FOREST ENTOMOLOGY
Susceptibility of Adult Hymenopteran Parasitoids of the Nantucket Pine Tip Moth (Lepidoptera: Tortricidae) to Broad-Spectrum and Biorational Insecticides in a Laboratory Study J. T. NOWAK,1 K. W. MCCRAVY, C. J. FETTIG,
AND
C. W. BERISFORD
Department of Entomology, University of Georgia, 413 Biological Sciences Building, Athens, GA 30602
J. Econ. Entomol. 94(5): 1122Ð1129 (2001)
ABSTRACT Currently, there is an elevated interest in reducing feeding damage caused by the Nantucket pine tip moth, Rhyacionia frustrana (Comstock), a common regeneration pest of loblolly pine, Pinus taeda L. The toxicity of several insecticides was tested in a laboratory against four common R. frustrana parasitoids. There were no differences in parasitoid mortality between the control and indoxacarb treatments. However, the pyrethroids, permethrin and lambda-cyhalothrin, caused signiÞcantly more mortality initially (up to 240 min exposure time) than other insecticides. Spinosad was less toxic than the pyrethroids initially, but the spinosad related mortality increased with time until it reached a level similar to the pyrethroids. For the most part, spinosad and the pyrethroids caused more mortality than the control and indoxacarb treatmtents within the 1-d sample period. These results may have important implications for decisions concerning which insecticides are best suited for reducing pest damage while conserving natural enemies in timber and agricultural systems. Large-scale Þeld trials are required to further deÞne the impacts of these insecticides on natural enemies. KEY WORDS Rhyacionia frustrana, parasitoids, indoxacarb, pyrethroids, spinosad, insecticide toxicology tests
THE NANTUCKET PINE tip moth, Rhyacionia frustrana (Comstock), is an important regeneration pest of loblolly pine, Pinus taeda L., plantations and its impact is likely to increase as forest management practices intensify (Sun et al. 1998). Insecticide control is expensive and not normally conducted except in high value plantings such as Christmas tree plantations and progeny tests (Berisford 1988, Fettig et al. 2000b). However, because damage from R. frustrana in intensively managed plantations has been shown recently to reduce volume yields (Fettig et al. 2000b, Nowak and Berisford 2000), there is increasing interest in using insecticides, which can be effective in reducing volume losses (Fettig et al. 2000b, Nowak and Berisford 2000). To reduce the impact of extensive use of insecticides on R. frustrana natural enemies, it is necessary to use insecticides that are efÞcacious and selective to the target insect. Although there have been several recent publications on the use of insecticides to control R. frustrana (Kudon et al. 1988; Fettig and Berisford 1999; Fettig et al. 2000a, 2000b; Nowak et al. 2000), less emphasis has been placed on their impact on natural enemies (McCravy et al. 2001). Several insecticides are currently registered for management of R. frustrana in conifer stands, including permethrin (Pounce), lambda-cyhalothrin (Warrior T), and spinosad (SpinTor 2 SC) (Fettig and Berisford 1999, 1 Current address: USDA Forest Service, 2500 Shreveport Highway, Pineville, LA 71360 (e-mail:
[email protected]).
