Factors Affecting the Flight Activity of Winthemia fumiferanae (Diptera: )

CHRISTIAN HEBERT, CONRAD CLOUTIER, ANDJACQUES REGNIEREI Departement de Biologie, Universite Laval, Sainte-Foy, Quebec, Canada GIK 7P4

Environ.Entomol.19(2):293-302(1990)

ABSTRACT The influence of variousenvironmental factors on flightactivity of Winthemia Downloaded from https://academic.oup.com/ee/article/19/2/293/468373 by guest on 01 October 2021 fumiferanae Tothill (Diptera: Tachinidae) was studied in southern Quebec from 1985 to 1987. Adults of both sexes were strictly diurnal and much more active in the presence of sunlight. Flight activity was positively related to maximum air temperature above 150Cand, to a much lesser degree, negatively related to precipitation. Males and females showed different spatial distribution patterns. Males were more numerous in the lower canopy of the forest, whereas females were more abundant in the higher canopy. Malesalsowere found more often in deciduous vegetation than on conifers, the inverse being observed for females. We conclude that sylvicultural practices that might enhance habitat diversity and natural lighting should favor the activity of W. fumiferanae as a parasitoid of the spruce budworm, Choristoneura fumiferana Clemens (Lepidoptera: Tortricidae).

KEY WORDS Insecta, Winthemia fumiferanae, flight activity, environment

PARASITOIDEFFICACYis determined to a large ex- gence period when males were most active and tent during adult life (Vinson 1976, Nyrop & Sim- females were maturing eggs, and during the peak mons 1986). Early during the adult stage, parasit- oviposition period of females on spruce bud worm oids select areas where host searching will be larvae (Hebert et al. 1989). We also studied the concentrated. Host density is an important factor effects of weather conditions, tree species, and influencing parasitoid adult activity (Hassell 1982), height in the canopy on activity levels. but environmental factors also are critical. In forest habitats, factors such as stand composition (Sim- mons et al. 1975), height in the canopy (Weseloh Materials and Methods 1981), and the presence of food sources (Leius 1967) The study was conducted in 1985 and 1986 in are all factors which can influence flight activity a site near Armagh, Quebec (46°46'N, 70"39'W, or levels of parasitism, or both. Parasitoid flight 270 m altitude). The environment of the plot was activity also is affected by weather conditions such diverse and dominated by a heterogeneous stand as temperature, humidity, and light (Weseloh 1976, of balsam fir (Abies balsamea (L.) Miller), white Vinson 1976). Detailed knowledge of factors af- spruce (Picea glauca (Moench) Voss), and several fecting flight activity is needed to evaluate the po- deciduous tree species including trembling aspen tential effects of sylvicultural practices on parasit- (Populus tremuloides Michaux), and white birch ism. Such understanding would help in the (Betula papyrifera Marshall). A limited amount of development of parasitoid augmentation and con- data also was obtained from two other sites, the servation strategies as part of integrated pest man- Lac Ii I'Epaule plot in the Laurentian Wildlife Re- agement programs. serve, Quebec (47°18'N, 71°12'W, 750 m altitude) Winthemia fumiferanae Tothill is a common in 1985, and the Lac Solitaire plot in the St-Maurice parasitoid attacking late instars of the spruce bud- Wildlife Reserve (47°12'N, 73°00'W, 350 m alti- worm, Choristoneura fumiferana (Clemens). It tude) in 1987. The Armagh and Lac Ii I'Epaule overwinters in a puparium within the first few plots were described in detail by Lethiecq & Re- centimeters of the forest floor under conifer trees; gniere (1988). adults emerge in late spring, and males emerge Trapping. In Armagh in 1985, two Malaise traps several days before females (Hebert et al. 1989). (Townes 1972) were operated (one at ground level, A 2-wk preoviposition period insures that mature the other at a height of 8 m above ground) in a eggs become available when spruce budworm lar- narrow abandoned forest road where parasitoid vae enter the sixth stadium, the preferred instar flight activity was likely to be higher than within for oviposition (e.H. & e.e., unpublished data). the forest (Townes 1972). A third trap, placed at Our paper reports daily patterns of W. fumi- ground level within the forest, also was operated feranae flight activity near the end of the emer- between 24 and 29 May. In 1986, two additional traps were set up in the old road at 4 and 12 m

