Incidence and ecological relationships of parasitism in larval populations of Lymantria dispar (Lepidoptera: Lymantriidae)

BIOLOGICAL CONTROL

2, 35-43

(1992)

Incidence and Ecological Relationships of Parasitism in Larval Populations of Lymantria dispar (Lepidoptera: Lymantriidae) D.W. WILLIAMS ,* R.W. FUESTER,* W.W. METTERHOUSE,~ R.J. BALAAM,~ R. H. BULLOCK,? R. J. CHIANESE,~ AND R. C. REARDONS *Beneficial Insects Research Laboratory, USDA-ARS, 501 South Chapel Street, Newark, Delaware 19713; tNew Jersey Department of Agriculture, Division of Plant Zndustry, CN 330, Trenton, New Jersey 08625; and $lJSDA Forest Service, 180 Canfield Street, Morgantown, West Virginia 26505

Received October 11, 1991; accepted March 9, 1992

scelus; Phobocampe unicincta; Compsilura concinnata; Parasetigena silvestris; Blepharipa pratensis.

Larval parasitism of gypsy moth, Lymantria dispar (L.), was monitored in 11 study plots in northern New Jersey from 1978 to 1988. Five parasitoid species were commonly found. Parasitism by Cotesia melanoscelus (Ratzeburg) was highest at the peak of egg mass density during a gypsy moth outbreak. Phobocampe unicincta (Gravenhorst) had low and relatively constant parasitism levels through the outbreak, but parasitism fell near zero after the host population crashed. Parasitism by Compsilura concinnata Meigen peaked during the decline of gypsy moth populations and probably was related primarily to the presence of alternate hosts. Parasetigena silvestris (Robineau-Desvoidy) had the highest levels of parasitism overall. Levels remained high throughout the outbreak and declined with the host populations. Parasitism by Blepharipa pratensis (Meigen) was highest in the first year of the study, when egg mass density was increasing, and declined steadily thereafter, following the trend of host larval density. Parasitism by all species except C. concinnata was correlated significantly and positively with the density of host larvae. Three species showed delayed density dependence. Direct density dependence, density independence, or indeterminate density relationships were observed for all species across study plots within seasons. The relationship of parasitism to ecological factors was investigated through stepwise multiple regression analysis. Parasitism by C. melanoscelus was correlated primarily with winter and spring temperatures and gypsy moth egg mass density. For P. unicincta parasitism, most variation was explained by parasitism by C. melanoscelus and stand density. Parasitism by C. concinnata was correlated most strongly with stand composition and percentage infection by gypsy moth nuclear polyhedrosis virus. Percentage defoliation of oaks explained most variation in parasitism by P. silvestris and B. 0 1992 Academic Press, Inc. pratensts. KEY WORDS: Insecta; Lymantria dispar; gypsy moth; density dependence; biological control; Cotesia melano-

INTRODUCTION The gypsy moth, Lymantria dispar (L.), was introduced into the United States near Boston, Massachusetts, in the late 1860s and became a serious defoliator of forest and shade trees by the 1890s. This pest inspired the development by the U.S. Department of Agriculture of one of the earliest biological control programs in the United States (Howard and Fiske, 1911). The program eventually became one of the biggest in history and was active during the years 1905-1914 and 19221933 (Burgess and Crossman, 1929). During these years, many species of parasitoids were imported from Europe and the Far East. Ultimately, 10 species were established (Hay, 1976). Six of the 10 established species attack gypsy moth larvae: Cotesia melanoscelus (Ratzeburg), Phobocampe unicincta (Gravenhorst), Blepharipa pratensis (Meigen), Compsilura concinnata Meigen, Exorista larvarum (L.), and Parasetigena silvestris (Robineau-Desvoidy). Although these species are widespread and are continual components of larval mortality, their role in natural control has been unclear (Campbell and Sloan, 1977). Very little is known about most of them beyond laboratory studies associated with their original importation and mass rearing (Burgess and Crossman, 1929). Only one study (Ticehurst et al., 1978) has reported dynamics of larval parasitism in the United States for more than a few generations. A few others have investigated density-dependent responses in the field (Weseloh, 1973a; Liebhold and Elkinton, 1989; Gould et al., 1990). This paper reports the results of a long-term commitment to investigate gypsy moth populations through all phases of their dynamics. The New Jersey Department 35

1049.9644/92$5.00 Copyright 0 1992 by Academic Press, Inc. All rights of reproduction in any form reserved.

