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Is parasitism of numerically dominant species inmacrolepidopteran assemblages independent oftheir abundance?

Pedro Barbosaa,*, Toomas Tammarub,c, Astrid Caldasa

aDepartment of Entomology, University of Maryland, College Park, MD 20742, USAbInstitute of Zoology and Hydrobiology, University of Tartu, Vanemuise 46, EE-51014, Tartu, EstoniacInstitute of Zoology and Botany, Estonian Agricultural University, Riia 181, EE-51014, Tartu, Estonia

Received 29 July 2003; accepted 10 December 2003

SummaryRefuge theory proposes that a determinant of species richness (and percentparasitism) is the presence of host refuges. Plant structural refuges are goodpredictors of species richness for endophytic herbivores, but not for exophyticherbivores. For exophytic herbivores other traits such as relative abundance mayprovide refuge from parasitism. Using unbiased data on both relative abundance andlarval parasitism of species in macrolepidopteran assemblages we tested the nullhypothesis that percent parasitism was independent of abundance. Numericallysubdominant species do not gain refuge from parasitism by persisting at lowabundance. Parasitism was not different from what would be expected based ontheir numbers. Among numerically dominant species there was, nevertheless, asignificant positive association between abundance and parasitism rate. However,dominant herbivores displayed high levels of parasitism even in the years when theirabundance was low relative to other years. This suggests that dominant species maypossess other traits that enhance their susceptibility to parasitoids.& 2004 Published by Elsevier GmbH.

ZusammenfassungDie Refugien-Theorie schl.agt vor, dass eine Determinante der Artenzahl (und derprozentualen Parasitierung) die Verf .ugbarkeit von Wirtsrefugien ist. Strukturellepflanzliche Refugien liefern eine gute Vorhersage f .ur die Artenzahl endophytischerHerbivorer, jedoch nicht f .ur exophytische Herbivore. For exophytische Herbivorem.ogen andere Eigenschaften, wie die relative Abundanz, ein Refugium vorParasitismus bieten. Unter der Verwendung von erwartungsgetreuen Daten sowohlf .ur die relative Abundanz und als auch die larvale Parasitierung der Arten inmakrolepidopteren Ansammlungen untersuchten wir die Null-Hypothese, dass die

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KEYWORDSScarce species;Box elder;Black willow;Salix nigra;Acer negundo;Refuge theory;Host abundance;Parasitoids

*Corresponding author. Tel. þ301-405-39-46; fax: þ301-314-63-34.E-mail address: pbarbosa@umd.edu (P. Barbosa).

1439-1791/$ - see front matter & 2004 Published by Elsevier GmbH.doi:10.1016/j.baae.2003.12.001

Basic and Applied Ecology 5 (2004) 357–366

prozentuale Parasitierung unabh.angig von der Abundanz ist. Anzahlm.a�ig subdomi-nante Arten erreichen kein Refugium vor Parasitismus indem sie bei niedrigenAbundanzen persistieren. Die Parasitierung unterschied sich nicht von der, dieaufgrund ihren Anzahlen erwartet w .urde. Unter den anzahlm.a�ig dominanten Artengab es nichtsdestoweniger eine signifikante positive Verbindung zwischen derAbundanz und der Parasitierungsrate. Dennoch wiesen die dominanten Herbivorensogar in den Jahren, in denen ihre Abundanz im Vergleich zu anderen Jahren geringwar, hohe Parasitierungsgrade auf. Dies l.a�t vermuten, dass dominante Arten andereEigenschaften besitzen k.onnten, die ihre Anf.alligkeit gegen .uber Parasitoiden erh-.ohen.& 2004 Published by Elsevier GmbH.

Introduction

Differences in herbivore traits, which are importantto natural enemies searching for hosts, resultin differential vulnerability to parasitoids. In thestudy of parasitoid community ecology thisrelationship was formalized by Hochberg andHawkins (1992, 1993, 1994) and Hawkins, Thomas& Hochberg (1993) in the ‘‘Refuge Hypothesis’’which argues that (plant-associated) structuralrefuges, e.g., host feeding niche, influence theease with which parasitoids find hosts and, thus,parasitoid richness/species load (i.e., the numberof parasitoids to which host species are vulner-able). Originally, the refuge theory was supportedby data on assemblages of endophagous herbivoresbut failed to predict observed patterns of para-sitoid richness for exophytic herbivores (Hochberg& Hawkins, 1994). Alternatively, for exophyticherbivores, protection from parasitism may beachieved by mechanisms other than structuralrefuges.