Nowak et al. 2000). Permethrin, a third generation pyrethroid, is currently considered the industry standard for R. frustrana control (Fettig et al. 2000b). It has low mammalian toxicity (oral LD50 ⬎ 4,000 mg/kg), and is effective in reducing R. frustrana damage levels (Fettig et al. 2000b, Nowak and Berisford 2000, Nowak et al. 2000). Lambda-cyhalothrin, a fourth generation pyrethroid, was given a special local needs designation (Section 24-C) in 1999 by the Georgia Department of Agriculture. It has a higher mammalian toxicity (oral LD50 ⫽ 243 mg/kg) than permethrin and has also been shown to reduce R. frustrana damage, with a longer optimal spray timing window than permethrin and spinosad (Nowak et al. 2000). Although, pyrethroids are effective at low rates and are relatively inexpensive (Croft 1990), studies have shown that they are harmful to hymenopteran parasitoids and other beneÞcial insects (Theiling and Croft 1988, Croft 1990). Hymenopteran parasitoids are important enemies of many pest insect populations, including R. frustrana (Gargiullo and Berisford 1983). Repeated applications of broad-spectrum insecticides, such as pyrethroids, can cause secondary pest outbreaks (McClure 1977, Clarke et al. 1990) and contribute to rapid resurgence of primary pest insects because of the reduction or elimination of natural enemies (Johnson et al. 1982, Metcalf and Luckmann 1994). Spinosad is a relatively new insecticide available for R. frustrana control. It is derived from a soil actino-
0022-0493/01/1122Ð1129$02.00/0 䉷 2001 Entomological Society of America
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Table 1. Insecticide treatments used in a study on the susceptibility of Eurytoma pini, Haltichella rhyacioniae, Bracon sp., and Macrocentrus ancylivorus to broad-spectrum and biorational insecticides in a laboratory study Common name
Trade name and formulation
Manufacture, location
Application rate
Permethrin Lambda-cyhalothrin Spinosad Indoxacarb
Pounce 3.2 EC Warrior T SpinTor 2SC Steward SC
FMC, Philadelphia, PA Se´ ance, Wilmington, DE Dow AgroSciences, Indianapolis, IN Dupont, Wilmington, DE
0.17 kg(AI)/ha 0.05 kg(AI)/ha 0.098 kg(AI)/ha 0.1235kg(AI)/ha
mycete bacterium, Saccharopolyspora spinosa, and is a mixture of spinosyn A and spinosyn D (Saldago et al. 1997). It was Þrst labeled in 1997 for cotton, (Saldago et al. 1997) and has since received a supplemental label for use in tree farms or plantations. Spinosad has been shown to be effective against lepidopterous insects, including R. frustrana (Nowak et al. 2000) and has very low mammalian toxicity (oral LD50 ⬎ 5000 mg/kg). Nowak et al. (2000) showed that in the Georgia Piedmont it had similar efÞcacy and spray timing values as permethrin, but it is reported to be compatible with the conservation of beneÞcial insects (Hendrix et al. 1997). Other reports have concluded that it is toxic to important hymenopteran parasitoids, such as Trichogramma exiguum (Suh et al. 2000) and Cotesia spp. (Pietrantonio and Benedict 1999). Indoxacarb (Steward SC) is the Þrst available product in a new class of insecticides, oxadiazines (McCann et al. 2001). It may become available for use in cotton for control of lepidopteran and hemipteran pest species, and also has low mammalian toxicity (Seay et al. 1999). Ruberson and Tillman (1999) showed that it has low toxicity to some hymenopteran parasitoids, and preliminary tests indicate that it is effective in reducing R. frustrana feeding damage (unpublished data). Few studies have compared any combination of these four insecticides on their toxicity to hymenopteran parasitoids (Pietrantonio and Benedict 1999, Ruberson and Tillman 1999, Suh et al. 2000). The objective of this study was to evaluate the susceptibility of several common adult