Reproduction and Development ofOrius insidiosusin a Blue Light-Supplemented Short Photoperiod

9, 59–65 (1997) BC970520

BIOLOGICAL CONTROL ARTICLE NO.

Reproduction and Development of Orius insidiosus in a Blue Light-Supplemented Short Photoperiod1 Philip A. Stack* and Francis A. Drummond† *Maine Agricultural and Forest Experiment Station, 5762 Roger Clapp Greenhouses, Orono, Maine 04469-5762; and †Department of Biological Sciences, 5722 Deering Hall, University of Maine, Orono, Maine 04469-5722 E-mail: [email protected] Received August 21, 1996; accepted February 18, 1997

INTRODUCTION An important limitation in using the insidious flower bug, Orius insidiosus (Say) (Hemiptera: Anthocoridae), as a biological control agent in north temperate winter greenhouse crop production is its tendency to enter reproductive diapause during short photoperiods. Laboratory experiments assessed the effect of a blue light-supplemented short photoperiod over a range of temperature regimes on female reproductive diapause induction, nymph development and survival, ovarian maturation period, and oviposition of O. insidiosus. In experiment one, all O. insidiosus life stages were exposed to a broad-spectrum photoperiod of 15:9 (L:D) h, a blue light-supplemented photoperiod of 9:15 (L:D) h, consisting of 9 h broad-spectrum light followed by 6 h blue light, or a broad-spectrum photoperiod of 9:15 (L:D) h, all at 24 6 1°C. Approximately 75% of mated females reproduced in the broad-spectrum long photoperiod and the blue light-supplemented short photoperiod regimes, whereas over 50% of the bugs diapaused in the broad-spectrum short photoperiod regime. There was no difference among the light treatments for all other measured responses. In experiment two, all O. insidiosus life stages were exposed to the blue lightsupplemented short photoperiod over a range of temperature regimes (19–28°C). At least 90% of mated females reproduced at each temperature. A linear relationship occurred for temperature and nymph development and for temperature and ovarian maturation period. The oviposition rate was similar at 22°, 25°, and 28°C. This study indicates the potential for using supplemental blue light to enhance O. insidiosus reproduction in a short photoperiod and may be important as a biological control strategy in winter greenhouse production systems. r 1997 Academic Press KEY WORDS: Orius insidiosus; Frankliniella occidentalis; Dendranthema grandiflora; reproductive diapause; photoperiod; blue light.

The insidious flower bug, Orius insidiosus Say (Hemiptera: Anthocoridae), preys on small arthropods on flowering plants in North America (Herring, 1966). It feeds on a variety of pest species, including thrips, whiteflies, aphids, lace bug nymphs, eggs and young larvae of Lepidoptera, and spider mites and mite eggs, as well as plant sap and pollen (Barber, 1936; Kiman and Yeargan, 1985). O. insidiosus is reared and distributed commercially in North America and Europe as a biological control agent of western flower thrips, Frankliniella occidentalis Pergande (Thysanoptera: Thripidae), in greenhouse production systems (van den Meiracker and Sabelis, 1993; Hunter, 1994). F. occidentalis causes serious plant damage and economic loss by polyphagy and by vectoring tospoviruses (Robb and Parrella, 1995). O. insidiosus is primarily used to control thrips in greenhouse vegetable production (van den Meiracker and Ramakers, 1991). Limited control has been achieved on greenhouse ornamentals. Fransen et al. (1993) reported successful suppression of F. occidentalis by O. insidiosus on chrysanthemum, Dendranthema grandiflora (Ramat.) Kitamura, and African violet, Saintpaulia ionantha Wendland. A significant constraint in O. insidiosus’ success as a biological control agent of F. occidentalis on chrysanthemum is the contrasting photoperiodic sensitivities of O. insidiosus and chrysanthemum. O. insidiosus undergoes a facultative reproductive diapause at a critical photoperiod between 11 and 13 h at 18–25°C, characterizing its long photoperiod response (Beck, 1980; Kingsley and Harrington, 1982; Ruberson et al., 1991; van den Meiracker, 1994). Chrysanthemum is a quantitative short photoperiod flowering plant. A photoperiod of less than approximately 13.5 h is required for flower initiation and optimum flower development (Post, 1948). F. occidentalis reportedly does not enter reproductive diapause in short photoperiod greenhouse conditions (van den Meiracker, 1994; P.A.S., unpublished data).

