Laboratory Assessment of the Effects of Bacillus Thuringiensis on Native Lepidoptera
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BIOLOGICAL CONTROL Laboratory Assessment of the Effects of Bacillus thuringiensis on Native Lepidoptera 1 2 3 3 JOHN W. PEACOCK, DALE F. SCHWEITZER, JANEL. CARTER, AND NORMAND R. DUBOIS Environ. Entomol. 27(2): 450-457 (1998) ABSTRACT The effect of 2 formulations of Bacillus thuringiensis subsp. kurstaki (Foray 48B and Dipel 8AF) was evaluated on 42 species of native Lepidoptera in laboratory bioassays using instars that are present in the field at the time of gypsy moth suppression applications. Mortality was significant for 27 of the 42 species evaluated against Foray 48B, and 8 of 14 species evaluated against Dipel 8AF. Susceptible species were noted in 5 of 6 families assayed-Papilionidae, Nymphalidae, Geometridae, Lasiocampidae, Satumiidae, and Noctuidae. The 1 species treated in the Lymantriidae family was not susceptible to B. thuringensis. Treated individuals that survived for a week were likely to reach adulthood. Intrageneric differences in susceptibility to B. thuringiensis were recorded among 8 species of Catocala and 3 species of Lithophane assayed. Of the 18 species assayed as 1st or 2nd instars, mortality was significant, usually exceeding 95%. By contrast, 9 of 11 species not susceptible to B. thuringiensis were assayed as penultimate or ultimate instars. However, species susceptible to B. thuringiensis were found in both early and late instars. KEY WORDS Bacillus thuringiensis, nontarget Lepidoptera, microbial control Bacillus thuringiensis subsp. kurstaki is one of the in ication program. Sample et al. (1996) also reported a secticides most commonly used to control forest insect significant reduction in species abundance and rich pests. B. thuringiensis has been used extensively in ness in both larval and adult nontarget Lepidoptera suppression and eradication programs against gypsy from field studies in eastern West Virginia. In west moth, Lymantria dispar (L.). From 1980 to 1993, > 1.9 central Virginia, Wagner et al. (1996) found that the million ha (4.9 million acres) were sprayed with B. abundance of micro- and macrolepidopteran caterpil thuringiensis. In 1994, > 151,000 ha were treated with lars was consistently lower in treated plots. However, B. thuringiensis, including >57,000 ha in Michigan and the differences were modest, and nearly every lepi 20,000 ha in both Pennsylvania and Maryland. In 1994, dopteran species recovered within a year of treat B. thuringiensis was used on >55% of the area sprayed ment. James et al. (1993) demonstrated that B. thu for gypsy moth suppression (Anonymous 1994). Be ringiensis is toxic to late, but not early, instars of the sides suppression activities aimed at the European cinnabar moth, Tyria jacobaeae (L.), an introduced gypsy moth, eradication efforts for both the European biocontrol agent. and Asian strain of the gypsy moth also occur yearly. Significant reductions in numbers of larvae of non In 1992, efforts to eradicate the Asian gypsy moth in target lepidopterans following the use of B. thurin certain locations in Oregon, Washington, and the Van giensis can indirectly affect other animals that rely on couver area ofBritish Columbia resulted in >67,000 ha lepidopterous larvae as a primary source of food. Ro being sprayed with B. thuringiensis (Anonymous denhouse and Holmes (1992) found that a significant 1992). In 1994, >56,000 ha were sprayed near Wil reduction in biomass oflarvae following B. thuringien mington, NC, in attempts to eradicate the Asian gypsy sis application led to significantly fewer nesting at moth (McGovern 1994). tempts by certain birds. Bellocq et al. (1992) showed Although there is a growing concern over the non that the use of B. thuringiensis increased emigration target effects of B. thuringiensis, there has been limited rates and caused dietary shifts in shrews in treated research aimed at determining its effects on native areas. North American species of Lepidoptera. In Oregon, Krieg and Langenbruch (1981) presented an exten Miller (1990) demonstrated that both richness and sive summary of the toxicity of B. thuringiensis to diversity of native Lepidoptera associated with Garry Lepidoptera, which suggests extremely broad impacts oak, Quercus garryana Dougl., were reduced following within the order. Navon (1993) reported on bioassay treatment of oak habitat as part of a gypsy moth erad- techniques and results for various agricultural and forest lepidopteran pests. Faust and Bulla (1982) re 1 U.S. Forest Service, retired. Current address: 185 Benzler Lust ported on the susceptibility of 57 lepidopteran species, Road, Marion, OH 43302. most of which also were agricultural and forest pests. z The Nature Conservancy, 1761 Main Street, Port Norris, NJ 08349. Again, broad taxonomic effects were evident within 3 U.S. Forest Service, Northeastern Forest Experiment Station, Northeastern Center for Forest Health Research, 51 Mill Pond Road, the order. Most bioassays have been conducted to Hamden, Cf 