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COMMUNITY AND ECOSYSTEM ECOLOGY Lepidopteran Communities in Two Forest Ecosystems During the First Gypsy Moth Outbreaks in Northern Michigan TIMOTHY T. WORK1, 2 AND DEBORAH G. MCCULLOUGH2, 3 Environ. Entomol. 29(5): 884Ð900 (2000) ABSTRACT We assessed lepidopteran communities in replicated stands representing two hardwood forest ecosystems in northern Michigan during a 3-yr period that coincided with the Þrst gypsy moth outbreaks experienced by this area. Adult Lepidoptera were collected at 4-wk intervals each summer in 1993Ð1995 in eight forest stands. Four stands were classiÞed as ecological landtype phase (ELTP) 20, and they were dominated by oaks (Quercus spp.), a favored host of gypsy moth, Lymantria dispar (L.). The other four stands were classiÞed as ELTP 45, and they were dominated by northern hardwood species with few preferred hosts of gypsy moth. Gypsy moth populations and defoliation ßuctuated dramatically in ELTP 20 stands during the 3 yr, reaching outbreak levels in at least one year in all four stands. In ELTP 45 stands, gypsy moth populations and defoliation were minimal. More than 12,000 adult Lepidoptera representing 453 taxa were collected from the eight stands. Lepidopteran species composition differed signiÞcantly between ELTPs for species collected in early season months (May and June), but not for late season months (July and August). Within ELTP 45 stands, abundance and species richness of Lepidoptera were not affected by differences between years, stands, or the interaction of the two factors. In ELTP 20 stands, the interaction of stand and year affected overall lepidopteran abundance and diversity of late season species. Species composition of late season lepidopteran communities in ELTP 20 stands may have been affected by gypsy moth population ßuctuations, although patterns were not consistent in all years. A subset of oak-feeding species appeared to be negatively affected during outbreak years, but other native Lepidoptera appeared to be resilient, perhaps reßecting the spatially and temporally limited duration of gypsy moth outbreaks. KEY WORDS gypsy moth, forest insect communities, biological diversity, exotic species invasion, ecological classiÞcation INSECTS AND RELATED arthropods account for a high proportion of species diversity in forest ecosystems, and play critical roles in many ecological processes. Insects serve as prey for other animals, and are involved in decomposition and nutrient cycling, pollination, predation and parasitism of potential pest insects, and regulation of forest productivity (Mattson and Addy 1975, Schowalter and Crossley 1984, Probst and Crow 1991, Kremen 1994). Despite their ecological importance, insects are frequently excluded from surveys of biological diversity in forest ecosystems because of the difÞculty and time needed to sample, process, and identify insects to species level (Biological Survey of Canada 1994). Without baseline information on the species composition, diversity and abundance of insect communities in forest ecosystems, effects of natural or anthropogenic disturbances are difÞcult to document or predict. In many national forests in the United States, ecological classiÞcation systems have been developed that 1 Current address: Department of Biological Sciences, CW 405, Biological Sciences Building, University of Alberta, Edmonton, AB T6G-2E9. 2 Department of Entomology, Michigan State University, 243 Natural Science Building, East Lansing, MI 48824 Ð1115. 3 Department of Forestry, Michigan State University, 243 Natural Science Building, East Lansing, MI 48824 Ð1115. integrate soil, climatic, vegetation, and physiographic features into hierarchical units (Barnes et al. 1982; Bailey 1987; Host et al. 1987, 1988; Sims et al. 1996). Maps of these ecological units can be used to estimate potential productivity of speciÞc sites or identify appropriate management options based on the quality and characteristics of a site (Host et al. 1993, Sims et al. 1996). Such a classiÞcation system could also be useful in evaluating effects of disturbance on forest insect communities if insect communities that are consistently associated with speciÞc ecological units can be identiÞed. Establishment of exotic insect species represents one type of disturbance with potentially long-term and broad consequences for native insects in forest ecosystems (Liebhold et al. 1995b, Niemela and Mattson 1996). Forest invaders can displace native species by altering availability and quality of food resources or habitat, and affecting predator-prey interactions. Use of insecticides, or introductions of generalist biological control agents to control exotic species (Howarth 1991, Simberloff 1992, NaÞus 1993), can also potentially affect nontarget insects. Invasion of gypsy moth, Lymantria dispar (L.), a major defoliator of oak (Quercus spp.), aspen (Populus spp.) and many other species, and subsequent management activities during gypsy moth outbreaks, may 0046-225X/00/0884Ð0900$02.00/0 䉷 2000 Entomological Society of America October 2000 WORK AND MCCULLOUGH: LEPIDOPTERAN COMMUNITIES IN TWO FOREST SYSTEMS create a situation of double jeopardy for native lepidopteran communities. Currently, gypsy moth management in most states centers on application of the microbial insecticide Btk (Bacillus thuringiensis variety kurstaki) to eradicate new gypsy moth infestations or to suppress gypsy moth outbreaks in generally infested areas (Reardon et al. 1994). Recent studies addressed the effects of Btk on native, nontarget species and found that many species of Lepidoptera are susceptible to Btk, although the extent and duration of impacts vary (Miller 1990a, Miller 1990b, Johnson et al. 1995, Lih et al. 1995, Sample et al. 1996, Wagner et al. 1996, Papp-Hermes et al. 1997, Peacock et al. 1998). Less consideration has been given to the impacts of gypsy moth on native species in the absence of Btk suppression programs or other management activities, despite recognition of the need for these kinds of data (Peacock et al. 1993, 1998; Wagner et al. 1996). Intuitively, establishment of gypsy moth populations and subsequent outbreaks could affect native Lepidoptera by depleting foliage available for larval feeding (Wagner et al. 1996), inducing allelochemical defenses in some host plants (Schultz and Baldwin 1982, Hunter 1987, Karban and Myers 1989, Faeth 1992, Wold and Marquis 1997), or altering species composition or abundance of natural enemies (Elkinton et al. 1990, Gould et al. 1990, Williams et al. 1992, Ferguson et al. 1994). Severe defoliation also increases light penetration, affecting microclimatic conditions that may in turn, impact diversity or composition of native species (Work 1996). Here we report results from a 3-yr Þeld study of adult Lepidoptera in forested stands in northern lower Michigan. Our Þrst objective was to acquire baseline data on the abundance, species diversity, and species composition of native Lepidoptera in two hardwood ecosystems, one dominated by oaks and the other dominated by northern hardwoods. Second, we evaluated impacts of high gypsy moth populations on native lepidopteran communities in the oak-dominated ecosystem during the Þrst gypsy moth outbreak these stands experienced. Changes in native lepidopteran species composition over time, between ecosystems, and between defoliated and undefoliated stands were assessed using multivariate community classiÞcation techniques. Materials and Methods Study Sites. This research was conducted in eight stands in the Manistee portion of the Huron-Manistee National Forest in northwestern lower Michigan. The Manistee National Forest has been mapped using an ecological classiÞcation system (Cleland et al. 1993). The ecological classiÞcation system is a hierarchical classiÞcation that groups ecosystem components at spatial scales varying from the landscape to the standlevel. Ecological