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Releases of Trichogramma platneri (Hymenoptera: Trichogrammatidae) in Apple Orchards under a Sterile Codling Moth Release Program
Biological Control 18, 179 –186 (2000) doi:10.1006/bcon.2000.0828, available online at http://www.idealibrary.com on
Releases of Trichogramma platneri (Hymenoptera: Trichogrammatidae) in Apple Orchards under a Sterile Codling Moth Release Program J. E. Cossentine and L. B. M. Jensen Pacific Agri-Food Research Centre, Agriculture and Agri-Food Canada, Summerland, British Columbia, Canada V0H 1Z0 Received January 22, 1998; accepted March 2, 2000
Based on the premise that augmented host numbers may help multiply and support parasitoid populations, the egg parasitoid Trichogramma platneri Nargarkatti was released in apple orchards which were participating in a sterile codling moth, Cydia pomonella (L.), release program. Nonviable eggs resulting from matings involving at least one sterile codling moth partner can be successfully parasitized by T. platneri. Grain moth-reared, as well as codling mothreared, T. platneri were released either in the spring or in the spring and summer oviposition period(s) of wild codling moth. Sentinel codling moth eggs were hung weekly, for 3-day periods, from May until September to determine fluctuations in T. platneri populations both during and between releases. Low numbers of wild or nonviable codling moth eggs or other susceptible host eggs resulted in sufficient eggs to maintain low spring- or summer-introduced T. platneri populations. T. platneri reduced codling moth damage in trees in which the Trichogramma were released. © Minister of Public Works and Government Services Canada 2000 Key Words: Cydia pomonella; codling moth; Trichogramma platneri; Sitotroga cerealla; Angoumois grain moth; sterile release.
INTRODUCTION
In the Okanagan Valley of British Columbia, Canada, codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), oviposit during May and early June for the first of two to three annual generations (Madsen and Proctor, 1982). As is frequently seen in the appearance, activity, and abundance of naturally occurring parasitoids in relation to their host species (Basso and Morey, 1990; Knipling and McGuire, 1968), the indigenous codling moth egg parasitoid, Trichogramma platneri Nagarkatti (Hymenoptera: Trichogrammatidae), does not significantly influence the first generation of codling moth eggs in this region (J.C., unpublished data). Whether this is the result of spring emergence possibly being uncoordinated with the host, excessively low parasitoid populations, and/or an in-
ability of the parasitoids to function in the cool spring temperatures is uncertain. Summer inundative releases of Trichogramma spp. versus wild codling moth in Europe and the United States have resulted in varying degrees of host control (Dolphin et al., 1972; Hassan et al., 1988; Yu et al., 1984). Management of other pest populations has been demonstrated through the simultaneous release of the host with a parasitoid species, providing the parasitoid with sufficient host numbers in which to establish and multiply (Liebhold and Elkinton, 1989; Parker et al., 1971; Parker and Pinnell, 1972). Using this hypothesis, Nagy (1973) recommended augmenting codling moth control in apple orchards by releasing a Trichogramma species in combination with the release of sterile moths. Bloem et al. (1998) released a combination of sterile codling moths and T. platneri in large orchard field cages and recorded that apple damage was significantly less than when either tactic was used alone. Since 1994, millions of irradiated codling moth male and female adults have been reared and released from May until September in the Okanagan Valley of British Columbia in a valley-wide sterile codling moth release program (Dyck and Gardiner, 1992). Eggs resulting from a mating involving at least one sterile codling moth partner are nonviable (Proverbs and Newton, 1962), and Bloem et al. (1998) estimated that 30,000 – 40,000 nonviable eggs per hectare are in the orchards receiving sterile moths at any given time. T. platneri can successfully parasitize nonviable codling moth eggs, although the parasitoid prefers viable eggs (Cossentine et al., 1996). In our study, T. platneri reared on Angoumois grain moth, Sitotroga cerella (Oliver) (Lepidoptera: Gelechiidae), and codling moth were both released in apple orchards during the oviposition period of the first or the first and second codling moth generation. We measured the capacity of T. platneri to maintain their numbers in orchards within the sterile codling moth release program and the influence of the parasitism on remaining wild codling moth populations.
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MATERIALS AND METHODS
Studies in 1995 and 1996 were conducted in four apple orchards in Summerland, British Columbia that had not been treated with insecticides. All orchards received male and female codling moth, rendered sterile through exposure to 32 krad from a source of cobalt 60. Moths were released twice weekly at a rate of 1000/ha from late April until the end of September by the Okanagan–Kootenay Sterile Insect Release Program (Osoyoos, British Columbia). In each of four test orchards three (1995) or four (1996) 25-m 2 treatment blocks were used to assess the affects of parasitoid release. Treatments included (1) 3000 female grain moth-reared T. platneri/ha purchased from Rincon–Vitova Insectaries, Inc. (Ventura, CA) released twice over a 6- to 9-day period (May 14 and 19, 1995 and May 15 and 23, 1996), attempting to coincide with egg oviposition of the first codling moth generation; (2) a similar spring release of grain mothreared T. platneri (as above) with an additional release coinciding with the oviposition period of the second codling moth generation (July 13 and 20, 1995 and July 25 and August 2, 1996); and (3) T. platneri, reared at 15–25°C on codling moth eggs rendered nonviable through irradiation, released at 3000 female T. platneri/ha on May 17 and 23, 1996. A similar block of trees covering 25 m 2 in each orchard was used as a control. All parasitoids were released from five trees or from five pairs of trees located in the center of each plot (Fig. 1). Four trees or four pairs of trees positioned next to the release trees are hereafter referred to as ”adjacent“ trees and four trees or four pairs of trees on the corners of the plots are hereafter referred to as ”outside“ trees (Fig. 1). Grain moth-reared T. platneri were held at 15°C until they were used. In preparation for release, three samples were removed from the parasitized egg card, and the parasitoids were allowed to emerge at 25°C to determine percentage emergence and the sex ratio. The appropriate portions of parasitized cards necessary to provide 3000 female T. platneri per tree or pair of trees were divided into a small paper bag which contained a cotton wick dampened with a honey-water suspension, as well as a thin streak of honey. The top of each bag was folded over a string and stapled. The bags were incubated at 25°C until the parasitoids emerged, the bags were then tied into the center of the release trees in treatment plots and small holes were cut into the sides of the bags to allow the parasitoids to escape. To obtain T. platneri from codling moth eggs, T. platneri reared on grain moth eggs were purchased from Rincon–Vitova Insectaries, Inc. and allowed to emerge and mate in 4-L sealed plastic buckets with a honey-and-water-soaked cotton wick attached to the inside of each lid. Sheets of codling moth eggs, obtained from the Okanagan–Kootenay codling moth rearing
FIG. 1. Release (filled), adjacent inside (striped), and outside (criss-crossed) trees within 25-m 2 treatment blocks. (A) Standard and (B) high-density plantings.
