Biological Control 20, 113–121 (2001) doi:10.1006/bcon.2000.0898, available online at http://www.idealibrary.com on

Biology and Seasonal Abundance of Parasitoids of the Banded Sunflower (: Tortricidae) in Sunflower

Laurence D. Charlet Northern Crop Science Laboratory, Agricultural Research Service, U. S. Department of Agriculture, Fargo, North Dakota 58105-5677

Received November 30, 1999; accepted November 8, 2000

America. As such, it is produced in close proximity to Mortality, parasitization, and overwintering devel- its progenitors. Although a number of herbivores opment through pupation of the banded sunflower have been reported from native sunflowers, to date moth, Cochylis hospes Walsingham, larvae and two of only about six species consistently cause economic its endoparasitoids, Glypta prognatha Dasch and Che- problems in major commercial sunflower production lonus phaloniae Mason, were followed over a 2-year areas (Hilgendorf and Goeden, 1981; Rogers, 1988a,b; period (1987 to 1989). Development of parasitoids in Charlet et al., 1997). During the development of the the field was determined for each species by examina- crop in the northern Plains in the 1960s and 1970s, the tion of moth eggs and larvae during the 1989 season. Parasitoids of C. hospes, recovered from cultivated banded sunflower moth, Cochylis hospes Walsingham, sunflower, Helianthus annuus L., from North and was reported by Schulz (1978) to be a noneconomic South Dakota and Minnesota in 1994 and 1995, para- problem requiring no management practices. However, sitized 24 and 17% of larvae, respectively. Species of since the early 1980s, cultivated sunflower fields in Hymenoptera collected included G. prognatha and North Dakota, Minnesota, and South Dakota have fre- Trathala sp. (Ichneumonidae), C. phaloniae and Mac- quently had economic damage caused by the moth rocentrus ancylivorus Rohwer (Braconidae), and Per- (Charlet and Busacca, 1986; Charlet and Brewer, ilampus robertsoni Crawford (Pteromalidae). The 1997). The banded sunflower moth also occurs on sun- most abundant parasitoid was G. prognatha. In 1994 flower in the Canadian prairie provinces of Manitoba, and 1995, C. phaloniae, an egg-larval parasitoid, Saskatchewan, and Alberta (Westdal, 1975; Arthur emerged earlier but was less abundant than the later and Campbell, 1979) and populations have also been occurring larval parasitoid G. prognatha. Species of increasing in Kansas (Aslam and Wilde, 1991). Banded parasitoids collected from cultivated sunflower and sunflower moth larvae have been recovered from about five species of native sunflowers were similar. An ad- nine species of native sunflowers in the United States ditional parasitoid, Mastrus sp. (Ichneumonidae), was (Rogers, 1988a,b; Beregovoy and Riemann, 1987; Char- recovered only from the native sunflowers H. annuus let et al., 1992). and H. tuberosus L. Results from 1994 and 1995 showed The biology and economic impact of the banded sun- that parasitization rates for the total season by the flower moth have been described (Westdal, 1975; Char- two most abundant parasitoids were similar in fields using three planting dates. These results suggest that let and Gross, 1990; Charlet and Barker, 1995). Infor- altering planting date could be successfully used as a mation on parasitoids associated with the banded sun- pest management strategy without disrupting the bi- flower moth in its native hosts and in cultivated ological control of the banded sunflower moth. Con- sunflower is mainly limited to museum or collection servation of these parasitoids in the sunflower agro- records. Westdal (1975) reported that in Manitoba, ecosystem is needed since they play an important role Chelonus phaloniae Mason (Braconidae) and Glypta in the management of C. hospes. sp. (Ichneumonidae) attacked banded sunflower moth Key Words: conservation biological control; Cochylis larvae and were able to maintain the pest below levels hospes; Hymenoptera; Lepidoptera; sunflower; Heli- causing economic losses. Chelonus shoshoneanorum anthus; natural enemies; parasitoids. Viereck was noted to be an important larval parasitoid of the banded sunflower moth in Manitoba by Macnak (1955), but was not included in the list of parasitoids of INTRODUCTION head-infesting of cultivated and native sun- flower from Canada by Sharkey et al. (1987). In Can- Sunflower (Helianthus annuus L.) is one of only a ada, two additional braconid parasitoids reared from very few domesticated crops that are native to North banded sunflower moth larvae are Bassus arthurellus

