Larviposition of Compsilura concinnata (meigen) (diptera: Tachinidae), a parasitoid of the gypsy moth,Lymantria dispar (L.) (lepidoptera: Lymantriidae)

Larviposition of Compsilura concinnata, a polyphagous tachinid parasitoid of Lepidoptera, is described. The conventional assessment, long‐established in the literature, places the site of larval deposition by C. concinnata as directly into the host's gut. New evidence, reported here, contradicts the earlier view. Dissection of 38 freshly parasitized gypsy moth (Lymantria dispar) larvae revealed as many maggots (n = 26) situated in the lumen of the midgut as were free in the hemocoel. Observations on maggot behavior and morphology in dissected hosts are briefly presented.     

Reproductive biology of the microtype tachinid fly Zenillia dolosa (Meigen) (Diptera: Tachinidae)

Reproductive biology including mating, adult longevity, fecundity and development of the tachinid fly Zenillia dolosa was investigated for optimizing rearing procedures using Mythimna separata as a host in the laboratory. Females lay microtype eggs containing a first instar larva on food plants of the host and then the eggs must be ingested by the host for parasitization. Mating success was 58.5% with mating duration of 80.7 min. Mating was most successful when day 0–1 females were kept with day 2–4 male flies. Female body size was positively correlated with its fecundity but not with longevity. However, females that survived longer produced more eggs during their lifetime. Parasitoids successfully developed in 4th to 6th instar host larvae. Host instars at the time of parasitoid egg ingestion significantly influenced development time of the immature parasitoid, but did not affect body size of the emerging parasitoid. We suggest that pairing newly emerged females with day 2–4 males should result in higher mating success and using the last instar hosts for parasitization should minimize development time of the parasitoid for rearing.     

Effects of the parasitization of a braconid, Apanteles, on the blood of its host, Pieris

Parasitization of a braconid wasp, Apanteles glomeratus, of larvae of a common cabbage butterfly, Pieris rapae crucivora, caused changes in differential haemocyte count (DHC), total haemocyte count (THC), and encapsulative capacity against dead eggs of Apanteles in the fourth and fifth instar host larvae.However, no correlation could be found between the number of Apanteles eggs deposited and THC of the middle fourth instar host larvae or between the number of parasitoid larvae and specific gravity of the haemolymph from the late fifth instar host larvae.From the changes in DHC and in THC of both non-parasitized and parasitized Pieris larvae, an increase in the number of plasmatocytes of non-parasitized Pieris larvae in the early fourth instar period was supposed to be due to transformation of prohaemocytes into plasmatocytes, and a low population of plasmatocytes of parasitized larvae in the comparable period was assumed to be due to a suppression of transformation of prohaemocytes by some factor released from the parasitoid eggs.Failure of the parasitized fourth instar Pieris larvae to encapsulate injected dead eggs of Apanteles indicated that the parasitoid embryos were, in some way, actively inhibiting the encapsulation reactions of the host.The increase in THC of the parasitized fifth instar larvae could not be ascribed to a decrease in the volume of host haemolymph. Rather it could be interpreted by a suppression of adhesive capacity of haemocytes in the host haemocoel to tissue surfaces.Reduced encapsulative capacity of the parasitized fifth instar larvae might be attributed either to a depression of the adhesive activity of plasmatocytes resulting from a depletion of energy source for haemocytes in the host haemolymph by parasitization, or from an active suppression of adhesiveness of the plasmatocytes by secretions from ‘giant cells’ (teratocytes) originated from the parasitoid.     

A novel parasitoid and a declining butterfly: cause or coincidence?