facility (Osoyoos, British Columbia), were irradiated at 3.7 krad from a source of cobalt 60. Portions of the egg sheets, carrying approximately 82,500 eggs, were placed into each bucket of T. platneri and the buckets incubated at 15–25°C, 24 h L. After 48 h of exposure to the parasitoids, the egg sheets were transferred to parasitoid-free, 4-L sealed plastic buckets and incubated at similar temperatures. Five days after exposure to the parasitoids, a water soaked cotton wick was added to each bucket. Two days later the total eggs and percentage parasitism were determined from at least seven samples of 200 –300 eggs/bucket. A sample of T. platneri was allowed to emerge, and parasitized eggs, percentage emergence, sex ratio, and the number of adults/egg were determined. The appropriate portion of parasitized egg sheets required to provide 3000 T. platneri/tree upon release were partitioned and bagged before parasitoid emergence as described above. To monitor the population densities of T. platneri through the season, viable sentinel codling moth eggs were hung weekly, for 3-day periods, on each of the five release, four adjacent, and four outside trees or pairs of trees (Fig. 1) in the treatment and control blocks from May 1 until September 19 in both years. Sentinel egg
RELEASE OF T. platneri WITH STERILE CODLING MOTHS
cards included 25–50 viable codling moth eggs, ⱕ24 h postoviposition, on waxed paper, attached to a plastic label with a wire (1995). Many of the sentinel eggs were lost from June until September 1995, probably due to earwig predation. For this reason sentinel eggs were hung within 4 ⫻ 11 cm screen cages in 1996. Sentinel eggs were stored at 25°C for at least 1 week after they were retrieved, until parasitism was assessed. In 1996 sentinel obliquebanded leafroller (Choristoneura rosaceana L., Lepidoptera: Tortricidae) egg masses were also hung in the five central trees (Fig. 1) of treatment and control blocks. In both species of sentinel eggs, the incidence, rather than percentage parasitism, was used as an indicator of Trichogramma survival and fecundity because the number of Trichogramma wasps parasitizing a single egg card was not observed and the presentation of codling moth eggs provided an unnaturally large number of hosts. If a single egg on a sentinel egg card was parasitized, the card was considered parasitized. To estimate the incidence of codling moth eggs resulting from the release of sterile codling moths, 200 leaves on each of 24 trees within two of the orchard sites were inspected for codling moth eggs in 1996. Percentage fruit damaged by first-generation codling moth was assessed at the end of June each year. In 1995, all fruit were removed in June at the request of the Sterile Insect Release program, as the codling moth populations exceeded the limits set by the program. Twenty undamaged apples were then rehung on each of the trees in the treatment and control blocks to assess second-generation damage. In 1996, first-generation damage was assessed from all apples on each of the 13 trees/treatment. All fruit was removed in September in both years and total codling moth, leafroller, and eye-spotted budmoth, Spilonota occellana (Lepidoptera: Tortricidae), damage determined. After arcsin transformation, percentage means were compared using an ANOVA and Duncan’s multiple range test (SAS, 1985). Temperatures through the summer were obtained from the Pacific Agri-Food Research Centre’s daily records. RESULTS AND DISCUSSION
First Generation Releases. In both 1995 and 1996, sentinel eggs in all blocks receiving grain moth-reared T. platneri in the spring exhibited a high incidence of parasitism during the period of the release (Figs. 2 and 3). As expected, the incidence of parasitism was most evident in the trees in which Trichogramma were released (x ⫽ 0.80 ⫾ 0.22, 1995; x ⫽ 0.84 ⫾ 0.33, 1996). High incidence of parasitism was also found in adjacent (x ⫽
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0.78 ⫾ 0.24, 1995; x ⫽ 0.69 ⫾ 0.34, 1996) and outside (x ⫽ 0.64 ⫾ 0.30, 1995; x ⫽ 0.48 ⫾ 0.32, 1996) trees. In 1996, release of codling moth-reared T. platneri did not provide higher levels of parasitism of sentinel eggs than did grain moth-reared T. platneri (Fig. 3). In 1995, parasitism in control blocks (Fig. 2) was probably indicative of the movement of released Trichogramma through the orchard. Dispersal of Trichogramma is significantly affected by wind (Hendricks, 1967; Yu et al., 1984). T. minutum have been shown able to move a distance of at least five peach trees, separated by 5.4 m, in the course of 3 days (Schread, 1932) and Trichogramma semifumatum have moved as much as 600 m in alfalfa fields (Stern et al., 1965). For these reasons, four more-widely separated orchards were chosen for the test in 1996 and the level of parasitism within control plots was lower (Fig. 3). Parasitoid maintenance on orchard host eggs. Incidence of parasitism in the sentinel eggs decreased 1 week postrelease to 0 –15% (Figs. 2 and 3). Temperatures at this time ranged from 4.3 to 26.5°C in 1995 and from 4 to 24°C in 1996. Laboratory trials have shown grain moth-reared T. platneri to survive an average of 8.7 days at 5–10°C and 4.3 days at 10 –15°C (J.C., unpublished data). T. platneri reared on codling moth eggs at 15–25°C survived for an average of 25.4 days at 5–10°C and 14.1 days at 10 –15°C. Evidence that T. platneri propagated itself on nonviable codling moth eggs was expected to be seen through continued parasitism of the sentinel eggs after the release peak. Approximately 12 days after release (June 6, 1995; June 4, 1996) the incidence of parasitism in both Trichogramma release plots began to increase above parasitism in the control checks (Figs. 2 and 3), suggesting that some released Trichogramma had been able to reproduce in viable and/or nonviable codling moth eggs and were beginning to emerge and search for new host eggs. By June 15, 1995, sentinel eggs began to disappear. Earwigs were abundant in all of the plots and may have consumed sentinel eggs and/or very high summer temperatures (max ⫽ 34°C) may have caused the eggs to desiccate and flake off. In early September 1995, sentinel eggs were hung only during the daytime when earwigs did not appear to consume them and in 1996 the eggs were hung inside screen cages. Parasitism of sentinel eggs within release trees fluctuated between 0 and 38% from June to the oviposition of the second generation in July 1995 (Fig. 2). When sentinel eggs were held within screen cages in 1996, the incidence of T. platneri parasitism within release trees from June to the second generation in July was found to range from 0 to 25%, with no parasitism found for periods of 4 to 7 weeks (Fig. 3). Maintenance of T.