1 Mention of a proprietary product does not constitute a recommendation for use by the authors or indicate exclusion of other suitable products.

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1049-9644/97 $25.00 Copyright r 1997 by Academic Press All rights of reproduction in any form reserved.

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O. insidiosus AND SUPPLEMENTAL BLUE LIGHT

Arthropods and plants also exhibit different sensitivities to spectral light quality. Danks (1987) reviewed over 60 years of investigations on light intensity and quality as environmental cues for photoperiodic responses in arthropods, including diapause induction and development. Specific wavelengths at which the least photic energy is required for measurable diapause responses are predominantly in the blue and blue– green (400–500 nm) spectral regions. For flower initiation and development, plants respond maximally to red light (600–660 nm) and minimally to blue light (400– 480 nm) (Withrow and Withrow, 1940). During short photoperiods, an interruption of the dark period with red light induces flowering in long photoperiod plants and prevents flowering in short photoperiod plants. The intensity threshold affecting optimal wavelength response for both diapause in arthropods and flowering in plants can be very low (,1 µW · cm22 · s21) (Salisbury, 1963; Lees, 1981). Fluorescent and incandescent lamps are the conventional sources of artificial light used to enhance or alter biological processes in insects and plants (Cathey and Borthwick, 1970; Shields, 1989). Both sources emit broad-spectrum light. Supplemental broad-spectrum, low-energy light alters photoperiod for diapause prevention in insects and mites (Gilkeson and Hill, 1986). However, increasing photoperiod greater than a critical threshold with red-biased light conflicts with the short photoperiod requirement for flowering in chrysanthemum and seemingly eliminates the biological control enhancement option in greenhouse production. Stack (1995) manipulated light quality to promote chrysanthemum flowering in a blue light-supplemented short photoperiod. Plants were exposed to a broad-spectrum photoperiod of 15:9 (L:D) h, a photoperiod of 9:15 (L:D) h, consisting of 9 h broad-spectrum light supplemented by 6 h blue light, and a broadspectrum photoperiod of 9:15 (L:D) h. At an intensity ,3.5 µmol · m22 · s21, the blue light regime resulted in no adverse effect on flower initiation or development compared with the short photoperiod control. As expected, no flowering occurred in the long, red-biased photoperiod regime. Collectively, these reports on the biological interactions of O. insidiosus, F. occidentalis, and D. grandiflora indicate that O. insidiosus is reproductively inactive and, therefore, inefficient as a predator of reproductively active F. occidentalis during chrysanthemum flower production periods in north temperate greenhouses. However, differences in light quality that influence plant flowering and insect diapause suggest the possibility of manipulating this part of the photic environment to overcome the incompatibility of O. insidiosus as a predator of F. occidentalis in inoculative releases on flowering chrysanthemum plants.

The objective of the present study was to determine the effect of a blue light-supplemented short photoperiod at a range of temperature regimes on reproductive diapause induction, nymph development and survival, adult ovarian maturation period (preoviposition period), and oviposition of O. insidiosus. MATERIALS AND METHODS

Predator Acquisition and Rearing Insectary-reared O. insidiosus adults were obtained from a commercial distributor of biological control agents for both experiments. A random sample of individuals from each experimental batch was identified to confirm species. O. insidiosus voucher specimens are located at the University of Maine Insect Museum (Orono, Maine). For tests, adult predators were sexed and groups of 10 mated pairs were placed in 8 3 15 cm Tupperware plastic dishes with a 5 3 10 cm, 0.15-mm (150 3 150 µm) mesh screen attached to each dish cover for ventilation. Laboratory-reared Helicoverpa zea Boddie eggs and mixed plant pollen were provided as food. Two 5- to 6-cm sections of snap bean pods (Phaseolus vulgaris L.) were used as an oviposition substrate in each dish, along with a moistened cotton ball as a water source, and a section of corrugated filter paper to provide refugia and reduce cannibalism. Adults were held in a broad-spectrum photoperiod of 15:9 (L:D) h at 24 6 1°C. After 2 days, bean pod sections were removed and placed in separate dishes to monitor nymph eclosion. Randomly selected first-generation progeny were used as test insects in both experiments. Experiment One We investigated the effect of light quality and photoperiod on O. insidiosus nymph development and survival, adult female reproductive diapause induction, ovarian maturation period, and oviposition. Three first instar nymphs were placed in each of 90, 9 3 9 cm plastic dishes covered with a 5 3 5 cm, 0.15-mm mesh screen for ventilation. Prey provisioning was as previously described and fresh eggs were provided every 2 days. A moistened cotton ball, snap bean section, and corrugated filter paper were provided as needed. A set of 30 dishes was placed in each of three growth chambers and exposed to one of three light treatments. Treatments were replicated three times. Each light treatment was used in each of the three growth chambers over the experiment’s duration to protect against a growth chamber effect. Temperature was 24 6 1°C. Lamp irradiance (light intensity) was measured as total light energy in W · m22 and spectral photon flux (light quality) was determined from 300 to 850 nm in