1. The small tortoiseshell butterfly (Aglais urticae L.) is considered to be a widespread and abundant generalist species in Northern Europe. However, it declined sharply in the U.K. between 2003 and 2008, coinciding with the arrival and spread of a parasitoid, Sturmia bella Meig. (Diptera: Tachinidae), which specialises on nymphalid butterflies. 2. Whether the decline in A. urticae is associated with the arrival of S. bella was investigated using data from a large‐scale butterfly monitoring scheme, and by collecting larvae to assess parasitoid incidence and parasitism frequency. Similar data were compiled for a related butterfly (Inachis io) which is also parasitised by S. bella but which is not declining. 3. Sturmia bella was recorded as far north as north Lincolnshire (53.53°N). Aglais urticae has declined significantly to the south of this latitude, but not to the north. 4. Sturmia bella was present in 26% and 15% of the larval groups of A. urticae and I. io, respectively, and now kills more individuals of A. urticae (but not I. io) than any native parasitoid. 5. Survival was 25–48% lower in batches of A. urticae larvae where S. bella was present, indicating that S. bella causes host mortality in addition to that caused by native parasitoids. 6. Our results suggest that S. bella may be playing a role in the recent decline of A. urticae. However, further research is needed to establish its effects relative to other potential drivers of trends in the abundance of this butterfly.     

Changes in haemolymph proteins of the fall armyworm, Spodoptera frugiperda (J. E. Smith), associated with parasitism by the braconid parasitoid Cotesia marginiventris (Cresson)

Changes in haemolymph proteins of the fall armyworm, Spodoptera frugiperda, associated with parasitism by the parasitoid Cotesia (= Apanteles) marginiventris were monitored by sodium dodecyl sulphate polyacrylamide gel electrophoresis. As early as hour 4 after parasitization treatment, several electrophoretically slow-migrating, high-molecular-weight proteins were detected in the host's haemolymph. These proteins were detected earlier in haemolymph from parasitized larvae than in haemolymph from control larvae, and their concentrations were higher in heavily parasitized host larvae (≥ 3 eggs/host) than in lightly parasitized larvae (1 egg/host). Additionally, unique proteins that migrated electrophoretically with bovine serum albumin appeared in the haemolymph of parasitized larvae at hour 8 after parasitization treatment and were evident in haemolymph collected through to hour 64.     

Host regulation and the embryonic development of the endoparasitoid Toxoneuron nigriceps (Hymenoptera: Braconidae)

Insect endoparasitoids modulate the host physiology through the injection of maternal-derived substances into the host, inducing physiological and hormonal changes in the host's internal environment to benefit parasitoid development. These changes are direct to control host development and regulate nutrient availability to the developing parasitoid, and they are synchronized with parasitoid development. Eggs of some of these parasitoids have low yolk content and require nutrients from the host hemolymph to initiate and complete embryogenesis. We report changes in the amino acid composition and protein profile of the host hemolymph of the endoparasitoid Toxoneuron nigriceps, and improved the in vitro culture of pre-germ band stage eggs. The protein profile of parasitized larvae was similar to controls throughout the embryonic development, but total amino acid concentration decreased in the first 2 h after parasitization, significantly increasing in the following hours up to 8 h. Amino acid levels were higher in parasitized larvae from 16 to 28 h after parasitization. Comparison of single amino acids indicated amino acids involved in energy metabolism (Krebs cycle) followed a trend during parasitoid embryogenesis, and their changes were correlated with embryonic development. Improvement in the in vitro development of 6 h-old eggs of T. nigriceps was obtained by adding factors released by the host fat body to the artificial medium, while a cell lysate stimulated embryogenesis and allowed the full development of newly laid eggs in vitro.     

Tritrophic interactions among coumarin, the herbivore Spodoptera litura and a gregarious ectoparasitoid Bracon hebetor

The secondary metabolites that play a defensive role in plants not only affect the growth and development of herbivores, but they can also influence their natural enemies. In the present study, the effect of coumarin was evaluated on a braconid parasitoid, Bracon hebetor (Say) (Hymenoptera: Braconidae) using polyphagous pest, Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae). Reproductive potential of the parasitoid declined significantly due to parasitization of host larvae feeding on coumarin supplemented diet. Total development period of B. hebetor extended significantly (2.17–2.38 days) when the host larvae were reared on diet amended with higher concentrations (625–3,125 parts per million) of coumarin as compared to unamended diet. Ingestion of coumarin supplemented diet by S. litura adversely affected the emergence and parasitization potential of B. hebetor. As compared to the control a significant decline in hatching of eggs was recorded when parasitoid wasps developed on host larvae fed on diet containing higher concentrations of coumarin (625–3,125 ppm). Negative effects of coumarin were also recorded from the next generation of the parasitoid.     

