Download Lepidopteran Communities in Two Forest Ecosystems During the

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
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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.
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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)