landtype phases, referred to as ELTPs, are delineated on the basis of soils, landscape position, and natural vegetation, and are subsets of larger spatial scale units such as ecological landtypes and landtype associations (Barnes et al. 1982; Bailey 885 1987; Host et al. 1987, 1993; Sims et al. 1996). Because stands within the same ELTP have similar overstory and understory vegetation, soil type and hydrology, nitrogen cycling, productivity, and geological history, use of the ecological classiÞcation system allowed us to select replicates of “ecosystems” across space and time with a high level of conÞdence that our experimental sites were as similar as possible. We randomly chose four stands classiÞed as ELTP 20 and four stands classiÞed as ELTP 45 from ecological classiÞcation system maps provided by the Manistee National Forest. All stands ranged from ⬇12Ð16 ha in area. ELTP 20 stands are characterized by an overstory dominated by northern red oak (Quercus rubra L.) and white oak (Quercus alba L.), both of which are highly preferred hosts for gypsy moth (Mauffette et al. 1983, Liebhold et al. 1995a). Soils in the ELTP 20 stands are classiÞed as overwashed moraines with sandy soils, (mixed, frigid Entic Haplorthods at the family level), and some spodic horizon development (Cleland et al. 1993). Ground ßora includes mapleleaf viburnum (Viburnum acerifolium L.), bracken fern (Pteridium aquilinum L.), red maple (Acer rubrum L.) seedlings, juneberry (Amelanchier spp.), and Carex spp. Two stands, 2.4 km apart, were located at ⬇44⬚ 00⬘ N, 86⬚ 00⬘ W near the town of Branch, MI, and two stands, 1.5 km apart, were located at roughly 44⬚ 08⬘ N, 86⬚ 09⬘ W near the town of Freesoil, MI. ELTP 45 stands have an overstory dominated by sugar maple (Acer saccharum Marsh) and lesser components of white ash (Fraxinus americana L.), American basswood (Tilia americana L.), and red maple (Acer rubrum L.). Other species, including black cherry (Prunus serotina Ehrh.), beech (Fagus grandifolia Ehrh.), and trembling aspen (Populus tremuloides Michx.), are occasionally present. Most overstory tree species in ELTP 45 stands are nonpreferred host plants of gypsy moth (Liebhold et al. 1995a), although a few preferred species such as American basswood and aspen are present. Soils are well to moderately welldrained morainal sands with 5Ð7% clay and 5Ð10% silt, and Þne-textured substrata (Cleland et al. 1993). ELTP 45 stands have notably high productivity and nitrogen availability (Zak et al. 1986; Host et al. 1987, 1988; Zak et al. 1989) and are characterized by a diverse and abundant ground ßora including wild leek (Allium tricoccum), sweet cicely (Osmorhiza spp.), and various other species (Cleland et al. 1993). Two stands, 1 km apart, were located at roughly 44⬚ 22⬘ N, 86⬚ 44⬘ W near Mesick, MI, and two stands, 1.6 km apart, were located at 44⬚ 19⬘ N, 86⬚ 44⬘ W near Harrietta, MI. Gypsy Moth Populations. Gypsy moth populations began expanding through much of northern lower Michigan in the late 1980s and early 1990s (Gage et al. 1990). Aerial videography maps of gypsy moth defoliation provided by the Huron-Manistee National Forest and the Michigan Department of Natural Resources indicated that no gypsy moth defoliation occurred in the stands we studied until 1993, which was consistent with our own observations during visits to this area in 1992 (D.G.M., unpublished data, Huron- 886 ENVIRONMENTAL ENTOMOLOGY Manistee National Forest 1992). From 1993 to 1995, gypsy moth became established in localized areas of the Manistee forest, causing moderate to high defoliation in some stands. Outbreak-level populations typically persisted for 1Ð2 yr, then subsided (F. Sapio, MI, DNR, unpublished data; S. Katovich, USDA Forest Service, NA State and Private Forestry, unpublished data). By 1996, gypsy moth populations in northern Michigan had largely collapsed and defoliation was not observed in the Huron-Manistee National Forest. We estimated the size of gypsy moth populations each year using mean egg mass counts from four to Þve 0.01-ha plots randomly located in each stand (Kolodny-Hirsch 1986). Because gypsy moth egg masses can remain evident for one or more years after larval eclosion, the ratio of uneclosed egg masses to total egg masses was also determined for egg masses up to 3 m high on tree stems. The total number of egg masses observed was then multiplied by the proportion of uneclosed egg masses to estimate current-year gypsy moth population density. Defoliation was visually estimated in each stand as high (76 Ð100%), moderate (51Ð75%), low (26 Ð50%), and negligible (⬍25%) during each of our lepidopteran sampling periods (see below). Defoliation was also quantiÞed in 1994 and 1995 using a portable PAR sensor (Sunßeck Ceptometer Model SF-80) (Decagon Devices, Inc., Pullman, WA) to estimate leaf area index (Pierce and Running 1988) in defoliated and undefoliated stands as part of a related study (Work and McCullough 1996). Eight PAR samples were taken with the ceptometer held parallel to the ground, ⬇1 m above the forest ßoor, at 45⬚ angles until a complete 360⬚ was sampled. Readings were then averaged and stored in a portable data recorder. This was repeated at 10-m intervals along each of four 100-m transects radiating in the cardinal directions from the center of the stand. Lepidoptera Collection. Adult Lepidoptera were collected in each stand at roughly 4-wk intervals during the summers of 1993, 1994, and 1995. Sampling dates were selected to correspond with important periods in gypsy moth phenology and were based on phenological development of vegetation in the stands, which was typically 1 wk more advanced in ELTP 20 stands than in ELTP 45 stands. Lepidoptera were collected in mid-May, when Btk is typically applied for gypsy moth suppression, in June when most gypsy moth larvae were fourth instars, in July at peak defoliation, and in August after refoliation. Sampling was delayed until the following day if rain or high winds occurred. In 1993, insects were collected on 12Ð13 May, 15Ð17 June, 13Ð15 July, and 10 Ð12 August from ELTP 20 stands, and on 21Ð22 May, 22Ð23 June, 20 Ð22 July, and 18 Ð20 August from ELTP 45 stands. In 1994, insects from ELTP 20 stands were collected on 10 Ð12 May, 15Ð16 June, 11Ð13 July, and 9 Ð10 August, and from ELTP 45 stands on 18 Ð20 May, 20 Ð21 June, 19 Ð20 July, and 15Ð17 August. In 1995, collection dates were 15Ð17 May, 12Ð14 June, 10 Ð11 July, and 15Ð16 August in ELTP 20 stands and 22Ð24 May, 19 Ð20 June, 17Ð19 July, and 21Ð22 August in ELTP 45 stands. Vol. 29, no. 5 Insects were collected from the canopy and shrub strata using a variety of sampling methods in an effort to adequately represent the lepidopteran community within each stand. In all years, the canopy stratum in each stand was sampled with a suspendable UV trap consisting of a 22-W UV bulb connected to a photosensor (BioQuip, Gardena, CA) and powered by a 6-V motorcycle battery. UV traps were operated continuously between sunset and sunrise (⬇8 h) each sampling period. A collection funnel and bucket loaded with insecticidal pest strips (Vapona) were attached below the bulb. We used a bow and arrow rigged with a draw line to raise the trap into the canopy of a dominant or co-dominant tree located in the center of each stand. Placement of traps within the canopy and the use of a rain cover over the UV bulb likely restricted long-distance attraction of nocturnal insects and represented a localized sample of insect populations within our study sites (Bowden 1982). Lepidoptera were collected from the shrub stratum and understory vegetation using malaise traps and sweepnets in all 3 yr. One malaise trap with an insecticidal pest strip was set up in the center of each stand for 24 h during each sampling period. A sweepnet, 38 cm in diameter, was used to collect insects from ground ßora and shrub-level vegetation. Sixteen sweeps (four at each cardinal direction) were made six