R. frustrana parasitoids to permethrin, lambda-cyhalothrin, spinosad, and indoxacarb. Materials and Methods Approximately 40,000 R. frustrana-infested loblolly pine shoots were collected between 25 April and 7 July 2000 from Þve 3- to 5-yr-old loblolly pine stands. Shoot collection sites were located in Halifax County, NC, and the Georgia counties of Bullock, Candler, Taylor, and Wilkes. Collections were timed to coincide with the presence of R. frustrana pupae in the shoots and before emergence of the larval-pupal parasitoids. Shoots were collected using hand clippers, placed in plastic bags, and returned to the laboratory on ice in a cooler. In the laboratory, pine shoots were spread evenly on chicken wire shelves (8 cm gauge), and were occasionally sorted by hand to improve air circulation. Shelves were placed in Þne mesh (0.35 mm) Lumite screen enclosures (Synthetic Industries, Gainesville,
GA), 1.8 m3 in size, as in McCravy and Berisford (1998). A ßuorescent light source was placed at one end of the cages to attract emerging parasitoids. Honey water (20% honey) was streaked on three index cards (10 by 15 cm) placed near the ceiling of the screen enclosures to provide a food source. Parasitoids were collected from the screen enclosures in 20-m1 glass scintillation vials, and randomly placed into test chambers, described below, just before adding the insecticide-treated pine shoots. Treatments were applied to loblolly pine shoots that had been clipped from trees (⬍10 yr old) growing near the laboratory with hand-pump backpack sprayers (Solo, Newport News, VA) at recommended Þeld rates (Table 1) until runoff. Shoots were left outside to dry for ⬇1 h before being placed in test chambers. Chambers were clear Plexiglas tubes 15 cm (diameter) by 45 cm (height) with Plexiglas bottoms and removable tops. Two holes (5 cm in diameter) were cut on the sides, and were covered with Þne mesh (0.30 mm) to provide ventilation (Fig. 1). One parasitoid species was tested in a test replicate on a given day. Because no species are commercially available except Trichogramma spp. and there are no continuous rearing procedures for R. frustrana parasitoids, it was necessary to rely on the individuals that emerged. Parasitoid species were included in the data analysis only if enough specimens were collected to run Þve replications. Four to eight insects were used per treatment per replicate depending on availability. Although many parasitoid species emerged from pine shoots, Eurytoma pini Bugbee (Eurytomidae), Haltichella rhyacioniae (Gahan) (Chalcididae), Bracon sp. (Braconidae), and Macrocentrus ancylivorus Rohwer (Braconidae) were the only species that were present in sufÞcient numbers to be included in the study. McCravy and Berisford (2000) found that these species accounted for ⬇40% of R. frustrana larval/ pupal parasitism in a study conducted in the coastal plain of Georgia and other studies have found them associated with R. frustrana (Eikenbary and Fox 1965, Freeman and Berisford 1979). Percent parasitoid mortality was recorded for 24 h (1,440 min) at the following time intervals after initial exposure. 15, 30, 45, 60, 90, 120, 180, 240, and 1,440 min. An insect was classiÞed as dead when all movement ceased. The study was designed as one way analysis of variance (ANOVA) with Þve treatments. Depending on parasitoid availability, there were Þve to seven replicates per species. Percent mortality data were arcsine squareroot (angular) transformed and subjected to ANOVA (Sokal and Rohlf 1995). The means
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Fig. 1. Test chambers used in a laboratory study on the susceptibility of Eurytoma pini, Haltichella rhyacioniae, Bracon sp., and Macrocentrus ancylivorus to broad-spectrum and biorational insecticides.
