R. G. Van Driesche

Greenhouse Trials of Aphidius colemani (Hymenoptera: Braconidae) Banker Plants for Control of Aphids (Hemiptera: Aphididae) in Greenhouse Spring Floral Crops

Abstract Banker plants with Aphidius colemani Viereck were tested in greenhouses in Massachusetts and New York for control of cotton aphid Aphis gossypii Glover, and green peach aphid Myzus persicae (Sulzer) on 2 spring flower crops, pansies (Viola tricolor hortensis) and Marguerite daisies (Argyranthemum hybrid). Banker plants consisted of pots of barley plants infested with the bird cherry-oat aphid Rhopalosiphum padi (L.), inoculated at the start of the crop with adults of A. colemani purchased from a commercial insectary. Initial trials were conducted in University of Massachusetts greenhouses containing flats of the crop plants. Sentinel plants in flats were infested uniformly with aphids, and particular greenhouses were subjected to the presence of banker plants or left as controls. Prior to University trials, a survey was conducted in commercial greenhouses in Massachusetts and New York to determine the frequency and species of aphid infestation in spring flower crops. After University trials, the efficacy of banker plants was tested in commercial greenhouses in both states. In surveys of commercial greenhouses, M. persicae was the most frequently detected species, accounting for 53% of all infestations. In University greenhouse trials, in absence of parasitism, A. gossypii increased fastest on daisy, followed by M. persicae on daisy, M. persicae on pansy, and A. gossypii on pansy. Parasitoid suppression of population increase was strongest for A. gossypii on daisy and poorest for M. persicae on pansy. The presence of 2 aphid species in the same greenhouse did not alter the level of biological control in our trial. In commercial greenhouses, banker plants failed to control M. persicae deployed on infested pansies as sentinel hosts. In the laboratory, a 12-h exposure to dried residues of pyriproxyfen or pymetrozine, insecticides commonly used to control aphids, reduced survival of A. colemani adults, compared to a water control (82% survival), to 71% and 53%, respectively. Adult parasitoid emergence from pesticide-treated aphid mummies was reduced from 68% for the controls to 56% for pyriproxyfen and 62% for pymetrozine.

Introduced braconid parasitoids and range reduction of a native butterfly in New England

Abstract Pieris napi oleracea Harris is a native pierid butterfly that has suffered a range reduction in New England that began after the invasion of its range by the non-native congener Pieris rapae L. and one of its braconid parasitoids, Cotesia glomerata (L.). P. napi has nearly disappeared from Massachusetts, but remains common in northern Vermont. We investigated food plant abundance and Cotesia spp. larval parasitism as possible factors to explain the historical changes in P. napi ’s distribution. We found that the current range of P. napi was not explained by the abundance of its key first generation food plant (two-leafed toothwort, Cardamine diphylla [Michx.]). We also found that levels of Cotesia spp. parasitism in meadows in the second generation were similar in Vermont and Massachusetts. Further, we found that both C. glomerata and the related introduced Pieris spp. parasitoid Cotesia rubecula (Marshall) forage for hosts predominantly in sunny meadows and not in woods, where the first generation of P. napi occurs. We found that under field conditions in meadow habitats, C. glomerata parasitizes P. napi at higher rates than P. rapae . We postulate that the persistence of P. napi in Vermont and its disappearance in Massachusetts is caused by high parasitism of the second generation by C. glomerata in meadow habitats, coupled with a north–south cline in the rate of commitment of first generation P. napi pupae to diapause, such that northern populations act functionally as univoltine species developing in a parasitoid free habitat (woods), while southern populations acted as a bivoltine species and went extinct due to low survival in the second generation in meadows due to C. glomerata parasitism.

Biological Control Of Pieris Rapae in New England: Host Suppression and Displacement of Cotesia glomerata by Cotesia rubecula (Hymenoptera: Braconidae)

A survey of the imported cabbageworm, Pieris rapae (Lepidoptera: Pieridae), in cole crops in Massachusetts found that a Chinese strain of Cotesia rubecula (Hymenoptera: Braconidae), released in 1988, has spread and become the dominant parasitoid of this pest in central and western Massachusetts, with an average of 75% parasitism. The previously dominant parasitoid of this host, Cotesia glomerata (Hymenoptera: Braconidae), has been displaced and is now present only at trace levels (<1% of total parasitism).Abstract A survey of the imported cabbageworm, Pieris rapae (Lepidoptera: Pieridae), in cole crops in Massachusetts found that a Chinese strain of Cotesia rubecula (Hymenoptera: Braconidae), released in 1988, has spread and become the dominant parasitoid of this pest in central and western Massachusetts, with an average of 75% parasitism. The previously dominant parasitoid of this host, Cotesia glomerata (Hymenoptera: Braconidae), has been displaced and is now present only at trace levels (<1% of total parasitism).