I Centrede Foresleriedes Laurenlides,C. P. 3800,1055rue above the ground (total of four traps). Traps sus- du Peps,Sainte-Foy,Quebec,CanadaG1V 4C7. pended above the ground were operated with pul-

0046-225X/90/0293-0302$02.00/0© 1990EntomologicalSocietyof America 294 ENVIRONMENTAL ENTOMOLOGY Vol. 19, no. 2 leys (Nyrop & Simmons 1986). Traps were emptied the ground. More traps also were placed in clear- daily, except for 1-2 wk at the beginning and to- ings and in an abandoned field at 1 m above the ward the end of both seasons. On three sunny days ground in grasses and shrubs. Traps were collected (7, 8, 21 June 1985), traps were inspected every 2 and replaced three times per week from early May h from 0500 to 2100 hours Eastern Summer Time to late August. caught on these traps were (EST) to establish daily patterns of activity. Flies identified, sexed, and counted in the laboratory. were identified, sexed, and counted in the labo- An automatic weather station installed within ratory. W, fu.miferanae is the largest tachinid para- the Armagh study plot provided daily minimum sitoid of the spruce bud worm and is readily rec- and maximum air temperatures and precipitation ognized by its yellow scutellum and antennae. The in 1985 and 1986. males (eyes contiguous rather than separate) also Data Analysis. Mean daily times of capture of bear yellow stripes on the abdomen. adult W. fumiferanae on different trap types and

White sticky traps also were used in Armagh and locations were compared with Watson-Williams Downloaded from https://academic.oup.com/ee/article/19/2/293/468373 by guest on 01 October 2021 Lac a l'Epaule in 1985. These traps, described by tests (Zar 1974). The number of flies captured on Regniere & Fletcher (1983), consisted of a pair of sticky traps exposed or not to sunlight during the cylindrical cardboard containers (trapping surface peak flight activity was compared with x2 tests. area 0.19 m2) coated with Stickem Special (Sea- Differences in total seasonal catch on different plant bright Enterprises, Emeryville, Calif,) and hung on species and habitats (yellow sticky traps, Armagh a metal coat hanger. Pairs of traps were suspended 1986) were compared by analysis of variance (AN- at 2, 4, 6, 8, 10, and 12 m above the ground on a OVA) and Duncan's multiple range test (Duncan vertical loop attached to a rope hanging between 1955, SAS Institute 1985). The seasonal trends in the tops of dominant trees; five trapping loops were the percentage of both sexes captured in conifers set up in each plot within the stand. These traps within the forest (as opposed to deciduous tree (hereinafter, intercrown traps) were inspected every species, mostly within the regeneration plot, with 2-3 d from 6 June to 6 July in f\rmagh and from the exception of trembling aspen and white birch 24 June to 31 July in Lac a l'Epaule (periods of which were common within the forest) were com- maximum flight activity of females). On three sun- pared by regression analysis. Sex ratios and vertical ny days (7, 8, and 21 June), traps were inspected distributions of catch of both sexes on conifer trees every 2 h, from 0500 to 2100 hours (EST) in Ar- were compared with x2 tests. magh to establish daily patterns of activity. On 21 The relationship between daily capture of W. June, trap pairs set up at 2 m above ground, one fumiferanae in Malaise traps and meteorological pair in each cardinal direction on two balsam fir conditions was determined with a nonlinear regres- and two white spruce trees located around a clear- sion model developed by Lavallee et al. (1988) ing, also were monitored every 2 h, Flies were which has the general form: identified, sexed, and counted in the field. To relate the flight activity of W. fumiferanae Y = g(x) f(T,P) (1) to host and nonhost tree species in various habitats more closely, yellow sticky cardboard traps (Sea- where Y is the number of flies per day, x is time bright Enterprises, Emeryville, Calif.) were used (days) after the onset of the flight season, T is max- in Armagh in 1986 and Lac Solitaire in 1987. These imum daily air temperature (0C), and P is the total traps have a rectangular trapping area (0.03 m2), daily precipitation (mm). Maximum rather than Seven such traps were attached to a rope loop run- mean daily air temperature was used because, as ning from the ground to the top of each of five will be shown later, W. fumiferanae flies by day. balsam fir and five white spruce trees, in a manner Equation 1 is based on the assumption that the such that the traps lay closely parallel to the edge daily rate of capture is a composite function of of the foliage at 0, 2, 4, 6, 8, 10, and 12 m above time and weather. The g(x) term represents the the ground, The traps were located on the south seasonal trend in abundance as measured with sides of the trees to receive the longest sunlight Malaise traps. This is determined by population exposure. In Armagh in 1986, additional traps were density, emergence of flies from the soil, longevity, placed at various heights in one or two trees of five and migration. Sex-related differences in flight ac- other species: trembling aspen, white birch, sugar tivity and trap efficiency also are included in the maple (Acer saccharum Marshall), white pine (Pi- g(x) term. Thus, g(x) represents the potential num- nus strobus L.), and larch, Larix laricina (Du Roi) ber of flies available for capture over time. Because K. Koch. Traps also were placed outside of the the processes underlying this trend are different forested area in a wide clearing covered with young between the sexes and from season to season (He- deciduous regrowth (10-15 yr old) the trees being bert et al. 1989), a different g(x) function was fitted approximately 3.5 m high (hereinafter, the regen- to data from each year and for each sex. The Wei- eration plot). One trap per tree was placed at 2.5 bull function (see Yang et al. 1978) was used to m above the ground on four specimens of trem- describe g(x) because of its characteristic shape and bling aspen, white birch, sugar maple, common flexibility, and because it has only two parameters: chokecherry (Prunus virginiana L.), and in bushes of red raspberry (Rubus idaeus L.) at 1 m above g(x) = :r'-l e-(rM· (2) April 1990 HEBERT ET AL.: FLIGHT ACTIVITY OF Winthemia fumiferanae 295