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FIG. 2.
Mean incidence of parasitism (1995) in sentinel codling moth eggs. (a) Release trees; (b) adjacent trees.
platneri in release and adjacent trees was minimal and higher in 1995 than in 1996. Apple damage. Damage from first-generation codling moth was significantly (P ⬍ 0.05) lower in blocks receiving T. platneri releases in May 1995 (Table 1). Damage levels were high in 1995, indicating that sub-
stantial numbers of wild codling moth and thus viable codling moth eggs were available for parasitism and maintenance of released T. platneri populations. Percentage codling moth damage was not significantly (P ⬎ 0.05) lower in blocks receiving T. platneri releases in May 1996 (Table 1). Wild codling moth
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FIG. 3.
Mean incidence of parasitism (1996) in sentinel codling moth eggs. (a) Release trees; (b) adjacent trees.
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TABLE 1 Percentage Codling Moth Damage after First and Second Generation in T. platneri Release and Control Plots (Four Replications) Mean percentage codling moth damage a,b Treatment release period
T. platneri host source
Release trees
Adjacent
Outside
First-generation assessment 1995 Spring Spring & summer Control 1996 Spring Spring Spring & summer Control
Grain moth Grain moth — Grain moth Codling moth Grain moth —
7.7 a (1591) 6.9 a (1761) 15.8 b (1538)
7.1 a (1127) 8.3 a (934) 21.9 b (1011)
7.4 a (693) 11.0 a (2029) 26.8 b (604)
0.0 a (2793) 0.04 a (2594) 0.06 a (2093) 0.0 a (2444)
0.07 a (1750) 0.05 a (2008) 0.0 a (1743) 0.0 a (1766)
0.08 a (1520) 0.13 a (2069) 0.0 a (1346) 0.0 a (1306)
Second-generation assessment 1995 Spring Spring & summer Control 1996 Spring Spring Spring & summer Control a b
Grain moth Grain moth — Grain moth Codling moth Grain moth —
31.5 a 35.8 a 50.5 b
(375) (386) (391)
0.5 a 0.1 a 0.2 a 1.3 b
(2875) (3105) (2075) (2118)
32.1 a 35.9 a 54.5 b
(294) (304) (309)
0.7 ab (2104) 0.5 a (2234) 0.2 a (1829) 1.4 b (1636)
35.9 a 36.9 a 49.1 b
(304) (310) (313)
1.4 b (1458) 0.1 a (2166) 0.2 a (1393) 1.1 ab (907)
Means within year and column followed by the same letter are not significantly different (Duncan’s multiple range test, P ⬍ 0.05). Total number of apples sampled in parentheses.
infestation levels were very low and damage was negligible in all plots. Second Generation Releases. In both 1995 and 1996, sentinel eggs in all blocks receiving grain moth-reared T. platneri in the summer exhibited an incidence of parasitism for the 3 (1995) or 4 (1996) week period following the July–August releases (Figs. 2 and 3). The mean parasitism over these weeks was most evident in the trees in which the Trichogramma were released (x ⫽ 0.39 ⫾ 0.34, 1995; x ⫽ 0.78 ⫾ 0.36, 1996); however, high mean levels of parasitism over these weeks were also displayed in the adjacent (x ⫽ 0.18 ⫾ 0.24, 1995; x ⫽ 0.54 ⫾ 0.35, 1996) and outside (x ⫽ 0.31 ⫾ 0.35, 1995; x ⫽ 0.64 ⫾ 0.42, 1996) trees. At harvest in 1995, 69 and 70% of codling moth eggs on fruit from trees receiving first-generation T. platneri releases, and first- and second-generation T. platneri releases, respectively, were parasitized. The viability of the unparasitized eggs was not determined. Parasitoid maintenance on orchard host eggs. The incidence of T. platneri parasitism on the sentinel egg card fluctuated between 0 and 38% after the secondgeneration releases in 1995 and between 0 and 13% after the second-generation releases in 1996. If the
parasitoid had increased within the orchards we could expect more evidence of its presence in the weekly sentinel egg survey. Only 29 codling moth eggs (of which 2 were parasitized) were located on the 4800 leaves inspected in 1996, suggesting that host densities were insufficient to allow the released parasitoids to maintain their populations above these low levels. Apple damage. Mean percentage codling moth damage after the second generation was significantly (P ⬍ 0.05) lower at harvest within blocks receiving both first-generation only and first- and second-generation T. platneri releases in 1995 (Table 1). This reduction in codling moth damage was seen within all trees within the treatment block. The damage levels at harvest in 1995 far exceeded the economic threshold for a commercial orchard; however, damage was undoubtably higher than normal due to the removal of the fruit from the rest of the orchard and the low number of fruit (20/tree) repositioned manually in the trees to allow an assessment of damage. Codling moth damage was significantly lower (P ⬍ 0.05) at harvest within blocks receiving all T. platneri treatments within the release trees in 1996 (Table 1). This significant (P ⬍ 0.05) reduction in codling moth damage found at harvest was also evidenced in fruit from adjacent trees in blocks receiving codling moth-
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TABLE 2 Percentage Summer Leafroller Damage in T. platneri Treated and Untreated Plots, September 1996 Assessment (Four Replications) Mean percentage sumer leafroller damge a,b Treatment release period
T. platneri host source
Release trees
Adjacent trees
Outside trees
Spring Spring Spring & summer Control
Grain moth Codling moth Grain moth —
2.31 a (2875) 1.42 ab (3105) 1.23 b (2075) 2.22 a (2118)
2.34 a (2104) 1.65 ab (2234) 1.13 b (1829) 1.95 ab (1636)
1.70 a (1458) 1.60 a (2166) 1.60 a (1393) 1.80 a (907)
a b
Means within column followed by the same letter are not significantly different (Duncan’s multiple range test, P ⬍ 0.05). Total number of apples sampled in parentheses.