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1049-9644/01 $35.00 114 LAURENCE D. CHARLET

Sharkey and Bracon mellitor (Say) (Sharkey, 1985; was divided into four blocks and 2–5 heads were ran- Sharkey et al., 1987). Krombein et al. (1979) also in- domly collected from each block (8–20 heads total) cluded Macrocentrus ancylivorus Rohwer as a banded twice weekly. Heads were examined in the laboratory sunflower moth parasitoid. In cultivated sunflower and the number of banded sunflower moth eggs and fields of North Dakota and Minnesota, the banded sun- larvae counted. Eggs were placed on wet filter paper flower moth is parasitized by the braconids C. pha- and held until hatching and then first instars were loniae and M. ancylivorus and the ichneumonid wasps dissected and examined under a microscope for inter- Glypta prognatha Dasch, Glypta sp., Mastrus sp., and nal parasitoids. The instar of each banded sunflower Trathala sp. (Charlet, 1988, 1998; Bergmann and Os- moth larva collected from the heads was determined eto, 1990). and then all larvae were dissected to calculate the rate Plant domestication provides an opportunity to ex- of parasitism and determine the species of the parasi- amine the effect of plant variation on insect herbivores toids. Sampling ceased in early September when larvae and their natural enemies. Comparison can then be had exited the heads to overwinter in the soil. made by examining the guilds of natural enemies and Parasitoid species. Mature banded sunflower moth their relative impact on the host on both the wild relative and cultivated plant. Two recent papers have larvae from 8 cultivated sunflower fields in North Da- examined the interaction of parasitoids and their in- kota were sampled in 1994 and from 19, 5, and 3 fields sect hosts on wild plant species and a related cultivated in North Dakota, South Dakota, and Minnesota in crop (wheat, Brassica, and Phaseolus) (Benrey et al., 1995, respectively. A total of 15 sunflower heads were 1998; Morrill et al., 1998). The goals of this study were randomly collected from each field, placed in paper to examine both cultivated and native sunflower in the bags, and returned to the laboratory. Heads were held major production region of North and South Dakota in large plastic pans and mature banded sunflower and Minnesota to (1) determine the species of parasi- moth larvae were recovered as they left the heads in toids attacking the banded sunflower moth larvae and search of overwintering sites. Mature larvae were their rates of parasitization, (2) investigate the sea- placed in 1-liter soil-filled plastic containers and al- sonal occurrence, development, and overwintering of lowed to move into the soil before being placed in a cold the major parasitoid species recovered, and (3) deter- room maintained at 5°C. The containers were chilled mine the effect of altered planting dates on rates of for a minimum of 6 weeks before being moved to a parasitism. rearing room at 25°C, 50–60% RH, and a photoperiod of 16:8 (L:D) h. Larvae were held until eclosion of adult MATERIALS AND METHODS , emergence of parasitoids, or death. Dead larvae were not dissected to look for the presence of parasi- Parasitoid development in banded sunflower moth toids. Percentage parasitization was determined for larvae. A total of 42 and 21 soil-filled 40 dram round each parasitoid species based on total number of larvae plastic cylinders (vented on lid, bottom, and sides with reared, including those that died. wire mesh) with 25 mature banded sunflower moth Seasonal abundance. Field plots of approximately larvae each were buried in early September under the 0.5 ha were planted in 1994 and 1995 near Prosper, in soil surface in 1987 and 1988, respectively. In 1987– southeastern North Dakota. Plots were seeded in May 1988, two containers were removed at monthly inter- each year with sunflower hybrid ‘894’ in rows 76 cm vals beginning on 30 September and weekly intervals apart with plants spaced 30.5 cm within the row for a beginning mid-May to determine the stage of develop- final plant population of about 47,000 plants per hect- ment of the overwintering banded sunflower moth lar- are. Fields received a preplanting application of herbi- vae. The larvae also were dissected to calculate the percentage of unknown larval mortality, the percent- cide, but no chemical treatments, were used during the age of parasitism, and the developmental stage of the rest of the season in either year. Plants were sampled parasitoids. Containers were removed and evaluated twice weekly by visually counting adult parasitoids on until 10 August. In 1988–1989, based on the previous the sunflower head beginning at the R1 (early bud) year’s results showing an absence of development dur- growth stage (Schneiter and Miller, 1981). Counts ing the winter and spring, two containers were re- were made by examining 10 plants in the field at five moved and evaluated on 28 September and at weekly randomly selected sites in each of four blocks per plot intervals only from 7 June until 11 August. (200 plants total) and the mean number of parasitoids In 1989, a sunflower plot of approximately 0.5 ha was calculated. Sunflower heads (10) also were sam- was seeded with sunflower hybrid ‘894’ in rows 76 cm pled twice weekly in 1994 and counts made in the apart with plants spaced 30.5 cm within the row near laboratory of the number of banded sunflower moth Prosper, North Dakota. Sampling began 9 July when eggs and larvae. In 1995, heads were examined weekly adult banded sunflower moth were initially detected in to determine the presence or absence of eggs and lar- pheromone traps located in the same field. The field vae, with counts made only at random intervals. BANDED SUNFLOWER MOTH PARASITOIDS 115