Vulnerability of herbivores to parasitoids isaffected by differences in behavior, chemistry, ormorphology (Zw .olfer & Kraus, 1957; Arthur, 1962;Herrebout, 1969; Stiling, 1980; Ankersmit, Acre-man, & Dijkman, 1981; Vinson, 1984; Carton &David, 1985; Damman, 1987; Jaenike, 1986; Gross& Price, 1988; deJong & van Alphen, 1989; Gauld,Gaston, & Janzen, 1992; Gross, 1993; Gentry &Dyer, 2002). However, the relative abundance atwhich a species typically persists also may be afactor in its vulnerability to parasitoids. Most insectspecies typically exist at relatively low densities,i.e., most insect species are scarce (Williams, 1964;Ward & Spalding, 1993). However, even in assem-blages of scarce species, abundance is not uni-formly distributed across species. In any giveninsect assemblage (regardless of the number ofspecies present) only a few (numerically dominant)species account for the vast majority of totalnumber of individuals in the assemblage. In con-

trast, most other (numerically subdominant) spe-cies in assemblages occur at extremely low levels;often represented in samples as singletons (i.e.,represented by single individuals in samples). Thispattern of species abundance distribution amonginsect taxa and their natural enemies is relativelycommon and widespread in natural and managed,tropical and temperate habitats (Williams, 1964;Butler, 1992; Butler & Kondo, 1993; Allison,Samuelson, & Miller, 1997; Basset, 1997; Didham,1997; Floren & Linsenmair, 1997; Harada & Adis,1997; Barbosa, 1998; Barbosa, Segarra, & Gross,2000). Although many herbivore, parasitoid, andpredator assemblages consist of dominant andsubdominant species, the impact of this dichotomyon parasitoid–host interactions, and in particularon susceptibility to parasitism, has received littleattention (Lawton, 1978; Price, 1980; Price, Bou-ton, Gross, MePheron, & Weis, 1980; Lawton &Strong, 1981; Strong, Lawton, & Southwood, 1984;Hawkins & Sheehan, 1994).

Parasitoid responses to increasing host density, intime and space, have been investigated (Royama,1977; Hassell, 1987; Berryman, 1999). However,whether differentially abundant co-occurring her-bivores vary in their susceptibility to parasitism hasyet to be determined. The abundance of certainhost species, relative to that of others, may makethem more or less easily found by parasitoids ormore or less vulnerable to parasitism. For example,when given a choice between high and low densitypatches, some parasitoids are observed in high hostdensity patches (Waage, 1983; Summy, Gilstrap, &Hart, 1985; Nealis, 1990). Thus, existence atrelatively low abundance may provide refuge fromparasitism. The association between host abun-dance and parasitoid richness (Sheehan, 1994) andthe correlation between parasitoid richness andpercent parasitism (Hawkins & Gagn !e, 1989;Hawkins and Gross, 1992; Hawkins, 1993) suggestthat relative abundance influences susceptibility toparasitoids.

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358 P. Barbosa et al.

Overall, patterns of parasitism of species inassemblages remain insufficiently documented todraw comprehensive generalizations. Whether therange of percent parasitism for numerically domi-nant and subdominant species are equivalentremains an open question, if only because of thesampling error associated with low density species.There is a high probability of error associated withthe statistical assessment of parasitism of subdo-minant species (just because they occur in such lownumbers).

The macrolepidopteran species on two ripariantree species, box elder Acer negundo L. and blackwillow Salix nigra (Marsh), form assemblages inwhich (as in other assemblages) a few speciesdominate numerically and most species are scarce(Barbosa et al., 2000). In general, only about 1–5larvae were collected per year for about 60% of thespecies on black willow and box elder (Barbosaet al., 2000). In this study, we use data from 5 yearsof intensive, unbiased and representative samplingof larval parasitism (Barbosa & Caldas, 2004) totest the null hypothesis that percent parasitism isequal among numerically dominant or subdominantspecies (i.e., is independent of abundance). Wetested this hypothesis using a simulation approachthat avoided the problems caused by samplingerror. We also tested the hypothesis noted abovefor the most abundant or the scarcest speciesonly. Further, we asked if parasitism of dominantspecies was solely dependent on their relativeabundance.