reared T. platneri and spring- and summer-released grain moth-reared T. platneri (Table 1). However, only one of the four replicate orchards showed evidence of substantial wild codling moth populations. Mean percentage summer leafroller damage was significantly (P ⬍ 0.05) lower at harvest within the release trees receiving first- and second-generation T. platneri releases in 1996 (Table 2). It should be noted that summer leafroller damage was low in comparison to eye-spotted bud moth damage (4.5–11.7%) which was not significantly (P ⬎ 0.05) reduced by T. platneri releases. CONCLUSIONS
The original premise that T. platneri populations could be sustained when released in orchards where sterile codling moths are released has not been refuted; however, the extent to which the nonviable codling moth eggs resulting from the release of sterile moths support the T. platneri is unclear. From our limited egg search in sterile insect release orchards in August 1996, we calculated that the number of codling moth eggs available to maintain the released T. platneri (x ⫽ 0.6 egg/100 leaves, n ⫽ 24) is close to what we could expect from a sterile codling moth releases of approximately 1000 moths/ha/week. It should also be noted that oviposition from sterile x sterile codling moth matings result in fewer eggs than from fertile matings under laboratory conditions (Bloem et al., 1998). How many nonviable codling moth eggs are sufficient to maintain a Trichogramma population? With 3000 T. platneri released per tree, it seems unlikely that there would be sufficient nonviable codling moth eggs to maintain the released population at this high level. However, there would be an excellent chance of thorough parasitism of the eggs available. This would explain the increase in the mean percentage parasitism of sentinel eggs approximately 2 weeks after release, as it would take that long for a second generation of the T. platneri to emerge. T. platneri reared at 15– 25°C on codling moth eggs, which were expected to be
more vigorous and fecund at low spring temperatures, seemed to practically disappear after the high-release parasitism and 2-week postrelease increase as described above. We propose that T. platneri derived from codling moth did not exhibit an obvious advantage over the grain moth-reared T. platneri, as both treatments showed very high parasitism upon release. Similarly, high populations of T. platneri were maintained over 2 (1995) and 4 (1996) week periods after their release in July–August, after which the population numbers decreased and rose again as the next generation of Trichogramma emerged. Based on damage data from these field releases, we conclude that the release of T. platneri significantly decreased wild codling moth numbers within release trees. ACKNOWLEDGMENTS Partial funding for this work was provided by grants from the Washington State Tree Fruit Research Commission and by the U.S.D.A. Area-Wide Research Funding. The researchers are grateful for the support provided by the Sterile Insect Release Program, Osoyoos, British Columbia and by N. Klassen, Institute for National Measurement Standards, National Research Council of Canada, Ottawa, Ontario and appreciate the work of K. Thompson and P. Rydings. We thank G. J. R. Judd and M. J. Smirle for reviewing the manuscript. This paper is contribution number 1061 of the Pacific Agri-Food Research Centre, Summerland, British Columbia, Canada.
REFERENCES Basso, C., and Morey, C. 1990. Biological control of the sugarcane borer Diatraea saccharalis Fabricius (Lepidoptera:Pyralidae) with Trichogramma spp. (Hymenoptera: Trichogrammatidae) in Uraguay. In “Trichogramma and Other Egg Parasitoids” (E. Wajnberg and S. B. Vinson, Eds.), pp. 165–169. 3rd International Symposium, 23–27 September, 1990, San Antonio, TX, Institut National de la Recherche Agronomique, Paris. Bloem, S., Bloem, K. A., and Knight, A. L. 1998. Oviposition by sterile coding moths, Cydia pomonella (Lepidoptera: Tortricidae) and control of wild populations with combined releases of sterile moth and egg parasitoids. J. Entomol. Soc. British Columbia 95, 99 –109.
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Cossentine, J. E., Lemieux, J., and Zhang, Y. 1996. Comparative host suitability of viable and nonviable codling moth (Lepidoptera: Tortricidae) eggs for parasitism by Trichogramma platneri (Hymenoptera: Trichogrammatidae). Environ. Entomol. 25, 1052–1057. Dolphin, R. E., Cleveland, M. L., Mouzin, T. E., and Morrison, R. K. 1972. Releases of Trichogramma minutum and T. cacoeciae in an apple orchard and the effects on populations of codling moths. Environ. Entomol. 1, 481– 484. Dyck, V. A., and Gardiner, M. G. T. 1992. Sterile-insect release programme to control the codling moth Cydia pomonella (L.) (Lepidoptera: Olethreutidae) in British Columbia, Canada. Acta Phytopathol. Entomol. Hung. 27, 219 –228. Hassan, S. A., Kohler, E., and Rost, W. M. 1988. Mass production and utilization of Trichogramma 10. Control of the codling moth Cydia pomonella and the summer fruit tortrix, Adoxophyes orana [Lep.: Tortricidae] Entomophaga 33, 413– 420. Hendricks, D. E. 1967. Effect of wind on dispersal of Trichogramma semifumatum. J. Econ. Entomol. 60, 1367–1373. Knipling, E. F., and McGuire, J. U. 1968. Population models to appraise the limitations and potentialities of Trichogramma in managing host insect populations. U. S. Dept. Agric. Res. Serv. Tech. Bull. 1387. Liebhold, A. M., and Elkinton, J. W. 1989. Elevated parasitism in artificially augmented populations of Lymantria dispar (Lepidoptera: Lymantriidae). Environ. Entomol. 18, 986 –995.