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1-nm increments with a spectroradiometer (LI-1800, LI-COR, Inc., Lincoln, NE). In treatment one, a 9-W broad-spectrum fluorescent lamp (F9TT/27K Dulux S, Osram Corp., Montgomery, NY) powered with 120-V AC with an intensity of <0.96 W · m22 (Fig. 1A) provided a long photoperiod control of 15:9 (L:D) h. In treatment two, a 9-W broad-spectrum fluorescent lamp (F9TT/27K Dulux S, Osram Corp.) provided 9 h light. This was supplemented by 6 h light from a 9-W blue-biased fluorescent lamp (F9TT/Blue Dulux S, Osram Corp.) powered with 120-V AC with an intensity of <0.98 W · m22 (Fig. 1B). The lamps in sequence provided a blue light-supplemented short photoperiod of 9:15 (L:D) h. In treatment three, a fluorescent lamp with similar specifications as treatment one provided a short photoperiod control of 9:15 (L:D) h. O. insidiosus stadia were monitored every 1–2 days, depending on nymph stage. Development time from

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second instar to adult was recorded. Development and survival data for male and female bugs were combined in each light treatment. Instars were identified by exuviae and morphological traits described by Isenhour and Yeargan (1981). Eclosed adults were sexed and as many pairs as possible were mated within the same light treatment. Paired bugs were exposed to the light treatment in which they had developed and were provided prey and other provisions as previously described. Bean pods were replaced every 2 days. Ovarian maturation period was recorded for each fecund female. Beans containing eggs were transferred to separate 9 3 9 cm plastic dishes and monitored for nymph eclosion. Males were kept with females at least until oviposition occurred. Oviposition period was monitored for 21 days from the day each female deposited her first egg. Bugs which failed to oviposit 18 days after mating were considered to be in reproductive diapause. This period of time represents four to five times the ovarian maturation period of a normally nondiapausing female (Ruberson et al., 1991; Bush et al., 1993). A random sample of diapausing females in each treatment was dissected to determine ovary maturation. Absence of oocyte development verified reproductive diapause. Experiment Two We investigated the effect of a range of constant temperature regimes in a supplemental blue light photoperiod on O. insidiosus nymph development and survival, adult female reproductive diapause induction, ovarian maturation period, and oviposition. Twenty dishes, each containing four first instar nymphs, were placed in each of four growth chambers and provided the same blue light-supplemented short photoperiod of 9:15 (L:D) h as treatment two in experiment one. Light intensity was <0.97 W · m22. Four temperature regimes were tested: 19 6 1°; 22 6 1°; 25 6 1°; and 28 6 1°C. Cage provisioning and prey and bean replenishment were as previously described. Protocol for determining nymph development and survival, adult female reproductive diapause induction, ovarian maturation period, and oviposition were as described in experiment one. Statistical Analysis

FIG. 1. (A) Action spectral distribution curve for the 9-W broadspectrum fluorescent lamp used in experiments one and two and (B) action spectral distribution curve for the 9-W blue-biased fluorescent lamp used in experiments one and two.