were separated using PROC GLM and the Tukey studentized range test (SAS Institute 1989). Results and Discussion Mortality rates ranged from 34 to 68% after 1,440 min, and varied signiÞcantly among the four species. A signiÞcantly higher percentage of M. ancylivorus died during the trials than H. rhyacioniae and E. pini (F ⫽ 22.60; df ⫽ 3, 12; P ⫽ 0.0001). Parasitoid mortality ranged from ⬍25% for indoxacarb and the control treatments to ⬎60% for spinosad and the pyrethroids for all of the parasitoids tested (Table 2). However, there was a signiÞcant interaction between species and treatment (P ⬍ 0.05) and thus the data were separated by species before further statistical analysis (Sokal and Rohlf 1995). Indoxacarb did not cause signiÞcantly higher mortality than the control treatment for any sample time or species (Table 2). Also, mortality was signiÞcantly lower in the control and indoxacarb treatments than in the lambda-cyhalothrin treatment from 45 to 180 min of exposure time for all species and from 45 to 1,440 min for M. ancylivorus (Table 2). Ruberson and
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Tillman (1999) found similar results between the indoxacarb and control treatments when tested on Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae) and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) in a laboratory study. They also found signiÞcantly higher survival in the indoxacarb treatments than in the lambda-cyhalothrin treatment. Indoxacarb may be a valuable option for R. frustrana control because of its low toxicity to the natural enemies tested in this study and to T. pretiosum, which is also an important R. frustrana egg parasitoid (McCravy and Berisford 1998). Spinosad was similar to the control and indoxacarb treatments and tended to be less toxic than the pyrethroids initially, but mortality increased with exposure time until it reached a level similar to the pyrethroids and higher than the control treatment (Fig. 2). For example, for M. ancylivorus, mortality was signiÞcantly lower in the spinosad treatment than for either of the pyrethroids at the 45 to 180 min sample periods (Table 2). Mortality was also initially lower for E. pini and H. rhyacioniae in the spinosad treatment than the lambda-cyhalothrin treatment (Table 2). However, at 1,440 min, no signiÞcant differences were found between spinosad and the pyrethroids except in one case where E. pini mortality was higher in the spinosad treatment than in the permethrin treatment (Table 2). Furthermore, for all of the species, mortality was signiÞcantly higher in the spinosad treatments than in the control and indoxacarb treatments at the end of the trial period (Table 2). Ruberson and Tillman (1999) also found mortality of C. marginiventris to be similar for spinosad and lambda-cyhalothrin treatments after 24 and 48 h of continuous exposure. Other studies showed signiÞcantly greater mortality in spinosad treatments over the lambda-cyhalothrin and control treatments for Trichogramma exiguum (Suh et al. 2000) and Cotesia plutella (Kurdjumov) (Pietrantonio and Benedict 1999). Trichogramma exiguum is an important R. frustrana egg parasitoid (McCravy and Berisford 1998), which might make spinosad less desirable for R. frustrana control. This is particularly important because T. exiguum is being evaluated for inundative releases to control R. frustrana (Orr