Parasitoids in native and cultivated sunflowers. dates, with a season long mean of 19.7 (Ϯ2.3 SE)%. The Sunflower heads (approximately 75) were collected level of unknown mortality in 1988 to 1989 was similar from plants of one species of native sunflower (H. an- (24.2 Ϯ 4.0%). Based on dissection of C. hospes larvae, nuus) near Prosper, North Dakota, during late August total parasitization averaged 40.6 (Ϯ2.3) and 26.0 and early September, 1994. Heads (approximately 65) (Ϯ2.2)% in 1987–1988 and 1988–1989, respectively. C. were also recovered from a cultivated sunflower field at phaloniae was the most abundant parasitoid during the same location. In 1995, heads (25–50 per site) from both years, with parasitism ranging from 16 to 58% five species of Helianthus were collected from popula- among the 21 samples (1987 to 1988), with a mean of tions found at 14 sites in southeastern North Dakota. 38.4 (Ϯ2.3)%. Samples from 1988 to 1989 showed an The sunflower species, with number of collection sites overall reduction in parasitism, and mean parasitism indicated in parentheses, included H annuus (3), H. by C. phaloniae among sampling dates was only 16.4 nuttallii Torrey and Gray (4), H. maximiliani Schrader (Ϯ2.1)% (range ϭ 8–32%) for the overwintering period. (4), H. tuberosus L. (2), and H. petiolaris Nuttall (1). As Mean parasitism by G. prognatha during 1987 to 1988 mentioned above, cultivated fields had been sampled in was 2.2 (Ϯ0.6)% (range ϭ 0–10%) and increased in the southeastern North Dakota in 1994 for banded sun- 1988 to 1989 sampling period to 9.6 (Ϯ2.3)% (range ϭ flower moth larvae. Larvae were recovered and para- 0–22%). These levels of parasitism were much lower sitoid species reared as previously described. than the 80% reported by Westdal and Barrett (1955) Impact of planting date. Sunflower plots of approx- in Canada, but were similar to those reported in Min- imately 0.5 ha each were planted near Prosper, North nesota by Bergmann and Oseto (1990). Based on dis- Dakota, 11 and 23 May and 3 June in 1994, and 23 May sections at the beginning of the overwintering period, and 2 and 12 June in 1995. Seeding dates were planned parasitization was 55.3 and 48.4% in 1986 and 1987, to correspond to an early, mid, and late schedule uti- respectively (Bergmann and Oseto, 1990). In my study, lized by producers. The planting dates in 1995 were preoverwintering parasitism was 54% and 34% in 1987 delayed because of wet soil conditions. All trials were and 1988, respectively. Final parasitism (postoverwin- seeded with sunflower hybrid ‘894’ in rows 76 cm apart tering) reported by Bergmann and Oseto (1990) was with plants spaced 30.5 cm within rows. Except for a extremely low for both C. phaloniae (1986–1987 ϭ 0%; fall application of herbicide, no chemical treatments 1987–1988 ϭ 0.3%) and G. prognatha (1986–1987 ϭ were used during the growing season either year. Sun- 8%; 1987–1988 ϭ 18.2%) in contrast to my results. flower heads (17–30 per plot) were harvested from late However, they recorded parasitism based on emer- September to early October as they reached physiolog- gence traps and noted that overwintering mortality of ical maturity (R9 growth stage), but prior to the exodus moth larvae was high, due either to consumption by of mature larvae into the soil. Heads were returned to predatory beetles or to unknown factors. the laboratory and larvae were recovered and reared as There were no changes in development stage of ei- described earlier to determine the mean number of ther the overwintering banded sunflower moth larvae larvae per head and percentage parasitized. Sub- or their internal parasitoids from 30 September to 23 samples of larvae also were collected and dissected to June during the 1987 to 1988 sampling period and estimate parasitization rates for comparison with re- from 28 September to 5 July during the 1988 to 1989 sults from larval rearings. The ANOVA option of GLM sampling period (Table 1). Banded sunflower moth pu- procedure was used to compare the number of larvae pation first occurred in mid-July both years and by and rates of parasitism among the three planting dates early August, all larvae had pupated. C. phaloniae and significantly different means were separated using overwintered as a first instar and G. prognatha as LSD. Percentages were transformed using arcsine be- second instar. Development of C. phaloniae was ini- fore analysis (SAS Institute, 1990). tially detected from samples examined 28 June 1988, Parasitoid species for all studies were determined by with 46.2% in the second instar; by mid-July 54.5% of a comparison with specimens previously identified by C. phaloniae had developed to the second instar and the Systematic Entomology Laboratory (USDA, ARS, 9.1% had pupated (Table 1). By late July in both 1988 Beltsville, MD), Biological Resources (Central Re- and 1989 the majority of C. phaloniae had completed search Farm, Agriculture and Agri-Food Canada, Ot- development and pupated. In mid-July 1988, G. prog- tawa, Ontario, Canada), or the Royal Ontario Museum natha had begun development and by early August had (Toronto, Ontario, Canada). pupated. Results were similar in 1989, with all G. prognatha pupated by 11 August (Table 1). These data RESULTS AND DISCUSSION are consistent with the field studies from 1994 and 1995 (Figs. 1 and 2) showing that C. phaloniae emerges Parasitoid development in banded sunflower moth and is active in the fields earlier than G. prognatha. larvae. In 1987 and 1988, mortality of overwintering C. phaloniae was present in the field by mid-July in banded sunflower moth larvae, from disease or un- 1989, shortly after host eggs were initially detected in known causes, varied from 4 to 44% among sampling the field, and by 17 July, 28.6% of the eggs sampled 116 LAURENCE D. CHARLET