Biological control of Bemisia argentifolii (Hemiptera: Aleyrodidae) on poinsettia with inundative releases of Eretmocerus eremicus (Hymenoptera: Aphelinidae) : do release rates affect parasitism ?

The effectiveness of inundative releases of the parasitoid Eretmocerus eremicus n. sp. Rose & Zolnerowich for control of Bemisia argentifolii Bellows & Perring on poinsettia in replicated experimental greenhouses was determined. We evaluated two release rates of E. eremicus: a low release rate (one female per plant per week, released in two greenhouses, in spring 1995) and a high release rate (three females per plant per week, released in two greenhouses, in spring 1994), each over a 14 week growing season. Each release trial had either one (1995) or two (1994) control greenhouses in which B. argentifolii developed on poinsettia in the absence of E. eremicus . Life-tables were constructed for B. argentifolii in the presence and absence of E. eremicus by using a photographic technique to follow cohorts of whiteflies on poinsettia leaves. Weekly population counts of whiteflies were also made. In the absence of E. eremicus , egg to adult survivorship of B. argentifolii on poinsettia was 75–81%. At the low release rate, egg to adult survivorship of B. argentifolii was 12% and parasitism was 34%. At the high release rate, egg to adult survivorship of B. argentifolii was 0.9% and parasitism was 10%. The average net reproductive rates (R o ) for populations of B. argentifolii in the absence of E. eremicus ranged from 20.5 to 26.1, indicating a rapidly increasing population density. Net reproductive rates for whitefly populations subject to parasitoid releases were 3.7 in the low release rate greenhouses, and 0.25 in the high release rate greenhouses, indicating substantially reduced B. argentifolii population growth. At week 14 of the trial, densities of immature whiteflies were lower in greenhouses at the low release rate when compared to the high release rate greenhouses. This was attributed to high levels of in-house reproduction by parasitoids at the low release rate.

Laboratory and field host preferences of introduced Cotesia spp. parasitoids (Hymenoptera: Braconidae) between native and invasive Pieris butterflies

Abstract In laboratory tests, Cotesia glomerata (Hymenoptera: Braconidae) exhibited a clear preference in small cage tests for first or second instars of the native butterfly Pieris napi oleracea (Lepidoptera: Pieridae) vs larvae of the invasive non-native species Pieris rapae (Lepidoptera: Pieridae), under both choice and no-choice test designs. Under the same conditions, Cotesia rubecula (Hymenoptera: Braconidae), either showed no preference (no-choice test) or preferred P. rapae (choice test). These laboratory data predict that both of these Cotesia species should attack P. napi oleracea and thus under modern biological control protocols, both should be rejected as candidate biological control agents (if they were being currently considered for introduction, rather than as is the case, already introduced, in North America). The predicted attack by C. glomerata on P. napi oleracea under field conditions was confirmed by field choice tests in which C. glomerata attack rates on P. napi were found to be fivefold greater than on P. rapae. In contrast, in the same field-based choice tests, attacks on P. napi by C. rubecula were never observed, even when and where attacks on P. rapae were consistently observed. This lack of attack on P. napi oleracea is unexplained at present and suggests a need for better understanding of the influences present in laboratory tests that are able to affect estimates of parasitoid host ranges. Such improvements are critical for future enhancement of safety in classical biological insect control.

Classical biological control of environmental pests.

Exotic species commonly invade areas of conservation concern. Such species may threaten native species or ecosystems, either attacking individual species, or changing ecosystem characteristics in ways that make them less suitable for the continued existence of one or more native species. Among the potential effects of exotic species are crowding, changes in water table levels, fire frequency or intensity, altered soil fertility or chemistry, and altered levels of predation or disease. Chemical, mechanical and biological methods each may be used to control exotic species in some cases. Chemical and mechanical methods are difficult to apply to large areas and must be repeated periodically to prevent pest resurgence. Classical biological control often has high initial costs but is permanent in nature and self propagating, such that large areas can be treated economically. Risks of biological control are minimal if agents are appropriately screened to determine host range prior to introduction and if introductions are conducted using appropriate quarantine procedures. Biological control is a useful approach for control of a variety of kinds of environmental pests that threaten the conservation of native species and ecosystems, including exotic plants, herbivorous and predacious arthropods, other invertebrates, and in some instance vertebrates.

