Larval development of two parasitic flies (Conopidae) in the common host Bombus pascuorum

Abstract.

• 1 Whenever parasitism by more than one female occurs, larvae of parasitoids not only have to resist host defence but also face competition with other (unrelated) larvae. Competition is particularly important in solitary parasitoids where only one larva is able to complete its development. Such a situation is found in Conopidae (Diptera) parasitizing adult bumble bees where larvae of two species of conopid flies, Sicus ferrugineus L. and Physocephala rufipes F. often compete within the common host Bombus pascuorum Scopoli. This study analysed the larval development of the two species and asks how competition among larvae may be regulated.
• 2 Parasitized workers of B.pascuorum were caught in the field and kept according to different experimental schedules in the laboratory. This provided stage-structured data for the temporal course of development of the parasitic larvae. For the analysis, a simulation model was constructed that estimated the duration of all parasitic stages (Manly, 1990, first method). In both species the egg stage was found to be approximately 2 days, first instar 3 days, second instar 4 days, and third instar 3 days. The total development time is an estimated 10.8 days from oviposition in S.ferrugineus and 11.4 days in P.rufipes. S.ferrugineus develops faster in the beginning, probably because of its larger egg size, whereas P.rufipes pupates at larger size. First-instar larvae of both species possess strong, pointed mandibles.
• 3 The success of conopid larvae seems only marginally affected by host defence, for a single larva per host almost always completes development. Under competition, however, mortality rate increases substantially, and most larvae die in their first instar. Moreover, they show signs of melanization. The estimates for developmental times and the patterns found in this study suggest that conopid larvae seem capable of physical attacks, particularly during the first instar, when elimination of competitors is most common, and that S.ferrugineus has a time advantage because of its faster early development. Because most studies have previously been carried out with hymenopteran parasitoids, this study provides new information about the other large group of parasitoid insects, the Diptera, and demonstrates convergent patterns.

     

Field evidence that host selection by conopid parasitoids is related to host body size

Summary The body size of the host insect in which a parasitoid develops can have important effects on its development and life history. Large and small host body size have both been suggested to be advantageous to parasitoids, depending on the life-history of the species concerned. We test field data on the bumblebeeBombus terrestris and its conopid parasitoids for evidence of differences in size between parasitised and unparasitised worker bees. Bees acting as hosts for conopid parasitoids are on average larger-bodied than unparasitised bees. This result holds for bees collected in two different years, and whether bees are collected while foraging or from the nest. The results we present demonstrate differential parasitism of hosts of different body sizes, but do not necessarily indicate active host choice by conopids. However, they are in agreement with independent evidence that conopids develop more successfully in large-than in small-bodied hosts.     

Dynamic effects of parasitism by an endoparasitoid wasp on the development of two host species: implications for host quality and parasitoid fitness

1. The study reported here examined growth and developmental interactions between the gregarious larval koinobiont endoparasitoid Cotesia glomerata (Hymenoptera: Braconidae) and two of its hosts that vary considerably in growth potential: Pieris rapae and the larger P. brassicae (Lepidoptera: Pieridae). At pupation, healthy larvae of P. brassicae are over twice as large, in terms of fresh body mass, as those of P. rapae. 2. Clutch size of C. glomerata was manipulated artificially, and the relationship between parasitoid burden and the maximum weight of the parasitised host (= host–parasitoid complex) was measured. In both hosts, the maximum complex weight was correlated positively with parasitoid burden. Compared with unparasitised hosts, however, the growth of P. rapae was increased at significantly lower parasitoid burdens than in P. brassicae. Emerging wasp size was correlated negatively with parasitoid burden in both host species, whereas development time was less affected. 3. After larval parasitoid egress, the weight of the host carcass increased slightly, but not significantly, with parasitoid burden, although there was a strong correlation between the proportion of host mass consumed by C. glomerata larvae during development and parasitoid burden. 4. Clutch size was generally correlated positively with instar parasitised in both hosts, and greater in P. brassicae than in P. rapae. Sex ratios were much more female biased in L1 and L2 P. rapae than in all other host classes. Adult parasitoid size was correlated inversely with host instar at parasitism, and wasps emerging from P. brassicae were larger, and completed development faster, than conspecifics emerging from P. rapae. 5. The data reveal that parasitism by C. glomerata has profound species‐specific effects on the growth of both host species. Consequently, optimality models in which host quality is often based on host size at parasitism or unparasitised growth potential may have little utility in describing the development of gregarious koinobiont endoparasitoids. The results of this investigation are discussed in relation to the potential effectiveness of gregarious koinobionts in biological control programmes.     