TABLE 1 Development of Overwintering Larvae of Two Generations of C. hospes and Its Internal Parasitoids, 1987–1989

Parasitoids in each developmental stage

Chelonus phaloniae Glypta prognatha C. hospes pupated 1st 2nd 3rd Pupated 1st 2nd 3rd Pupated Sampling Season date No. % No. % No. % No. % No. % No. % No. % No. % No. %

1987–1988 30 Sept– — 0 18 100 — — — — — — — 0 14 100 — — — — 23 June 28 June — 0 7 53.8 6 46.2 — — — — — 0 3 100 — — — — 5 July — 0 6 50.0 6 50.0 — — — — — 0 3 100 — — — — 13 July 1 4.5 — 0 7 50.0 6 42.8 1 7.1 — 0 3 75.0 1 25.0 — — 20 July 2 8.3 — 0 5 27.8 10 55.6 3 16.7 — — — — — — — — 27 July 8 38.1 — 0 2 10.0 2 10.0 16 80.0 — 0 — 0 — 0 2 100 3 Aug 14 93.1 — 0 — 0 — 0 18 100 — — — — — — — — 10Aug20100———————————————— 1988–1989 28 Sept– — 0 45 100 — — — — — — — 0 36 100 — — — — 5 July 14 July 4 22.2 4 36.4 6 54.5 — 0 1 9.1 — 0 4 50.0 4 50.0 — 0 19 July 12 57.1 1 9.1 3 27.3 2 18.2 5 45.4 — — — — — — — — 28 July 15 71.4 — 0 — 0 — 0 8 100 — 0 1 50.0 1 50.0 — 0 2 Aug 16 66.7 — — — — — — — — — — 1 100 — — — — 11 Aug 16 100 — — — — — — — — — — — 0 — 0 5 100

