Seasonal occurrence of postharvest dried fruit insects and their parasitoids in a culled fig warehouse

Parasitoids of dried-fruit insects were surveyed at a culled fig warehouse in Fresno, CA. Three parasitoids of pyralid larvae were found: Habrobracon hebetor (Say), Venturia canescens (Gravenhorst), and at least one species in the genus Goniozus F?rster. Two parasitoids of pyralid pupae also were noted: Mesostenus gracilis (Cresson) and a new species of Psilochalcis Keifer. The latter is a new host association. Several beetle parasitoids were present, including Anisopteromalus calandrae (Howard), three species of Cephalonomia Westwood, Laelius centratus (Say), and Cerchysiella utilis Noyes. C. utilis, a parasitoid of driedfruit beetle, Carpophilus hemipterus (L.), is a new record for California. Most activity by parasitoids (detected by yellow flight traps) occurred directly above the fig mass. Pyralid parasitoids exhibited two peaks of seasonal activity; one in late summer through early fall, shortly after new figs were brought into the warehouse, and one in the spring. H. hebetor generally attacked older host larvae, whereas V. canescens equally attacked older and younger larvae, indicating that these two parasitoids may coexist by exploiting different portions of the host population. H. hebetor was active throughout the winter, suggesting that winter release of H. hebetor could be used to control diapausing pyralid populations in dried fruit and nut storage areas.     

Venturia canescens parasitizing Galleria mellonella and Anagasta kuehniella: differing suitability of two hosts with highly variable growth potential

Venturia canescens (Grav.) (Hymenoptera: Ichneumonidae) is a solitary larval koinobiont endoparasitoid, ovipositing in several larval instars of different pyralid moth species that are pests of stored food products. After oviposition, the host larva continues to feed and grow for at least several days, the precise time doing so depending on the stage attacked. We examined the relationship between host stage and body mass on parasitoid development in late second to fifth instars of two hosts with highly variable growth potential: the wax moth, Galleria mellonella (L) and the flour moth, Anagasta kuehniella (Zeller)(Lepidoptera: Pyralidae). G. mellonella is the largest known host of V. canescens, with healthy larvae occasionally exceeding 400mg at pupation, whereas those of A. kuehniella rarely exceed 40 mg at the same stage. Parasitoid survival was generally higher in early instars of G. mellonella than in later instars. By contrast, percentage adult emergence in A. kuehniella was highest in late fifth instar and lowest in late second instar. A. kuehniella was the more suitable host species, with over 45% adult emergence in all instars, whereas in G. mellonella we found less than 35% adult emergence in all instars. Adult parasitoid size increased and egg-to-adult development time decreased in a host size- and instar-specific manner from A. kuehniella. The relationship between host size and stage and these fitness correlates was less clear in G. mellonella. Although both host species were parasitized over a similar range of fresh weights, the suitability weight-range of A. kuehniella was considerably wider than G. mellonella for the successful development of V. canescens. However, in hosts of similar weight under 5 mg when parasitized, larger wasps emerged from G. mellonella than from A. kuehniella. Parasitoid growth and development is clearly affected by host species, and we argue that patterns of host utilization and resource acquisition by parasitoids have evolved in accordance with host growth potential and the nutritional requirements of the parasitoid.     

Life tables of Habrobracon hebetor (Hymenoptera: Braconidae) parasitizing Anagasta kuehniella and Plodia interpunctella (Lepidoptera: Pyralidae): effect of host density

The reproductive performance of the parasitoid Habrobracon hebetor (Say) (Hymenoptera: Braconidae) against the moths Anagasta kuehniella Zeller and Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae) was studied in the laboratory. The analysis was based on the comparison of parasitoid's life table parameters related to those of its hosts at various conditions of host density (daily supply of 1, 5, 15, and 30 full-grown host larvae). The estimated parameters were the intrinsic rate of natural increase (rm), the net reproductive rate (R0), the mean generation time (G), the finite capacity of increase (lambda), the gross reproductive rate (GRR), the doubling time (DT), the reproductive value (Vx), and the life expectancy (ex). The rm of H. hebetor proved to be significantly higher than those of its hosts at all host densities. When only one host per day was supplied, the wasp had the lowest reproductive potential, whereas it was maximized when 15 hosts per day were exposed. Maximum values of R0 and GRR were obtained at densities > or =15 host larvae per day. Any increase in host supply above this threshold did not cause significant changes in life table parameters. Variation of rm as a function of host density can be described by the linear regression. Sex ratio of wasp progeny (females/total) ranged from 0.36 to 0.42, irrespective of host density or species. Newly emerged adults recorded maximum ex and Vx. The results of this study can be used to improve mass rearing programs and inoculative release applications of H. hebetor against moth pests of stored products.     