times along a random transect through the stand at 20-m intervals. Two stands were sampled with the sweepnet in 1 d during each sampling period; order of sampling was determined by random draw. Lepidoptera were carefully retrieved from sweepnets and placed into enclosed containers with insecticide strips. Lepidoptera Identification. All Lepidoptera were placed in plastic containers lined with tissue paper and stored in a freezer until identiÞcations could be made. Only adult Lepidoptera were identiÞed to species; few larvae were collected and resources did not permit the rearing of immatures. Species identiÞcations were made by John Wilterding, Robert Kriegel, and Mogens Nielson at Michigan State University. Voucher specimens were deposited at the Michigan State University Center for Insect Diversity, East Lansing, MI. Lepidoptera were grouped into two classes for some analyses: early season species, which included adults collected in May and June, and late season species which included adults collected in July and August. We assumed that many of the species collected as adults in the early season overwintered as pupae or late instar larvae, or completed larval development relatively early in the summer. Similarly, we assumed that many of the species collected as adults in the late season completed larval development earlier in the summer during the same year that they were collected. Therefore, potential interactions with gypsy moth may have differed for early season and late season species. Statistical Analysis. Total abundance and species richness (number of species) of adult Lepidoptera were determined for each sampling date in each stand. Abundance and species richness of adult Lepidoptera collected in the early season months (May and June) October 2000 WORK AND MCCULLOUGH: LEPIDOPTERAN COMMUNITIES IN TWO FOREST SYSTEMS were analyzed separately from late season (July and August) species, using a one-way analysis of variance (ANOVA) with repeated measures (Sokal and Rohlf 1995) to evaluate effects of defoliation on the two groups over three years. Species composition of lepidopteran communities was evaluated over 3 yr using nonmetric multidimensional scaling ordination to assess differences between the two ELTPs, and between defoliated and undefoliated stands within ELTP 20. All multivariate analyses were conducted using PCOrd software (McCune and Medford 1999). Ordinations were initially performed on a community matrix consisting of 48 sample units (or sampling events) ⫻ 374 Lepidoptera species. The 48 sample units represented early and late season data from our eight study stands during the three years. Because we expected high variation between early and late seasons, additional analyses were performed on early and late season subsets of the complete community matrix. The early season community matrix consisted of 24 sampling units ⫻ 207 species collected in May and June. The late season community matrix consisted of 24 sampling units ⫻ 253 species collected in July and August. In addition, to nonmetric multidimensional scaling, we tested seasonal, annual and ecosystem differences in species composition using multiresponse permutation procedures (Mielke 1984). Indicator species analysis (Dufrene and Legendre 1997) was also performed to identify species and guilds that were important indicators of differences among seasons, ecosystems, or levels of defoliation. Nonmetric Multidimensional Scaling Ordination. The original community matrix was transformed to presence/absence data for nonmetric multidimensional scaling ordination. This transformation reduced the coefÞcient of variation among sample units and species from 88 and 381%, to 49 and 130%, respectively. Likewise, this transformation focused our analysis on changes in species composition rather than changes in abundance of any particular taxa. Rare species (those occurring in only one sampling event) were retained in our analysis. Like all ordination methods, nonmetric multidimensional scaling represents complex systems with many variables as a smaller set of summary variables deÞned as ordination axes. Nonmetric multidimensional scaling differs from other ordination techniques in that it is based on ranked distances, and is thus free from many of the problems associated with other ordination techniques that require assumptions of multivariate normality within the data structure (Minchin 1987; McCune 1992, 1994). Consequently, nonmetric multidimensional scaling has been used widely in ecological studies (Clarke 1993). In nonmetric multidimensional scaling, each summary variable or axis has a degree of stress, or a difference in distance between the ordination and the original pdimensional space. Because nonmetric multidimensional scaling provides different stress solutions depending on the dimensionality of the ordination, an initial six dimensional solution and subsequent tests against Monte-Carlo simulations were performed to 887 assess the appropriate number of dimensions for the Þnal ordination. Three dimensions reduced the majority of stress within the dataset. Additional axes were assessed but did not substantially contribute to reduction of the stress of the ordination solution. The Þnal ordination was performed by Þtting a three dimensional solution to the initial dataset (Kruskal 1964). To prevent our solutions from reßecting local minima, an initial Bray-Curtis ordination (Magurran 1988, Ludwig and Reynolds 1988) was used as a starting point for the ordination. Finally, the validity of the solution was tested against a Monte-Carlo simulation to determine whether our results explained more variance than could be obtained by chance. Nonmetric multidimensional scaling ordination of early and late season Lepidoptera data were performed following the same procedures used to analyze the complete matrix. Multi–response Permutation Process. Differences in species composition between early and late seasons, and among years were assessed using multiresponse permutation process. The multiÐresponse permutation process is similar to a Student t-test, in that it compares differences in observed values to expected values deÞned by the distribution of standard deviations about the mean. The multiÐresponse permutation process uses the mean and standard deviations of the weighted mean within-group distance to produce a similar test statistic. In our analysis, within-group distances were generated using SorrensonÕs distance (Ludwig and Reynolds 1988) and using the natural weighting recommended by Mielke (1984). The multiÐresponse permutation process also provides an estimate of the magnitude of treatment effects through the chance-corrected within group-agreement (R). The variable R reßects a comparison of the homogeneity within a group to an expected value generated by the null hypothesis (in this case the expected value is random). If R ⫽ 1, all members within a group are identical; if R ⫽ 0, heterogeneity in the group is equal to that observed by chance (McCune and Medford 1999). Typically in ecological studies, an R ⬎ 0.3 is indicative of strong differences (McCune and Medford 1999). Indicator Analysis. Indicator species analysis (Dufrene and Legendre 1997) was used to detect and describe the relative importance of different Lepidoptera species for differentiating between early and late season Lepidoptera communities, the two ecosystems, and defoliated and undefoliated stands. This analysis combined the relative abundance and the relative frequency of a species into an indicator value that ranged between 0 (no indication) and 100 (perfect indication). Indicator values were then evaluated against a Monte-Carlo test statistic. Changes in Lepidoptera communities were evaluated by classifying Lepidoptera species into functional feeding guilds (Root 1973). We divided Lepidoptera species into 42 feeding guilds (see Appendix 1) on the basis of host plant preference, following (Forbes 