Classical Arthropod Biological Control: Measuring Success, Step By Step

Classical biological control of invasive species of arthropods is a well established discipline that has a long and distinguished record (DeBach, 1964; Huffaker and Messenger, 1976; Clausen 1978; Van Driesche and Bellows, 1996; Bellows and Fisher, 1999). Laws governing the conduct of classical biological control vary by country, or may not exist at all. An international code of conduct for the practice of natural enemy introductions has been developed by the Food and Agriculture Organization of the United Nations and can be consulted for an overview of good practice (Anon., 1997).

COMPATIBILITY OF SPINOSAD WITH PREDACIOUS MITES (ACARI: PHYTOSEIIDAE) USED TO CONTROL WESTERN FLOWER THRIPS (THYSANOPTERA: THRIPIDAE) IN GREENHOUSE CROPS

Abstract Releases of predacious mites are recommended for use in greenhouse flower crops for suppression of western flower thrips, Frankliniella occidentalis (Pergande). Control from predacious mites alone, however, is not adequate and must be supplemented with the use of insecticides. The principal material currently used by growers in the northeastern United States for western flower thrips control is spinosad (Conserve®). In laboratory tests on direct toxicity, we found that fresh residues (2 h) of this material were not toxic to motile stages of Neoseiulus (=Amblyseius) cucumeris (Oudemans) (74 vs 78% survival for the treated group and the untreated water controls, respectively), the principal species of predacious mites used for control of western flower thrips, but did lower survival of Iphiseius degenerans (Berlese) (56 vs. 73% survival for the treated group and the untreated water controls, respectively). There were no differences for either species from exposure to older (24 h) residues. In contrast, using the same assay we observed 10 and 3% survival of first instar and adult western flower thrips. We found no indication of that either mite species was repelled by freshly dried (2 h post application) residues of this compound. Spinosad did, however, reduce oviposition of mites when confined in glass vials with pollen, a water source, and pesticide-treated foliage. Oviposition in the first 24 h period after confinement was not affected but in the second and third days, it was reduced by 48 and 76% for N. cucumeris and 41 and 70% for I. degenerans, compared with oviposition in the same periods by mites in untreated vials. These data indicate that the use of spinosad may not be compatible with releases of these predacious mites in a western flower thrips suppression program.

Field measurement of population recruitment of Apanteles glomeratus (L.) (Hymenoptera: Braconidae), a parasitoid of Pieris rapae (L.) (Lepidoptera: Pieridae), and factors influencing adult parasitoid foraging success in kale

The attack rate by the parasitoid Apanteles glomeratus (L.) on laboratory-reared larvae of Pieris rapae (L.) exposed for 3–4 day periods in a kale field in Massachusetts was greater when five larvae rather than two were placed on plants. The attack rate was greatest if host larvae were in the first instar when placed in the field, and little or no attack occurred when second- or third-instar larvae were exposed. The co-occurrence of unoccupied P. rapae larval feeding sites on plants where larvae were exposed reduced attack rates. Parasitism rates in trap-host larvae and in field-collected larvae (counting only cases in which the parasitoid was still in the egg stage) did not differ as estimators of recruitment to the population of parasitized hosts either in terms of total recruitment achieved per host generation or in the temporal pattern of the recruitment. In both simple and multiple linear regressions, the density of young P. rapae larvae (either parasitized or not) was the strongest correlate of parasitoid recruitment for the whole season, whereas average air temperature was the strongest correlate in the last month of observations (September).