36

WILLIAMS ET AL.

of Agriculture established 17 permanent study plots in 1970 with the primary goal of monitoring the establishment and relative effectiveness of parasitoids that were imported and mass reared in a renewed biological control effort against gypsy moth during the 1970s. Through this monitoring, considerable information has been gathered on the established larval parasitoids over an 11-year period. In the following, we present analyses of these data with the following objectives: to examine the dynamics of parasitism relative to the phases of a gypsy moth outbreak, to investigate the strength and types of density dependent responses of individual species, and to elucidate other environmental factors relevant to parasitism by individual species. MATERIALS AND METHODS

Study plot and weather station locations, forest stand characteristics, and the method of estimating gypsy moth egg mass density were described by Williams et al. (1990). The first infestations by gypsy moth at these locations were reported from 1954 to 1969 and the outbreak during this study (1980-1982) was the second or third in all plots. Consistent monitoring of larval and pupal populations began in 1978. Two 91-m crossed transects oriented along N-S and E-W axes were established in the center of each 1.5-ha plot. Six trees spaced evenly along each transect were selected for sampling. The trees selected were in the “most-preferred” category as gypsy moth hosts (Houston, 1974). Burlap bands were fastened around each tree at a height of 1.5 m to collect gypsy moth larvae and pupae. Collections generally were made from the same 12 trees over the course of the study. In some cases, tree mortality necessitated relocating a burlap to an adjacent tree. Sampling was carried out at weekly intervals from May through July. On each sample day, all early instars (i.e., I-III), late instars (IV-VI), and pupae were collected under the burlap bands on each of the 12 trees in a plot. The sampling procedure probably underestimated the density of early instars because they generally do not congregate under burlap bands. Larvae were reared individually in the laboratory (12:12 L:D at 21-24°C) on an artificial diet (Bioserve Inc., Frenchtown, NJ). Pupae were held in individual containers. After 3 weeks, individuals were recorded as healthy, killed by disease, including gypsy moth nuclear polyhedrosis virus (NPV) or unidentified pathogens, killed by parasitoids, or killed by unknown causes. Parasitism was identified by the emergence of one or more parasitoids from a host. In cases of multiple parasitism or superparasitism, each parasitoid was counted as a fraction of an individual with the value equal to the inverse of the number of parasitoids that emerged. For each species, parasitism was quantified as peak percent-

age parasitism, which was the highest percentage observed in a plot during the season in a sample of at least 50 hosts. Peak percentage parasitism was selected as the measure most likely to provide a good estimate of the stage-specific impact of parasitoids under the sampling plan used (Gould et al., 1989). In computing percentage parasitism, the sum of early and late instars i n a sample was used as the denominator for C. melanoscelus and P. unicincta because these species are known to attack and emerge from larvae exclusively. The sum of late instars and pupae was the denominator for B. pratensis, C. concinnata, and P. silvestris. These tachinids most commonly attack late instars, but may emerge from either late instars or pupae in varying proportions depending upon the species (Burgess and Crossman, 1929). Parasitism percentages were transformed using the arcsine-square root transformation for all analyses. Several study plots had gypsy moth populations so sparse that fewer than half of the years had even one weekly sample large enough (i.e., >50) to determine percentage parasitism. Therefore, only 11 of the 17 plots were used in the analyses, and these plots had at least 7 years of adequate sample sizes. Although the potential number of observations in the data set was 121 (i.e., 11 plots times 11 years), the actual number used in the analyses was lower as a result of missing data. To investigate density dependence, transformed percentage parasitism was regressed against larval density for each species [PROC GLM in SAS (SAS Institute, 1988)]. The independent variable for the hymenopterous species was the common log of the peak number of small and large larvae collected in a sample during the season in each of the study plots. The density estimate for the tachinids was the common log of the peak number of large larvae. Peak larval counts were chosen as the density variable because they provide the best relative estimate of the host population subject to parasitism early in the season. Thus, they are not biased by the parasitism process itself. In a further analysis, the plots were partitioned along the lines of average density from 1978 to 1988; the six highest density plots and the five lowest were analyzed separately for density dependence. To investigate the possibility of delayed density dependence, transformed percentages of parasitism were regressed against the common log of the peak larval density in the previous year using the methods described above. Within-season patterns of parasitism among study plots also were investigated by regressing transformed percentage parasitism for each species on log larval density year by year. The effects of environmental factors on parasitism were investigated using forward stepwise multiple regression analyses [i.e., PROC REG in SAS (SAS Institute, 1988)]. Transformed percentage parasitism was the dependent variable. The independent variables are listed in Table 1. A significance level of 0.10 was the