1948, 1954, 1960) and (Tietz 1972). Information on host plant preferences was available for 227 Lepidoptera 888 ENVIRONMENTAL ENTOMOLOGY Vol. 29, no. 5 Fig. 1. Mean density of gypsy moth egg masses per hectare in (A) ELTP 20 (red oak) stands and (B) ELTP 45 (northern hardwood) stands. species. Indicator analysis (Dufrene and Legendre 1997) was used to evaluate whether feeding guilds in either the early or late seasons were related to severity of gypsy moth defoliation. Results Gypsy Moth Populations. In the oak-dominated ELTP 20 stands, gypsy moth populations ßuctuated dramatically among years. In 1993, egg mass densities were substantially higher in the stands near Branch, MI, than the stands near Freesoil, MI (Fig. 1A), and Branch stands sustained severe defoliation (Table 1). In 1994, egg mass densities were high at Branch stands (Fig. 1A), but an epizootic of nucleopolyhedrosis virus killed most larvae before substantial defoliation occurred. In 1994, however, the gypsy moth population began building in Freesoil stands, largely because Table 1. Visual estimation of peak defoliation and mean leaf area index (ⴞSE) using photosynthetically active radiation transmittance of sites in ELTP 20 (red oak) and ELTP 45 (northern hardwood) ecosystems 1993 1994 1995 Peak visual estimation of defoliation ELTP 20 Branch Freesoil ELTP 45 Harietta Mesick 76Ð100% 0Ð25% 0Ð25% 51Ð75% 0Ð25% 76Ð100% 0Ð25% 26Ð50% 0Ð25% 0Ð25% 0Ð25% 0Ð25% Estimated leaf area indexa ELTP 20 Branch Freesoil ELTP 45 Harrietta Mesick a 2). 4.48 (0.221) 2.73 (0.076) 4.71 (0.115) 2.72 (0.151) 10.9 (0.226) 11.9 (0.189) 8.61 (0.229) 8.14 (0.222) Means and standard errors were calculated from two sites (n ⫽ early instars were blown in from heavily infested stands on surrounding hills. The Freesoil stands experienced moderate defoliation in 1994, despite relatively low egg mass counts, while Branch stands had little defoliation (Table 1; Fig. 1A). In 1995, gypsy moth populations were high and defoliation was severe in Freesoil stands and was again minimal in Branch stands (Table 1; Fig. 1A). Trees in stands that were heavily defoliated reßushed by late July and we observed no tree mortality in any stand during the course of this study. Gypsy moth populations were much lower in the ELTP 45 stands dominated by sugar maple than in the ELTP 20 stands in every year (Fig. 1 A and B). Population densities in ELTP 45 stands ßuctuated annually but never exceeded 200 egg masses per hectare (Fig. 1B). Defoliation was negligible in ELTP 45 stands, although a few isolated American basswood trees were moderately defoliated by gypsy moth. Lepidopteran Communities. In total, 12,348 Lepidoptera representing 453 taxa were collected over the course of this study. Four families and one superfamily, Noctuidae, Tortricidae, Geometridae, Pyralidae, and Gelechioidea, accounted for 77% of all Lepidoptera collected (Table 2). Taxonomic richness was greater in ELTP 20 stands (324 taxa) than ELTP 45 stands (297 taxa). In contrast, overall abundance was greater in ELTP 45 (6,870 individuals) than in ELTP 20 stands (5,478 individuals). We collected 168 taxa (37% of the total richness) in both ecosystems. Of the total taxa collected, species level identiÞcations were possible for 7,279 individuals representing 374 species. A detailed listing of lepidopteran species collected in each ecosystem by month, year and trap type was presented by Work et al. (1998). Temporal Differences in Lepidopteran Communities. Seasonal differences in species composition were more pronounced than annual differences in species composition (Fig. 2). Axes presented in Fig. 2A rep- October 2000 Table 2. WORK AND MCCULLOUGH: LEPIDOPTERAN COMMUNITIES IN TWO FOREST SYSTEMS 889 Total Lepidoptera abundance and species richness in ELTP 20 (red oak) and ELTP 45 (northern hardwood) sites Family Agonoxenidae Arctiidae Argyresthiidae Blastobasidae Cosmopterigidae Cossidae Drepanidae Eriocraniidae Gelechiidae Geometridae Glyphipterigidae Hesperiidae Lasiocampidae Limacodidae Lymantriidae Noctuidae Notodontidae Oecophoridae Pieridae Plutellidae Pyralidae Satyridae Sesiidae Sphingidae Thyatiridae Tortricidae Yponomeutidae ELTP 20 sites ELTP 45 sites 1993 1994 1995 Total 1993 1994 1995 Total 0/0 20/4 1/1 0/0 0/0 1/1 0/0 1/1 1/1 50/14 0/0 0/0 8/1 1/1 54/2 379/49 17/7 10/2 1/1 0/0 36/11 0/0 0/0 1/1 1/1 280/21 0/0 0/0 12/4 0/0 0/0 0/0 0/0 0/0 0/0 0/0 20/11 0/0 0/0 4/1 2/2 0/0 376/52 32/6 21/2 0/0 0/0 65/4 6/1 3/1 6/2 0/0 426/17 0/0 1/1 77/6 12/1 0/0 2/1 0/0 0/0 0/0 0/0 42/16 0/0 6/2 10/2 3/2 1/1 225/60 4/3 15/4 0/0 3/1 84/16 0/0 0/0 1/1 0/0 815/20 1/1 1/1 109/9 13/1 0/0 2/1 1/1 0/0 1/1 1/1 112/34 0/0 6/2 22/2 6/3 55/2 980/106 53/11 46/4 1/1 3/1 185/24 6/1 3/1 8/4 1/1 1,521/41 1/1 1/1 29/5 5/1 1/1 0/0 0/0 0/0 0/0 0/0 56/17 0/0 0/0 9/3 2/2 30/1 145/46 46/7 1/1 2/1 0/0 10/7 1/1 0/0 3/2 0/0 1,185/20 0/0 0/0 9/2 0/0 0/0 0/0 0/0 0/0 0/0 0/0 31/8 0/0 0/0 33/1 10/3 0/0 126/47 12/7 2/1 0/0 0/0 3/3 0/0 0/0 1/1 0/0 352/13 2/1 0/0 9/4 35/1 0/0 0/0 0/0 1/1 0/0 2/1 110/23 1/1 0/0 43/1 12/1 0/0 373/70 15/3 10/5 0/0 2/1 63/11 0/0 0/0 4/3 1/1 1,353/20 1/1 1/1 47/8 40/1 1/1 0/0 0/0 1/1 0/0 2/1 197/36 1/1 0/0 85/3 24/4 30/1 644/112 73/10 13/5 2/1 2/1 76/18 1/1 0/0 8/3 1/1 2,890/35 3/2 resent differences in species composition of sites in early season months (May and June) and later season (June and July) months. Year-to-year differences in species composition among sites were also overlaid on the ordination and among-year variation is presented in Fig. 2B. The three dimensional solution had relatively low stress of 17.9% and explained 70.6% of the total variation observed (Table 3). Seasonal variation was strongly correlated with axis 1 and axis 2, whereas annual variation was only weakly correlated with axis 3 (Table 3). Likewise, the multiÐresponse permutation process analysis of the complete community matrix (374 species and 48 sampling units) also indicated that lepidopteran species composition differed between early and late seasons (t ⫽ 21.40, P ⬍ 0.0001), as well as among years (t ⫽ 8.48, P ⬍ 0.0001) but the differences were not strong (R ⫽ 0.07 and 0.04, respectively). When seasonal differences in species composition data were analyzed separately, differences among years were more pronounced within both the early season (t ⫽ 6.69, P ⬍ 0.0001, R ⫽ 0.069) and late season months (t ⫽ 8.16, P ⬍ 0.0001, R ⫽ 0.080). Patterns Within and Between Ecosystems. Within the oak-dominated ELTP 20, overall lepidopteran abundance did not signiÞcantly differ between Branch and Freesoil stands (F ⫽ 12.88; df ⫽ 1, 2; P ⫽ 0.07) or among years (F ⫽ 4.32; df ⫽ 2, 4; P ⫽ 0.10). However, overall species richness showed a signiÞcant stand ⫻ year interaction (F ⫽ 9.46; df ⫽ 2, 4; P ⫽ 0.03). In 1993, when gypsy moth defoliation was severe in Branch stands, species richness was lower in Branch stands (30.0 ⫾ 2.00) than in Freesoil stands (57.5 ⫾ 2.50). In 1994, when defoliation was moderate in Freesoil but negligible in Branch stands, Freesoil had lower species richness than Branch stands (38.0 ⫾ 8.00 and 48.5 ⫾ 2.50, respectively). However, in 1995, when defoliation was severe in Freesoil stands, species richness was greater in Freesoil stands (69.0 ⫾ 9.00) than in Branch stands (50.5 ⫾ 0.50). When the total collection of Lepidoptera within the ELTP 20 stands was divided into early and late season species, stand ⫻ year interactions did not signiÞcantly affect species richness in the early season (F ⫽ 1.28; df ⫽ 2, 4; P ⫽ 0.37) (Fig. 3A), but did signiÞcantly affect late season species richness (F ⫽ 276.35; df ⫽ 2, 4; P ⬍ 0.001) (Fig. 3B). In Branch stands, late season species richness was similar in 1994 and 1995 when defoliation was low to negligible, but species richness was over 60% lower in 1993 when defoliation was severe. In Freesoil stands, late season species richness was much lower in 1994 when moderate gypsy moth defoliation occurred than in 1993 when virtually no defoliation was