dispar (L.) (Lep- studies of Varley and Gradwell, parasitism by C. albi- idoptera: Lymantriidae). Can. Entomol. 95: 337Ð345. DeBach, P. 1974. Biological control by natural enemies. cans was generally low, but it was highest in 1950 after Cambridge University Press, London, Engl. the 1949 outbreak and then increased slightly after 2 Dubrovin, U. V. 1990. Peculiarities of the distribution of periods of high densities in 1957 and 1965 (Varley et Operophtera brumata L. (Lepidoptera: Geometridae) in al. 1973). Because the principal study of Varley and plantations in Vorenezh province. Entomol. Obozr. 2: Gradwell (i.e., 1968) did not cover outbreak densities, 281Ð286 (translated from Russian). the biological control potential of C. albicans was not Embree, D. G. 1965a. The population dynamics of winter obvious. However, Tenow (1972) had associated high moth in Nova Scotia 1954Ð1962. Mem. Entomol. Soc. Can. levels of parasitism (by unknown parasitoids) with the 46: 1Ð57. Embree, D. G. 1965b. Population studies of Operophtera decline of winter moth outbreaks in Scandinavia. This species, O. brumata (L.), O. bruceata (Hulst) and lends support to the recommendation of Myers et al. Pseudexentera cressoniana (Clem.) in Nova Scotia. Inter- (1989) to select, as agents of biological control, natural nal Report M-2. Forest Research Laboratory, Moncton, enemies that are normally rare in their native habitat. New Brunswick. February 1999 HORGAN ET AL.: NEW INTRODUCTION OF WINTER MOTH AND PARASITOID 107

Embree, D. G. 1966. The role of introduced parasites in the Pearsall, I. A., and S. J. Walde. 1994. Parasitism and preda- control of the winter moth in Nova Scotia. Can. Entomol. tion as agents of mortality of winter moth populations in 98: 1159Ð1167. neglected apple orchards in Nova Scotia. Ecol. Entomol. Embree, D. G. 1991. The winter moth, Operophtera bru- 19: 190Ð198. mata, in eastern Canada, 1962Ð1988. For. Ecol. Manage. Roland, J. 1988. Decline of winter moth populations in 39: 47Ð54. North America: direct verses indirect effect of introduced Embree, D. G., and P. Sisojevic. 1965. The bionomics and parasites. J. Anim. Ecol. 57: 523Ð531. population density of Cyzenis albiicans (Fall.) (Tachini- Roland, J. 1990. Interaction of parasitism and predation in dae: Diptera) in Nova Scotia. Can. Entomol. 97: 631Ð639. the decline of winter moth in Canada. In A. D. Watt, N. Feeny, P. P. 1970. Seasonal changes in oak leaf tannins and Kidd, S. Leather, and M. Hunter [eds.], Population dy- nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51: 565Ð581. namics of forest insects. Intercep, Andover, Germany. Fitzpatrick, S. M., J. J. Troubridge, and B. Peterson. 1991. Roland, J. 1994. After the decline: what maintains low win- ter moth density after successful biological control? J.

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