LARVAL PARASITISM IN L. d&par

TABLE 1 Environmental Variables Used in the Multiple Regressions 1. Mean monthly maximum temperatures (“C) in September-May 2. Mean monthly minimum temperatures (“C) in September-May 3. Cumulative seasonal precipitation (cm) for fall (SeptemberNovember), winter (December-February), and spring (MarchMay) 4. Annual estimate of peak percentage defoliation of oak spp. 5. Index of stand preference for feeding by gypsy moth 6. Total basal area (m’/ha) of study plotb 7. Basal area (m’/ha) of white and red oak spp. 8. Common log of number of egg masses per ha in the current season 9. Common log of the peak number of larvae collected over all sampling dates in the current season 10. Peak percentage parasitism (arcsine-square root transformed) by each of the parasitoid species 11. Peak percentage infection (transformed) by gypsy moth NPV ’ See text for definition. * Basal area is the total cross sectional area (m’) of tree stems at breast height in 1 ha and provides an index of tree foliage density in a stand.

criterion for a variable to remain in a regression model. Independent variables in the regressions were tested for collinearity using PROC REG in SAS (Sall, 1981). Criteria for assessing collinearity were from McGiffen et al. (1988). Significantly collinear variables were dropped from the regressions. Temperature and precipitation data were obtained from weather stations as close as possible to the study plots (NOAA, 1978-1988) [see Williams et al. (1990) for locations]. The preference index (Table 1) was an average of the preference classes for feeding by gypsy moth (Houston, 1974) of tree species in a study plot weighted by their relative abundance. The index was calculated for each plot as

I = ~ PROPi. PREFi, i=l

where PROPi is the stand proportion of tree species i and PREFi is the preference class of species i (Houston, 1974). Species 1 included species in the white oak group (preference class l), and species 2 included those in the red oak group (class 2). Species 3 and 4 were the other two most common species in a plot (classes 3-5). As an example, an index of one indicated a stand composed entirely of species highly preferred by gypsy moth (e.g., Quercus alba L.), and higher values indicated the presence of less-preferred hosts. RESULTS

Incidence of parasitism. Five parasitoid species were found commonly attacking gypsy moth: C. melanoscelus,