observed. But species richness, as well as lepidopteran abundance (Table 2) was high again in 1995, even though these stands were severely defoliated. Within the ELTP 45 stands dominated by northern hardwoods there were no signiÞcant differences in lepidopteran abundance between the Harrietta and Mesick stands (F ⫽ 0.12; df ⫽ 1, 2; P ⫽ 0.76), among years (F ⫽ 3.44; df ⫽ 2, 4; P ⫽ 0.14), or caused by stand ⫻ year interactions (F ⫽ 0.85; df ⫽ 2, 4; P ⫽ 0.49). Likewise, there was no signiÞcant effect of stand (F ⫽ 0.75; df ⫽ 1, 2; P ⫽ 0.48) or the stand ⫻ year interactions (F ⫽ 0.88; df ⫽ 2, 4; P ⫽ 0.48) on overall species richness, but annual changes in species richness were signiÞcant (F ⫽ 10.40; df ⫽ 2, 4; P ⫽ 0.03). When data 890 ENVIRONMENTAL ENTOMOLOGY Fig. 2. Nonmetric multidimensional scaling ordination of 374 Lepidoptera species representing differences in species composition (A) between early and late season and (B) between eight stands that were sampled over 3 yr (48 sample units). were divided into early and late seasons, species richness was not signiÞcantly affected by stand ⫻ year interactions in either early (F ⫽ 0.65; df ⫽ 2, 4; P ⫽ 0.57) or late (F ⫽ 0.27; df ⫽ 2, 4; P ⫽ 0.78) seasons (Fig. 4). When early season Lepidoptera species were ordinated using NMS, differences in species composition between the ELTP 20 and ELTP 45 ecosystems were Table 3. Vol. 29, no. 5 apparent within each year. Ordination of early season species revealed a clear separation between the oakdominated ELTP 20 stands and the northern hardwood-dominated ELTP 45 stands along axis 1 and axis 2 (Fig. 5). This ordination provides a Þnal stress of 14.8%, and explains 70.9% of the variation observed (Table 4). Axis 1 and axis 2 had relatively high correlations with compositional differences between ecosystems (r2 ⫽ 0.447 and r2 ⫽ 0.446, respectively) (Table 4). Compositional differences among years were less pronounced and were only low to moderately correlated with axis 1 (Table 4). When indicator species analysis was used to examine differences in early season Lepidoptera between ELTP 20 and ELTP 45 stands, we found that three species were speciÞc to ELTP 20 and Þve species were speciÞc to ELTP 45 (Table 5). Of the three indicator species within ELTP 20 stands, host plant information was available for only one species, Phoberia atomaris Hübner. P. atomaris was described as feeding predominately on Quercus spp. in the overstory (Forbes 1954). Of the indicator species for ELTP 45, Clepsis melaleucana (Walker) and Cerastis tenebrifera (Walker) feed predominately on herbaceous plants on the forest ßoor. Two general overstory feeders, Plagodis phlogosaria (Guenée) and Gluphisia septentrionalis Walker, were also indicators of ELTP 45. Host plant information was not available for Lomographa glomeraria (Grote). Other early season Lepidoptera that co-occurred with the indicator species, but were not indicative of either ELTP, are reported in Table 6. These species were collected from both ecosystems and further represent the lepidopteran assemblage present in the early season. With the exception of Protorthodes oviduca (Guenée), a species that feeds on herbaceous vegetation, all species are generalist overstory feeders on hardwood trees. Differences in species composition between the oak-dominated ELTP 20 stands and the northern hardwood-dominated ELTP 45 were also apparent within the late season months (Fig. 6). Within this ordination, the Þnal stress of was low (13.2%), and the total variance explained was high (83.1%) (Table 7). Differences in species composition between ecosystems were largely correlated with axis 2 (r2 ⫽ 0.787) (Table 7). Again, differences in species composition between years were less apparent than ecosystem differences. Year to year differences in Lepidoptera composition were only moderately correlated with axis 1 and axis 3 (r2 ⫽ 0.154 and r2 ⫽ 0.363, respectively) (Table 7). Indicator species analysis of late season Lepidoptera identiÞed six species as important indicators of ELTP Results of three dimensional nonmetric scaling ordination of 374 adult Lepidoptera species collected from 48 sampling units Pearson correlation (r2) Axis Stress P Variance explained, % Cumulative variance explained, % Season Year 1 2 3 38.066 23.242 17.900 0.0196 0.0196 0.0196 0.277 0.271 0.158 0.277 0.548 0.706 0.519 0.566 0.205 0.059 0.000 0.177 October 2000 WORK AND MCCULLOUGH: LEPIDOPTERAN COMMUNITIES IN TWO FOREST SYSTEMS 891 Fig. 3. Mean species richness in ELTP 20 stands in (A) early season months and (B) late season months. 20 stands, and Þve species as important indicators of ELTP 45 (Table 8). Within ELTP 20, four species, Raphia frater Grote, Cosmia calami (Harvey), Argyrotaenia quercifoliana (Fitch), and Acronicta ovata Grote, are predominately overstory feeders with the last two feeding exclusively on oaks. Both Idia species are associated with dead leaves. Three of the Þve indicators of ELTP 45 stands are understory feeders associated with herbaceous plants, and one species, Zanclognatha laevigata (Grote), is associated with dead leaves. Of the remaining two species, Xestia normaniana (Grote) is a cutworm and Proteoteras moffatiana C. H. Fernald is a specialist on Acer spp. Other species within the late-season Lepidoptera assemblage that co-occurred with indicator species are presented in Table 9. Six species are associated with overstory plants, whereas one species, Hypoprepia fucosa Hübner, is associated with lichen and moss in the canopy. Species associated with overstory trees included Archips argyrospila (Walker), Sparganothis pettitana (Robinson), Choristoneura rosaceana (Harris), Sunira bicolorago (Guenée), and Anavitrinelia pampinaria (Guenée). Seven species are associated with understory plants, including Ostrinia nubilalis (Hübner), Aglossa cuprina Zeller, Apantesis parthenice (W. F. Kirby), Herculia olinalis (Guenée) Hypenodes Fig. 4. Mean species richness in ELTP 45 stands in (A) early season months and (B) late season months. 892 ENVIRONMENTAL ENTOMOLOGY Vol. 29, no. 5 indicative of moderate or severe gypsy moth defoliation (indicator variable ⫽ 81.5, P ⬍ 0.018) (Table 10). Discussion Fig. 5. Nonmetric multidimensional scaling ordination of 207 lepidopteran species collected in early season months. In this ordination, circles represent ELTP 20 (red-oak) stands, triangles represent ELTP 45 (northern hardwood) stands, black symbols indicate stands sampled in 1993, gray symbols indicate stands sampled in 1994, and white symbols indicate stands sampled in 1995. fractulinea (J. B. Smith), Olethreutes fasciatana (Clemens), and Crambus albellus Clemens. When the level of gypsy moth defoliation was overlaid on the ordination of late season Lepidoptera, stands with moderate to severe defoliation clustered separately from stands with light defoliation within each year (Fig. 7). When indicator analysis was performed on individual species data, eight species were signiÞcantly associated with gypsy moth defoliation level. Two species, C. rosaceana and S. pettitana, were negatively indicative of moderate or severe gypsy moth defoliation (indicator variable ⫽ 66.7, P ⬍ 0.008 and indicator variable ⫽ 66.7, P ⬍ 0.012). Of the six species positively associated with gypsy moth defoliation, only one species, Meganola minuscula (Zeller), had a relatively high indicator value (indicator variable ⫽ 50.0, P ⬍ 0.006). The remaining Þve species, although statistically signiÞcant, had low indicator values (indicator variable ⬍33 in all cases). We further classiÞed species into guilds based on host-plant preference and performed indicator analysis to compare guilds in defoliated and undefoliated stands. Only oak-feeding Lepidoptera were negatively Our ability to sample lepidopteran communities within the eight stands was limited by our resources, particularly the time needed to process and identify specimens to species level. Therefore, rather than attempting to collect