Intraspecific competition and density dependence in an Ephestia kuehniella–Venturia canescens laboratory system

A model host-parasitoid system of Ephestia kuehniella and Venturia canescens was used to examine the influence of host and parasitoid density on host and parasitoid life-history parameters via a two-way factorial experimental design (5 initial host densities×3 parasitoid densities). In the absence of parasitoids, E. kuehniella experienced scramble-type competition with reduced growth, diminished adult size and a subsequent fecundity trade-off for mortality. The mortality that did occur was confined to the late larval and pupal stages. In the presence of parasitoids attacking the late larval stage, competition changed from scramble for food to contest for enemy-free space, with hosts escaping parasitism being small with low fecundity and reduced egg size, and with parasitoid adult size inversely dependent on host density. Total insect emergence (host+parasitoid), a measure of the influence of host resource competition on survivorship, exhibited a threshold effect as a function of initial host density; the threshold value was increased to a higher initial host density in the presence of parasitoids. Models of host self-limitation were fitted to the data, with the generalized Beverton-Holt model that incorporates a threshold effect providing the best fit, and the Ricker model with no threshold providing a very poor fit to the data.     

The development of the endoparasitoid wasp Venturia canescens in superparasitised Ephestia kuehniella

Using a molecular marker that allows the differentiation of two strains of the solitary endoparasitoid wasp Venturia canescens, the study investigated the influence of host mass and the time interval between ovipositions on the survival and development of larvae from both the first and second laid eggs in superparasitised Ephestia kuehniella. As the time interval between ovipositions increased both overall and superparasitism success decreased, however, time between, and order of, ovipositions had little effect on other developmental parameters. Adult size increased with host mass under both parasitism and superparasitism, while host mortality decreased with host mass under superparasitism. In addition, wasps emerging from superparasitised hosts were larger than wasps from parasitised hosts. The results confirm that for V. canescens on the host E. kuehniella both self- and conspecific-superparasitism will be an adaptive strategy when hosts are the limiting factor.     

Effect of Bacillus thuringiensis on Habrobracon hebetor during combined biological control of Plodia interpunctella

Abstract  The suitability of combining microbial pesticides and an insect parasitoid for pest management of stored cereal in China was evaluated using laboratory assays. For this purpose, interactions between Bacillus thuringiensis ( Bt ), Bt -intoxicated host larvae and the parasitoid Habrobracon hebetor (Say) (Hymenoptera: Braconidae) were tested against Plodia interpunctella Hübner (Lepidoptera: Pyralidae) . Bt or H. hebetor alone caused 41.67% and 35.35% P. interpunctella larval mortality respectively. The Bt –parasitoid combined treatment significantly increased mortality of P. interpunctella (86%). Progeny development of H. hebetor was dependent upon its susceptibility to Bt . Fewer parasitoids emerged from Bt –parasitoid combined treatment than in non- Bt treatments. However, since Bt did not prevent parasitoid development, a combined treatment with Bt and parasitoid release could produce better protection against P. interpunctella than either treatments when used singly, because their lethal effects were additive to each other.     

First field evidence that parasitoids use upwind anemotaxis for host-habitat location

The direction of flight of natural populations of Phradis interstitialis (Thomson), Tersilochus obscurator Aubert (both Hymenoptera: Ichneumonidae), and Platygaster subuliformis (Kieffer) (Hymenoptera: Platygastridae), parasitoids of three crucifer‐specialist herbivores, to and from their hosts’ host plant [oilseed rape, Brassica napus L. (Brassicaceae)] was studied in the field within a heterogeneous arable environment. Double‐sided Malaise traps encircling a plot of winter oilseed rape (cultivar Lutin) were used to sample the parasitoids as they flew towards and away from the plot during spring and summer. Daily trap catch of parasitoids and trap air flow were compared using Spearman's rank correlation. For all 14 insect days analysed, and for each species, the correlations between daily catch of parasitoids into distal halves of traps (relative to the plot) and wind direction were negative, significantly so on half the days analysed. This confirmed that flights towards the plot were by upwind anemotaxis. In contrast, the correlations between daily catch of parasitoids into proximal halves of traps (relative to the plot) and wind direction were most often crosswind; they were never strongly nor significantly either negative or positive. Implications of the results for integrated pest management strategies incorporating biological control with these parasitoids are discussed.     