37

P. unicincta, C. concinnata, P. silvestris, and B. pratensis. Exorista larvarum was never reared from larval or pupal samples. Gypsy moth populations were in outbreak phase in the early years of the study (1980-1983) and began to crash in 1984 (Fig. 1). Although timing varied, all plots had peak egg mass populations from 1980 to 1982. Parasitism by C. melanoscelus was in synchrony with the outbreak (Fig. 1A). Parasitism was less than 5% in most years, but exceeded 8% in 1981 and 1982 when gypsy moth populations were highest. Parasitism by P. unicincta was consistently low (Fig. lB), rarely exceeding 5% in individual plots. Low parasitism levels were maintained during the decline in gypsy moth populations, but parasitism decreased to near zero after the final crash in 1986. Patterns of parasitism varied among the three species of tachinids. Parasitism by C. concinnata was low, usually less than 5%, during the outbreak years (Fig. 1C). Parasitism was highest before the outbreak (1978) and in the decline phase (1985). Parasitism by P. silvestris was the highest of all parasitoid species (Fig. lD), exceeding 20% on average in the years of the outbreak and decline, and only dropping below this level after 1983 as host populations were crashing. Parasitism by B. pratensis was highest at 10% in the first year of the study and declined steadily thereafter, averaging less than 1% after 1983 (Fig. 1E). Density dependence. Visual comparisons of percentage parasitism (Figs. lA-1E) with larval density (Fig. 1F) suggested density dependence for most parasitoid species. The linear regressions of percentage parasitism on larval density were highly significant for all species except C. concinnata (Table 2). Percentage parasitism by C. concinnata was uncorrelated with gypsy moth density in all regressions. All regression slopes were positive. Slopes for the low-density plots were higher than those for the high-density plots in all species except B. pratensis. Despite the statistical significance, the variation in parasitism accounted for by density was uniformly low; the best regression, that for B. pratensis, accounted for only 22%. In the analysis of delayed density dependence, regressions of parasitism on larval density in the previous season were significant for C. melanoscelus, P. unicincta, and B. pratensis (Table 3). Slopes were positive in all cases. The r2 values for these three species were equal to or lower than those for regressions on larval density in the current year (Table 2). When percentage parasitism was regressed on density across plots within years (Table 4), significant density dependence was found for at least one species in six of the 11 years of the study. Slopes in all the significant regressions were positive, indicating direct density dependence. Each of the parasitoids showed significant

38

WILLIAMS ET AL. 15

Cores/a

70

7 9 00

A

melanoscelus

8102

03

84

a 5 86

tm

4

8 7 88

Phobocampe

7 8 7 9 a0

w

Year 15

F

Compsllura

0

C

1amo

40

8 3 84

85

00

8 7 08

Parssetlgeno

01

sllvertrlr

1ooa

A

,,,,,,, 7 0 79 00 81.32 03 04 05

: ’ :,/’ :, 00 a7 08

1

Year 10

82

E

Year

conclnnat.9

.*---‘..

unlclncte

Blepharlpa pretensls

0

,,,,,,, 7 8 79 80 8102 83 84

05

:.,,” :. 00 8 7

1 88

Year

toooo

1

FIG. 1. Comparison of peak percentage parasitism by five larval parasitoids (circles, solid line), gypsy moth peak larval density (circles, solid line), and gypsy moth egg mass density (dots, broken line) over time. The parasitism percentages were retransformed from plot means calculated under the arcsine-square root transformation. (A) C. melanoscelus, (B) P. unicincto. (C) C. concinnata, (D) P. siluestris, (E) I?. pratensis, and (F) larval density (common log scale).

density dependence for at least 1 year. C. melanoscelus led the other species with three occurrences. Ecological relationships. The five-variable model for C. melanoscelus explained 57% of the variation in parasitism (Table 5). Temperature effects predominated, three variables were monthly temperatures. A fourth temperature variable, the October maximum, was found to be collinear with the others and was dropped from the analysis. Parasitism by C. melanoscelus was related positively to gypsy moth egg mass density and to percentage parasitism by P. unicincta. The model for P. unicincta also included five variables and explained 32% of the variation (Table 5). Parasitism was correlated posi-

tively with percentage parasitism by C. melanoscelus and P. silvestris and negatively with plot basal area, percentage infection by NPV, and temperature in May. The regression model for C. concinnata was dominated by the stand preference index and percentage infection by NPV, which were both related inversely to percentage parasitism (Table 6). The remaining two variables were abiotic factors, average monthlytemperatures in the fall and spring. A fifth variable, log of large larvae, was removed from the model because it was found to be collinear with the others. The regression model for P. silvestris was unique in including only biotic variables (Table 6). The dominant

39

LARVAL PARASITISM IN L. &spar

TABLE 2 Correlation of Peak Percentage Parasitism (Arcsine-Square Root Transformed) with Peak Larval Density (Log Transformed) for Five Parasitoids of the Gypsy Moth over Plots Grouped into Two Density Classes High-density plots