Materials and methods

Study system and data collection

Leaf-feeding macrolepidopteran larvae were col-lected from four (1994–1997) or six (1993) wood-land riparian sites in central Maryland, USA,specifically Colmar Manor Park of the Dueling CreekNature Area, Calvert Community Park, the Centraland North Tracts of the Patuxent Wildlife ResearchCenter, Paint Branch, and Rock Creek RegionalPark, Needham Lake, Montgomery Co. At each site,20 trees of either black willow or box elder wereeach visually searched for 10min by two indivi-duals. Each week, only 10 of 20 trees per specieswere searched and the alternate 10 trees weresampled the following week to minimize oversampling. This approach also allowed residentlarvae to develop to older instars, available forparasitism by parasitoids with a later phenology.Similarly, it allowed for the detection of multi-

parasitism if it occurred. Absolute sampling byfogging of the two tree species indicated that lowercanopy visual sampling, a relative measure ofabundance, provided an accurate assessment ofall macrolepidopteran species (Barbosa et al.,unpublished data). Sampling occurred between 31May and 20 August. Larvae were reared individuallyon appropriate foliage (disinfected to preventmortality due to disease), sorted by species, andthe number of larvae collected recorded. Levels oflarval parasitism for each macrolepidopteran spe-cies (sorted by the host’s tree species) werecalculated.

Box elder and black willow were selectedbecause they differ in growth habits and leafmorphology. In box elder, shoots and their leavesdifferentiate from overwintering buds. In contrast,black willow has both short shoots and long shootsfrom which early leaves form (at budbreak) andlate leaves, later in the season (Barbosa & Wagner,1989). Box elder leaves are pinnately compoundwith 3–5 leaflets, whereas in black willow leavesare narrow and lance-shaped with broad bases andtapering tips.

Statistical analyses of percent parasitism

The four-step approach used to determine ifspecies’ abundance and percent parasitism wereassociated involved the use of sets of specificstatistical (Monte Carlo-like) simulations. In thefirst step, an ordinary logistic analysis was con-ducted. The second step involved estimating theparameters of the underlying distribution of spe-cies-specific percent parasitism and was followedby step three, in which we assigned a simulatedpercent parasitism value to each species, creatingsimulated data sets. In the final, fourth step, thevalue of the slope from the original logisticregression was compared to the distribution ofslope values generated from the data sets in thesimulations.

Thus, in step one, a logistic regression wasapplied to evaluate the overall association betweenspecies’ abundance and percent parasitism (PROCGENMOD of SAS: SAS Institute, 1994). Total numberof larvae collected over 5 years, for each species inthe assemblages, was treated as the measure ofspecies’ abundance and used as the independentvariable in analyses. The binomial proportion (thenumber of larvae parasitized/total number oflarvae collected for each species) was treated asthe response variable; each species was treated asan independent observation. A binomial probabilitydistribution was assumed and logit was chosen as

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Parasitism of numerically dominant species 359

the link function. The DSCALE option was used tocorrect for overdispersion. Due to the samplingerror associated with the strong correlation be-tween the dependent variable (percent parasitism)and the size of the independent variable (i.e.,sample size) the reliability of the results waschecked using further simulation-based steps ofthe analysis.

In step two we estimated the parameters ofthe underlying distribution of species-specific le-vels of parasitism. That is, we asked how the levelsof parasitism were distributed among differentspecies, under the assumption of no sampling errorand no association between abundance and para-sitism. To determine the variance of these under-lying species-specific values, a subset of 31 specieswith sufficiently large sample sizes (n420) wasused. Logarithms of percent parasitism for thesespecies were found to fit a normal distribution(Shapiro-Wilk’s W ¼ 0:969; P ¼ 0:49). The inclusionof lower threshold sample sizes (N410) tendedto generate a platykurtic distribution althoughestimates of variance were similar. The varianceof the logarithm of the percentages was estimatedfrom these data and the mean of the resultinglog-normal distribution was set as a value equal tothe overall mean percent parasitism (14.6%) forthe entire data set. In step three, we assigneda simulated percent parasitism value to each ofthe 81 species in the actual data set. Eachparasitism value, assigned to a particular species,was randomly drawn from the log-normal distribu-tion (described above). The value each speciesreceived was thus independent of its abundance.One thousand independent simulations were con-ducted, resulting in percent parasitism values forall 81 species in 1000 different, independentiterations.