and rear larvae, we focused on adults, the reproductive phase that represents the sum of all mortality agents acting on that generation. In addition, we could efÞciently collect Lepidoptera with the UV traps and other sampling methods, although the height of the canopy in these mature stands made it difÞcult to clip foliage or branches. Despite these limitations, our results indicate that our trapping methods were sensitive enough to detect differences in the lepidopteran communities related to yearly variation, seasonal differences perhaps partially related to effects of severe defoliation, and differences between the two ELTPs. Within each ecosystem we were able to identify lepidopteran species that were closely associated with the dominant overstory plants (Quercus spp. in ELTP 20 and Acer saccarum in ELTP 45) that characterized each ecosystem. We were also able to distinguish between lepidopteran assemblages that were speciÞc to one ELTP versus assemblages that were common to both ecosystems. Our trapping methods, therefore, appear appropriate for stand-level spatial scales and could be useful in future monitoring programs. Temporal Variation in Lepidopteran Communities. Overall abundance of Lepidoptera was fairly consistent from year to year in ELTP 20 and ELTP 45 stands. This consistency may be important for bats, birds, and other animals that feed exclusively on insects (Lih et al. 1995, Sample et al. 1996, Kurta and Whitaker 2000). The number of species that were collected in ELTP 45 stands was also consistent among years while species richness varied in ELTP 20 stands, perhaps caused in part by ßuctuating gypsy moth populations. Although abundance was relatively consistent, we observed signiÞcant changes in the species comprising the lepidopteran communities within and between years. Large differences in lepidopteran species assemblages from one year to another have been reported by Sample et al. (1996), who attributed annual variation to weather conditions. In our study, differ- Table 4. Results of three dimensional nonmetric scaling ordination of 207 adult Lepidoptera species collected early season months (May and June) from 24 sampling units Pearson correlation (r2) Axis Stress P Variance explained, % Cumulative variance explained, % Year ELTP 1 2 3 37.407 20.822 14.808 0.0196 0.0196 0.0196 0.264 0.258 0.187 0.264 0.522 0.709 0.313 0.056 0.007 0.447 0.446 0.001 October 2000 WORK AND MCCULLOUGH: LEPIDOPTERAN COMMUNITIES IN TWO FOREST SYSTEMS 893 Table 5. Indicators of differences between ELTP 20 (red oak) and ELTP 45 (northern hardwoods) in adult Lepidoptera collected in early season months (May and June) over 3 yr Indicator value from randomized tests Family Species ELTP Observed indicator value Mean ⫾ SD P Tortricidae Geometridae Notodontidae Geometridae Noctuidae Noctuidae Noctuidae Noctuidae Clepsis melaleucana (Walker) Plagodis phlogosaria (Guenée) Gluphisia septentrionalis Walker Lomographa glomeraria (Grote) Cerastis tenebrifera (Walker) Ulolonche culea (Guenée) Meganola minuscula (Zeller) Phoberia atomaris Hübner 45 45 45 45 45 20 20 20 75.8 59.3 56.3 51.0 41.7 69.4 59.3 41.7 32.6 ⫾ 7.71 28.4 ⫾ 7.53 33.5 ⫾ 7.93 25.6 ⫾ 8.29 19.3 ⫾ 7.05 33.9 ⫾ 8.29 28.5 ⫾ 7.47 19.2 ⫾ 6.83 ⬍0.001 0.010 0.028 0.030 0.044 0.006 0.012 0.037 ences in species composition between years was less pronounced than seasonal differences. Differences in the species composition of the lepidopteran community between early season and late season months were consistently signiÞcant and may have implications for those interested in assessing or monitoring native biological diversity. Single year surveys provide a snapshot of local assemblages, but probably do not adequately describe the true extent of species diversity in a forest stand or similar spatial unit. In our stands, the lepidopteran community in both ecosystems was dynamic and changed substantially over a short period. Depending on the objectives and life stage of interest, biotic inventories based on periodic monitoring during the year may be more effective at describing or detecting change in lepidopteran communities than short-term intensive surveys. Ecosystem Differences. Although there were no major differences in abundance of Lepidoptera between ELTP 20 and ELTP 45 stands, relatively large numbers of species (274 species or 66% of the total species) were collected within only one of the ecosystems. Likewise, differences in species composition between the ELTP 20 and ELTP 45 stands were apparent between seasons and among years, suggesting Lepidoptera species composition has a high degree of Þdelity with the ecological classiÞcation system. In contrast, Rykken et al. (1997) found little correspondence between carabid beetles and a large-scale ecological classiÞcation system developed for northeastern hardwood forests, suggesting that the Þdelity of these associations may vary with the general habits or trophic level of arthropods. Table 6. Species diversity of herbivorous insects has been predicted to be associated with diversity and complexity of host plants (Lawton 1978, Southwood et al. 1979). We originally expected that lepidopteran species diversity would be greater in the ELTP 45 stands that had a mixture of northern hardwood species in the overstory, compared with the relatively simple, oakdominated ELTP 20 stands. In addition, the high nitrogen availability and productivity associated with ELTP 45 stands (Zak et al. 1986, 1989) suggest that herbivorous insects should have access to higher foliar nutrient levels than insects feeding on plants in the less productive ELTP 20 stands (Mattson 1980, Scriber and Slansky 1981, Mattson and Scriber 1987). Likewise, we expected diversity of lepidopteran species associated with understory vegetation to be higher in ELTP 45 stands than in ELTP 20 stands. The ground ßora in ELTP 45 stands is more abundant and diverse in species and structure than the ground ßora in ELTP 20 stands (Cleland et al. 1993). However, more lepidopteran taxa were actually collected in ELTP 20 stands than in ELTP 45 stands, whereas overall species richness and diversity of Lepidoptera associated with understory vegetation was similar in both ecosystems. The dense, often closed canopy in ELTP 45 stands may have resulted in cooler temperatures than in the relatively open ELTP 20 stands, perhaps reducing lepidopteran activity in the ELTP 45 stands. Gypsy Moth Impacts. Our 1993Ð1995 survey of Lepidoptera coincided with the Þrst major gypsy moth outbreak in the stands that we studied in northwestern lower Michigan. Gypsy moth populations varied considerably between and within stands, but were con- Lepidoptera speces assemblages that co-occurred within early season months (May and June) with ecosystem indicator species Family Species Observed indicator value Noctuidae Noctuidae Noctuidae Noctuidae Noctuidae Noctuidae Noctuidae Geometridae Noctuidae Achatia distincta Hübner Cissusa spadix (Cramer) Egira dolosa Grote Elaphria festivoides (Guenée) Crocigrapha normani (Grote) Protorthodes oviduca (Guenée) Orthosia hibisci (Guenée) Plagodis alcoolaria (Guenée) Orthosia rubescens (Walker) 50.0 45.8 41.7 55.1 33.3 33.8 20.8 25.5 20.8 Indicator value from randomized tests Mean ⫾ SD P 18.3 ⫾ 5.37 17.4 ⫾ 4.70 15.8 ⫾ 4.76 24.0 ⫾ 4.95 13.2 ⫾ 4.75 15.6 ⫾ 4.83 9.7 ⫾ 3.31 13.3 ⫾ 4.39 9.8 ⫾ 3.57 ⬍0.001 ⬍0.001 ⬍0.001 ⬍0.001 0.006 0.010 0.029 0.037 0.045 894 ENVIRONMENTAL ENTOMOLOGY Fig. 6. Nonmetric multidimensional scaling ordination of 253 lepidopteran species collected in late season months, with annual variation and ecosystem differences overlaid (24 sample units). In this ordination, circles represent ELTP 20 (red-oak) stands, triangles represent ELTP 45 (northern hardwood) stands, black symbols indicate stands sampled in 1993, gray symbols indicate stands sampled in 1994, and white symbols indicate stands sampled in 1995. sistently much higher in the oak-dominated ELTP 20 stands than