Resource utilization and sex allocation in response to host size in two ectoparasitoid wasps on subcortical beetles

Patterns of host resource utilization and sex ratio manipulation in relation to host size were investigated for two solitary ectoparasitoid wasps,Atanycolus initiator andSpathius brevicaudis (Hymenoptera Braconidae). Both species parasitize subcortical beetles on the trunks of Japanese pine trees.A. initiator is on average 8 times larger in body weight and has an ovipositor that is 3.7 times longer than that ofS. brevicaudis. In both parasitoids, the size of emerging wasps was positively correlated with host size, but the host/wasp size regressions were linear for all three major host species inA. initiator, whereas inS. brevicaudis the regression was logarithmic for a relatively large host species. The sex ratios (proportion of males) of both parasitoids emerging from different host species decreased with increasing host size, but the overall sex ratio on each host species was male-biased inA. initiator, while female-biased inS. brevicaudis. How the proportion of host consumed changed in response to host size, differed between the two parasitoids for the same host species. In the field survey, the size and sex ratio of the emerging two parasitoids from a dead tree were closely related to host size. However, the spatial distribution of the two parasitoids depended on the bark thickness of the trunk. The data suggest that differences in the relative evaluation of host size and in ovipositor length may enable the coexistence of the two parasitoid wasps.     

Fecundity and development of the ectoparasitic waspNasonia vitripennis are dependent on host quality

The gregarious, ectoparasitoidNasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) was offered pupae representing seven fly species, but only members of two families (Sarcophagidae and Muscidae) were parasitized. Host acceptance as an oviposition site did not imply host suitability for parasitoid growth:N. vitripennis produced fewer progeny, a higher proportion of males, required a longer development time, and produced smaller adult wasps onMusca domestica L. (Diptera: Muscidae) than on the three sarcophagid species tested [Sarcophaga bullata Parker,S. crassipalpis Macquart, andPeckia abnormis (Enderlein) (Diptera: Sarcophagidae)]. The physiological and nutritional status of a preferred host,S. bullata, influenced oviposition behavior and development ofN. vitripennis. Progeny allocation and sex ratio, which were regulated by the female parasitoid during oviposition, differed on living and dead nondiapausing hosts and on diapausing pupae. Differences in the host's nutritional condition was reflected in changes of the wasp's development time and adult body size. Envenomation was essential for successful development of the parasitoid on nondiapausing hosts, but venom injection byN. vitripennis did not increase the suitability of diapausing or dead pupae. The results suggest that wasp development is enhanced by changes induced in the host by parasitism.     

Intraguild interactions between two biological control agents in citrus fruit: implications for biological control of medfly

The parasitoid wasp Spalangia cameroni and the predatory beetle Pseudoophonus rufipes have long been studied for use as biological control agents against the Mediterranean fruit fly Ceratitis capitata, particularly in citrus fruit orchards. Nevertheless, these two species of natural enemies, when competing for a common resource, may experience intraguild predation (IGP) interactions. These possible interactions, affecting parasitism and predation, have been evaluated in the present work, under laboratory conditions, through potential changes in functional response. Regarding host/prey density, both natural enemies, when acting alone, showed a type II functional response. Nevertheless, due to IGP, S. cameroni, in the presence of P. rufipes, showed a higher fertility rate and a type III functional response. The parasitism behaviour of S. cameroni was affected by the presence of the predator, reducing the host handling time. Conversely, the parasitism rate of S. cameroni did not vary in the presence of P. rufipes but the degree of superparasitism decreased and led to an increased fertility rate and an increasingly female‐biased sex ratio. Meanwhile, the predatory efficiency of P. rufipes was not affected by the presence of S. cameroni but discrimination between parasitised and unparasitised pupae of C. capitata, with a preference for the latter, was reported for this predator species. Our results suggest that in biological control programmes, the use of only one of these species is recommended at low infestation levels, whilst at high densities of the pest, the combination of both natural enemies seems to be the most appropriate strategy.     