Structure of a herbivore–parasitoid community: Are parasitoids shared by different herbivore guilds?

Plant–herbivore–parasitoid interactions are a common occurrence in terrestrial food webs. Few parasitoids are thought to be shared by host insects of different feeding guilds because different parasitism strategies are required to use hosts of different feeding types. However, this assumption has rarely been tested using data from nature. To clarify whether parasitoids are shared among host guilds, I examined the structure of parasitoid communities on herbivore guilds associated with two Rhododendron species (Ericaceae) in a temperate secondary forest in central Japan. Leaf- and flower-feeding insects were collected from Rhododendron reticulatum and Rhododendron macrosepalum shrubs and reared in the laboratory for 3 years from April 1999 to March 2002. In total, 79 species of holometabolous herbivores (Lepidoptera, Diptera, Coleoptera, and Hymenoptera) were recorded, with 62 species on R. reticulatum and 51 species on R. macrosepalum. A total of 81 parasitoid species (Hymenoptera and Diptera) was recorded from the sampled herbivores, with 48 species from those on R. reticulatum and 50 species from those on R. macrosepalum. In total, 36 herbivore species were parasitised by 1–18 parasitoid species per host species, although the number of parasitoid species was strongly affected by sample size. Parasitoids that had two or more host species frequently attacked herbivore species from different families or on different host plants, whereas they did not attack species from different herbivore guilds; no parasitoids were shared between external feeders and rollers. Therefore, my results support the hypothesis that few parasitoids are shared among herbivores of different feeding guilds.     

The α-amylase inhibitor acarbose does not affect the parasitoid Venturia canescens when incorporated into the diet of its host Ephestia kuehniella

Amylase inhibitors (AIs) are suitable candidates for protecting plants and their products from attacks by herbivorous and granivorous insects. However, detailed studies of the suppressive effects of AIs on target and non‐target insects are necessary before their application in post‐harvest protection. To address this issue, laboratory bioassays were used to test the effect of the non‐proteinaceous inhibitor acarbose on a stored product pest, the flour moth Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae), and its parasitoid Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae). Two sublethal concentrations (0.001 and 0.0001%, wt/wt) of acarbose were incorporated into the diet of parasitized and unparasitized larvae of E. kuehniella. Development time and fresh body weight of the larvae, together with the size of the wasps, were compared for insects reared on acarbose‐treated and control diets. On the diet containing 0.001% acarbose, the developmental time was longer and relative weight gains of the E. kuehniella larvae were lower, but the weight of the larvae prior to pupation was similar to that of the control. The acarbose did not have a suppressive effect on the parasitoid V. canescens; in fact the wasps that emerged from the hosts reared on a diet containing 0.0001% acarbose were on average larger and heavier than the controls. These results demonstrate that it might be possible to enhance the control of stored product pests by using both biological control and AIs.     

Life tables of Venturia canescens (Hymenoptera: Ichneumonidae) parasitizing the Mediterranean flour moth (Lepidoptera: Pyralidae)

Effects of temperature, adult feeding, and host instar on life table parameters of Venturia canescens Gravenhorst (Hymenoptera: Ichneumonidae) parasitizing larvae of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) were studied in the laboratory. Experimental adults lived under various regimes of temperature (15, 20, 25, and 30 degrees C), food supply (with or without access to honey), and host instar (second, third, fourth, and fifth). Temperature increase resulted in higher values of the intrinsic rate of natural increase (r(m)), the net reproductive rate (R(o)), the finite capacity of increase (lambda), and the gross reproductive rate (GRR), whereas it was followed by decrease of the mean generation time (G) and the doubling time (DT) values. Feeding on honey caused remarkable increase of r(m), R(o), and GRR, whereas r(m) and lambda reached their maximum when full-grown hosts (fifth instar) were parasitized. This is the first time life table parameters of V. canescens have been studied. The findings of the current study are discussed on the basis of improving V. canescens performance as a biological agent against moth pests of stored products.     