Low-density plots

All plots

Species

n

b

r2

P

n

b

r2

P

n

b

r’

P

Cotesia melanoscelus Phobocampe unicincta Compsilura concinnata Parasetigena siluestris Blepharipa pratensis

57 57 55 55 55

0.182 0.086 0.039 0.245 0.238

0.13 0.11 0.01 0.11 0.26


42 42 41 41 41

0.187 0.135 0.113 0.326 0.176

0.20 0.21 0.04 0.19 0.19

<0.01** <0.01** 0.21
99 99 96 96 96

0.184 0.111 0.075 0.286 0.207

0.16 0.16 0.02 0.15 0.22

<0.01** <0.01** 0.15 <0.01** <0.01**

variables were two host density factors, density of large larvae and percentage defoliation of oaks, related variables with slopes of opposite sign. The inverse relationship between parasitism and percentage defoliation is shown in Fig. 2. At the highest levels of defoliation (>50%), parasitism by P. silvestris was generally low (~25%). Percentage parasitism was correlated inversely with parasitism by C. concinnata and directly with parasitism by C. melanoscelus. The regression model for B. pratensis contained six variables, which were split evenly between biotic and abiotic factors (Table 6). Parasitism was correlated directly with percentage defoliation of oaks and egg mass density, and inversely with percentage parasitism by C. concinnata. The remaining variables were average temperatures in fall and winter months. Another temperature variable, the September maximum, was collinear with the others and was dropped from the analysis. DISCUSSION Incidence ofparasitism. In general, patterns of parasitism by the five species with respect to gypsy moth egg mass density contrasted with published studies. Ticehurst (1981) reported highest parasitism by C. melanoscelus in the year following peak egg mass populations in Pennsylvania, whereas peak parasitism coincided with peak egg mass density in this study. This pattern held in

TABLE 3 Correlation of Peak Percentage Parasitism (ArcsineSquare Root Transformed) with Peak Larval Density (Log Transformed) in the Previous Season Species C. P. C. P. B.

melanoscelus unicincta concinnata siluestris pratensis

n

b

r2

P

82 82 76 76 76

0.180 0.117 0.052 0.096 0.138

0.13 0.16 0.01 0.02 0.12

<0.01** <0.01** 0.40 0.29 <0.01**

6 of the 11 study plots and the other 5 were split between the years just before and just after the egg mass peak. Ticehurst (1981) and Fuester et al. (1983), who worked in Austria, reported highest levels of parasitism by P. unicincta in the second to third year of the decline phase. In our study, parasitism was highest at the gypsy moth peak, but did not vary widely from 1978 until the population crash in 1986, Parasitism by P. unicincta also was considerably lower in New Jersey than in Pennsylvania, where the highest parasitism was 6.5%, or in Austria, where levels peaked at 27-28%. The dynamics of C. concinnata parasitism were similar to those reported by Sisojevic (1975) in Yugoslavia; the highest levels of parasitism were reported in the increase phase of an outbreak and during the innocuous phase (cf. Fig. 1C). C. concinnata is a highly polyphagous parasitoid (Webber and Schaffner, 1926) and some of the activity observed probably resulted from hosts other than gypsy moth. After 1978, qualitative observations were made of defoliation by other lepidopterous species. Activity by other defoliators was low in 1983. The relatively high parasitism in this year may have resulted from delayed density dependence occurring just after the peak of gypsy moth outbreak. During the period of 1984-1986, several species of Lepidoptera, including an Archips sp., Ennomos subsignarius (Hiibner), Malacosoma americanurn (F.), and M. disstria Hiibner, caused moderate damage in the plots. The high levels of parasitism in these years likely resulted from the presence of these defoliators, known hosts of C. concinnata (Webber and Schaffner, 1926; Schaffner, 1959). Their increased numbers could have triggered a buildup of parasitoid populations. Our observations of parasitism by P. silvestris and B. pratensis contrasted with those reported by other researchers. Sisojevic (1975) and Ticehurst (1981) reported highest levels of parasitism by P, silvestris 1 to 2 years after the peak of the outbreak. In our study, the highest levels occurred as host populations were increasing and at the peak of the outbreak, and parasitism tracked the population decline for the following 2 years. Sisojevic (1975) and Ticehurst (1981) found high levels

40

WILLIAMS ET AL.