0.7 Sticky traps in a clearing (n-55) Sticky traps Males 0•.18 and 17 0.3 0.• •0 Females n_31 and 18 0.5 0.2

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et~ 0.2 0 > 0.1 ...• :J: :« 0 Q l- et LL Sticky traps in the stand (0-21) 0 ...•0 0.• Z et 0 0.• Malaise traps Males n••23 and 10 b 0.' !i; l- Downloaded from https://academic.oup.com/ee/article/19/2/293/468373 by guest on 01 October 2021 0 0.5 LL D.. • Females n_17 and 7 0 0 0 a: Z 0.2 D.. 0.' 0 1= a: 0.3 0 D.. 0 a: 0.2 D..

0.1 0.' Malaise traps in the old road (n-29) 0.3 5 7 9 11 13 15 17 19 21 23 1 3 5 7 9 11 13151719

7 June I 8 June 0.2

TIME OF DAY (EST) 0.1 Fig. 1. Bi-hourly catches of adult W. fumiferanae on Malaise and sticky traps on 7 and 8 June at Armagh in 1985. 11 13 1S 17 19 21

TIME OF DAY (EST) where u represents the spread of the seasonal trend Fig. 2. Bi-hourly catches of female W. fumiferanae (analogous to the standard deviation of a proba- on Malaise and sticky traps in different locations on 21 bility distribution function) and A determines its June at Armagh in 1985. symmetry. The f(T,P) function in Equation 1 is of primary ent values of parameters {3,u, and A for males and interest here because it models the effect that females in each year. In a first round of analysis, weather conditions have on the expression of the data from 1985 and 1986, and then for males and seasonal trend g(x) in determining daily catches. females (pooling years), were treated separately by We assumed that flight activity is directly propor- nonlinear regression (BMDP-AR, Dixon et al. 1985). tional to T and inversely proportional to P. Thus, The model also was fitted to data from both years Ta and both sexes combined to obtain pooled estimates f(T,P) = (P + l)b ' (3) of parameters a and b. Significance of parameter values and of differences was determined with t where parameters a and b give f(T,P) its flexibility. tests. The +1 term in the denominator insures that f(T,P) has a finite value when P = o. Results The full regression model is thus: Daily Activity Patterns. Daily activity patterns T" Y = {3 XA-1 e-(%/a'f --- (4) were studied first near the end of the adult emer- (P + l)b' gence period (7-8 June 1985). W. fumiferanae is where {3is a proportionality constant. Dummy vari- strictly diurnal, as no flies were caught at night ables (Gujarati 1970) were used to estimate differ- (Fig. I). Few flies were caught before 0700 and

Table 1. Mean daily time of capture (EST) of adult W.fumiferanae on traps placed in different locations in a forest stand on 7,8, and 21 June 1985 in Armagb