ESTABLISHMENT OF A CHINESE STRAIN OF COTESIA RUBECULA (HYMENOPTERA: BRACONIDAE) IN THE NORTHEASTERN UNITED STATES

Cotesia rubecula (Marshall) is a braconid parasitoid of Pieris spp. larvae that is relatively specific to Pieris rapae (L.) (Lepidoptera: Pieridae), a pest of cabbage and related cole crops. The establishment of this parasitoid in the eastern United States to help suppress this garden pest has been long sought. Efforts to establish it in North America have a complex history. A self-introduced population of uncertain origin was discovered on Vancouver Island in British Columbia in 1963 (Wilkinson 1966), and the range of this population has extended as far south as Oregon (Biever 1992). This strain was later released in Missouri, New Jersey, South Carolina, and Ontario (near Ottawa) (Puttler et al. 1970; Williamson 1971, 1972). This strain appears not to have established in Missouri (Parker & Pinnell 1972), but may have established in Ontario (Corrigan 1982). Poor establishment of this strain was attributed to an improperly timed diapause induction response (Nealis 1985). A second population, from the former Yugoslovia, was released in Missouri in the mid 1980s, and subsequently released in Virginia and Ontario. In 1988, the Yugoslavian strain was recovered in Virginia, but this population later appeared to have died out, perhaps due to high level of hyperparasitism (McDonald & Kok 1991). In 1993, C. rubecula, of uncertain origin, was found to be the dominant parasitoid in Quebec, in farming areas near Montreal (about 160 km east of Ottawa) (Godin & Boivin 1998). In 1988, a population of C. rubecula was collected by David Reed of the USDA in Shenyang, China (42 north latitude, 123 east longitude), for release in the eastern United States. This location matched the intended release location in Massachusetts in latitude, and both locations have continental type climates. Parasitized host larvae (P rapae) were shipped to the USDA quarantine laboratory in Newark, Delaware. Adult parasitoids were allowed to emerge and, following confirmation of species identity, 99 female and 49 male C. rubecula adults from this shipment were shipped to the senior author in Amherst, Massachusetts in July of 1988 and all were released in field cages in a pesticide-free, 0.1 ha collard plot in Deerfield, Massachusetts (42 n. 1.). That C. rubecula was not present at this site before the release (through spread, perhaps from some distant source) is demonstrated by the absence of C. rubecula in large numbers of hosts collected at this location and dissected for parasitism rates in a population dynamics study I ran in 1985 and 1986 (Van Driesche 1988). We subsequently reared this strain both in the laboratory and from field-collected larvae between 1988 and 1993 and made 12 other releases in Massachusetts, three in Connecticut, and one in Rhode Island, for 17 release locations in total (Fig. 1, two sets of MA sites overlap on map). Same-year recoveries of the parasitoid were made at seven of these sites, and recoveries were made after one or more years at seven other sites. Among the seven sites at which recoveries were made in subsequent years, we observed the parasitoid at three sites one year after release and at single sites 2, 3, 5, and 8 years after last release. Recovery efforts varied in different years and not all sites were visited yearly. To assess spread away from release sites, we periodically collected groups of P rapae larvae from non-release locations. We have recovered C. rubecula from 13 non-release sites, from just north of Hartford, Connecticut to Craftsbury, Vermont (north of St. Johnsbury) (Fig. 1). Recoveries have been made both along the Connecticut River Valley and in various locations in the Litchfield Hills in Connecticut, the Berkshire Hills in Massachusetts, and the Champlain Valley of Vermont. Towns in which recoveries have been made either at non-release sites or, if a release site, one or more years after the release include Winsor and Falls Village, Connecticut; Williamstown, Lanesboro, Westhampton, Northampton, Amherst, Hadley, Deerfield, Northfield, and Barre, Massachusetts; and Stamford, Rockingham, Hartland, South Royalton, Plainfield, Burlington, and Craftsbury, Vermont (Fig. 1), all of which indicate extensive range expansion in both agricultural valleys and adjacent forested hill country. Recoveries throughout Vermont bring the known range of C. rubecula near the Canadian border. Godin and Boivin (1998)s report of recovery of C. rubecula of uncertain origin in southern Quebec, seen in the light of the data presented here, may be a further northward extension of the Chinese population, rather than an eastward extension of releases from near Ottawa. This is uncertain, as no molecular markers have been identified to separate these populations. Because establishment of C. rubecula has been associated with declines in density of the other introduced P. rapae parasitoid, Cotesia glomerata (L.), in Oregon and Washington (Biever 1992), we also counted numbers of P rapae larvae and Cotesia parasitoid cocoons (as single cocoons for the solitary species C. rubecula and as cocoon groups for the gregarious species C. glomerata) on entire