O. insidiosus nymph development and percentage survival, the percentage of diapausing females, adult ovarian maturation period, and oviposition were compared among treatments in experiments one and two with univariate analysis of variance for each measured response using the software SuperANOVA (Abacus Concepts, 1989). Means that differed by a significant F ratio (P # 0.05) were separated with the Student– Newman–Keuls (SNK) post hoc test (P # 0.05). Nymph

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O. insidiosus AND SUPPLEMENTAL BLUE LIGHT

development, ovarian maturation period, and oviposition (eggs · female21 · day21) were transformed to 1/days (rates) to achieve normality (Logan et al., 1985). Linear regression was used to determine the relationship between temperature and nymph development rate, ovarian maturation period, and oviposition rate in experiment two (Abacus Concepts, 1993). RESULTS AND DISCUSSION

Experiment One O. insidiosus exhibited a long photoperiodic reproductive diapause induction response at 24 6 1°C (Table 1). Approximately 76% of mated females oviposited in both the blue light-supplemented short photoperiod of 9:15 (L:D) h and the long broad-spectrum photoperiod of 15:9 (L:D) h. Photoperiod and light quality significantly affected diapause induction in these treatments compared with the short broad-spectrum photoperiod (F(2, 4) 5 106.17, P 5 0.0003). In each of the three light regimes, each randomly sampled ovipositing female (n 5 10) produced fertile eggs. Dissected diapausing females revealed underdeveloped ovaries and reduced or absent oocyte development. O. insidiosus’ physiological long photoperiod response has been reported in other studies investigating induction or maintenance of photoperiodic reproductive diapause using broad spectrum light exposures. Kingsley and Harrington (1982) reported the termination of diapause in 100% of O. insidiosus females in a photoperiod of 16:8 (L:D) h and diapause maintenance in 80% of females in a photoperiod of 12:12 (L:D) h. Ruberson et al. (1991) found that 87% of O. insidiosus females oviposited in a photoperiod of 15:9 (L:D) h at 20°C, whereas nearly 100% of mated females entered diapause in a photoperiod of 10:14 (L:D) h. The critical photoperiod for diapause induction was between 12 and 13 h. Van den Meiracker (1994) reported that more than 90% of O. insidiosus females diapaused in photope-

riods shorter than 11 h at 18°C. However, 25–42% of the females entered reproductive diapause at photoperiods above 11–12 h. Our experimental results support the hypothesis that extending photoperiod with blue light can avert diapause induction in O. insidiosus. Blue light was as effective as broad-spectrum light; the latter typically being associated with artificially modifying reproductive diapause in arthropods (Gilkeson and Hill, 1986; Danks, 1987). However, we found a less intense photoperiodic response than other studies at similar temperature. Nearly 50% of adult females in our experiment did not enter reproductive diapause in the short photoperiod control, whereas nearly 25% of the females entered diapause in the broad-spectrum long photoperiod and blue-supplemented short photoperiod. This anomaly may be an experimental artifact. It could also be a normal response in a genetically variable population of insects or possibly an inbred trait of the laboratoryreared bugs used in our study. Genetic variation and adaptation can be major considerations when evaluating responses in laboratory studies of diapause (Mackauer, 1976; Tauber et al., 1986). On the other hand, the selection of nondiapausing individuals under environmental conditions normally favoring diapause presents a potential solution in averting short photoperiod effects in a biological control strategy (Honeˆk, 1972). Temperature may have modified diapause intensity in our short photoperiod treatment (Tauber et al., 1986). This has been reported in other species of Hemiptera (Dingle, 1974; Fielding, 1988). In O. insidiosus, Kingsley and Harrington (1982) found that at 25°C, without an accompanying long photoperiod, diapause was averted in 20% of the insects tested. Van den Meiracker (1994) observed that when diapause conditions were altered by raising the temperature to 30°C, diapause is terminated in most O. insidiosus within 2 weeks; however, he reported no diapause termination at 25°C. Temperature effects in a blue light-supple-

TABLE 1 Reproductive and Developmental Responses of O. insidiosus to Light Quality and Photoperiod (24 6 1°C)a Mean Light quality and photoperiodb