were parasitized, confirming earlier records in the lit- were consistent over time even though moth densities erature (Westdal, 1975) that C. phaloniae is an egg- were extremely low; peak density only reached Ϸ6 eggs larval parasitoid (Table 2). C. phaloniae continued to per head. C. hospes larval density also was low, with a attack C. hospes eggs the entire 2-week oviposition peak of just 13.3 larvae per plant. Although parasiti- period and was the primary parasitoid species de- zation rates varied among sampling times and moth tected. This was different than in later years (see Table instars, by the final sampling date, 23.8% of larvae 3) when G. prognatha supplanted it. A total of 93.1% of were parasitized (Table 2). Westdal and Barrett (1955) the 87 parasitoids dissected from mid-July to late Au- and Westdal (1975) also felt that parasitism was im- gust 1989 were C. phaloniae. The remainder were G. portant and in most years maintained banded sun- prognatha, which were initially detected in first instars flower moth below economic levels. collected 27 July. C. phaloniae was effective in locating Parasitoid species. In 1994, 256 parasitoids were and parasitizing C. hospes, since parasitization rates recovered from 1074 banded sunflower moth larvae

FIG. 1. Seasonal abundance of adult C. phaloniae and G. prog- FIG. 2. Seasonal abundance of adult C. phaloniae and G. prog- natha, parasitoids of the banded sunflower moth, occurrence of the natha, parasitoids of the banded sunflower moth, occurrence of the egg and larvae of C. hospes, and sunflower (H. annuus) developmen- egg and larvae of C. hospes, and sunflower (H. annuus) developmen- tal stages at Prosper, North Dakota, 1994. tal stages at Prosper, North Dakota, 1995. BANDED SUNFLOWER MOTH PARASITOIDS 117

TABLE 2 Number of C. hospes Eggs and Larvae Dissected and Percentage Parasitization of Banded Sunflower Moth Stages by Two Species of Internal Parasitoids, Chelonus phaloniae and Glypta prognatha, 1989

C. hospes stage

Egg 1st 2nd 3rd 4th 5th Total Sampling date No. % No. % No. % No. % No. % No. % No. %

13 July 1 0 — — — — — — — — — — 1 0 17 July 21 28.6 — — — — — — — — — — 21 28.6 20 July 45 24.4 2 50.0 — — — — — — — — 47 25.5 24 July 29 31.0 4 75.0 — — — — — — — — 33 36.4 27 July 4 0 15 33.3 8 12.5 — — — — — — 27 22.2 31 July 21 19.0 3 0 8 25.0 2 0 — — — — 34 17.6 3 Aug — — — — 3 33.3 17 47.1 13 61.5 — — 33 51.5 7 Aug — — — — — — 6 16.7 36 36.1 3 33.3 45 33.3 21 Aug — — — — — — — — — — 45 17.8 45 17.8 29 Aug — — — — — — — — — — 21 23.8 21 23.8

Note. 87 parasitoids detected (93.1%, C. phaloniae; 6.9%, G. prognatha); first G. prognatha recovered in 1st instar 27 July.

(parasitization rate ϭ 23.6%) reared from heads col- sites, with means of 11.9 and 11.3%, respectively. Each lected at eight locations throughout North Dakota (Ta- species also occurred in 75% of the sites sampled. ble 3). The most common parasitoid, of the four hyme- Sampling in 1995 occurred in three states, but nopteran species recovered, was G. prognatha, a soli- yielded just one additional species, Macrocentrus an- tary larval endoparasitoid, representing 68% of the cylivorus, representing only 2 of the 605 parasitoids parasitoids reared. It appears to be specific to Cochylis reared (Table 3). The most abundant parasitoid (ap- sp. and is only known from specimens collected in proximately 79% of species reared) from all three Colorado, Wyoming, North Dakota, Minnesota, and states was G. prognatha, occurring in 24 of the 27 Manitoba and Saskatchewan, Canada (Dasch, 1988; collection sites. The average parasitism rate by G. Sharkey et al., 1987; Charlet, 1988; Bergmann and prognatha among the three states was 13.8%, with the Oseto, 1990). A total of 29% of the parasitoids emerging highest in South Dakota and lowest in Minnesota (Ta- were C. phaloniae, an egg-larval parasitoid. C. pha- ble 3). C. phaloniae was the second most common para- loniae also is specific to the Cochylis and was sitoid (approximately 20% of parasitoids reared), but originally described by Mason (1959) from specimens was not as prevalent as in 1994 as shown by collections reared from C. hospes in Manitoba. About 2% of the in North Dakota (11.3% parasitization in 1994; 3.1% in specimens recovered were Perilampus robertsoni 1995). Overall, C. phaloniae parasitized 2.8% of larvae Crawford (Pteromalidae), a hyperparasitoid that prob- among all the sites in the three states sampled, but ably attacks either C. phaloniae or G. prognatha. Only was recovered from larvae in 74% of the collection one individual of Trathala sp. was recovered from the sites. Two individuals each of M. ancylivorus and larvae collected in 1994. Both G. prognatha and C. Trathala sp. were collected in North Dakota, the phaloniae showed similar parasitism rates among former from just one site and the latter from two sites.