Madsen, H. F., and Procter, P. J. 1982. “Insects and Mites of Tree Fruits in British Columbia.” Ministry of Agriculture and Food. Nagy, B. 1973. The possible role of entomophagous insects in the genetic control of the codling moth with special reference to Trichogramma. Entomophaga 18, 185–191. Parker, F. D., Lawson, F. R., and Pinnell, R. E. 1971. Suppression of Pieris rapae using a new control system: Mass release of both the pest and its parasitoids. J. Econ. Entomol. 64, 721–735. Parker, F. D., and Pinnell, R. E. 1972. Further studies of the biological control of Pieris rapae using supplemental host and parasite releases. Environ. Entomol. 1, 150 –157. Proverbs, M. D., and Newton, J. R. 1962. Influence of gamma radiation on the development and fertility of the codling moth, Carpocapsa pomonella (L.) [Lepidoptera: Olethreutidae]. Can. J. Zool. 40, 401– 419. SAS. 1985. SAS user’s guide. Statistics, Version 5ed. SAS Institute, Cary, NC. Schread, J. C. 1932. Behaviour of Trichogramma in field liberations. J. Econ. Entomol. 25, 370 –374. Stern, V. M., Schlinger, E. I., and Bowden, W. R. 1965. Dispersal studies of Trichogramma semifumatum (Hymenoptera: Trichogrammatidae) tagged with radioactive phosphorus. Ann. Entomol. Soc. Am. 58, 234 –240. Yu, D. S. K., Laing, J. E., and Hagley, E. A. C. 1984. Dispersal of Trichogramma spp. (Hymenoptera: Trichogrammatidae) in an apple orchard after inundative releases. Environ. Entomol. 13, 371–374.
Releases of Trichogramma platneri (Hymenoptera: Trichogrammatidae) in Apple Orchards under a Sterile Codling Moth Release Program J. E. Cossentine and L. B. M. Jensen Pacific Agri-Food Research Centre, Agriculture and Agri-Food Canada, Summerland, British Columbia, Canada V0H 1Z0 Received January 22, 1998; accepted March 2, 2000
Based on the premise that augmented host numbers may help multiply and support parasitoid populations, the egg parasitoid Trichogramma platneri Nargarkatti was released in apple orchards which were participating in a sterile codling moth, Cydia pomonella (L.), release program. Nonviable eggs resulting from matings involving at least one sterile codling moth partner can be successfully parasitized by T. platneri. Grain moth-reared, as well as codling mothreared, T. platneri were released either in the spring or in the spring and summer oviposition period(s) of wild codling moth. Sentinel codling moth eggs were hung weekly, for 3-day periods, from May until September to determine fluctuations in T. platneri populations both during and between releases. Low numbers of wild or nonviable codling moth eggs or other susceptible host eggs resulted in sufficient eggs to maintain low spring- or summer-introduced T. platneri populations. T. platneri reduced codling moth damage in trees in which the Trichogramma were released. © Minister of Public Works and Government Services Canada 2000 Key Words: Cydia pomonella; codling moth; Trichogramma platneri; Sitotroga cerealla; Angoumois grain moth; sterile release.
INTRODUCTION
In the Okanagan Valley of British Columbia, Canada, codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), oviposit during May and early June for the first of two to three annual generations (Madsen and Proctor, 1982). As is frequently seen in the appearance, activity, and abundance of naturally occurring parasitoids in relation to their host species (Basso and Morey, 1990; Knipling and McGuire, 1968), the indigenous codling moth egg parasitoid, Trichogramma platneri Nagarkatti (Hymenoptera: Trichogrammatidae), does not significantly influence the first generation of codling moth eggs in this region (J.C., unpublished data). Whether this is the result of spring emergence possibly being uncoordinated with the host, excessively low parasitoid populations, and/or an in-
ability of the parasitoids to function in the cool spring temperatures is uncertain. Summer inundative releases of Trichogramma spp. versus wild codling moth in Europe and the United States have resulted in varying degrees of host control (Dolphin et al., 1972; Hassan et al., 1988; Yu et al., 1984). Management of other pest populations has been demonstrated through the simultaneous release of the host with a parasitoid species, providing the parasitoid with sufficient host numbers in which to establish and multiply (Liebhold and Elkinton, 1989; Parker et al., 1971; Parker and Pinnell, 1972). Using this hypothesis, Nagy (1973) recommended augmenting codling moth control in apple orchards by releasing a Trichogramma species in combination with the release of sterile moths. Bloem et al. (1998) released a combination of sterile codling moths and T. platneri in large orchard field cages and recorded that apple damage was significantly less than when either tactic was used alone. Since 1994, millions of irradiated codling moth male and female adults have been reared and released from May until September in the Okanagan Valley of British Columbia in a valley-wide sterile codling moth release program (Dyck and Gardiner, 1992). Eggs resulting from a mating involving at least one sterile codling moth partner are nonviable (Proverbs and Newton, 1962), and Bloem et al. (1998) estimated that 30,000 – 40,000 nonviable eggs per hectare are in the orchards receiving sterile moths at any given time. T. platneri can successfully parasitize nonviable codling moth eggs, although the parasitoid prefers viable eggs (Cossentine et al., 1996). In our study, T. platneri reared on Angoumois grain moth, Sitotroga cerella (Oliver) (Lepidoptera: Gelechiidae), and codling moth were both released in apple orchards during the oviposition period of the first or the first and second codling moth generation. We measured the capacity of T. platneri to maintain their numbers in orchards within the sterile codling moth release program and the influence of the parasitism on remaining wild codling moth populations.