Diapause induction (%) c

Ovarian maturation period (days) c

Oviposition (eggs · female21 · day21) c

Survival (%) d,c

Development dayse, f

Broad-spectrum 15L:9D Blue-spectrum 9L:15D Broad-spectrum 9L:15D

24.5 6 6.6a 22.9 6 8.6a 52.6 6 9.1b

4.7 6 0.3a 4.9 6 0.6a 4.8 6 0.3a

9.0 6 0.9a 11.6 6 2.0a 8.5 6 2.0a

60.1 6 7.4 a 67.8 6 11.4a 53.7 6 8.7 a

10.4 6 0.5a 10.3 6 0.2a 10.5 6 0.5a

a

Mean 6 SEM; means within columns followed by the same letter are not significantly different (P . 0.05). Blue light-supplemented short photoperiod of 9 h broad-spectrum light and 6 h blue-biased light. c Broad-spectrum 15L:9D, n 5 41; blue-spectrum 9L:15D, n 5 51; broad-spectrum 9L:15D, n 5 32. d n 5 90 for each treatment. e Data for males and females were pooled. f Broad-spectrum 15L:9D, n 5 54; blue-spectrum 9L:15D, n 5 61; broad-spectrum 9L:15D, n 5 48. b

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mented short photoperiod regime were tested in experiment two. Ruberson et al. (1991) found a significant effect of photoperiod on the ovarian maturation period (preoviposition period) of O. insidiosus at 20°C. At a photoperiod of 12:12 (L:D) h, ovipositing females had an average ovarian maturation period of 13.2 days. At a photoperiod of 15:9 (L:D) h, the average ovarian maturation period was 6 days. Van den Meiracker (1994) reported no differences in the ovarian maturation period at a photoperiod varying from 8:16 (L:D) h to 16:8 (L:D) h at either 18° or 25°C. We found no differences in the ovarian maturation period of O. insidiosus in any of the light treatments (Table 1). The mean ovarian maturation period was slightly less than 5 days. A similar response (3.8–4.7 days) was reported by Bush et al. (1993) for O. insidiosus reared on different diets at a photoperiod of 15:9 (L:D) h and 25°C. In our study, the range of ovarian maturation periods was similar in the blue lightsupplemented short photoperiod (3–16 days) and the broad-spectrum short photoperiod (3–13 days), whereas the range in the broad-spectrum long photoperiod was 3–8 days. O. insidiosus females in the blue light regime deposited the most eggs per day (11.6) (Table 1); however, this was not significant at the 0.05 level (F(2, 4) 5 4.62, P 5 0.111). These data on average daily fecundity are 20–41% greater than the average daily fecundity reported by Bush et al. (1993) and three to four times greater than the average daily fecundity reported by Kiman and Yeargan (1985). One could attribute the differences to a maximum oviposition period of 21 days in our study resulting in a larger mean; however, Bush et al. (1993) noted that O. insidiosus produced eggs at a constant rate throughout their adult life. Experiment one results indicate that the blue light-supplemented

short photoperiod is as effective as the broad-spectrum long photoperiod in inducing and maintaining reproduction in O. insidiosus females. Nymph development rate from second instar to adult at 24 6 1°C did not differ significantly among treatments of spectral light quality or photoperiod (Table 1). Mean nymph development was similar to those reported by McCaffrey and Horsburgh (1986) in a photoperiod of 15:9 (L:D) h at 23°C and approximately 1.6 days shorter than those of Isenhour and Yeargan (1981) in a photoperiod of 16:8 (L:D) h at 25°C. This contrasts with Ruberson et al. (1991), who found that nymph development at 20°C is faster in a photoperiod of 10:14 (L:D) compared with longer photoperiods. Askari and Stern (1972) also reported shorter development times of O. tristicolor White at 25.5°C in a photoperiod of 12:12 (L:D) than in 16:8 (L:D). No difference was observed in O. insidiosus nymph survival among light treatments (Table 1). Experiment Two At least 90% of O. insidiosus females avoided reproductive diapause in the blue light-supplemented short photoperiod of 9:15 (L:D) h at each temperature tested (Table 2). No differences were observed among temperature regimes. Nearly 20% more females averted diapause at 25 6 1°C in experiment two than in the blue light regime at 24 6 1°C in experiment one. Experimental protocol was similar in both experiments and no clear reason is evident to explain this variation. Diapause induction data in experiment two correspond more closely with the results of two previously cited studies (Kingsley and Harrington, 1982; Ruberson et al., 1991). In each of the four temperature regimes, each randomly sampled ovipositing female (n 5 12) produced fertile eggs. Dissected diapausing females

TABLE 2 Reproductive and Developmental Responses of O. insidiosus to a Blue Light-Supplemented Short Photoperiod of 9:15 (L:D) h at Different Temperature Regimesa,b Mean