TABLE 4 Correlation

of Peak Percentage Parasitism (Transformed) with Peak Larval Density (Log Transformed) for Five Parasitoids of the Gypsy Moth across All Plots by Year C. melanoscelus

Year

n

1978

11 11 11 7 6 8

1981 1983 1984 1986 1988 Note. All

2

0.42

NS NS

P. unicincta

P

I^2

0.03

o,43 0.40

0.73 0.62

p

P NS

NS

P

0.58 o,03 0.04

rL

P

to.01

NS NS NS NS NS

NS NS NS NS NS

NS NS NS

0.03 0.02

P. siluestris

C. concinnata

0.60

H. pratensis r2

P NS NS NS

0.77

10.01 NS NS

0.02

slopes of significant regressions (P 2 0.05) were positive.

of parasitism by B. pratensis in the year preceding the peak of the outbreak and in the second year following. Across all our study plots, parasitism started high in 1978 and decreased steadily over the course of the study, with no apparent relationship to the egg mass dynamics. The dynamics of B. pratensis parasitism appeared more dependent upon the dynamics of larval populations, which they more closely paralleled (Fig. lF), than those of egg masses. Density dependence. Other researchers (Reardon, 1976; Ticehurst et al., 1978) have reported moderate to strong negative correlations of percentage parasitism and egg mass density. This likely occurred because their investigations focused primarily on high-density populations during outbreaks. Correlations of percentage parasitism with egg mass density in our data were generally

weaker than those with larval density and, thus, are not reported. Egg mass density explained more variance than larval density only for C. melanoscelus (r2 = 0.21, P < 0.001). Patterns of parasitism by C. melanoscelus, P. unicincta, P. silvestris, and B. pratensis, which are specific to gypsy moth, generally followed the trend of larval density. Regression slopes for C. melanoscelus, P. unicincta, and P. silvestris were higher in the low-density plots than the high, suggesting that their attack responses were higher in endemic populations or that they were relatively less efficient in outbreak populations. Conversely, the higher slope for B. pratensis was in the high-density plots, suggesting that this parasitoid might be more effective in building populations. The lack of correlation for C. concinnata reflects its polyphagy, suggesting that other hosts are more important

TABLE 5 Parameters for the Regressions of Peak Percentage Parasitism (Transformed) by C. melunoscelus on

Several

Variable”

Environmental

Slope

Variables

for

the

Years

and P. unicincta

1978-1988

SEM

Partial r2

P

0.27 0.11 0.08 0.08 0.05

to.001
0.17 0.09 0.03 0.03 0.03

10.001 0.005 0.040 0.049 0.053 to.001

C. melanoscelus (n = 99, adjusted r* = 0.57, P < 0.001)

Mean maximum temp. in Jan.

-0.026 0.032 0.023 0.548 0.010 -0.031

Log EM/ha* in current year Mean minimum temp. in May % Paras. by P. unicincta Mean minimum temp. in Feb.

Intercept

0.004 0.007 0.006 0.116 0.003 0.066

P. unicincta (n = 99, adjusted r2 = 0.32, P < 0.001)

% Paras. by C. melanoscelus Plot basal area % Infection by NPV % Paras. by P. silvestris Mean minimum temp. in May Intercept a Parameters were fit using a forward stepwise

b Egg masses per hectare.

0.211 PO.003 -0.071 0.063 -0.009 0.212

0.055 0.001 0.034 0.031 0.005 0.049

procedure and are ordered according to their sequence of entry into the model.