In the final fourth step, simulated samples weretaken from the large hypothetical population ofeach species. The samples taken were equal in sizeto those associated with the species in the actualdata set. As a result, 1000 simulated data sets weregenerated that corresponded to the null hypothesisof no association between species’ abundance andlevel of parasitism. Logistic regressions betweensample size and percent parasitism were thenperformed for all of the 1000 simulated samples.Thus, 1000 values of the slope of the regressionwere obtained. The value of the slope from theoriginal logistic regression (determined in step 1)was then compared to the distribution of thesimulated slope values in order to determine whatportion of the slopes obtained for simulationsequaled or exceeded that obtained using the actualdata. Determination of the statistical significance

of the association between species’ abundance andlevels of parasitism in the actual data set was basedon this comparison. If less than five percent of thesimulated slopes exceeded the actual value theassociation in the actual data set was consideredsignificant.

In addition to the overall analysis, noted above,the entire analysis was repeated with the threemost abundant (dominant) species removed fromthe data set. The simulated data sets were furtherused to determine whether the three most abun-dant species displayed higher than average levels ofparasitism. For this purpose, the average percentparasitism of the three dominant species wascalculated for all of the 1000 simulated data setsand for the actual data set. Again determination ofsignificance was based on the number of simula-tions that produced a value equal or greater thanthose based on actual data. An analogous proce-dure was performed with the scarcest (subdomi-nant) species only (species in which No10) todetermine if these least abundant species displayedlevels of parasitism different from the average.

We further determined if host use by parasitoidsis equally biased towards the dominant herbivoresirrespective of the current-year abundance of thedominants, i.e., we checked for the possibility thatparasitoids switch to the dominants only in theyears of high abundance of the respective dominantspecies. For this purpose, individual parasitismstatus in the actual data set (as a binary variable:parasitized or not) was treated as the responsevariable in the corresponding logistic regressions,and the analysis was performed separately for thethree dominant lepidopterans. There were twoindependent variables: ‘‘year type’’ and ‘‘species.’’Year type was included as a two-level variable. Theyear of the highest abundance of the respectiveparasitoid was contrasted to the remaining yearscombined (data pooled over these 4 years). Such anapproach was chosen due to the fact that for allthree dominant species, remarkably, high abun-dance was reached in one year of the survey, therest of the years having population densities thatwere similar to each other. Similarly, ‘‘species’’ wasa two-level variable: the respective dominant vs.all alternative host species in the sample (datapooled over these species). In this analysis, onlyshared parasitoids were considered, i.e., thespecies that were reared from the respectivedominant species, and at least one of the sub-dominant species in the assemblage. Similarly, theherbivores not known to have shared parasitoidswith the respective dominants were not consideredalternative hosts and were omitted from thesample in respective analyses.

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360 P. Barbosa et al.

In the described analysis, the ‘‘year type’’ X‘‘species’’ interaction term was of primary interest.Significance of this term would indicate thatthe distribution of parasitism between the domi-nant and alternative hosts was different in peakyears and average years, i.e., dependent on theabundance of the host. If the dominants weredisproportionately preferred in the years of theirpeak abundance, this could indicate that theparasitoids were able to switch to the hosts thathappen to be abundant in a particular year.

Results

In five years, a total of 4152 larvae of 81macrolepidopteran species were collected. TheGeometridae (25 species, 29% of all individuals)and Noctuidae (22 species, 26% of all individuals)were most well represented of nine macrolepidop-teran families. Most lepidopteran larvae wereidentified to the species level, although in 9 cases,larvae of closely related species (e.g., in thegenera Limentis and Lithophane) could not bereliably distinguished and were treated as onespecies in the analyses. Mean number of larvaecollected per species was 51.9, the median being11.2. The low density of most species in theseassemblages has been confirmed by absolutesampling obtained by fogging tree canopies (Bar-bosa et al. unpubl. data). Of the larvae collected,940 were parasitized. About 69% of reared para-sitoids were identified to species (see Barbosaet al., 2001). Parasitoids belonged to 61 identifiedspecies, representing the Braconidae (66% ofindividuals), Ichneumonidae (20%), Tachinidae(11%) and Eulophidae (3%).