Time of capture in h:min, f ± SO Parasitoid sex Date F" df P Malaise, road Sticky, stand Sticky, clearing Male 7 June 14:56 ± 3:47 9:08 ± 1:22 28.39 1,39 <0.0005 8 June 13:24 ± 2:26 9:44 ± 1:49 16.17 1,25 <0.0005 Female 7 June 13:04 ± 3:04 11:52 ± 2:23 5.34 1,46 <0.05 8 June 13:24 ± 2:04 9:00 ± 1:11 10.16 1,23 <0.005 21 June 13:36 ± 2:01 9:20 ± 1:47 10:48 ± 2:44 10.49 2,102 <0.0005

a Watson-Williams test. 296 ENVIRONMENTAL ENTOMOLOGY Vol. 19, no. 2

Table 2. Estimates of parameters (±SD) describing the patterns may be caused by trap exposure to direct effects of maximum daily air temperature (T) and rainfall sunlight. Because of their location, intercrown traps (P) on flight activity of male and female W. fumifero.no.e at Armagh in 1985 and 1986 were in full sun before 1100 hours (of 30 traps, 18- 21 were exposed to direct sunlight from 0900 to Source 1100 hours compared with only 4-7 traps from a" ba n R2 of data 1300 to 2100 hours), whereas Malaise traps were 1985 2.74 ± 0.39 0.11 ± 0.06 110 0.787 fully exposed after 1100 hours. At the time of peak 1986 3.23 ± 0.52 0.14 ± 0.09 102 0.625 activity on sticky traps (combined catches at 0900 Males 2.52 ± 0.41 0.14 ± 0.06 106 0.845 and 1100 hours), a significantly greater proportion Females 3.03 ± 0.44 0.10 ± 0.06 106 0.661 Pooled 2.79 ± 0.29 0.11 ± 0.04 212 0.790 of flies of both sexes were caught on those traps exposed to sunlight than on traps not under direct a f(T, P) = T"/(P + l)b. exposure (males: 91.7%, x2 = 11.25; df = 1; P <

0.001; females: 87.8%, x2 = 11.15; df = 1; P < Downloaded from https://academic.oup.com/ee/article/19/2/293/468373 by guest on 01 October 2021 0.001). Dependence on sunlight also is indicated after 1900 hours, and there was no consistent dif- by the fact that the Malaise trap placed within the ference in the daily catch patterns of males and forest in the Armagh stand in 1985 caught only females (Watson-Williams tests: P > 0.05, except five flies from 24 to 29 May, whereas a similar trap for 7 June on sticky traps where 0.025 < P < 0.05). placed in the abandoned road caught 84 over the On intercrown traps, adult flight activity peaked same period. in the morning, whereas Malaise traps caught most Daily activity also was studied on 21 June during flies in the afternoon. Mean daily times of capture peak oviposition on the spruce bud worm. Only data on the two types of traps were significantly differ- on females are presented because males had almost ent for both sexes (Table 1). This difference in daily disappeared from the population. Again, the pat-

1985 1986 90 20 • •• MALES • MALES I" ,I ,I I 60 I I ~ Seasonal trend I I Predicted 10 I >- A-----A Observed « 30 Cl ......

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o o o 20 40 60 TIME (DAYS) Fig. 3. Predicted and observed male and female catches of W. fumiferanae at Amargh in 1985 and 1986. April 1990 H~BERT ET AL.: FLIGHT ACTIVITY OF Winthemia fumiferanae 297