Field responses of stink bugs to the natural and synthetic pheromone of the Neotropical brown stink bug, Euschistus heros (Heteroptera: Pentatomidae)

Abstract.The synthetic racemic mixture of methyl 2,6,10‐trimethyltridecanoate, a component of the male produced pheromone of Euschistus heros (F.) (Heteroptera, Pentatomidae), was attractive to pentatomid species in a field test, using homemade pheromone trap designs. The pentatomid Piezodorus guildinii was caught in high numbers in field traps, during two field experiments, indicating a consistent response of this species to the E. heros pheromone. A correlation was found between the range of insects caught in the pheromone‐baited traps and a random sampling method. The synthetic stereoisomeric mixture of methyl 2,6,10‐trimethyldodecanoate, a minor component of E. heros pheromone, was also field tested and caught no pentatomids. Egg parasitoids were caught in traps baited with E. heros pheromone, indicating that this pheromone can be exploited as a kairomone. A synchrony in the periodicity of trap catch, between the egg parasitoids and their host, was also recorded.     

Presence of a novel small RNA-containing virus in a laboratory culture of the endoparasitic wasp Venturia canescens (Hymenoptera: Ichneumonidae)

Parasitoid wasps use a variety of mechanisms to alter their host's physiology to the benefit of the developing endoparasite inside the host larva. Association of certain wasps with viruses and virus-like particles (VLPs) that contribute to their success in parasitism is one of the fascinating evolutionary adaptations conferring active or passive protection for the endoparasite from the host immune system. Venturia canescens has been shown to produce VLPs that provide protection for the developing parasitoid egg inside the host, Ephestia kuehniella. Here, we report on the presence of a novel small RNA-containing virus from V. canescens, designated as VcSRV, occurring in the ovaries of the wasp. The virus particles are found together with VcVLPs in the lumen of the calyx region of the ovaries and are injected together with the egg and VcVLPs into E. kuehniella larvae where they enter hemocytes. Alignment of the RNA-dependent RNA polymerase gene of VcSRV indicates that the virus most likely belongs to the recently described genus Iflavirus.     

Biological, nutritional, and histochemical basis for improving an artificial diet for Bracon hebetor Say (Hymenoptera: Braconidae)

The biology of Bracon hebetor Say (Hymenoptera: Braconidae) reared on fifth instars of Anagasta kuehniella (Zeller) (Lepidoptera: Pyralidae) (natural diet) and in vitro (artificial diet) was evaluated. Data on the number of instars, development time and food intake were collected, and histochemical tests were conducted to detect proteins and lipids in the parasitoid's digestive tract. The data disclosed differences that can help to improve artificial rearing of B. hebetor. B. hebetor had three instars in both diets, but the developmental time on the artificial diets was prolonged due to the increase in larval and pupal development times. Larvae grew faster on the natural host and required a lower food intake (2.7 microl) as compared to that required by the larvae feeding on the artificial diet (3.8 microl). Analysis of diet protein content and host hemolymph and the observations on the parasitoid larvae gut content indicated altogether the artificial diets requires the addition of others sources of proteins and lipids to improve the overall nutrition quality of the in vitro rearing system for this ectoparasitoid.     

Biological control of Indianmeal moth (Lepidoptera: Pyralidae) on finished stored products using egg and larval parasitoids