et al. 2000). Unlike the current study, these studies do not report mortality before the 24-h period, and it is unlikely that parasitoids would remain in continuous contact with treated material for 24 h. Our study showed that different results are found at 4 h postexposure than were found at 24 h after exposure. At 4 h postexposure, spinosad causes less mortality than the pyrethroids, but there are no differences at 24 h (Fig. 2). For example for M. ancylivorus, 50% of the parasitoids were dead after 60 min of exposure time to the pyrethroids, but mortality did not reach 50% in the spinosad treatment until after 240 min (Fig. 2). Similar patterns were found for Bracon sp. (Fig. 2). It is not known from this study or the others mentioned whether it takes 24 h of continuous exposure for spinosad to cause mortality or if it takes longer for insects to die from spinosad than from the pyrethroids after an initial exposure.
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Table 2. Percent mortality (ⴞSE) of Eurytoma pini, Haltichella rhyacioniae, Bracon sp., and Macrocentrus ancylivorus to broadspectrum and biorational insecticides in a laboratory study Treatment Eurytoma pini C P L-C Sp I Haltichella rhyacioniae C P L-C Sp I Bracon sp. C P L-C Sp I Macrocentrus ancylivorus C P L-C Sp I
# of Reps
Mean # per rep
15
30
45
60
90
120
5 5 5 5 5
4.4 4.4 4.4 4.4 4.4
0 ⫾ 0a 0 ⫾ 0a 4 ⫾ 4a 0 ⫾ 0a 0 ⫾ 0a
0 ⫾ 0a 0 ⫾ 0a 8 ⫾ 5a 0 ⫾ 0a 0 ⫾ 0a
0 ⫾ 0b 9 ⫾ 6ab 30 ⫾ 11a 5 ⫾ 5ab 0 ⫾ 0b
0 ⫾ 0b 13 ⫾ 5ab 38 ⫾ 10a 5 ⫾ 5b 0 ⫾ 0b
0 ⫾ 0b 13 ⫾ 5ab 46 ⫾ 13a 9 ⫾ 6b 0 ⫾ 0b
0 ⫾ 0b 18 ⫾ 9ab 38 ⫾ 10a 18 ⫾ 9ab 0 ⫾ 0b
6 6 6 6 6
5.0 5.0 5.0 5.0 5.0
0 ⫾ 0b 10 ⫾ 4ab 36 ⫾ 12a 10 ⫾ 7ab 0 ⫾ 0b
0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0b 13 ⫾ 7ab 23 ⫾ 6ab 27 ⫾ 4ab 33 ⫾ 7ab 40 ⫾ 10ab 36 ⫾ 15a 36 ⫾ 15a 36 ⫾ 15a 36 ⫾ 18a 33 ⫾ 18a 17 ⫾ 10ab 17 ⫾ 10ab 20 ⫾ 10ab 32 ⫾ 10ab 36 ⫾ 10ab 0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0a
5 5 5 5 5
5.4 5.4 5.4 5.4 5.4
0 ⫾ 0a 7 ⫾ 5a 7 ⫾ 7a 0 ⫾ 0a 0 ⫾ 0a
0 ⫾ 0a 21 ⫾ 9a 23 ⫾ 16a 0 ⫾ 0a 0 ⫾ 0a
7 7 7 7 7
6.4 6.4 6.4 6.4 6.4
0 ⫾ 0a 2 ⫾ 2a 9 ⫾ 7a 0 ⫾ 0a 0 ⫾ 0a
0 ⫾ 0c 0 ⫾ 0c 0 ⫾ 0b 25 ⫾ 10ab 37 ⫾ 15ab 62 ⫾ 7a 38 ⫾ 10a 65 ⫾ 9a 76 ⫾ 8a 0 ⫾ 0c 0 ⫾ 0c 0 ⫾ 0b 2 ⫾ 2c 4 ⫾ 3bc 4 ⫾ 3b
Minutes
0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0b 19 ⫾ 13a 26 ⫾ 12a 0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0b
0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0b 35 ⫾ 15ab 42 ⫾ 17ab 42 ⫾ 17ab 49 ⫾ 17a 41 ⫾ 16a 45 ⫾ 16a 48 ⫾ 17a 48 ⫾ 17a 4 ⫾ 4ab 4 ⫾ 4ab 9 ⫾ 6ab 9 ⫾ 6ab 0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0b 0 ⫾ 0b 70 ⫾ 7a 78 ⫾ 8a 2 ⫾ 2b 4 ⫾ 3b
0 ⫾ 0b 79 ⫾ 7a 85 ⫾ 8a 11 ⫾ 4b 4 ⫾ 3b
180
240
4 ⫾ 4ab 4 ⫾ 4a 18 ⫾ 9ab 17 ⫾ 8a 42 ⫾ 11a 42 ⫾ 11a 23 ⫾ 14ab 37 ⫾ 13a 0 ⫾ 0b 4 ⫾ 4a
0 ⫾ 0b 0 ⫾ 0a 53 ⫾ 19a 57 ⫾ 21a 49 ⫾ 17ab 51 ⫾ 16a 26 ⫾ 14ab 48 ⫾ 16a 0 ⫾ 0b 7 ⫾ 7a 2 ⫾ 2b 85 ⫾ 6a 85 ⫾ 8a 17 ⫾ 7b 4 ⫾ 3b
2 ⫾ 2c 88 ⫾ 6a 90 ⫾ 9a 36 ⫾ 8b 9 ⫾ 4c
1440
8 ⫾ 5b 17 ⫾ 8b 52 ⫾ 16a 76 ⫾ 12a 16 ⫾ 7b 0 ⫾ 0c 53 ⫾ 12a 43 ⫾ 15ab 67 ⫾ 10a 13 ⫾ 10bc 10 ⫾ 7b 60 ⫾ 19ab 69 ⫾ 18ab 89 ⫾ 4a 34 ⫾ 11b 27 ⫾ 7b 90 ⫾ 6a 100 ⫾ 0a 93 ⫾ 3a 32 ⫾ 10b
Parasitoids were exposed for 1 d to insecticides applied to loblolly pine shoots. The treatments were control (C), permethrin (P), lambda-cyhalothrin (L-C), and indoxacarb (I). For each species, means in a column followed by the same letters are not signiÞcantly different (P ⬎ 0.05; Tukey studentized range test).