Temperature (°C)

Diapause induction (%) c

Ovarian maturation period (days) c

Oviposition (eggs · female21 · day21) c

Survival (%) d

Development (days)e, f

19 6 1 22 6 1 25 6 1 28 6 1

9.2 6 3.6a 9.4 6 2.1a 6.4 6 1.9a 10.1 6 2.8a

6.6 6 0.2a 5.1 6 0.2b 3.9 6 0.3 c 2.4 6 0.2d

3.4 6 0.9a 7.5 6 1.6b 7.0 6 0.8b 8.3 6 1.7b

48.8 6 7.1a 62.5 6 9.4a 51.3 6 7.6a 52.5 6 6.9a

19.7 6 0.2a 13.0 6 0.4b 10.1 6 0.7 c 6.7 6 0.5d

a

Blue light-supplemented short photoperiod of 9 h broad-spectrum light and 6 h blue-biased light. Mean 6 SEM; means within columns followed by the same letter are not significantly different (P . 0.05). c 19 6 1°C, n 5 21; 22 6 1°C, n 5 23; 25 6 1°C, n 5 20; 28 6 1°C, n 5 24. d n 5 80 for each treatment. e Data for males and females were pooled. f 19°C, n 5 39; 22°C, n 5 50; 25°C, n 5 41; 28°C, n 5 42. b

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revealed underdeveloped ovaries and reduced or absent oocyte development. Nymph development rate (r2 5 0.96) and ovarian maturation rate (r2 5 0.91) were linearly correlated with temperature (Figs. 2A and 2B; Table 2). Mean nymph development time and ovarian maturation period were shortest at 28°C. Oviposition was also correlated with temperature (r2 5 0.97), with the highest oviposition rates occurring at 22–28°C (Fig. 2C). It is noteworthy that there was no difference in oviposition

at 22°C. Since greenhouse chrysanthemum grows optimally at a temperature around 22°C (Crater, 1992), this is an important consideration in an eventual crop management strategy using O. insidiosus as a biological control agent (Stack, 1995). In addition, conservation of winter fuel is an important economic consideration for north temperate greenhouse growers. However, nymph development was lengthened by approximately 3 days and ovarian maturation period was increased by more than a day at 22° than at 25°C. No difference was observed in O. insidiosus nymph survival among the light treatments (Table 2). Prospects for Biological Control

FIG. 2. Regression of means for O. insidiosus: (A) nymph development rate; (B) adult ovarian maturation rate; and (C) oviposition rate, all plotted against four temperature regimes in a blue lightsupplemented short photoperiod of 9:15 (L:D) h.

Several methods have been proposed to circumvent seasonal limits and maintain an active reproductive state in long photoperiod insects exposed to short photoperiods. These include: increasing photoperiod with broad-spectrum artificial light (Gilkeson and Hill, 1986); selecting natural enemies with temperaturemediated diapause aversion (Morewood and Gilkeson, 1991); identifying strains, clinal variants, or geographic races of natural enemies having a shorter than normal critical photoperiod for diapause induction (Taylor and Spalding, 1986); and selecting nondiapausing individuals from feral or laboratory populations (van Houten and van Stratum, 1993). The results of our study indicate that extending photoperiod with supplemental blue light averts reproductive diapause over a range of temperature regimes in the majority of O. insidiosus. Coupled with optimal flowering of short photoperiod plants, such as chrysanthemum, in a blue light-supplemented photoperiod (Stack, 1995), this strategy circumvents an important obstacle when releasing long photoperiod biological control agents in a yearround greenhouse biological control program and provides a solution to the previously reported incompatibility of short photoperiod plants and long photoperiod insects. At least three Orius spp. used worldwide to control F. occidentalis have long photoperiod diapause responses (O. insidiosus, O. tristicolor, and O. majusculus Reuter) (van den Meiracker, 1994). We used low-intensity lamps with a narrow bluebiased spectral energy distribution. The low irradiance allows optimal flowering in D. grandiflora. Maintaining a low light intensity is essential for chrysanthemum flowering but not necessarily for O. insidiosus reproduction. Higher irradiances can be used to prevent reproductive diapause in O. insidiosus if diapause prevention is the only concern. Another lamp that provides an approximately identical spectral energy distribution to that of the 9-W fluorescent blue lamp used in our study (Fig. 1B) is the Super Diazo Blue fluorescent lamp (F40T12/SDB/65, Osram Corp.). While this is designated for 65-W operation, it can operate at 40 W. The lamp provides a higher