TABLE 3 Parasitoid Species Recovered and Rates of Parasitization from C. hospes Larvae Collected on Cultivated Sunflower (H. annuus) in North and South Dakota and Minnesota, 1994, 1995

% Sites No. Mean % Ϯ SE banded sunflower moth larvae parasitized by No. with C. hospes collection parasitized larvae Glypta Chelonus Perilampus Trathala Macrocentrus Year State sites larvae reared prognatha phaloniae robertsoni sp. ancylivorus Total

1994 ND 8 87.5 1074 11.9 Ϯ 3.0 11.3 Ϯ 5.8 0.3 Ϯ 0.2 0.1 Ϯ 0.1 0 23.6 Ϯ 4.9 1995 ND 19 94.7 3171 12.7 Ϯ 1.5 3.1 Ϯ 0.5 0.11 Ϯ 0.07 0.05 Ϯ 0.04 0.02 Ϯ 0.02 16.1 Ϯ 1.6 SD 5 60.0 47 22.7 Ϯ 0.5 0.7 Ϯ 0.7 0 0 0 23.3 Ϯ 0.9 MN 3 100 206 5.9 Ϯ 1.6 4.3 Ϯ 2.1 0 0 0 10.1 Ϯ 3.3 Mean 84.9 13.8 Ϯ 2.3 2.8 Ϯ 0.5 0.08 Ϯ 0.05 0.04 Ϯ 0.03 0.01 Ϯ 0.1 16.8 Ϯ 2.3 118 LAURENCE D. CHARLET

TABLE 4 Parasitoid Species and Parasitization Rates from C. hospes Larvae Recovered from 5 Species of Native and Cultivated Sunflowers (Helianthus spp.) in North Dakota, 1994, 1995

Parasitoid species and parasitization rates

No. C. hospes Glypta Chelonus Perilampus Mastrus Year Sunflower species No. sites larvae reared prognatha phaloniae robertsoni sp. Total

1994 H. annuus 1 354 15.3% 3.4% 0.6% 0 19.2% Cultivated sunflower 1 1417 20.3% 6.7% 0.6% 0 27.7% 1995 H. annuus 2 66 9.1% 0 3.0% 1.5% 13.6% H. nuttallii 51900000 H. maximiliani 41900000 H. tuberosus 2 17 0 0 0 11.8% 11.8% H. petiolaris 11500000