Patterns of parasite infection in bumble bees (Bombus spp.) of Northern Virginia

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Development ofBrachymeria ovata [hymenoptera: chalcididae] in three noctuid hosts reared on artificial diet and insect-resistant and susceptible soybean genotypes

The development of the pupal parasitoidBrachymeria ovata (Say) was studied in 3 lepidopterous hosts reared on artificial diet and insect-susceptible and insectresistant soybena genotypes.Pseudoplusia includens (Walker),Anticarsia gemmatalis Hubner andHeliothis zea (Boddie) pupae from larvae reared on soybean leaves were less suitable forB. ovata development than pupae from larvae reared on artificial diet.B. ovata emergence rates, size and sometimes development period were adversely affected on plant-reared hosts. Dissection of hosts 6 days after parasitisation byB. ovata showed a higher proportion of diet-reared host pupae contained large parasitoid larvae than plant-reared hosts. Suitability differences were also detected among hosts reared on different soybean genotypes but these differences did not parallel closely the response of the lepidopterous hosts to soybean genotypes.      

Host-size-dependent sex ratio in a parasitoid wasp

Charnov's host-size model explains parasitoid host-size-dependent sex ratio as an adaptive consequence when there is a differential effect of host size on the offspring fitness of parasitoid males versus females. This article tests the predictions and the assumptions of the host-size model. The parasitoid wasp Pimpla nipponica Uchida (Hymenoptera: Ichneumonidae) laid more female eggs in larger or fresher host pupae when choice among hosts of different sizes or ages was allowed. Then, whether an asymmetrical effect of host size and age on the fitness of females versus males existed in P. nipponica was examined. Larger or fresher host pupae yielded larger wasps. Larger females lived longer, whereas male size did not influence male longevity. Large males mated successfully with relatively large females but failed with small females, whereas small males could mate successfully either with small or with large females. Thus, small-male advantages were found, and this held true even under male–male competition. Ovariole and egg numbers at any one time did not differ among females of different sizes. Larger females attained higher oviposition success and spent less time and energy for oviposition in hosts. Larger females produced more eggs from a single host meal. Taken together, females gained more, and males lost more, by being large. Host size and age thus asymmetrically affected the fitness of offspring males versus females through the relationships between host size or hast age and wasp size, which means the basic assumption of the host-size model was satisfied. Therefore, sex ratio control by P. nipponica in response to host size and age is adaptive. Received: November 13, 1998 / Accepted: January 18, 1999     

Interactions between the ParasitoidAmetadoria misella(Diptera: Tachinidae) and the Granulovirus ofHarrisina brillians(Lepidoptera: Zygaenidae)

Interactions between a granulovirus (HbGV), a tachinid parasitoidAmetadoria misella,and their host, the western grapeleaf skeletonizerHarrisina brillians,were investigated. In field populations, the occurrence ofA. misellain HbGV-infectedH. brillianspupae was less frequent than would have been expected by random assortment of the virus and the parasitoid. Furthermore, enzyme-linked immunosorbent assay detected granulovirus less frequently and in lower concentrations in parasitized pupae than in nonparasitized pupae. Finally, in the host pupae that tested positive for virus, parasitoids were more likely to survive pupation than hosts. When laboratory-rearedH. brillianslarvae were exposed to naturally occurringA. misellain a field experiment, the parasitoid oviposited more often in older than in younger host larvae and more often in healthy than in HbGV-infected host larvae. These results are consistent with the hypothesis that selective oviposition byA. misellaleads to reduced overlap of the parasitoid and HbGV in hosts, resulting in greater parasitoid survival.     