41

LARVAL PARASITISM IN L. dispar

TABLE 6

Parameters for the Regressions of Peak Percentage Parasitism (Transformed) by Three Tachinid Species on Several Environmental Variables for the Years 1978-1988 Variable”

Slope

SEM

Partial F*

P

0.17 0.10 0.07 0.07

10.001 0.002
0.15 0.19 0.06 0.04


0.25 0.12 0.07 0.09 0.03 0.01 -

0.012 co.oo1
Compsilura concinnata (n = 96, adjusted r* = 0.39, P i 0.001) Preference index % Infection by NPV Mean minimum temp. in May Mean maximum temp. in Oct. Intercept

-0.139 -0.195 -0.035 0.026 0.585

0.025 0.063 0.009 0.008 0.140

Parasetigena silvestris (n = 96, adjusted r2 = 0.41, P c 0.001) Log larval dens. current year % Defoliation of oaks % Paras. by C. concinnata % Paras. by C. melanoscelus Intercept

0.426 -0.007 -0.325 0.357 -0.391

0.068 0.001 0.123 0.144 0.146

Hephuripa pratensis (n = 96, adjusted r2 = 0.54, P < 0.001) % Defoliation of oaks Mean minimum temp. in Feb. Mean minimum temp. in Nov. Log EM/ha* in current year Mean maximum temp. in Nov. % Paras. Ly C. concinnata Intercept D Parameters were fit using a forward stepwise * Egg masses per hectare.

0.002 -0.018 0.025 0.040 -0.017 -0.110 0.118

0.001 0.003 0.005 0.009 0.007 0.063 0.089

procedure and are ordered according to their sequence of entry into the model.

in explaining its dynamics. The only comparable published analyses were by Fuester et al. (1983) for C. melanoscelus and I? unicincta in Austria. Similar to the present study, they reported a low, positive response (r2 = 0.15) of C. melanoscelus to larval density in the same year and a positive response to density in the previous year (r2 = 0.33), suggesting delayed density dependence. Unlike this study, they found no correlation of P. unicinctu parasitism with larval density (r2 < 0.01). In recent years, inverse density dependence or density independence often have been observed more frequently than direct density dependence in field studies at single points in time (Weseloh, 1973a; Morrison and Strong, 1980). This observation has led to a greater appreciation of spatial relationships in the dynamics of parasitism and some rethinking of biological control theory (Waage and Greathead, 1988). Significant density dependence was observed in this study in 8 of the 55 combinations of parasitoid species and years. All other cases were nonsignificant, indicating density independence or indeterminate density dependence (Brown, 1989). Of the significant correlations, direct density dependence was observed consistently, with each parasitoid species showing significant within-season density dependence for at least 1 year. Although the plots were widely separated geographically and diverse in many en-

vironmental factors, the consistency of the relationships at this large spatial scale strongly suggests that direct density dependence occurred in gypsy moth populations in some years at least. The direct density dependence observed over the llyear duration of the study for C. melanoscelus, P. unicincta, P. silvestris, and B. pratensis underscored the need to observe the activity of a parasitoid over time to assess its performance as a biological control agent. Our results support recent findings that the detection of density dependence increases with the number of generations that populations are observed (Hassell et al., 1989). Ecological relationships. The well-known statistical maxim “correlation is not causation” is best kept in mind when interpreting the multiple regression analyses. An underlying mechanism for understanding the effects of many of the independent variables that were correlated significantly with percentage parasitism may not be apparent. Nevertheless, the roles of some of the ecological factors may be speculated upon in relation to knowledge of the biology of the parasitoid species. The effects of temperature on parasitism by C. melanoscelus may be interpreted in the light of its biology. The most significant winter temperature variable (i.e., maximum temperature in January) was correlated nega-

42

WILLIAMS ET AL 100 v = 28.05

- 0.254X

#=0.06, P=O.Ol

0

20

40

80

80

100

Percentage oak defoliation FIG. 2. Relationship between percentage parasitism by Parusetisiluestris and percentage defoliation of oaks. Note that percentage defoliation explains appreciably less variation in parasitism in the single regression shown than in the multiple regression (Table 6).