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light intensity per unit area. Both blue light-biased fluorescent lamps are readily available, powered with 120 V AC, and can be easily incorporated into existing greenhouse lighting systems. ACKNOWLEDGMENTS We thank Elson Shields (Cornell University, Ithaca, NY) and Lois Berg Stack, John Tjepkema, Richard Storch, James Dill, and David Lambert (University of Maine) for critical reviews of a previous version of the manuscript. The Insect Biology and Population Management Research Laboratory, USDA-ARS (Tifton, GA) supplied H. zea eggs. Donald Krizek (USDA Climate Stress Laboratory, Beltsville, MD) and Robert Levin (Osram Sylvania, Inc., Salem, MA) advised us on lamp specifications. Theodore Tibbitts and Thomas Frank (University of Wisconsin-Madison) generously loaned us scientific equipment. This project was supported in part by The Fred C. Gloeckner Foundation (Harrison, New York) and New England Floriculture Inc. (Newfane, VT). This is Maine Agricultural and Forest Experiment Station Journal Article 2075.

REFERENCES Abacus Concepts. 1989. ‘‘SuperANOVA Accessible General Linear Modeling.’’ Abacus Concepts, Berkeley, CA. Abacus Concepts. 1993. ‘‘StatView, the Ultimate Data Analysis and presentation system.’’ Abacus Concepts, Berkeley, CA. Askari, A., and Stern, V. M. 1972. Biology and feeding habits of Orius tristicolor (Hemiptera: Anthocoridae). Ann. Entomol. Soc. Am. 65, 96–100. Barber, G. W. 1936. ‘‘Orius insidiosus (Say), an Important Natural Enemy of the Corn Earworm.’’ U.S. Dept. Agric. Tech. Bull. 504. Beck, S. D. 1980. ‘‘Insect Photoperiodism,’’ 2nd ed. Academic Press, New York. Bush, L., Kring, T. J., and Ruberson, J. R. 1993. Suitability of greenbugs, cotton aphids, and Heliothis virescens eggs for development and reproduction of Orius insidiosus. Entomol. Exp. Appl. 67, 217–222. Cathey, H. M., and Borthwick, H. A. 1970. Photoreactions controlling flowering of Chrysanthemum morifolium (Ramat. and Hemfl.) illuminated with fluorescent lamps. Plant Physiol. 45, 235–239. Crater, G. D. 1992. Potted chrysanthemums. In ‘‘Introduction to Floriculture’’ (R. A. Larson, Ed.), 2nd ed., pp. 249–287. Academic Press, San Diego. Danks, H. V. 1987. ‘‘Insect Dormancy: An Ecological Perspective.’’ Biological Survey of Canada, Ottawa. Dingle, H. 1974. Diapause in a migrant insect, the milkweed bug Oncopeltus fasciatus (Dallas) (Hemiptera: Lygaeidae). Oecologia 17, 1–10. Fielding, D. J. 1988. Photoperiodic induction of diapause in the squash bug, Anasa tristis. Entomol. Exp. Appl. 48, 187–193. Fransen, J. J., Boogaard, M., and Tolsma, J. 1993. The minute pirate bug, Orius insidiosus (Say) (Hemiptera: Anthocoridae), as a predator of western flower thrips, Frankliniella occidentalis (Pergande), in chrysanthemum, rose and Saintpaulia. Bull. IOBC/WPRS 16(2), 73–77. Gilkeson, L. A., and Hill, S. B. 1986. Diapause prevention in Aphidoletes aphidimyza (Diptera: Cecidomyiidae) by low-intensity light. Environ. Entomol. 15, 1067–1069. Herring, J. L. 1966. The genus Orius of the western hemisphere (Hemiptera: Anthocoridae). Ann. Entomol. Soc. Am. 59(6), 1093– 1109. Honeˆk, A. 1972. Selection for non-diapause in Aelia acuminata and A. rostrata (Heteroptera: Pentatomidae) under various selection pressures. Acta. Entomol. Bohemoslov. 69, 73–77.