Suitability of the maize weevil and angoumois grain moth as hosts for the parasitoidsAnisopteromalus calandrae andPteromalus cerealellae

Two parasitoids,Pteromalus cerealellae (Ashmead) andAnisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae), were compared for their ability to parasitize two important internally-developing insect pests of stored maize (Zea mays L.). Parasitism byP. cerealellae was greater on Angoumois grain moth,Sitotroga cerealella (Olivier), than on maize weevil,Sitophilus zeamais Motschulsky, in no-choice experiments.Anisopteromalus calandrae parasitized more maize weevils than didP. cerealellae. The former parasitoid parasitized only a few Angoumois grain moths successfully in maize, but parasitized many in wheat if the hosts were younger than 3 weeks old. Thus, both host age and type of grain affect suitability for parasitism. The effects of parental host (species on which the female developed) and experimental host (species exposed to parasitism) on parasitism rate ofP. cerealellae were tested in a host-switching experiment. Parasitism by parasitoids reared on maize weevils was 23% lower than that of parasitoids reared on Angoumois grain moth. This effect was independent of which host the filial generation of parasitoids was tested on. However, the experimental host species had a much greater effect on parasitoid fecundity than the parental host species. Female progeny had smaller body sizes when emerging from maize weevil than from Angoumois grain moth, which may explain the parental host effect on fecundity. There was also a slight intergenerational effect of host species on parasitoid body size.     

Preference and performance of the hyperparasitoid Syrphophagus aphidivorus (Hymenoptera: Encyrtidae): fitness consequences of selecting hosts in live aphids or aphid mummies

Abstract.  1. Theoretical models predict that ovipositional decisions of parasitoid females should lead to the selection of the most profitable host for parasitoid development. Most parasitoid species have evolved specific adaptations to exploit a single host stage. However, females of the aphid hyperparasitoid Syrphophagous aphidivorus (Mayr) (Hymenoptera: Encyrtidae) display a unique and atypical oviposition behaviour by attacking either primary parasitoid larvae in live aphids, or parasitoid pupae in dead, mummified aphids.
2. In the laboratory, the correlation between host suitability and host preference of S. aphidivorus on the host Aphidius nigripes Ashmead parasitising the aphid Macrosiphum euphorbiae (Thomas) was investigated.
3. The relative suitability of the two host stages was determined by measuring hyperparasitoid fitness parameters (survival, development time, fecundity, sex ratio, and adult size of progeny), and calculating the intrinsic rate of population increase ( r _m). Host preference by S. aphidivorus females and the influence of aphid defence behaviour on host selection was also examined.
4. Hyperparasitoid offspring performance was highest when developing from hosts in aphid mummies and females consistently preferred this host to hosts in parasitised aphids. Although aphid defensive behaviour may influence host selection, it was not a determining factor. Ecological and evolutionary processes that might have led to dual oviposition behaviour in S. aphidivorus are discussed.     

Endoparasitic flies,pollen-collection by bumblebees and a potential host-parasite conflict

Summary Conopid flies (Conopidae, Diptera) are common larval parasites of bumblebees. The larva develops inside the abdomen of workers, queens and males. Development is completed within 10–12 days after oviposition when the host is killed and the parasite pupates in situ. Development results in parasitised bees becoming unable to carry large loads of nectar, as the conopid larvae reside where the honey crop is normally located. Furthermore, an addition to the bee's unloaden body mass is likely (average larval weight reached at pupation by the common parasite species Sicus ferrugineus: ±SD 36.3±12.3 mg, n=59; by Physocephala rufipes: 55.8±16.9 mg, n=108). We here asked whether the propensity of workers of the bumblebee Bombus pascuorum to collect nectar rather than pollen is related to the presence of conopid larvae. For samples of bees (n=2254 workers) collected over 3 years of field studies in northwestern Switzerland, there was no difference in the frequency of bees caught as pollen collectors among parasitised (38.1% of cases, n=210) as compared to non-parastised bees (43.9%, n=360) ( ²=1.83, n.s.). However, compared to the non-parasitised bees (n=360), those hosts containing a third (last) instar larva (n=9) were less likely to collect pollen than expected by chance ²=6.91, P=0.003. Similarly, hosts with short survival time between capture and being killed by the developing larva (which hence must have harboured a late instar parasite at time of capture) were less likely to collect pollen (8%, n=25) than those found not parasitised (37.6%, n=891 ²=9.16, P<0.001). Late instar larvae grow so big that they fill the entire abdomen. Although there was also a tendency for presumably older bees to collect less pollen, this is unlikely to explain the observations. We also discuss whether these changes in foraging behaviour of bumblebees may reflect a host-parasite conflict over the type of resource to be collected.     

Host species preference and larval performance in the wood-boring beetlePhoracantha semipunctata F.