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~4/,y1" 20 4(.( 10 6 (,0 • Ii, it.~~£.~~ilj~t. "'''') Fig. 4. Relationship between daily maximum air temperature (T), precipitation (P) and flight activity of male and female W. fumiferanae at Armagh in 1985 and 1986. Flight activity is Yl[fJ g(x) f(t,O)] where t is average daily maximum temperature. tern of flight activity was diurnal (Fig. 2). There ature (t = 9.62; df = 198; P < 0.001). Few flies was no clear difference in daily activity patterns were caught on days when the air temperature of females between preoviposition and oviposition remained below 15°C (Fig. 4). The effect of rainfall periods, as defined by the presence or absence of also was significant (t = 2.75; df = 198; P < 0.01) mature eggs in the uterus. Female flight activity but was far less pronounced. A distinct association again peaked at different times depending on trap between abundant rainfall and low maximum air type and exposure, or both (Table 1). Intercrown temperature may have masked the effect of pre- traps placed within the stand caught most flies in cipitation on flight activity. Values of parameters the morning. Malaise traps in the old road again a and b were very similar in 1985 and 1986 for were most effective in the afternoon. Sticky traps males and females (Table 2). None of the differ- placed in the clearing had the longest period of ences was significant (all differences with P > 0.50, exposure and caught flies throughout the day. Car- t tests). dinal direction significantly (X2 = 16.35; df = 3; P Spatial Distribution of Adults. The number of < 0.001) influenced the number of flies captured flies of both sexes caught on intercrown traps within on these traps, 45.4% being caught on the south the stand varied with height above the ground in side of trees compared with 21.8%,25.5%, and 7.3% both plots in 1985. Similar results were obtained on traps placed on the east, west, and north sides, with yellow sticky traps in 1986 and 1987 on both respectively. tree species (all differences with P < 0.001, X2 tests Weather and Flight Activity. Parameters a and of homogeneity). In all cases, more males were b in Equation 4 represent the effect of air tem- caught in the lower canopy and more females higher perature and rainfall on flight activity. Their es- up (Fig. 5). All differences were highly significant timated values for various combinations of field (P < 0.001, X2 tests of homogeneity). data are given in Table 2. Equation 4, fitted to the At Armagh in 1986, 2,798 flies were caught on pooled data on both sexes and from both years, the 149 traps set up in different habitats on various explained most of the variation (R2 = 0.79) in ob- plant species. Traps in clearings and in the open served daily trap catch (Fig. 3; Table 2). Fluctua- field caught few flies (Table 3). The sex ratio of tions about the seasonal trends were caused mostly flies was generally male-biased (67% male) around by a strong dependence on maximum air temper- deciduous plants and female-biased (36% male) in 298 ENVIRONMENTALENTOMOLOGY Vol. 19, no. 2

40 40 60 Males 1985 Malus 1986 Males 1987 • Armagh (na200) • Bf(n=25g) Bf (n-378) 50 iii Lac a I'~paule (n=33) 1m Ws(na247) •II Ws(n_466) 30 30 40

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HEIGHT (m) Fig. 5. C:atches of male and female W. fumiferanae at different heights on intercrown sticky traps at Armagh and Lac a I'Epaule in 1985, and on yellow sticky traps located on balsam fir (Bf) and white spruce (Ws) trees at Armagh in 1986 and Lac Solitaire in 1987. conifers, a highly significant difference (x2 = 263.7; that mating may take place in many different hab- df = 1; P < 0.001). The percentage of the male itats. population found in conifers remained below 50% throughout the season (regression of percentage Discussion males in conifers on Julian day; F = 0.05; df = I, 14; P > 0.83), but the proportion of females in Winthemia fumiferanae is a strictly diurnal flier, conifers increased steadily from the emergence pe- as are many other species of the (DeLoach riod until the end of the season (R2 = 0.64; F = & Rabb 1971, Danks 1975b). Indeed, most forest 35.8; df = 1, 20; P < 0.001) (Fig. 6). Traps in insect parasitoids are diurnal (Weseloh 1976). Air trembling aspen within the stand caught signifi- temperature during the day has a strong influence cantly more male flies than those in other tree on the flight activity of W. fumiferanae. This also species within the same habitat. This preference was reported for Apanteles fumiferanae Viereck remained throughout the season (Fig. 7). In the and Glypta fumiferanae Viereck (Elliott et al. regeneration plot, both males and females were 1986). The 15°C flight threshold estimated here for particularly abundant on trembling aspen. Sugar W. fumiferanae is close to the l4°C reported for maple seemed to attract more male flies in the Winthemia rufopicta Bigot (Danks 1975b). Tem- regeneration plot but not within the stand. A peak perature-dependence of flight may be a strong ex- of flight activity in late May-early June occurred ternal factor determining daily activity rhythm in during the presumed mating period (Hebert et al. these . Oviposition of W. rufopicta (Danks 1989), although mating in the field was not ob- 1975a) and Bessa harveyi Townsend (Turnock 1978) served during this study. This peak occurred in all is similarly affected by temperature. Sixth instars trapping locations (Fig. 7) except the field and of the spruce bud worm are abundant for <3 wk clearings where few flies were caught, an indication in the field (Hebert et al. 1989). Adverse weather April 1990 H~BERT ET AL.: FLIGHT ACTIVITY OF Winthemia fumiferanae 299