The hyperparasitoid P. robertsoni also was recovered loniae adults were first noted about a week later (Fig. only in North Dakota. Compared with 1994, total par- 1). Eggs could be found on heads through mid-August asitism in 1995 was lower (23.6 to 16.8%), but this may and C. phaloniae, an egg-larval parasitoid, was present be due to an increase in both the number and range of through early August with peak populations in mid- sites sampled in 1995. However, the incidence of par- July. Banded sunflower moth egg densities were great- asitism was similar between years, with parasitized est on 27 July with 37 eggs per head. Larvae of C. larvae occurring in 84.9% of fields sampled in 1995, hospes were present on sunflower heads beginning 18 and 87.5% in 1994. B. arthurellus, a species reported July. G. prognatha adults were first recorded on the by Sharkey et al. (1987) to be common in Canada, was heads 20 July just prior to the bloom stage (R4) and not recovered in either year. I previously reared two reached peak numbers in the field in early August specimens of B. mellitor (Charlet, 1988), but this spe- coinciding with maximum numbers of banded sun- cies was not recovered in either 1994 or 1995. B. mel- flower moth larvae occurring in mid-August at 36 lar- litor also was noted to be rare in the Canadian collec- vae per head. Early instars of C. hospes feed on the tions (Sharkey et al., 1987). However, Sharkey et al. bracts or closer to the surface of the sunflower head on (1987) did not mention recovery of Trathala sp., which the disk flowers and are more readily available to the I collected in both 1994 and 1995. In addition, I did not ovipositing female, whereas later instars move down to collect any specimens of C. shoshoneanorum, a species the base of the disk flowers and into the developing noted by Macnak (1955) to be an important parasitoid seeds to feed. G. prognatha was present for about 4 of C. hospes in Manitoba. weeks and densities were about three times greater The banded sunflower moth has a much reduced than C. phaloniae. parasitoid complex compared to the sunflower moth, C. phaloniae adults were detected in 1995 about 10 Homoeosoma electellum (Hulst), which causes exten- days later than in 1994, but again coincided with bud sive damage to cultivated sunflower, especially in the stage (R3) of the sunflower plants in the field and the central and southern Plains (Rogers, 1992; Charlet et presence of banded sunflower moth eggs on the heads al., 1997). The sunflower moth has been reported to be (Fig. 2). Although counts of C. hospes eggs and larvae attacked by about 36 species of hymenopteran and were not made at regular intervals during 1995, sev- dipteran larval parasitoids, approximately four times eral samples taken during the season revealed lower the number reported for the banded sunflower moth densities than in 1994. Populations of C. phaloniae (Charlet, 1999). The differences are probably due to a were lower in 1995 than 1994 and peak numbers oc- number of factors including a much wider host range curred during the first week of August. G. prognatha for the sunflower moth, many generalist parasitoids of adults were first found on the heads probing for larvae the sunflower moth, and the occurrence of multiple in early August at the beginning of flowering and num- generations of the sunflower moth over part of its bers peaked in mid-August at about one adult per 10 range (Charlet, 1999). The only parasitoid species that plants. Densities of G. prognatha also were lower in the two moth species are reported to share in common 1995 than in 1994 and adults were only present for are B. mellitor and M. ancylivorus, generalist parasi- about 3 weeks. toids with wide host ranges (Krombein et al., 1979; Parasitoids in native and cultivated sunflowers. Sharkey et al., 1987; Charlet, 1999). Collections in 1994 from both native and cultivated Seasonal abundance. In 1994, eggs of banded sun- sunflower heads yielded the same species of parasi- flower moth were present on the bracts of bud stage toids, with G. prognatha being the predominate species (R3) sunflower heads beginning 11 July, and C. pha- (Table 4). C. phaloniae was the second most common BANDED SUNFLOWER MOTH PARASITOIDS 119

TABLE 5 Number of Banded Sunflower Moth Larvae per Head, Larval Parasitization Rate, and Percentage Composition of Parasitoids Reared from C. hospes for Three Different Planting Dates at Prosper, North Dakota, in 1994 and 1995

Total parasitizationa Parasitoid composition (%) Mean no. C. hospes Year Planting date larvae per head (ϮSE) No. % G. prognatha C. phaloniae

1994 11 May 29.6 Ϯ 2.5a 212 26.1 Ϯ 3.0a 70.9 29.1 12 (48.0) (83.3) (16.7) 23 May 15.1 Ϯ 2.3b 99 34.4 Ϯ 5.2a 83.3 16.7 15 (65.2) (73.3) (33.3) 3 June 19.0 Ϯ 2.8b 81 27.5 Ϯ 3.1a 76.5 23.5 32 (76.2) (71.9) (28.1) 1995 23 May 12.2 Ϯ 1.0a 37 14.3 Ϯ 2.2a 50.0 50.0 25 (52.1) (76.0) (24.0) 2 June 31.1 Ϯ 3.2c 154 26.6 Ϯ 2.5b 72.7 27.3 29 (58.0) (86.2) (13.8) 12 June 22.7 Ϯ 3.2b 121 27.3 Ϯ 2.9b 82.5 17.5 33 (75.0) (84.8) (15.2)