Overall association between abundance andparasitism levels

A significant positive association was found be-tween parasitism rate and species abundance(b ¼ 0:0022; X2 ¼ 36:4; po0:0001). Logistic regres-sions performed on the 1000 simulated data setsprovided the expected distribution for the values ofthe ‘slope’ (b) for the null hypothesis (i.e., noassociation between abundance and parasitism)and the distribution was approximately normalwith a mean equal to zero (SD¼ 0.0013). Thus,there was no reason to expect a systematic bias inthe values of b: However, the p-value of the logisticregression applied to the actual data set wasunreliable because logistic regressions performedon the 1000 simulated data sets demonstrated a

heavily inflated probability of a type I error(po0:05 in 42% of simulations instead of 5%expected by chance). Therefore, the level ofstatistical significance for the association in theactual data had to be re-estimated using thedistribution of the b values in the simulated datasets. The value of b was equal or greater than theactual value in 37 simulations out of 1000, whichimplies a p-value of 0.037 (one-tailed test). This isconsiderably higher than the p-value obtained fromthe original logistic regression. Nevertheless, thepresence of a significant positive associationbetween abundance and parasitism rate was con-firmed.

Three dominant species have higherparasitism levels

The three species that clearly exceeded all othersin abundance (Fig. 1, note the logarithmic scale),Orgyia leucostigma (J.E. Smith) (Lymantriidae),Semiothisa aemulataria (Walker) (Geometridae)and Zale galbanata (Morr.) (Noctuidae), also dis-played considerably higher than average levels ofparasitism (Fig. 1, Table 1). The levels of parasitismin these abundant species were considerably higherthan predicted by simulations. This pattern wassignificant, i.e., the observed value of the averagepercentage parasitism among the three mostabundant species (33.0%) was equaled or exceededonly in 11 out of the 1000 simulations (p ¼ 0:011),under the H0 specified above (Table 1). The higherparasitism rate of the dominant species in the

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Abundance (Sample Size)

Per

cent

Par

asiti

sm

0

20

40

60

80

100

1 2 5 10 30 100 400

- 1 sp.- 2 spp.- 3 spp.- 5 spp.- 13 spp.

OL

SA

ZG

Figure 1. Percent parasitism in species represented bydifferent sample sizes. The three numerically dominantspecies were Semiothisa aemulataria (SA, 467 larvaecollected), Orgyia leucostigma (OL, 486) and Zalegalbanata (ZG, 602). Note logarithmic scale on theX-axis: the dominants were about twice as abundant asthe species of the next abundance class.

Parasitism of numerically dominant species 361

actual data set is thus unlikely to be explained bychance. When we excluded these three mostabundant species and repeated the analyses, thelogistic regression did not show any significantassociation (b ¼ 0:0008; X2 ¼ 0:36; p ¼ 0:55) be-tween percent parasitism and species abundance,and an analysis of the simulated data confirmed theconclusion (p ¼ 0:35). The average percent para-sitism for the 14 scarcest of the species in theactual data set was in accordance to the predic-tions of the simulations, i.e., it was not signifi-cantly lower than the average value for theassemblage (Table 1). It is thus clear that thepositive association between species’ abundanceand parasitism rate was due to the high parasitismrates of the three dominant species.

The pattern of higher percent parasitism amongthe three dominant species persists regardless ofthe data subset considered (i.e., results were thesame regardless of the year, parasitoid family, orhost tree species considered; Table 2). Levels of

parasitism of all the three dominant species werewell above average in all 5 years (ratio 15:0,po0:0001 by sign test). Thus, the correlationbetween level of parasitism and abundance of thethree dominant moth species was not a conse-quence of parasitoid–host interactions in any givenyear. Similarly, parasitism by braconids (the mostwell represented parasitoid taxon) in the threedominant species was higher than average, as wasthe case when all other parasitoid families werepooled (for this analysis, moths parasitized by otherfamilies were re-scored as not parasitized). Speciesin the Braconidae were responsible for most of theparasitism observed. Other parasitoid families wererepresented by numbers too low to analyzeseparately. Finally, O. leucostigma showed higherthan average levels of parasitism on both of treespecies sampled (the two other dominant speciesoccurred only on A. negundo).