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MATERIALS AND METHODS
Studies in 1995 and 1996 were conducted in four apple orchards in Summerland, British Columbia that had not been treated with insecticides. All orchards received male and female codling moth, rendered sterile through exposure to 32 krad from a source of cobalt 60. Moths were released twice weekly at a rate of 1000/ha from late April until the end of September by the Okanagan–Kootenay Sterile Insect Release Program (Osoyoos, British Columbia). In each of four test orchards three (1995) or four (1996) 25-m 2 treatment blocks were used to assess the affects of parasitoid release. Treatments included (1) 3000 female grain moth-reared T. platneri/ha purchased from Rincon–Vitova Insectaries, Inc. (Ventura, CA) released twice over a 6- to 9-day period (May 14 and 19, 1995 and May 15 and 23, 1996), attempting to coincide with egg oviposition of the first codling moth generation; (2) a similar spring release of grain mothreared T. platneri (as above) with an additional release coinciding with the oviposition period of the second codling moth generation (July 13 and 20, 1995 and July 25 and August 2, 1996); and (3) T. platneri, reared at 15–25°C on codling moth eggs rendered nonviable through irradiation, released at 3000 female T. platneri/ha on May 17 and 23, 1996. A similar block of trees covering 25 m 2 in each orchard was used as a control. All parasitoids were released from five trees or from five pairs of trees located in the center of each plot (Fig. 1). Four trees or four pairs of trees positioned next to the release trees are hereafter referred to as ”adjacent“ trees and four trees or four pairs of trees on the corners of the plots are hereafter referred to as ”outside“ trees (Fig. 1). Grain moth-reared T. platneri were held at 15°C until they were used. In preparation for release, three samples were removed from the parasitized egg card, and the parasitoids were allowed to emerge at 25°C to determine percentage emergence and the sex ratio. The appropriate portions of parasitized cards necessary to provide 3000 female T. platneri per tree or pair of trees were divided into a small paper bag which contained a cotton wick dampened with a honey-water suspension, as well as a thin streak of honey. The top of each bag was folded over a string and stapled. The bags were incubated at 25°C until the parasitoids emerged, the bags were then tied into the center of the release trees in treatment plots and small holes were cut into the sides of the bags to allow the parasitoids to escape. To obtain T. platneri from codling moth eggs, T. platneri reared on grain moth eggs were purchased from Rincon–Vitova Insectaries, Inc. and allowed to emerge and mate in 4-L sealed plastic buckets with a honey-and-water-soaked cotton wick attached to the inside of each lid. Sheets of codling moth eggs, obtained from the Okanagan–Kootenay codling moth rearing
FIG. 1. Release (filled), adjacent inside (striped), and outside (criss-crossed) trees within 25-m 2 treatment blocks. (A) Standard and (B) high-density plantings.
facility (Osoyoos, British Columbia), were irradiated at 3.7 krad from a source of cobalt 60. Portions of the egg sheets, carrying approximately 82,500 eggs, were placed into each bucket of T. platneri and the buckets incubated at 15–25°C, 24 h L. After 48 h of exposure to the parasitoids, the egg sheets were transferred to parasitoid-free, 4-L sealed plastic buckets and incubated at similar temperatures. Five days after exposure to the parasitoids, a water soaked cotton wick was added to each bucket. Two days later the total eggs and percentage parasitism were determined from at least seven samples of 200 –300 eggs/bucket. A sample of T. platneri was allowed to emerge, and parasitized eggs, percentage emergence, sex ratio, and the number of adults/egg were determined. The appropriate portion of parasitized egg sheets required to provide 3000 T. platneri/tree upon release were partitioned and bagged before parasitoid emergence as described above. To monitor the population densities of T. platneri through the season, viable sentinel codling moth eggs were hung weekly, for 3-day periods, on each of the five release, four adjacent, and four outside trees or pairs of trees (Fig. 1) in the treatment and control blocks from May 1 until September 19 in both years. Sentinel egg
RELEASE OF T. platneri WITH STERILE CODLING MOTHS
cards included 25–50 viable codling moth eggs, ⱕ24 h postoviposition, on waxed paper, attached to a plastic label with a wire (1995). Many of the sentinel eggs were lost from June until September 1995, probably due to earwig predation. For this reason sentinel eggs were hung within 4 ⫻ 11 cm screen cages in 1996. Sentinel eggs were stored at 25°C for at least 1 week after they were retrieved, until parasitism was assessed. In 1996 sentinel obliquebanded leafroller (Choristoneura rosaceana L., Lepidoptera: Tortricidae) egg masses were also hung in the five central trees (Fig. 1) of treatment and control blocks. In both species of sentinel eggs, the incidence, rather than percentage parasitism, was used as an indicator of Trichogramma survival and fecundity because the number of Trichogramma wasps parasitizing a single egg card was not observed and the presentation of codling moth eggs provided an unnaturally large number of hosts. If a single egg on a sentinel egg card was parasitized, the card was considered parasitized. To estimate the incidence of codling moth eggs resulting from the release of sterile codling moths, 200 leaves on each of 24 trees within two of the orchard sites were inspected for codling moth eggs in 1996. Percentage fruit damaged by first-generation codling moth was assessed at the end of June each year. In 1995, all fruit were removed in June at the request of the Sterile Insect Release program, as the codling moth populations exceeded the limits set by the program. Twenty undamaged apples were then rehung on each of the trees in the treatment and control blocks to assess second-generation damage. In 1996, first-generation damage was assessed from all apples on each of the 13 trees/treatment. All fruit was removed in September in both years and total codling moth, leafroller, and eye-spotted budmoth, Spilonota occellana (Lepidoptera: Tortricidae), damage determined. After arcsin transformation, percentage means were compared using an ANOVA and Duncan’s multiple range test (SAS, 1985). Temperatures through the summer were obtained from the Pacific Agri-Food Research Centre’s daily records. RESULTS AND DISCUSSION