There were few signiÞcant differences in parasitoid mortality between lambda-cyhalothrin and permethrin treatments. Mortality was higher for lambdacyhalothrin than permethrin for H. rhyacioniae ini-
Fig. 2. Combined mortality patterns of Eurytoma pini, Haltichella rhyacioniae, Bracon sp., and Macrocentrus ancylivorus to broad-spectrum and biorational insecticides in a laboratory study. Species were combined for sake of simplicity and the individual species patterns were similar to the combined patterns.
tially (Table 2). Lambda-cyhalothrin has been shown to be signiÞcantly more effective in reducing R. frustrana damage and it has a longer optimal spray timing window than permethrin (Nowak et al. 2000), but theirdeleterious effects on natural enemies are the same. In conclusion, indoxacarb was the least detrimental insecticide to R. frustrana parasitoids. Preliminary tests indicate that it is effective in reducing R. frustrana damage (unpublished data), but it is not currently registered for use in conifer plantations. Spinosad was initially less toxic than the pyrethroids, but was as toxic to the parasitoids as the pyrethroids after 24 h of continuous exposure. Further research is needed to determine the mechanisms behind these differences. If spinosad is less detrimental to natural enemies in Þeld applications because of the lower exposure times; it may be a viable option because there are no differences in efÞcacy between these two products (Nowak et al. 2000). In our study, the pyrethroids were the most toxic compounds to the parasitoids. These studies were intended to not only increase our knowledge about the acute toxicity of these insecticides to R. frustrana parasitoids but also to closely related parasitoid species that are important in agricultural systems. Although acute toxicity tests using plant substrate residues are commonly used because they are cheaper and easier than Þeld studies (Ruberson et al. 1998), they do not indicate all of the
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potential effects of insecticides on natural enemies. Other impacts may include reduced fecundity, survival time, and host searching ability (Ruberson et al. 1998). It is also difÞcult to extrapolate results from individual specimens to the population level. Field studies over large areas are needed to further evaluate the impacts of these insecticides on parasitoids of R. frustrana (Stark et al. 1995). Acknowledgments The authors thank G. Hammes (DuPont Agricultural Products) for providing the Steward SC product for this project. We also thank R. Garland and K. Seltmann for their help in collecting pine shoots for this project. The authors appreciate the time and effort put forth by C. Asaro and J. Ruberson reviewing an earlier version of the manuscript. This paper is partial fulÞllment of dissertation requirements by J.T.N. for Ph.D. This research was supported in part by the University of Georgia Pine Tip Moth Research Consortium directed by C.W.B.