A comparison of parasitism patterns betweenyears with high and low abundance of the dominantspecies indicates that preferences of parasitoidsdid not involve a direct response to changes inabundance of the dominant hosts: ‘year type’-� ‘species’ interaction terms (see Materials andmethods) were not significant for both O. leucos-tigma, (df¼ 1, X2 ¼ 0:21; p ¼ 0:65) and Z. galba-nata (df¼ 1, X2 ¼ 0:50; p ¼ 0:48). The actual levelsof parasitism imposed by parasitoids in the peakyear (9.6% and 28.8%, for the two species,respectively) were close to those expected underthe null hypothesis of density-independent prefer-ence (12.8% and 34.1%, respectively). However, forS. aemulataria, contrary to expectations, theactual percent parasitism in the year of maximalabundance (24.4%) was significantly lower (df¼ 1,

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Table 2. Percent parasitism in the three dominant species, compared to all other species.

Semiothisaaemulataria

Zale galbanata Orgyia leucostigma All other species

Year1993 26 (72)a 49 (45) 33 (60) 9.5 (460)1994 41 (12) 33 (9) 55 (65) 19 (333)1995 31 (16) 33 (15) 33 (9) 18 (298)1996 26 (321) 36 (502) 19 (103) 15 (807)1997 46 (46) 29 (31) 34 (249) 16 (699)

Tree speciesSalix nigra – – 32 (249) 8.2 (1834)Acer negundo 28 (467) 36 (603) 35 (237) 19 (763)

Parasitoid familyBraconidae 18 (85) 28 (169) 21 (104) 7.3 (198)Other 13 (48) 12 (52) 16 (60) 9.0 (233)

aFigures in the parentheses refer to sample sizes (no. of individuals collected).

Table 1. Levels of parasitism in lepidopteran specieswith different abundance.

Abundancecategory(individualsper species)

No. ofspecies

Species’meanpercentparasitism

p-value(differencefrom theaverage)a

N ¼ 1 14 7.1 0.38No3 21 11.9 0.29No10 34 13.5 0.40N4300 3 33.0 0.0011All species 81 14.9 F

aSignificance tests are based on simulations, see text.

362 P. Barbosa et al.

X2 ¼ 23:5; po0:0001) than expected (53.9%). How-ever, simultaneous occurrence of the peaks of Z.galbanata and S. aemulataria (year 1996, Table 2)may confound the pattern and may caution againstany conclusion about host selection by parasitoidsof S. aemulataria.

Discussion

Subdominant species do not appear to gain anyrefuge from parasitism by persisting at low abun-dance nor do they appear to possess traits thatresult in levels of parasitism different than wouldbe expected based on their numbers. In contrast,there was a positive association between species’abundance and parasitism rate, entirely due to thehigh parasitism rates of the three dominantspecies. However, dominant species displayed highlevels of parasitism even in the years when theirabundance was not particularly high. Thus,although abundance may be necessary it is notsufficient to explain the greater susceptibility ofdominant species. The observation of this unex-pected pattern would have been unlikely without along-term study of host–parasitoid interactionsand, thus, other such studies are needed todetermine how applicable this phenomenon is toother taxa.