Note. Numbers in parentheses represent C. hospes larval parasitization rate and composition of parasitoids based on dissection of C. hospes larvae. Means followed by the same letter within the same column are not significantly different (P Ͻ 0.05) using LSD. Percentages transformed using arc sine. a Data analyzed using arc sine transformation. species representing about 18% of the parasitoids flower, C. phaloniae was not reared from larvae ob- reared from moth larvae in native H. annuus and 24% tained from the five Helianthus species sampled. The in cultivated sunflower. Total parasitism was some- absence of C. phaloniae was probably due to low sam- what greater in cultivated sunflower. Benrey et al. ple size, because in 1990, C. hospes larvae collected (1998) also noted an increased parasitoid attraction to from H. maximiliani heads at three locations in east- and survival in herbivore hosts that fed on domesti- ern North Dakota yielded both G. prognatha and C. cated plants compared to wild relatives. phaloniae (L. D. Charlet, unpublished data). Neither In 1995, the parasitoid fauna recovered from five M. ancylivorus nor Trathala sp. was recovered, but species of native sunflowers, although low in number, these species also were rare in the 1994 and 1995 did produce an additional species, Mastrus sp. (Hyme- collections from banded sunflower moth in cultivated noptera: Ichneumonidae). Mastrus sp. was not present fields (Table 3). Although collections were small, the in the 1994 collection and also was not previously re- presence of C. hospes in native sunflowers provides a covered from the cultivated sunflower heads sampled reservoir for parasitoids that also attack the moth in in 1994 in North Dakota, nor from the three states cultivated fields. sampled in 1995 (Tables 3 and 4). This species was not Impact of planting date. In 1994 the density of among the Hymenoptera described by Sharkey et al. moth larvae occurring in the heads from the first plant- (1987) from heads of wild and cultivated sunflowers, but has been previously reported attacking C. hospes ing date was almost twice that found in the other two larvae in North Dakota (Charlet, 1988). Three individ- planting dates (Table 5). This was primarily due to the uals were reared from banded sunflower moth larvae discrete differences in the growth stages present when collected from heads of H. annuus (1) and H. tuberosus moth oviposition began on 11 July. The first planting (2). date had heads at a stage acceptable for egg laying, Parasitoids were recovered from only two of the five whereas the other two planting dates were still in the Helianthus species sampled. However, this is probably vegetative stage and not suitable for oviposition. How- because of the small number of moth larvae obtained ever, there was no significant difference in parasitism and because of poor larval survival during rearing. among the three planting dates (Table 5). Plant phenology and low plant density of native sun- Planting dates were shifted later in 1995 because of flowers affect C. hospes infestation (Charlet et al., wet soil conditions. Oviposition also began later (28 1992). The variability in flowering periods in the native July) and although sunflower growth stages were sim- species, which influences both moth oviposition and ilar among all three dates, head stage probably re- subsequent larval infestation, affects the availability of sulted in the significant differences in larval numbers hosts for parasitoid attack. Over 50% of the parasitoids among dates. The second planting (2 June) had heads reared were G. prognatha, but it was only recovered at the most vulnerable stage at the time of oviposition, from H. annuus. Although common in cultivated sun- which may account for the higher density of larvae that 120 LAURENCE D. CHARLET occurred (Table 5). Rates of parasitism were equal in densities. Although results from rearing of C. hospes the second and third planting dates; almost twice that showed levels of parasitism in the range of 25% or less, of the first date of planting. Studies of the seasonal dissections revealed much higher rates. Thus, the abundance of the parasitoids noted earlier (Figs. 1 and parasitoids undoubtedly play an important role in the 2) showed that both parasitoid species occurred later in natural control of the moth and conservation of these 1995 than 1994, which probably accounted for the dif- natural enemies should be one of the objectives in the ferences in parasitism. development of sustainable pest management pro- Parasitoid species composition was similar in 1994 grams. The ability of these natural enemies to fit into and 1995. Except for the first planting date in 1995, G. management strategies, like the altering of planting prognatha was much more abundant than C. pha- date, emphasizes that successful integration of IPM loniae, accounting for about 75% of parasitoids recov- practices to include biological control is feasible. Be- ered (Table 5). Dissection data were consistent with cause C. hospes is still a cause of economic loss in some data from rearings in showing parasitoid composition. years, research is needed to identify new parasitoid However, total percentage parasitism based on rearing species, or to develop methods to protect and augment compared with dissection of mature larvae clearly those currently present. showed that rearing underestimates the actual inci- dence of parasitism, in many cases by at least 50% ACKNOWLEDGMENTS (Table 5). The reason is partially due to the difficulty in successfully breaking diapause and rearing insects to the adult stage (Charlet, 1999). Also, as Day (1994) I thank Theresa Gross (USDA-ARS, Fargo, ND) for assistance in laboratory rearing and field collection of the insects used in this noted, rearing provides a lower estimate of parasitism investigation. 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