First Generation Releases. In both 1995 and 1996, sentinel eggs in all blocks receiving grain moth-reared T. platneri in the spring exhibited a high incidence of parasitism during the period of the release (Figs. 2 and 3). As expected, the incidence of parasitism was most evident in the trees in which Trichogramma were released (x ⫽ 0.80 ⫾ 0.22, 1995; x ⫽ 0.84 ⫾ 0.33, 1996). High incidence of parasitism was also found in adjacent (x ⫽
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0.78 ⫾ 0.24, 1995; x ⫽ 0.69 ⫾ 0.34, 1996) and outside (x ⫽ 0.64 ⫾ 0.30, 1995; x ⫽ 0.48 ⫾ 0.32, 1996) trees. In 1996, release of codling moth-reared T. platneri did not provide higher levels of parasitism of sentinel eggs than did grain moth-reared T. platneri (Fig. 3). In 1995, parasitism in control blocks (Fig. 2) was probably indicative of the movement of released Trichogramma through the orchard. Dispersal of Trichogramma is significantly affected by wind (Hendricks, 1967; Yu et al., 1984). T. minutum have been shown able to move a distance of at least five peach trees, separated by 5.4 m, in the course of 3 days (Schread, 1932) and Trichogramma semifumatum have moved as much as 600 m in alfalfa fields (Stern et al., 1965). For these reasons, four more-widely separated orchards were chosen for the test in 1996 and the level of parasitism within control plots was lower (Fig. 3). Parasitoid maintenance on orchard host eggs. Incidence of parasitism in the sentinel eggs decreased 1 week postrelease to 0 –15% (Figs. 2 and 3). Temperatures at this time ranged from 4.3 to 26.5°C in 1995 and from 4 to 24°C in 1996. Laboratory trials have shown grain moth-reared T. platneri to survive an average of 8.7 days at 5–10°C and 4.3 days at 10 –15°C (J.C., unpublished data). T. platneri reared on codling moth eggs at 15–25°C survived for an average of 25.4 days at 5–10°C and 14.1 days at 10 –15°C. Evidence that T. platneri propagated itself on nonviable codling moth eggs was expected to be seen through continued parasitism of the sentinel eggs after the release peak. Approximately 12 days after release (June 6, 1995; June 4, 1996) the incidence of parasitism in both Trichogramma release plots began to increase above parasitism in the control checks (Figs. 2 and 3), suggesting that some released Trichogramma had been able to reproduce in viable and/or nonviable codling moth eggs and were beginning to emerge and search for new host eggs. By June 15, 1995, sentinel eggs began to disappear. Earwigs were abundant in all of the plots and may have consumed sentinel eggs and/or very high summer temperatures (max ⫽ 34°C) may have caused the eggs to desiccate and flake off. In early September 1995, sentinel eggs were hung only during the daytime when earwigs did not appear to consume them and in 1996 the eggs were hung inside screen cages. Parasitism of sentinel eggs within release trees fluctuated between 0 and 38% from June to the oviposition of the second generation in July 1995 (Fig. 2). When sentinel eggs were held within screen cages in 1996, the incidence of T. platneri parasitism within release trees from June to the second generation in July was found to range from 0 to 25%, with no parasitism found for periods of 4 to 7 weeks (Fig. 3). Maintenance of T.
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FIG. 2.
Mean incidence of parasitism (1995) in sentinel codling moth eggs. (a) Release trees; (b) adjacent trees.
platneri in release and adjacent trees was minimal and higher in 1995 than in 1996. Apple damage. Damage from first-generation codling moth was significantly (P ⬍ 0.05) lower in blocks receiving T. platneri releases in May 1995 (Table 1). Damage levels were high in 1995, indicating that sub-
stantial numbers of wild codling moth and thus viable codling moth eggs were available for parasitism and maintenance of released T. platneri populations. Percentage codling moth damage was not significantly (P ⬎ 0.05) lower in blocks receiving T. platneri releases in May 1996 (Table 1). Wild codling moth
RELEASE OF T. platneri WITH STERILE CODLING MOTHS
FIG. 3.
Mean incidence of parasitism (1996) in sentinel codling moth eggs. (a) Release trees; (b) adjacent trees.
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TABLE 1 Percentage Codling Moth Damage after First and Second Generation in T. platneri Release and Control Plots (Four Replications) Mean percentage codling moth damage a,b Treatment release period
T. platneri host source
Release trees
Adjacent
Outside
First-generation assessment 1995 Spring Spring & summer Control 1996 Spring Spring Spring & summer Control
Grain moth Grain moth — Grain moth Codling moth Grain moth —
7.7 a (1591) 6.9 a (1761) 15.8 b (1538)
7.1 a (1127) 8.3 a (934) 21.9 b (1011)
7.4 a (693) 11.0 a (2029) 26.8 b (604)
0.0 a (2793) 0.04 a (2594) 0.06 a (2093) 0.0 a (2444)
0.07 a (1750) 0.05 a (2008) 0.0 a (1743) 0.0 a (1766)
0.08 a (1520) 0.13 a (2069) 0.0 a (1346) 0.0 a (1306)
Second-generation assessment 1995 Spring Spring & summer Control 1996 Spring Spring Spring & summer Control a b
Grain moth Grain moth — Grain moth Codling moth Grain moth —
31.5 a 35.8 a 50.5 b
(375) (386) (391)
0.5 a 0.1 a 0.2 a 1.3 b
(2875) (3105) (2075) (2118)
32.1 a 35.9 a 54.5 b
(294) (304) (309)
0.7 ab (2104) 0.5 a (2234) 0.2 a (1829) 1.4 b (1636)
35.9 a 36.9 a 49.1 b
(304) (310) (313)
1.4 b (1458) 0.1 a (2166) 0.2 a (1393) 1.1 ab (907)
Means within year and column followed by the same letter are not significantly different (Duncan’s multiple range test, P ⬍ 0.05). Total number of apples sampled in parentheses.