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Hunter, C. D. 1994. ‘‘Suppliers of Beneficial Organisms in North America.’’ Calif. Environ. Protect. Agency, Sacramento, CA. Isenhour, D. J., and Yeargan, K. V. 1981. Effect of temperature on the development of Orius insidiosus, with notes on laboratory rearing. Ann. Entomol. Soc. Am. 74, 114–116. Kiman, Z. B., and Yeargan, K. V. 1985. Development and reproduction of the predator Orius insidiosus (Hemiptera: Anthocoridae) reared on diets of selected plant material and arthropod prey. Ann. Entomol. Soc. Am. 78, 464–467. Kingsley, P. C., and Harrington, B. J. 1982. Factors influencing termination of reproductive diapause in Orius insidiosus (Hemiptera: Anthocoridae). Environ. Entomol. 11, 461–462. Lees, A. D. 1981. Action spectra for the photoperiodic control of polymorphism in the aphid Megoura viciae. J. Insect Physiol. 27(11), 761–771. Logan, P. A., Casagrande, R. A., Faubert, H. H., and Drummond, F. A. 1985. Temperature dependent development and feeding of immature Colorado potato beetles, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). Environ. Entomol. 14, 275–283. Mackauer, M. 1976. Genetic problems in the production of biological control agents. Annu. Rev. Entomol. 21, 369–385. McCaffrey, J. P., and Horsburgh, R. L. 1986. Biology of Orius insidiosus (Heteroptera: Anthocoridae): A predator in Virginia apple orchards. Environ. Entomol. 15, 984–988. Morewood, W. D., and Gilkeson, L. A. 1991. Diapause induction in the thrips predator Amblyseius cucumeris (Acarina: Phytoseiidae) under greenhouse conditions. Entomophaga 361, 253–263. Post, K. 1948. Daylength and flower bud development in chrysanthemums. Proc. Am. Soc. Hort. Sci. 51, 590–592. Robb, K. L., and Parrella, M. P. 1995. IPM of western flower thrips. In ‘‘Thrips Biology and Management’’ (B. L. Parker, M. Skinner, and T. Lewis, Eds.), pp. 365–370. Plenum, New York. Ruberson, J. R., Bush, L., and Kring, T. J. 1991. Photoperiodic effect on diapause induction and development in the predator Orius insidiosus (Heteroptera: Anthocoridae). Environ. Entomol. 20(3), 786–789. Salisbury, F. B. 1963. ‘‘The Flowering Process.’’ Pergamon, New York. Shields, E. J. 1989. Artificial light: Experimental problems with insects. Bull. Entomol. Soc. Am. 35(2), 40–44. Stack, P. A. 1995. ‘‘Effect of Blue Light on Reproduction and Development in Orius insidiosus Say (Hemiptera: Anthocoridae) and on Flowering in Dendranthema grandiflora (Ramat.) Kitamura.’’ M.S. thesis, University of Maine, Orono, ME. Tauber, M. J., Tauber, C. A., and Masaki, S. 1986. ‘‘Seasonal Adaptations of Insects.’’ Oxford Univ. Press, New York. Taylor, F., and Spalding, J. B. 1986. Geographical patterns in the photoperiodic induction of hibernal diapause. In ‘‘The Evolution of Insect Life Cycles’’ (F. Taylor and R. Karban, Eds.), pp. 66–86. Springer-Verlag, New York. van den Meiracker, R. A. F. 1994. Induction and termination of diapause in Orius predatory bugs. Entomol. Exp. Appl. 73, 127– 137. van den Meiracker, R. A. F., and Ramakers, P. M. J. 1991. Biological control of the western flower thrips Frankliniella occidentalis, in sweet pepper, with the anthocorid predator Orius insidiosus. Med. Landbouww. Rijksuniv. Gent. 56, 241–249. van den Meiracker, R. A. F., and Sabelis, M. W. 1993. Oviposition sites of Orius insidiosus in sweet pepper. Bull. IOBC/WPRS 16(2). 109–112. van Houten, Y. M., and van Stratum, P. 1993. Biological control of western flower thrips in greenhouse sweet peppers using nondiapausing predatory mites. Bull. IOBC/WPRS 16(2), 77–80. Withrow, R. B., and Withrow, A. P. 1940. The effect of various wavebands of supplemental radiation on the photoperiodic response of certain plants. Plant Physiol. 25, 609–624.