Adults of the wood-boring beetlePhoracantha semipunctata F. showed variability in their attractiveness to five varieties ofEucalyptus when presented with an array of logs in a natural setting. Logs of two host varieties (E. camaldulensis Dehnhardt and the hybridE. trabutii) attracted two to three times more adult beetles than did logs of other host species (E. cladocalyx F.,E. grandis Hill ex Maiden andE. tereticornis Small). In the field, high oviposition rates byP. semipunctata adults resulted in severe competition among larvae. Larval survivorship was low in field logs ofE. trabutii and high inE. cladocalyx logs, although these hosts were the most and least attractive to the adult beetles, respectively. However, when logs were hand infested at low larval densities, survivorship ofP. semipunctata larvae was highest in logs of bothE. camaldulensis andE. trabutii. These findings suggest that adult beetles in the field were most attracted to those logs ofEucalyptus species that represented the highest quality hosts for their progeny under conditions of reduced larval competition.     

Causal mechanisms underlying host specificity in bat ectoparasites

In parasites, host specificity may result either from restricted dispersal capacity or from fixed coevolutionary host-parasite adaptations. Knowledge of those proximal mechanisms leading to particular host specificity is fundamental to understand host-parasite interactions and potential coevolution of parasites and hosts. The relative importance of these two mechanisms was quantified through infection and cross-infection experiments using mites and bats as a model. Monospecific pools of parasitic mites (Spinturnix myoti and S. andegavinus) were subjected either to individual bats belonging to their traditional, native bat host species, or to another substitute host species within the same bat genus (Myotis). The two parasite species reacted differently to these treatments. S. myoti exhibited a clear preference for, and had a higher fitness on, its native host, Myotis myotis. In contrast, S. andegavinus showed no host choice, although its fitness was higher on its native host M. daubentoni. The causal mechanisms mediating host specificity can apparently differ within closely related host-parasite systems.     

The influence of plant species on attraction and host acceptance inCotesia glomerata (Hymenoptera: Braconidae)

Females of the larval parasitoidCotesia glomerata (L.) use plant-associated cues to locate their lepidopteran host,Pieris rapae L. In this study we investigated the influence of four host plant species,Brassica oleracea var.acephala (‘Vates’ kale),Tropaeolum majus (nasturtium),Lunaria annua (honesty), andCleome spinosa (spider flower), on two components of the host selection process inC. glomerata, namely, attraction and host acceptance. Choice tests in a flight tunnel showed that parasitoids were attracted to some host plant species more than to others in the absence of host larvae.B. oleracea was the most attractive plant species, followed byL. annua, T. majus, andC. spinosa. In previous studies it was shown thatB. oleracea carries highly suitable hosts forC. glomerata and that, in the field, parasitization rates on this plant were the highest. When host larvae were reared on the four host plant species and then transferred to a common substrate (B. oleracea var.capitata, cabbage), plant species that had served as diet for the hosts did not have a significant effect on acceptance for parasitization. Thus, parasitoids were attracted to host plant species differentially, but they did not discriminate among host larvae based on the dietary history of their hosts. ForC. glomerata, it appears that phytochemistry mediates host selection more by influencing parasitoid attraction than it does by affecting host acceptance.     

Plasmodium spp. (Apicomplexa: Plasmodiidae) of the flying lizardDraco volans (Agamidae)

The agamid lizardDraco volans from Palawan, Republic of the Philippines, was found to be parasitised by threePlasmodium species:P. draconis n. sp.,P. volans n. sp. andP. vastator, Laird 1960. BothP. draconis andP. volans, but notP. vastator, were also present inD. volans from Sarawak. The species are readily distinguished by schizont size, merozoite number, and gametocyte size and shape.P. volans has schizonts approximately one-half the size of those ofP. draconis and produces 4–6 merozoites in comparison to 4–16 in the larger species. Gametocytes of both new species are predominantly oval in the Palawan sample and elongate in that from Sarawak.P. draconis gametocytes are approximately twice the size ofP. volans gametocytes, but on average no more than one-half the size of gametocytes ofP. vastator.     