germ

tively with parasitism, whereas the spring variable (minimum temperature in May) was correlated positively. Using the regression model as a predictor, a cold winter followed by a warm spring would result in high parasitism, and, conversely, a warm winter followed by a cool spring in low parasitism. These patterns are reasonable considering the effects of temperature on diapause and postdiapause development. Termination of diapause is hastened by a long exposure to a cold temperature in the laboratory (Weseloh, 1973b) and, thus, by cold winter temperatures in the field by inference. The rate of postdiapause development in the spring increases with temperature, and the developmental rates of C. melanoscelus and gypsy moth are closer at higher temperatures, permitting a better synchrony of C. melanoscelus with susceptible stages of gypsy moth (Weseloh, 1976). Thus, the combination of winter and spring temperatures may influence the uniformity of termination of diapause and subsequent synchronization of the host and parasitoid populations to yield greater or lesser degrees of parasitism from season to season. The apparently lesser effect of gypsy moth egg mass density on parasitism probably resulted from the variability in survival of the overwintering parasitoid population caused by hyperparasitism (Muesebeck and Dohanian, 1927). The model for P. unicincta yielded the lowest correlation overall, and the independent variables were the least obvious for interpretation. Any positive roles of parasitism by C. melanoscelus and P. silvestris were not obvious. The inverse relationship between percentage parasitism and plot basal area suggests that parasitism is higher in more open forest stands, a notion in contrast with published observations that parasitism is more abundant in dense woodland than in open areas

(Muesebeck and Parker, 1933). The inverse correlation of parasitism with percentage infection by NPV is reasonable because the virus probably kills gypsy moth larvae before the emergence of adult parasitoids. P. unicincta is a relatively rare species and little is known about its biology. It is possible that other factors not accounted for may have obscured our correlations; specifically, P. unicincta may be subject to severe hyperparasitism and to host defense responses by gypsy moth (Muesebeck and Parker, 1933). The negative correlation with the preference index indicates that parasitism by C. concinnata was enhanced in stands with high proportions of preferred host trees. C. concinnata is a mobile parasitoid that readily aggregates in areas with elevated gypsy moth populations (Liebhold and Elkinton, 1989). Thus, a direct relationship between favorable host habitat and parasitism is reasonable. As with P. unicincta, the negative effect of NPV infection on parasitism likely resulted from mortality due to virus of hosts that were both parasitized and diseased. Correlations with temperature variables were less obvious. The multivoltine nature of C. concinnata and its overwintering in live hosts other than gypsy moth (Webber and Schaffner, 1926) likely obscure the effects of weather on parasitism. Host density and oak defoliation were clearly the dominant factors in parasitism by P. silvestris. Although these variables were positively correlated, oak defoliation and parasitism were negatively correlated, as seen in Fig. 2. The 16 observations above 25% defoliation had low levels of parasitism, and these points were important in determining the inverse relationship. These observations represent the highest larval densities, and high defoliation suggests larval crowding, which has been reported to interfere with oviposition by P. silvestris females (Sisojevic, 1975). The negative correlation of parasitism by P. silvestris with that by C. concinnata may reflect a competitive interaction with the other tachinid, which attacks the same host life stages (Burgess and Crossman, 1929). Percentage defoliation of oaks clearly was the most important factor in determining parasitism by B. pratensis. Because the parasitoid produces microtype eggs that are oviposited on leaves and ingested by gypsy moth larvae (Burgess and Crossman, 1929), a direct relationship between defoliation and parasitism is reasonable. As with C. concinnata, the effects of the several temperature variables were less obvious. Although we do not have control over the environmental variables discussed, it is important to understand their influence to appreciate better the limitations to natural control. It is hoped that future experimental studies will quantify these relationships and permit better understanding of the occurrence and dynamics of larval parasitism.

LARVAL PARASITISM IN L. dispar

ACKNOWLEDGMENTS We thank P. Mina, M. Mayer, and R. Ward for their assistance in collecting the data and J. J. Drea, J. S. Elkinton, and R. M. Weseloh for their thoughtful comments on the manuscript. This article reports the results of research only. Mention of a proprietary product does not constitute an endorsement or a recommendation for its use by the USDA.

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