Table 3. Catches of W. fumiferanae on yellow sticky traps in different habitats at Armagh in 1986

No. flies per trap (of ± SE) Proportion Habitat Vegetation &l 22 of 22 Stand Balsam fir" 8.3 ± 1.8d 18.2 ± 3.2ab 0.69 White spruce" 7.7 ± 1.5d 14.3 ± 2.1ab 0.65 Trembling aspcn 35.0 ± 9.5a 13.7 ± 2.6ab 0.28 Sugar maple 3.2 ± 0.6d 1.3 ± 0.4b 0.30 White birch 13.8 ± 4.0cd 10.7 ± 3.7ab 0.44 White pine 5.0 ± 4.Od 12.5 ± 4.5ab 0.71 Larch 1.5 ± 1.5d 7.5 ± 0.5ab 0.83 Regeneration plot White birch 12.8 ± 2.8cd 8.8 ± 2.6ab 0.41 Chokecherry 17.3 ± 6.9bcd 8.0 ± 1.5ab 0.32 Sugar maple 27.5 ± 16.7abc 11.0 ± 6.0ab 0.29 Trembling aspen 31.3 ± 1O.0ab 22.0 ± 6.1a 0.41 Downloaded from https://academic.oup.com/ee/article/19/2/293/468373 by guest on 01 October 2021 Raspberry bushes 5.9 ± 2.1d 3.9 ± 1.5ab 0.40 Clearings Various shrubs 1.3 ± 0.3d 3.5 ± 1.9ab 0.74 Grasses 4.5 ± 2.Od 2.3 ± 1.3b 0.34 Field Chokecherry 1.0 ± 0.6d 0.3 ± 0.3b 0.25 Grasses 0.3 ± 0.2d 0.6 ± 0.2b 0.67

In each column, means followed by different letters are significantly different (P < 0.05, Duncan's multiple range test). a Traps at ground level were not included in the analysis. conditions during that period may reduce ovipo- exposure to sunlight influenced catch in this study. sition by W. fumiferanae, as observed for G. fu- The Malaise trap placed at ground level within the miferanae (Nyrop & Simmons 1986). This would Armagh stand in 1985 caught 17 times less flies be particularly true in high-altitude areas such as than the trap placed in the abandoned road. Flies Lac a I'Epaule, where cool and rainy weather is were captured with sweep nets consistently in more frequent in midsummer (Lethiecq & Re- greater numbers on well-exposed trees. Under gniere 1988). cloudy conditions, W. fumiferanae flies were rare- Light also seems to play an important role in ly seen flying. It is likely that much of the variation determining flight activity of W. fumiferanae. Trap in trap catches left unexplained by the tempera-

100 • • D Males Females • 80 • •• U) a:: • • LLI • U- 60 • • • Z • 0 • • 0 • • D • D Z 40 D • - D • D 0~ D D 20 D D • D D D D• D D 0 130 140 150 160 170 180 190

MAY JUNE JULY JULIAN DAY Fig. 6. Seasonal trends in percentages of male and female W. fumiferanae captured on conifer, as opposed to deciduous tree species, at Armagh in 1986. Tree species considered were balsam £irand white spruce for conifers and trembling aspen, white birch, sugar maple and common chokecherry for the deciduous species. Percentage values were based on more than five individuals; only three of 16 values (males) and 4 of 22 values (females) were based on <20 individuals. 300 ENVIRONMENTAL ENTOMOLOGY Vol. 19, no. 2

3 Balsam fir + White spruce (60 traps) ••• Males (n••482) 2 Mating perlod -a- Females (n-967)

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0

> 3 White birch (6 traps) 4( Males (n=83) Q 2 Females (n,.,64) -.D.. < a:.... 0 U)-. w ::::i LL LL 3 0 Regeneration plot (16 traps) ... Males (nz355) -a- Females (n=199) a: 2 mW :)== Z 0

3 Raspberry bushes (10 traps) ... Males (n,.,59) 2 -a- Females (n=38)

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3 Clearings (14 traps) ••• Males (n,.,63) 2 -a- Females (n=32)