infestation levels were very low and damage was negligible in all plots. Second Generation Releases. In both 1995 and 1996, sentinel eggs in all blocks receiving grain moth-reared T. platneri in the summer exhibited an incidence of parasitism for the 3 (1995) or 4 (1996) week period following the July–August releases (Figs. 2 and 3). The mean parasitism over these weeks was most evident in the trees in which the Trichogramma were released (x ⫽ 0.39 ⫾ 0.34, 1995; x ⫽ 0.78 ⫾ 0.36, 1996); however, high mean levels of parasitism over these weeks were also displayed in the adjacent (x ⫽ 0.18 ⫾ 0.24, 1995; x ⫽ 0.54 ⫾ 0.35, 1996) and outside (x ⫽ 0.31 ⫾ 0.35, 1995; x ⫽ 0.64 ⫾ 0.42, 1996) trees. At harvest in 1995, 69 and 70% of codling moth eggs on fruit from trees receiving first-generation T. platneri releases, and first- and second-generation T. platneri releases, respectively, were parasitized. The viability of the unparasitized eggs was not determined. Parasitoid maintenance on orchard host eggs. The incidence of T. platneri parasitism on the sentinel egg card fluctuated between 0 and 38% after the secondgeneration releases in 1995 and between 0 and 13% after the second-generation releases in 1996. If the
parasitoid had increased within the orchards we could expect more evidence of its presence in the weekly sentinel egg survey. Only 29 codling moth eggs (of which 2 were parasitized) were located on the 4800 leaves inspected in 1996, suggesting that host densities were insufficient to allow the released parasitoids to maintain their populations above these low levels. Apple damage. Mean percentage codling moth damage after the second generation was significantly (P ⬍ 0.05) lower at harvest within blocks receiving both first-generation only and first- and second-generation T. platneri releases in 1995 (Table 1). This reduction in codling moth damage was seen within all trees within the treatment block. The damage levels at harvest in 1995 far exceeded the economic threshold for a commercial orchard; however, damage was undoubtably higher than normal due to the removal of the fruit from the rest of the orchard and the low number of fruit (20/tree) repositioned manually in the trees to allow an assessment of damage. Codling moth damage was significantly lower (P ⬍ 0.05) at harvest within blocks receiving all T. platneri treatments within the release trees in 1996 (Table 1). This significant (P ⬍ 0.05) reduction in codling moth damage found at harvest was also evidenced in fruit from adjacent trees in blocks receiving codling moth-
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TABLE 2 Percentage Summer Leafroller Damage in T. platneri Treated and Untreated Plots, September 1996 Assessment (Four Replications) Mean percentage sumer leafroller damge a,b Treatment release period
T. platneri host source
Release trees
Adjacent trees
Outside trees
Spring Spring Spring & summer Control
Grain moth Codling moth Grain moth —
2.31 a (2875) 1.42 ab (3105) 1.23 b (2075) 2.22 a (2118)
2.34 a (2104) 1.65 ab (2234) 1.13 b (1829) 1.95 ab (1636)
1.70 a (1458) 1.60 a (2166) 1.60 a (1393) 1.80 a (907)
a b
Means within column followed by the same letter are not significantly different (Duncan’s multiple range test, P ⬍ 0.05). Total number of apples sampled in parentheses.
reared T. platneri and spring- and summer-released grain moth-reared T. platneri (Table 1). However, only one of the four replicate orchards showed evidence of substantial wild codling moth populations. Mean percentage summer leafroller damage was significantly (P ⬍ 0.05) lower at harvest within the release trees receiving first- and second-generation T. platneri releases in 1996 (Table 2). It should be noted that summer leafroller damage was low in comparison to eye-spotted bud moth damage (4.5–11.7%) which was not significantly (P ⬎ 0.05) reduced by T. platneri releases. CONCLUSIONS
The original premise that T. platneri populations could be sustained when released in orchards where sterile codling moths are released has not been refuted; however, the extent to which the nonviable codling moth eggs resulting from the release of sterile moths support the T. platneri is unclear. From our limited egg search in sterile insect release orchards in August 1996, we calculated that the number of codling moth eggs available to maintain the released T. platneri (x ⫽ 0.6 egg/100 leaves, n ⫽ 24) is close to what we could expect from a sterile codling moth releases of approximately 1000 moths/ha/week. It should also be noted that oviposition from sterile x sterile codling moth matings result in fewer eggs than from fertile matings under laboratory conditions (Bloem et al., 1998). How many nonviable codling moth eggs are sufficient to maintain a Trichogramma population? With 3000 T. platneri released per tree, it seems unlikely that there would be sufficient nonviable codling moth eggs to maintain the released population at this high level. However, there would be an excellent chance of thorough parasitism of the eggs available. This would explain the increase in the mean percentage parasitism of sentinel eggs approximately 2 weeks after release, as it would take that long for a second generation of the T. platneri to emerge. T. platneri reared at 15– 25°C on codling moth eggs, which were expected to be
more vigorous and fecund at low spring temperatures, seemed to practically disappear after the high-release parasitism and 2-week postrelease increase as described above. We propose that T. platneri derived from codling moth did not exhibit an obvious advantage over the grain moth-reared T. platneri, as both treatments showed very high parasitism upon release. Similarly, high populations of T. platneri were maintained over 2 (1995) and 4 (1996) week periods after their release in July–August, after which the population numbers decreased and rose again as the next generation of Trichogramma emerged. Based on damage data from these field releases, we conclude that the release of T. platneri significantly decreased wild codling moth numbers within release trees. ACKNOWLEDGMENTS Partial funding for this work was provided by grants from the Washington State Tree Fruit Research Commission and by the U.S.D.A. Area-Wide Research Funding. The researchers are grateful for the support provided by the Sterile Insect Release Program, Osoyoos, British Columbia and by N. Klassen, Institute for National Measurement Standards, National Research Council of Canada, Ottawa, Ontario and appreciate the work of K. Thompson and P. Rydings. We thank G. J. R. Judd and M. J. Smirle for reviewing the manuscript. This paper is contribution number 1061 of the Pacific Agri-Food Research Centre, Summerland, British Columbia, Canada.
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