06514. determine the susceptibility of B. thuringiensis to lepi- Aprill998 PEACOCK ET AL.: AssESSMENT OF B. thuringiensis ON NATIVE LEPIDOPTERA 451 dopterous pests, but there have been few attempts to other host (usually oak) for the assays. These included evaluate the toxicity of B. thuringiensis against native, all Sericaglaea, Chaetaglaea, Eupsilia, Orthosia, Am nontarget species in the laboratory. We report the phipyra, and Alsophila. Oligophagous and monopha results of laboratory bioassays aimed at determining gous species were reared and assayed on the same the effect of B. thuringiensis on larvae of native, non species. target Lepidoptera. Larvae were bioassayed in an instar in which they occur in the field at the time when B. thuringiensis applications typically are scheduled. To obtain appro Methods Materials and priate instars for assay, all adults and eggs were held Selection of Species. Forty-two species of native outdoors in a screened, shaded enclosure at Port Nor Lepidoptera were evaluated in the laboratory assays. ris, Cumberland County, New Jersey, to ensure nor These included 1 papillionid species, 3 nymphalids, 7 mal eclosion times. Except for species assayed as 1st or geometrids, 1 lasiocampid, 3 saturniids, 1 lymantriid, 2nd instars, larvae were reared outdoors in muslin and 26 noctuids. Most of these are forest species sym sleeves. For most species, wild larvae of similar age patric with gypsy moths and, more importantly, are were observed at the rearing site. present as larvae at the time B. thuringiensis is applied Gypsy moth larvae from the continuous laboratory to control gypsy moth. Actias luna (L.), Antheraea culture maintained at the Northeastern Forest Exper polyphemus (Cramer), Eutrapela clemataria (J. E. iment Station at Hamden, CT, were reared on syn Smith), and Papilio glaucus (L.) also were assayed to thetic diet (BioScrv, Frenchtown, NJ) before the as add taxonomic diversity, although some spring brood says. larvae of these species usually hatch late enough to Treatment of Foliage, Bioassay Procedure. Foliage escape impact from B. thuringiensis applications. treatments consisted of undiluted applications of Larval Collections and Rearing. Larvae of most of Foray 48B or Dipcl8AF formulations of B. thuringien the species that we evaluated were reared from field sis subsp. kurstaki to potted seedlings or foliage bou collected ova or from ova obtained from wild females quets at rates equivalent to the aerial application of 89 that were taken at bait or light most often in southern (Foray) or 99 (Dipcl) BIU/ha in field programs. All New Jersey. In most assays, larvae were the progeny species were assayed against Foray, and 14 of the 42 of a single female. If progeny of 2 females were used, species also were assayed against Dipel. Multiple as offspring were similarly represented in the control and says for a species were conducted in different years treatment lots. Most of the Abagrotis alternata (Grote) with different batches of Foray. Bioassays with 2nd were collected as wild late instars; the 1993 Malaco and 4th-instar gypsy moth on treated and untreated soma disstria Hubner were collected as wild third foliage on each bioassay date confirmed the insecti instars. Details of!arval collections and rearing can be cidal activity of the Foray and Dipel preparations. obtained from D.F.S. The pesticide was appli ed using a pro-mist system Larvae were assayed on a plant species (or at least with a mini-Beecomist nozzle (Beecomist, Telford, genus in the case of oak feeders) that is a known host PA) rotated at 12,000 HPM to generate drops at 75-125 in the field. Polyphagous species that commonly use units VMD in a cylindrical spray tower (Hubbard and oaks were usually assayed on oaks because they are Lewis 1973) . The tower was =2.5 min diameter and often dominant or codominant in forests sprayed for 4 m high, with th e nozzle positioned in the center of gypsy moth control. Species not assayed on potted red the tower at a height of = 3.5 m above the plant ma oaks (usually Quercus rubra) and the food plants used terial to be treated. Foliage bouquets or potted seed are as follows: Papilio glaucus, Limenitis arthemis (F.), lings were placed on a rotating table that revolved 4 Euchlaena obtusaria (Hubner), Eupsilia vinulenta times during the ]-min spray period. Kromecote spray (Grote), Lithophane unirrwda (Lint), and L. petulca cards (Mcac.l. Dayton, OH) were placed next to each Grote on potted Prunus serotina; L. lemmeri (B & seedling or bouquet to monitor droplet size and dis Benjamin) on Juniperus virginian a bouquets; Ennomos tribution. For this spray procedure, the average num magnaria Guenee, Eutralepa clemataria, Lithophane ber of drops/ em2 generally ranges from 60 to 300 grotei Riley, and Sunira bicolorago (Guenee) on pot (N.R.D, unpublished data) An autoclaved sample of ted Acer rubrum; Actias luna, Catocala obscura Foray 48B was applied at a rate equivalent to 89 Strecker, and C. vidua (J. E. Smith) on Carya ovata BIU/ha to suitable host foliage and bioassayed against bouquets; C.