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(1979) reported an inverse distribution of males correlations between the frequency of egg and pu- Downloaded from https://academic.oup.com/ee/article/19/2/293/468373 by guest on 01 October 2021 and females of the tachinid Parasetigena silvestris pal parasitism in Malacosoma amerieanum F. and (Robineau-Desvoidy), a parasitoid of gypsy moth the abundance of nectar-producing flowers in the larvae. In this case, males were more abundant undergrowth. Moreover, such habitats sustain other higher up, whereas females were mostly found near lepidopterous species that spruce budworm para- the ground where they searched on tree trunks for sitoids may use as alternate hosts. host larvae moving to resting sites. The concentra- The preceding discussion has pointed out im- tion of female W. fumiferanae high in the canopy portant environmental factors (other than host den- may be a response to the distribution of host larvae sity) that influence the flight activity of W. fumi- (Regniere et al. 1989). Attraction to bright sunlight feranae and consequently its reproductive success. also may be involved. Two of these factors, temperature and precipita- Male W. fumiferanae were more abundant in tion, are unmanageable, but understanding their deciduous trees than in conifers, whereas the op- influence may help explain the fluctuations in the posite was true for females. Differences in habitat incidence of parasitism by W. fumiferanae. How- preferences between males and females have been ever, other factors such as sunlight and the presence reported for other species of this genus (Allen 1925, of various habitats are manageable. An increase in Thompson 1963, DeLoach & Rabb 1971). Females sunlight penetration and the presence of regener- have to search for hosts. During egg maturation ation patches of deciduous trees can be obtained and early in the oviposition period, female W. fu- Simultaneously through sylvicultural practices. In miferanae were caught as often in deciduous trees the future, such practices might be incorporated as in conifers. At that time, they may have been in forest pest management programs. in search of food and mates. Diptera are attracted by sap running from wounds in the bark of decid- uous trees (Martin 1983). It remains possible that Acknowledgment they were also searching for hosts other than spruce We thank A. Labrecque, J.-F. St-Pierre, A. Lavallee, bud worm (Coppel & Smith 1957). From late June C. Tremblay, and D. Lachance for their assistance in to the end of the season, females were more abun- field work. This study was supported by the Ministere dant on conifers, where they searched for spruce de I'Energie et des Ressourcesdu Quebec and by a grad- budworm larvae. Late in the season, surviving fe- uate scholarship from the National Sciences and Engi- males seemed to spend most of their time searching neering Research Council of Canada to C.lf. for hosts. Similar changes in plant preferences with age have been reported for females of the tachinid References Cited Eueareelia rutilla ViiI. (Herrebout 1967, 1969). This species was first attracted toward food sources dur- Allen, H. W. 1925. Biologyof the red-tailed tachina- ing egg maturation, and later toward trees with fly, Winthemia quadripustulata Fabr. Mississippi Agricultural Experiment Station Technical Bulletin potential hosts for oviposition. Male activity is not 12, State College. host-dependent, as indicated by habitat prefer- Coppel, H. C. & B. C. Smith. 1957. Studies on dip- ences which were similar to those of reproductively terous parasites of the spruce budworm, Choristo- immature or unmated females during the putative neura fumiferana (Clem.) (Lepidoptera: Tortrici- mating period (early June; Hebert et al. 1989). dae). V. Omotoma fumiferanae (Tot.) (Diptera: Trembling aspen was the deciduous tree species Tachinidae). Can. J. Zoo\.35: 581-592. preferred by both sexes of W. fumiferanae. Tach- Danks, H. V. 1975a. Seasonal cycle and biology of inids are known to be attracted by a substance Winthemia rufopicta (Diptera: Tachinidae) as a par- secreted by the opening of leafbuds of Populus asite of Heliothis spp. (Lepidoptera: Noctuidae) on tobacco in North Carolina. Can. Entomol. 107: 639- spp. and by the honeydew of aphids developing 654. on trees of this genus (Martin 1983). 1975b. Factors determining levels of parasitism by Knowledge of microhabitat preferences of W. Winthemia rufopicta (Diptera: Tachinidae), with fumiferanae should be useful in the design of bi- particular reference to Heliothts spp. (Lepidoptera: ological control programs aimed at enhancing Noctuidae) as hosts. Can. Entomo\. 107: 655-684. parasitoid activity. In particular, thinning to in- DeLoach, C. J. & R. 1. Rabb. 1971. Life history of 302 ENVIRONMENTAL ENTOMOLOGY Vol. 19, no. 2

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