It is unlikely that the pattern observed repre-sents the effects of a single or a few uniqueparasitoids. For both dominant and subdominantspecies, the suite of parasitoid species that causedthe highest levels of parasitism varied from year toyear (Barbosa et al. unpubl. data). Similarly, thereis no idiosyncracy of the parasitoid assemblage ofdominant herbivores that accounts for the observedresults. For example, there is no differential in theproportion of idiobionts and koinobionts among

dominant and subdominant species. In the assem-blages we studied there are no idiobiont parasitoidsother than a total of 5 individuals (representing twoof the three hyperparasitoid species collected) thatwere associated with primary parasitoids of larvaeon box elder (i.e., Mesochorus species) and 1hyperparasitoid species (of which 4 individualswere collected) which was associated with para-sitoids of larvae found on both box elder and blackwillow. Alternatively, the high rates of parasitismamong numerically dominant species may havebeen due to one or more unknown ‘‘unique’’ traitsassociated with these species and which enhancetheir susceptibility to parasitoids. Although ourtype of data do not allow a direct test of thisspeculation, our evidence supports the ‘‘uniquetrait’’ hypothesis, rather than a straight-forwardresponse to abundance. There are many aspects ofthe interactions between parasitoids and theirhosts that are critical to successful parasitism andthus may alter the susceptibility of host species.Future studies will explore relevant life-historytraits.

In a comparative study, one must control forpossible phylogenetic effects (Harvey & Pagel,1991). Unfortunately, phylogenetic relations withinLepidoptera are not yet sufficiently resolved tofacilitate a full phylogenetic analysis of levels ofparasitism. However, the four most species-richfamilies (i.e., those in which over 5 species wererecorded) showed very similar average species-specific rates of parasitism (ranging from 9.8% to10.7%) indicating that there was no strong phylo-genetic component. Species’ abundance did notappear to be associated with taxa. Moreover, mostof our conclusions are based on three dominantspecies which had high and similar levels ofparasitism, but were taxonomically unrelated,i.e., they represented three different families.

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Table 3. Number of parasitoid individuals reared from the three dominant lepidopteran species in the year of theirmaximum abundance (1996 for ZG and SA, 1997 for OL), and the rest 4 years of the study.

Dominantlepidopteran

No. of sharedparasitoidsa from thedominant species

No. of sharedparasitoidsa,b fromsubdominant species

No. of sharedparasitoidsa from thedominant species

No. of sharedparasitoidsa,b fromsubdominant species

Year of maximalabundance

Year of maximalabundance

Other 4 years(Pooled)

Other 4 years(Pooled)

O. leucostigma 24 3 44 10Z. galbanata 145 38 (8) 28 39S. aemulataria 63 139 (16) 28 33

aOnly parasitoids identified at the species level are included.bShared parasitoids refer to species that were recorded both on the respective dominant and subdominant species in the assemblage.Numbers in parentheses for Z. galbanata refer to the number of shared parasitoid species reared from species other than SA, or for S.aemulataria to the parasitoids reared from species other than ZG.

Parasitism of numerically dominant species 363

Thus, our ‘non-phylogenetic’ approach is unlikelyto seriously bias the conclusions drawn (see Bj-.orklund, 1997).Irrespective of the mechanisms involved, the

response of parasitoids to numerically dominantspecies may result in absolute numbers of para-sitoids (most of which are polyphagous) capable ofhaving a major impact on subdominant species,although less capable of regulating dominantspecies. Effective reduction of the abundance ofmany subdominant species could be achieved if theabundance of parasitoids shared by both dominantand subdominant species increases on abundantdominant host species. The number of parasitoidindividuals reared from the dominant species in thepeak years was greater than for any other species inthe assemblage (Table 3). A number of theparasitoids attacking dominant species also para-sitized other species in the macrolepidopteranassemblage. In the present study, 20 out of the 78subdominant species shared parasitoids with thedominants. The influence of dominant species onsubdominant species, mediated by shared para-sitoids (Table 3), is not likely to be the only or even,perhaps, the main factor maintaining low popula-tion densities of the subdominant species, althoughit may definitely contribute to it. Further work iscurrently underway to characterize differencesbetween dominant and subdominant species anddetermine the impact of these differences on levelsof parasitism.

Acknowledgements

We acknowledge the able assistance of HollidayObrecht of the Patuxent Wildlife Research Centerfor his invaluable assistance and support and themany University of Maryland undergraduates whosehard work made this study possible. This projectwas funded, in part, by the University of MarylandAgricultural Experiment Station Project MD-H-20I(PB & AC) and by an Estonian Science Foundationgrant No. 4076. Finally, we acknowledge theimmensely helpful suggestions provided by IgnacioCastellanos, Grant Gentry, Mary Christman, andRaul Medina.

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