Biological control using hymenopteran parasitoids presents an attractive alternative to insecticides for reducing infestations and damage from the Indianmeal moth, Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae), in retail and warehouse environments. We examined the potential for using combinations of the egg parasitoid Trichogramma deion Riley (Hymenoptera: Trichogrammatidae), and the larval parasitoid Habrobracon hebetor (Say) (Hymenoptera: Braconidae) for preventing infestations of P. interpunctella in coarse-ground cornmeal as well as the influence of packaging on parasitoid effectiveness. Treatments included one or both parasitoids and either cornmeal infested with P. interpunctella eggs or eggs deposited on the surface of plastic bags containing cornmeal. H. hebetor had a significant impact on the number of live P. interpunctella, suppressing populations by approximately 71% in both unbagged and bagged cornmeal. In contrast, T. deion did not suppress P. interpunctella in unbagged cornmeal. However, when released on bagged cornmeal, T. deion significantly increased the level of pest suppression (87%) over bagging alone (15%). When H. hebetor was added to bagged cornmeal, there was a significant reduction of live P. interpunctella compared with the control (70.6%), with a further reduction observed when T. deion was added (96.7%). These findings suggest that, in most situations, a combined release of both T. deion and H. hebetor would have the greatest impact; because even though packaging may protect most of the stored products, there are usually areas in the storage landscape where poor sanitation is present.     

Host hemolymph proteins and protein digestion in larval Habrobracon hebetor (Hymenoptera: braconidae)

Host plasma proteins and protein digestion in larval parasitoids were studied during trophic interactions of the ectoparasitoid Habrobracon hebetor Say (Hymenoptera: Braconidae), with a host, larvae of the Indianmeal moth, Plodia interpunctella Hübner (Lepidoptera: Pyralidae). We could detect no apparent differences in host hemolymph protein patterns up to 72 h after paralysation and/or parasitization by H. hebetor. A 190 kDa putative apolipophorin I present in host hemolymph could not be detected in the midguts of feeding H. hebetor larvae indicating that it is rapidly digested. The major 60 kDa storage proteins (putative hexamerins) in host hemolymph were detected in the parasitoid midgut and were completely digested 24 h after cessation of feeding and the beginning of cocoon formation. Host hemolymph had a pH of about 6.4. The pH optima of the midgut proteinases in the larval parasitoid were in the alkaline region, but midgut fluid in feeding parasitoid larvae was about pH 6. 8. Based on enzyme activity against selected artificial proteinase substrates including azocasein, N-alpha-benzoyl-L-Arg p-nitroanilide (BApNA), succinyl-Ala-Ala-Pro-Phe p-nitroanilide (SAAPFpNA), succinyl-Ala-Ala-Pro-Leu p-nitroanilide (SAAPLpNA), and inhibition by selected proteinase inhibitors, serine proteinases appear to be the predominant class of enzymes involved in protein digestion in the midguts of H. hebetor. There is also an active aminopeptidase (LpNA) associated with the microsomal fraction of midgut preparations. There was no evidence for preoral digestion or ingestion of proteinases from host hemolymph by the parasitoid larva. There was a very active BApNAase in the soluble fraction of midgut extracts. This activity increased on a per midgut basis up to 24 h after the beginning of cocoon formation but decreased rapidly by 48 h. Two major (P1 and P3) and several minor proteinases were detected in midgut extracts of H. hebetor analysed with gelatin zymograms. The apparent molecular mass of P1 varied from 95 to 49 kDa depending on protein loading. P3 had an apparent molecular mass of 39 kDa that was independent of protein loading. In summary, electrophoretic evidence indicates that host hemolymph protein patterns do not change significantly for at least 72 h after paralysation by H. hebetor. The role, if any, of envenomization in preventing breakdown of hemolymph proteins during this time remains to be determined. Because the predominant host hemolymph proteins, a putative apolipophorin I and the putative hexamerins, are readily digested by the serine proteinases present in the midguts of this parasitoid larva, these or similar proteins would provide an easily digested source of dietary amino acids that could be used for development of artificial diets for this beneficial insect.     

Effect of biotic and abiotic factors on reproductive parameters of the synovigenic endoparasitoid Venturia canescens

Abstract.  The main effects and interactions of adult age, access to food and host deprivation, on the egg load of Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae), a larval parasitoid of Ephestia kuehniella (Lepidoptera: Pyralidae) and other pyralids, were studied in the laboratory. Intraspecific variation in the number of ovarioles was also studied. There was a positive and significant correlation between wasp size and both egg load and ovariole number, with the reproductive system of large wasps containing significantly more ovarioles and mature eggs than small wasps. Newly emerged adult wasps contained 27 ± 2.4 ovulated (mature) eggs in their lateral oviducts. Access to food and host deprivation were the only conditions under which egg load increased with parasitoid age. Wasps that had access to hosts immediately after emergence showed a significant decline in their egg complement, irrespective of food presence. Under conditions of both host and food deprivation, there was practically no alteration of egg load with parasitoid age. A three-way analysis of variance revealed that egg load varies significantly with food or host access but not with parasitoid age. All interactions among the three factors were significant. It is confirmed that there is no egg resorption in V. canescens and that egg production stops in the absence of food.     