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Kudon, L. H., C. W. Berisford, and M. J. Dalusky. 1988. ReÞnement of a spray timing technique for the Nantucket pine tip moth (Lepidoptera: Tortricidae). J. Entomol. Sci. 23: 180 Ð186. McCann, S. F., G. D. Annis, R. Shapiro, D. W. Piotrowski, G. P. Lahm, J. K. Long, K. C. Lee, M. M. Hughes, B. J. Meyers, and S. M. Griswold. 2001. The discovery of indoxacarb: oxadiazines as a new class of pyrazoline-type insecticides. Pest Manage. Sci. 57: 153Ð164. McClure, M. S. 1977. Resurgence of the scale, Fiorinia externa (Homoptera: Diaspididae), on hemlock following insecticide application. Environ. Entomol. 6: 480 Ð 484. McCravy K. W., and C. W. Berisford. 1998. Parasitism by Trichogramma spp. (Hymenoptera: Trichogrammatidae) in relation to Nantucket pine tip moth (Lepidoptera: Tortricidae) egg density and location. Environ. Entomol. 27: 355Ð359. McCravy, K. W., and C. W. Berisford. 2000. Parasitoids of the Nantucket pine tip moth, Rhyacionia frustrana (Comstock) (Lepidoptera: Tortricidae), in the coastal plain of Georgia. J. Entomol. Sci. 35: 220 Ð226. McCravy, K. W., M. J. Dalusky, and C. W. Berisford. 2001. Effects of a broad spectrum and biorational insecticides on parasitoids of the Nantucket pine tip moth (Lepidoptera: Tortricidae). J. Econ. Entomol. 94: 112Ð115. Metcalf, R L., and W. H. Luckmann. 1994. Introduction to insect pest management, 3rd ed. Wiley, New York. Nowak, J. T., and C. W. Berisford. 2000. Effects of intensive forest management practices on insect infestation levels and loblolly pine growth. J. Econ. Entomol. 93: 336 Ð341. Nowak, J. T., C. J. Fettig, K. W. McCravy, and C. W. Berisford. 2000. EfÞcacy tests and development of spray timing models to control Nantucket pine tip moth (Lepidoptera: Tortricidae) infestations. J. Econ. Entomol. 93: 1708 Ð 1713. Orr, D. B., C.P.C. Suh, K. W. McCravy, C. W. Berisford, and G. L. Debarr. 2000. Evaluation of inundative releases of Trichogramma exiguum (Hymenoptera: Trichogrammatidae) for suppression of Nantucket pine tip moth (Lepidoptera: Tortricidae) in pine (Pinaceae) plantations. Can. Entomol. 132: 373Ð386. Pietrantonio, P. V., and J. H. Benedict. 1999. Effect of new cotton insecticide chemistries, tebufenozide, spinosad and chlorfenapyr, on Orius insidious and two Cotesia species. Southwest. Entomol. 24: 21Ð29. Ruberson, J. R, and P. G. Tillman. 1999. Effect of selected insecticides on natural enemies in cotton: laboratory studies. Proc. Beltwide Cotton Conf. 2: 1210 Ð1213. Ruberson, J. R., H. Nemoto, and Y. Hirose. 1998. Pesticides and conservation of natural enemies in pest management, pp. 207Ð220. In P. Barbosa [ed.], Conservation and Biological Control, Academic, New York. Saldago, V. L., G. B. Watson, and J. J. Sheets. 1997. Studies on the mode of action of spinosad, the active ingredient in Tracer insect control. Proc. Beltwide Cotton Conf. 2: 1082Ð1086. SAS Institute. 1989. UserÕs guide: statistics, version 6. SAS Institute, Cary, NC. Seay, R E., E. P. Castner, and R M. Edmund. 1999. Steward: a new control option for tarnished plant bug. Proc. Beltwide Cotton Conf. 2: 1225Ð1227. Sokal, R R., and F. J. Rohlf. 1995. Biometry, 3rd ed. Freeman, New York. Stark, J. D., P. C. Jepson, and D. F. Mayer. 1995. Limitations to use of topical toxicity data for predictions of pesticide side effects in the Þeld. J. Econ. Entomol. 88: 1081Ð1088. Suh, C.P.C., D. B. Orr, and J. W. Van Duyn. 2000. Effect of insecticides on Trichogramma exiguum (Trichogramma-
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tidae: Hymenoptera) preimaginal development and adult survival. J. Econ. Entomol. 93: 577Ð583. Sun, J., D. L. Kulhavy, and S. Yan. 1998. Prediction models of Nantucket pine tip moth, Rhyacionia frustrana (Comstock) (Lepidoptera: Tortricidae) infestation using soil and tree factors. J. Appl. Entomol. 122: 1Ð3.
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Theiling, K. M., and B. A. Croft. 1988. Pesticide side-effects on arthropod natural enemies: A database summary. Agric. Ecosys. Environ. 21: 191Ð218. Received for publication 17 October 2000; accepted 1 May 2001.