Growth,development, and behaviour of the parasitised and unparasitised larvae of a shelter‐building moth and consequences for the resulting koinobiont parasitoid

Most attention to size‐time trade‐offs of insects has focused on herbivore risk, with considerably less attention paid to parasitoids. Here, we focus on parasitoid risk, comparing the fates of unparasitised herbivore hosts and parasitised hosts that protect the parasitoids. Success of a koinobiont parasitoid (host grows after parasitisation) depends on maintaining a delicate balance with its host, thereby ensuring its own survival while the host grows. To evaluate growth rate–mortality rate relationships of host and parasitoid, we compared several aspects of the growth, phenology, and behaviour of unparasitised fern moth [Herpetogramma theseusalis (Walker) (Lepidoptera: Crambidae)] larvae and larvae parasitised by Alabagrus texanus (Cresson) (Hymenoptera: Braconidae), a solitary koinobiont (one parasitoid per host) wasp. Host larvae feed and construct shelters on sensitive fern, Onoclea sensibilis L. (Dryopteridaceae). Alabagrus texanus parasitise early‐instar moths in late summer, which overwinter in their host, emerging in mid‐summer to pupate and eclose. During the autumn following hatching and the immediately following spring, parasitised and unparasitised moth larvae did not differ in size, took similar time to choose between satisfactory and unsatisfactory foods, and built similar shelters. Prior to any other changes noted, more parasitised than unparasitised larvae also died when severely starved. Parasitised larvae subsequently grew less and pupated later than unparasitised ones (small size, slow growth), but consumed similar amounts of food. Although the numerically dominant parasitoid of fern moths, we concluded that A. texanus do not efficiently exploit their hosts.     

Parasitoid-induced mortality of house fly pupae by Pteromalid wasps in the laboratory

House fly, Musca domestica L., pupae were exposed to six species of pteromalid parasitoids, Muscidifurax zaraptor Kogan and Legner, M. raptor Girault and Sanders, M. raptorellus Kogan and Legner, Pachycrepoideus vindemiae (Rondani), Spalangia nigroaenea Curtis, and Urolepis rufipes Ashmead. Exposures were made for 48 h at six parasitoid-to-host ratios to measure the effect of parasitoid density on parasitoid-induced mortality (PIM) of hosts (excluding mortality as measured by parasitoid emergence). PIM was evident at all parasitoid-to-host ratios for all six species. Fly eclosion declined with a corresponding increase in the parasitoid-to-host ratio; the reverse was generally true for PIM. Parasitoid emergence increased initially with a corresponding increase in the parasitoid-to-host ratio to a point (depending on the parasitoid species), but then declined. The three Muscidifurax spp. and P. vindemiae exhibited similar behavior and generally avoided previously stung hosts until ovipositional restraints broke down at the higher parasitoid-to-host ratios. S. nigroaenea and U. rufipes exhibited little ovipositional restraint, resulting in a high proportion of PIM of hosts. Understanding factors that influence PIM will provide better evaluations of field releases of parasitoids to control flies and will aid in the development of the most economic procedures for large scale rearing of pteromalid parasitoids.     

The roles of foraging environment,host species,and host diet for a generalist pupal parasitoid

Even for parasitoids with a wide host range, not all host species are equally suitable, and host quality often depends on the plant the host feeds on. We compared oviposition choice and offspring performance of a generalist pupal parasitoid, Pteromalus apum (Retzius) (Hymenoptera: Pteromalidae), on two congeneric hosts reared on two plant species under field and laboratory conditions. The plants contain defensive iridoid glycosides that are sequestered by the hosts. Sequestration at the pupal stage differed little between host species and, although the concentrations of iridoid glycosides in the two plant species differ, there was no effect of diet on the sequestration by host pupae. The rate of successful parasitism differed between host species, depending on the conditions they were presented in. In the field, where plant‐associated cues are present, the parasitoid used Melitaea cinxia (L.) over Melitaea athalia (Rottemburg) (Lepidoptera: Nymphalidae), whereas more M. athalia were parasitised in simplified laboratory conditions. In the field, brood size, which is partially determined by rate of superparasitism, depended on both host and plant species. There was little variation in other aspects of offspring performance related to host or plant species, indicating that the two host plants are of equal quality for the hosts, and the hosts are of equal quality for the parasitoids. Corresponding to this, we found no evidence for associative learning by the parasitoid based on their natal host, so with respect to these host species they are truly generalist in their foraging behaviour.