Combining pheromone-baited and food-baited traps for insect pest control: Effects of additional control by parasitoids

Two age-structured population dynamic models are analyzed in which pheromone-baited trapping and food-baited trapping are used simultaneously to eradicate an insect pest. The pest species is assumed to be under partial control by a host-specific parasitoid species. The two models assume that density-dependent population regulation is accomplished either by host larval competition or by means of oviposition interference among the parasitoids. The two trap types interact in a positive synergistic manner and this combination appears to be very promising as a useful combination of pest control methods. Several features of the system are examined; the feature which appears to cause the greatest problem is the possibility of the parasitoids being attracted to the pheromone or the food traps. In either case, the degree of attraction does not have to be very great to undermine the control effort. It is seen that food trapping becomes indispensible if host pheromone is used by the parasitoids as a host-locating kairomone. If odor in the food traps is used by the parasitoids as kairomone, then the situation appears more optimistic, as the reduction in efficiency of the food traps appears much less than with the pheromone traps when pheromone acts as kairomone.     

Global diversity of hymenopterans (Hymenoptera; Insecta) in freshwater

A summary of the known species of aquatic Hymenoptera is presented. In total, 150 species from 11 families are recognized as aquatic (0.13% of the total described species). This number is likely an underestimate, because of the high percentage of undescribed species and a lack of knowledge of host range and behaviour for most species. All aquatic Hymenoptera are parasitoids. Many species have relatively dense pubescence to trap air and elongate, tarsal claws to grip the substrate, when underwater. Most species are known from the Holarctic and Oriental regions, but this is likely an artefact caused by lack of knowledge of other regions of the world. Aquatic behaviour has evolved independently at least 50 times within the order. Guest editors: E. V. Balian, C. Lévêque, H. Segers & K. Martens Freshwater Animal Diversity Assessment     

Effects of the Host Species and the Number of Parasitoids per Host on the Size of Some Trichogramma Species (Hymenoptera: Trichogrammatidae)

The size of some Trichogramma spp. adults and especially the ovipositor length depends on the species, but is also related to the host species and to the number of parasitoids per host. The length is greater in T. evanescens than in T. pretiosum itself greater than in T. exiguum, but the width is similar in the three species. For T. evanescens, the size obtained in Mamestra brassicae host when three or four insects emerged is similar to that obtained in Ephestia kuehniella host when singly parasitized. The size of the ovipositor is important because it may influence the possibility of in vitro egg laying in artificial host eggs. A shorter or a narrower ovipositor could cause difficulties in egg-laying into artificial host eggs composed of a membrane of unsuitable thickness.     

In-field production of parasitoids of Dysaphis plantaginea by using the rowan aphid Dysaphis sorbi as substitute host

A system was developed to provide the parasitic wasp Ephedrus persicae Froggatt (Hymenoptera: Braconidae: Aphidiinae), which attacks the rosy apple aphid Dysaphis plantaginea (Passerini) (Homoptera: Aphididae), with the alternative host Dysaphis sorbi Kaltenbach (Homoptera: Aphididae) in apple orchards. Rowan trees (Sorbus aucuparia L.) arranged along the side of an unsprayed orchard were artificially infested in late February 2002 with eggs of D. sorbi. Colonies of D. sorbi successfully developed from the introduced eggs and persisted on several trees until the end of June. The only primary parasitoid species emerging from a sample of mummified aphids collected in spring from the infested rowan trees was the braconid wasp species E. persicae. In a host-switching experiment, nymphs of D. plantaginea proved suitable for female parasitoids originating from mummified D. sorbi. A series of mummies collected from the rowan trees in early summer contained diapausing parasitoids and hyperparasitoids that only hatched in April of the following spring. These observations suggest the possibility of establishing a local population of E. persicae in apple orchards, so that D. plantaginea can be readily attacked by diapause-emerging parasitoids in early spring.