in the ELTP 45 stands with few preferred hosts of gypsy moth. All of the ELTP 20 stands we surveyed sustained severe defoliation during one year, but gypsy moth populations collapsed the following year. Other outbreaks of gypsy moth in northern Michigan forests have been similarly limited in duration and area, rarely persisting more than 1Ð2 yr in individual stands, and typically affecting areas ⬍65 ha in size (F. Sapio, Michigan Department of Natural Resources, unpublished data). The relatively short duration of the gypsy moth outbreaks in our stands resulted from nucleopolyhedrosis epizootics, although the gypsy moth fungal pathogen Entomophaga maimaiga was present in other stands in the Huron-Manistee National Forest by 1995 (Buss 1997, Buss et al. 1999). This pattern of temporal and spatial variability is consistent with other studies of gypsy moth dynamics (Elkinton and Liebhold 1990). The limited duration and area affected in any one year suggests that a gypsy moth outbreak may only affect a relatively small portion of the native Vol. 29, no. 5 lepidopteran community existing in this national forest. With the exception of one noctuid species (C. spadex Cramer), we did not detect reductions in abundance of native Lepidoptera in defoliated stands in the early season months of May and June. This is perhaps not surprising because these adults completed larval development either in the preceding year or in the current-year but before peak gypsy moth defoliation occurred in mid-July. Although there was no difference in early season species assemblages associated with gypsy moth dynamics, these assemblages did consistently differ between the two ELTPs, again emphasizing the need to consider program objectives when selecting methods for lepidopteran sampling. However, high gypsy moth populations and moderate to severe defoliation in ELTP 20 stands may have affected some of the native Lepidoptera species that were collected as adults during the late season months of July and August. Ordinations of late season species assemblages indicated that moderately to severely defoliated red oak stands clustered separately from undefoliated stands within each year. One important result of our analysis of indicator species was the negative association between severe gypsy moth defoliation and the abundance of the oakfeeding guild (see Appendix 1). Larval development of these species and gypsy moth presumably coincided, potentially exposing the native species to competition for foliage, altered host quality (Schultz and Baldwin 1982; Karban 1986, Hunter 1987, Wold and Marquis 1997) or microclimate, or abundant natural enemies associated with the high-density gypsy moth populations (Elkinton et al. 1990, Gould et al. 1990, Williams et al. 1992, Ferguson et al. 1994). Although competition between phytophagous insects may be generally rare (Lawton and Strong 1981, Denno et al. 1995), competitive interactions between herbivorous lepidopteran species would presumably be more common during outbreaks when defoliation is severe (Varley 1949, Ross 1957, Hansen and Ueckert 1970, McClure 1974, Karban 1986, Schreiner and Nafus 1992, Sample et al. 1996). Abundance of species described as generalist woody plant feeders or as specialist feeders on Populus spp., Hammemelis spp., or Betula spp. were seemingly unaffected by gypsy moth, again indicating that impacts associated with gypsy moth outbreaks may be largely limited to the subset of species that use oak species. Taken together, results of our study and other work suggest that the impacts of Btk application on native Table 7. Results of three dimensional nonmetric scaling ordination of 253 adult Lepidoptera species collected late season months (July and August) from 24 sampling units Axis Stress P Variance explained, % Cumulative variance explained, % 1 2 3 31.502 19.049 13.296 0.0196 0.0196 0.0196 0.180 0.384 0.268 0.180 0.564 0.831 Pearson correlation (r2) Year ELTP 0.154 0.008 0.363 0.014 0.787 0.007 October 2000 WORK AND MCCULLOUGH: LEPIDOPTERAN COMMUNITIES IN TWO FOREST SYSTEMS 895 Table 8. Indicators of differences between ELTP 20 (red oak) and ELTP 45 (northern hardwoods) in adult Lepidoptera collected in late season months (July and August) over 3 yr Family Species Noctuidae Tortricidae Noctuidae Tortricidae Noctuidae Noctuidae Tortricidae Noctuidae Noctuidae Noctuidae Noctuidae Zanclognatha laevigata (Grote) Proteoteras moffatiana C. H. Fernald. Homorthodes furfurata (Grote) Sparganothis reticulatana (Clemens) Xestia normaniana (Grote) Acronicta ovata Grote Argyrotaenia quercifoliana (Fitch) Idia julia (Barnes and McDunnough) Idia rotundalis (Walker) Cosmia calami (Harvey) Raphia frater Grote forest lepidopteran communities may be greater than impacts associated with gypsy moth outbreaks, at least during the relatively short period encompassed by our study. Effects of Btk on many nontarget species of Lepidoptera have been assessed in previous studies (Miller 1990a, Miller 1990b, Johnson et al. 1995, Lih et al. 1995, Wagner et al. 1996, Papp-Hermes et al. 1997, Peacock et al. 1998). Reduced survival, abundance, or species diversity of native Lepidoptera have been observed after Btk application, although extent and duration of impacts may vary with size of the treated area, the number of Btk applications, phenological synchrony of susceptible life stages, and physiological susceptibility to the toxic Btk crystals. A West Virginia study compared effects of aerial Btk application with effects of high gypsy moth populations. Their results indicated that Btk reduced abundance, species richness, and biomass of several native lepidopteran taxa (Sample et al. 1996). In contrast, few taxa were affected by gypsy moth, although severe defoliation Table 9. ELTP Observed indicator value 45 45 45 45 45 20 20 20 20 20 20 66.7 66.7 59.3 59.3 51.0 58.3 59.3 50.0 51.0 41.7 41.7 Indicator value from randomized tests Mean ⫾ SD P 25.5 ⫾ 8.53 25.7 ⫾ 8.35 28.0 ⫾ 7.25 28.3 ⫾ 7.37 25.8 ⫾ 8.26 23.8 ⫾ 7.30 28.2 ⫾ 7.30 21.1 ⫾ 8.22 25.2 ⫾ 8.04 19.4 ⫾ 6.60 19.3 ⫾ 6.94 0.001 0.002 0.006 0.010 0.026 0.005 0.008 0.014 0.022 0.028 0.040 (⬎75%) occurred in only one plot and in only one year during their study. In Virginia, Wagner et al. (1996) found that one aerial Btk application reduced abundance of univoltine, externally feeding macro-lepidoptera that specialized on oak foliage. Our results similarly suggest that oak-feeders may be the group that is most likely to be affected by gypsy moth outbreaks. In the Virginia study, several lepidopteran species associated with understory vegetation were also affected by the Btk application, presumably because of their inability to avoid spray residuals by feeding within rolled leaves or other refugia (Wagner et al. 1996). Our results indicate that understory Lepidoptera were an important component of the Lepidoptera community as a whole, but we did not detect associations between this group and gypsy moth dynamics. The resiliency of native lepidopteran communities to a gypsy moth outbreak, even in highly susceptible ecosystems like the ELTP 20 stands, is perhaps not Lepidoptera speces assemblages that co-occurred within late season months (July and August) with ecosystem indicator species Family Species Observed indicator value Tortricidae Oecophoridae Arctiidae Lasiocampidae Tortricidae Tortricidae Noctuidae Noctuidae Pyralidae Pyralidae Pyralidae Noctuidae Argyresthiidae Arctiidae Noctuidae Noctuidae Arctiidae Pyralidae Noctuidae Noctuidae Tortricidae Geometridae Pyralidae Archips argyrospila (Walker) Callima argenticinctella Clemens Hypoprepia fucosa Hübner Malacosoma disstria Hübner Sparganothis pettitana (Robinson) Choristoneura rosaceana (Harris) Xestia normaniana (Grote) Callopistria cordata (Ljungh) Ostrinia nubilalis (Hübner) Aglossa cuprina Zeller Eulogia ochrifrontella (Zeller) Abagrotis alternata (Grote) Argyresthia oreasella Clemens Crambidia pallida Packard Lithacodia albidula (Guenée) Sunira bicolorago (Guenee) Apantesis parthenice (W. F. Kirby) Herculia olinalis (Guenée) Hypenodes fractilinea (J. B. Smith) Rhynchagrotis anchocelioides (Guenée) Olethreutes fasciatana (Clemens) Anavitrinelia pampinaria (Guenée) Crambus albellus Clemens 58.6 50.0 62.5 54.2 79.9 65.6 33.3 42.9 29.2 29.2 25.0 25.0 29.6 25.0 25.0 25.0 20.8 20.8 32.1 20.8 30.7 20.8 20.8 Indicator value from randomized tests Mean ⫾ SD P 22.8 ⫾ 5.41 17.9 ⫾ 4.86 21.8 ⫾ 5.11 19.5 ⫾ 4.83 30.3 ⫾ 5.18 35.3 ⫾ 5.49 13.6 ⫾ 4.71 20.5 ⫾ 5.48 12.3 ⫾ 3.99 12.3 ⫾ 4.05 10.7 ⫾ 4.12 10.7 ⫾ 4.21 14.8 ⫾ 4.39 10.7 ⫾ 4.46 11.1 ⫾ 4.40 10.9 ⫾ 4.45 9.7 ⫾ 3.40 9.8 ⫾ 3.51 19.3 ⫾ 4.76 9.8 ⫾ 3.56 17.5 ⫾ 4.84 9.8 ⫾ 3.60 9.9 ⫾ 3.64 ⬍0.001 ⬍0.001 ⬍0.001 ⬍0.001 ⬍0.001 0.001 0.004 0.006 0.007 0.011 0.018 0.021 0.021 0.022 0.024 0.027 0.034 0.040 0.043 0.045 0.046 0.047 0.049 896 ENVIRONMENTAL ENTOMOLOGY Vol. 29, no. 5 recolonize the area after the outbreak collapses. We should be cautious, however, in concluding that gypsy moth effects are limited in scope and duration, given the high variability associated with these communities and the scarcity of information on life history and habitat needs for many of the Lepidoptera we collected. Long-term studies to monitor populations, especially those of native oak-feeding species, will be needed to detect subtle shifts in abundance, diversity, or species composition of native Lepidoptera related to establishment of gypsy moth in these forests. Acknowledgments Fig. 7. Nonmetric multidimensional scaling ordination of 253 lepidopteran species collected in late season months, with level of gypsy moth defoliation overlaid (24 sample units). In this ordination, circles represent undefoliated stands, triangles represent defoliated stands, black symbols indicate stands sampled in 1993, gray symbols indicate stands sampled in 1994, and white symbols indicate stands sampled in 1995. surprising. Outbreaks of other forest insects such as forest tent caterpillar, Malacosoma disstria Hübner, occur periodically and result in extensive defoliation in forested areas of the Great Lakes region (Witter et al. 1975, Witter 1979, Rose and Lindquist 1982). Populations of native Lepidoptera that co-occur with these episodic outbreak species presumably are able to persist in refugia or outside affected areas, then We particularly thank Brian Kopper for his efforts in both the Þeld and the laboratory, and his assistance in collecting and processing thousands of insects. We also thank Tom Ellis, Katie Albers, Kevin Ellwood, and Liz Weber for their help in the Þeld and acknowledge the support provided by Donald Zac (University of Michigan) and Rose Ingram (HuronManistee National Forests). Comments from Bruce McCune (Oregon State University) and two anonymous reviewers improved the manuscript. Funding for this study was provided by the McIntire-Stennis Cooperative Forest Research program and represents Michigan Agricultural Experiment Station Project No. MICL01710. References Cited Bailey, B. V. 1987. Suggested hierarchy of criteria for multiscale ecosystem mapping. Landsc. Urban Plann. 14: 313Ð 319. Biological Survey of Canada. 1994. Terrestrial arthropod biodiversity: planning a study and recommended sampling techniques. Supp. Bull. Entomol. Soc. Can. 26: 1Ð33. Barnes, B. V., K. S. Pregitzer, T. A. Spies, and V. H. Spooner. 1982. Ecological forest site classiÞcation, Cyrus McCormick Experimental Forest. J. For. 80: 493Ð 498. Table 10. Indicators of differences between ELTP 20 (red oak) sites sustaining moderate to severe defoliation and ELTP 20 sites with negligable or low defoliation based on host plant feeding preferences Feeding guild No. species in guild Observed indicator value Quercus Generalist herb feeder Generalist grasses Generalist woody plants Generalist fungus-dead leaves Cutworm Generalist low plants Robinia Acer Hammamelis Rosaceae Ulmus Betula Conifers O. virginiana, Rosaceae Pinus Populus Prunus Viburnum 13 4 12 15 9 16 5 1 1 3 3 1 1 2 1 2 6 1 2 81.5 66.1 71.7 61.6 68.8 55.2 47.1 33.3 33.3 33.3 43.5 32.3 16.7 22.2 16.7 18.2 26.5 16.7 16.7 Indicator value from randomized tests Mean ⫾ SD P 52.5 ⫾ 11.46 55.8 ⫾ 7.63 61.5 ⫾ 10.69 56.1 ⫾ 7.80 60.7 ⫾ 10.95 53.9 ⫾ 9.37 42.5 ⫾ 13.96 20.9 ⫾ 11.06 19.7 ⫾ 12.46 22.9 ⫾ 9.73 44.4 ⫾ 15.73 31.1 ⫾ 11.60 16.7 ⫾ 0.53 27.4 ⫾ 10.87 16.7 ⫾ 0.53 33.0 ⫾ 12.56 40.1 ⫾ 13.20 16.7 ⫾ 0.53 16.7 ⫾ 0.53 0.018 0.139 0.196 0.250 0.252 0.365 0.374 0.443 0.454 0.465 0.554 0.727 0.999 0.999 0.999 0.999 0.999 0.999 0.999 Based on the 98 species collected in late season months over 3 yr. 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Landscape variation in nitrogen mineralization and nitriÞcation. Can. J. For. Res. 16: 1258 Ð1263. Received for publication 28 July 1999; accepted 15 June 2000. Appendix 1. Feeding guild assignments for 98 species of Lepidoptera collected in late season months of July and August over 3 yr Quercus Acronicta haesitata (Grote) Acronicta inclara J. B. Smith Acronicta modica Walker Acronicta ovata Grote Ancylis metamelana (Walker) Archips fervidana (Clemens) Argyrotaenia quercifoliana (Fitch) Besma quercivoraria (Guenée) Catocala amica (Hübner) Catocala ilia (Cramer) Macrurocampa marthesia (Cramer) Melissopus latiferreanus Walsingham Peridea angulosa (J. E. Smith) General-Herbs Platynota idaeusalis (Walker) Sparganothis reticulatana (Clemens) Synchlora aerata (F.) Xanthorhoe ferrugata (Clerk) General-Grass Feeder Aglossa cuprina Zeller Cisseps fulvicollis (Hübner) Crambus agitatellus Clemens Crambus albellus Clemens Herculia olinalis (Guenée) Hypenodes fractilinea (J. B. Smith) Leucania pseudargyria Guenée Lithacodia muscosula (Guenée) Microcrambus elegans (Clemens) Munroessa icciusalis (Walker) Platytes vobisne Dyar Thaumatopsis gibsonella Kearfott General-Woody Plants Amphipoea americana (Speyer) Anavitrinelia pampinaria (Guenée) Ancylis nubeculana (Clemens) Archips argyrospila (Walker) Archips semiferana (Walker) Choristoneura obsoletana (Walker) Choristoneura rosaceana (Harris) Cosmia calami (Harvey) Euplexia benesimilis McDunnough Itame pustularia (Guenée) Nadata gibbosa (J. E. Smith) Pandemis limitata (Robinson) Scopula limboundata (Haworth) Sparganothis pettitana (Robinson) Sunira bicolorago (Guenée) General-Fungus, Dead Leaves Bleptina caradrinalis Guenée Idia aemula Hübner Idia americalis (Guenée) Idia diminuendis (Barnes & McDunnough) Idia julia (Barnes & McDunnough) Idia lubricalis (Geyer) Idia rotundalis (Walker) Zanclognatha ochreipennis (Grote) Cutworm Abagrotis alternata (Grote) Eueretagrotis attenta (Grote) Euxoa declarata (Walker) Euxoa tessellata (Harris) Feltia geniculata Grote & Robinson Lacinipolia implicata McDunnough Lacinipolia lustralis (Grote) Ochropleura plecta (L.) Peridroma saucia (Hübner) Polia detracta (Walker) Polia nimbosa (Guenée) Pseudoletia unipuncta (Guenée) Rhynchagrotis anchocelioides (Guenée) 900 ENVIRONMENTAL ENTOMOLOGY Vol. 29, no. 5 Spodoptera frugiperda (J. E. Smith) Xestia normaniana (Grote) Ulmus Hyperstrotia pervertens (Barnes & McDunnough) General-Low Plants Apantesis parthenice (W. Kirby) Holomelina aurantiaca (Hübner) Homorthodes furfurata (Grote) Orthodes cynica Guenée Plathypena scabra (F.) Betula Plagodis alcoolaria (Guenée) Ostrya virginiana and Rosaceae Lomographa vestaliata (Guenée) General-Conifers Caripeta divisata Walker Nepytia canosaria (Walker) Robinia Heliomata cycladata Grote & Robinson Acer Bomolocha baltimoralis (Guenée) Hammamelis Acronicta hamamelis Guenée Olethreutes footiana (C. H. Fernald) Synedoida grandirena (Haworth) Rosaceae Croesia albicomana (Clemens) Olethreutes permundana (Clemens) Pinus Petrova gemistrigulana (Kearfott) Semiothisa bisignata (Walker) Populus Gluphisia septentrionalis Walker Ipimorpha pleonectusa Grote Pheosia rimosa Packard Protitame virginalis (Hulst) Pseudosciaphila duplex (Walsingham) Raphia frater Grote Prunus Archips cerasivorana (Fitch) Viburnum Agriopodes fallax (Herrich-Schaeffer) Archips purpurana (Clemens)