The impact of co-infection by a nucleopolyhedrovirus and the endoparasitoid Microplitis pallidipes on the total hemocyte count and composition in larval beet armyworm,Spodoptera exigua

The physiological effects of nucleopolyhedrovirus (NPV) infection and parasitism by Microplitis pallidipes (Hymenoptera: Braconidae) on the hemocytes of Spodoptera exigua (Lepidoptera: Noctuidae) larvae were examined. We found that compared to healthy (control) larvae, the total hemocyte count (THC) and granulocyte count in parasitized larvae increased 1 day after parasitization and then decreased, while the plasmatocyte count was not significantly affected for the first 5 days but was significantly enhanced on day 6 after parasitization. In parasitized + infected larvae, both the THC and granulocyte counts began be lower from day 1 compared to parasitized larvae, while the plasmatocyte count was generally lower than in parasitized larvae. Compared to the control, THC, and granulocyte counts of virus-infected larvae were higher 1 day after infection. Compared to that in virus-infected larvae, THC and granulocyte counts in parasitized + infected larvae began to decrease from day 1 while the plasmatocyte count generally decreased. We concluded that the host immune response of cell communities to parasitization by M. pallidipes was elicited during the development of the parasitoid egg, but that immune response was inhibited during larval development of parasitoids in the host body. Meanwhile, we found that NPV infection impeded the regulatory effect of M. pallidipes on host cellular immune responses, and parasitization by M. pallidipes similarly inhibited the host cellular immune response caused by NPV infection.     

The effect of parasitism byHyposoter didymator [Hym.: Ichneumonidae] on food consumption and utilization bySpodoptera litura [Lep.: Noctuidae]

The effect of parasitism byHyposoter didymator (Thunb.) [Hym.: Ichneumonidae] on food consumption and utilization bySpodoptera litura (Fb.) [Lep.: Noctuidae] was studied for seven days, during which the parasitoid completed its larval development. Food consumption, weight gained and faeces produced were significantly less in parasitized larvae than in unparasitized larvae after the 4^th day following parasitization. Approximate digestibility was higher in parasitized larvae after the 2^nd day following parasitization. Efficiency of conversion of ingested and digested food into body weight was greater in unparasitized larvae after the 2^nd day of parasitization. There seems to be a definite immediate advantage to the crop on releasing the parasitoid due to the reduced consumption of food. Contribution No. 46004 of Biological Control Centre (NCIPM), Bangalore 560 024.     

Dose-dependent influence of Microplitis rufiventris factors on developmental rate and growth of last-instar Spodoptera littoralis larvae

The solitary endoparasitoid, Microplitis rufiventris, attacks and can develop in earlier instars of Spodoptera littoralis larvae with preference to third‐instar larvae. We used the last stadium (sixth instar), a stage which is not naturally parasitized. The newly moulted larvae (0–3 h old) of this stadium were more acceptable for parasitization by the wasp females than the older ones (24 h old). Parasitization by M. rufiventris wasp of last instar S. littoralis larvae leads to dose (no. of eggs + parasitoid factors)‐dependent effects which were more pronounced at 20°C than at 27°C. A single oviposition into a sixth instar host larva resulted in normal development of the host. However, superparasitization increased the proportions of developmentally arrested hosts and number of live wasp larvae. Development of supernumerary individuals of the parasitoid in the host larva leads to dose‐related adverse effects on host growth and development. The present study may provide interesting opportunities for studying the physiological bases of host–parasitoid interactions and parasitoid intra‐specific competition in the biological system considered.     

Mortality by parasitization in the association between the egg-pupal parasitoid Fopius arisanus and Ceratitis capitata

We studied the interaction betweenthe egg-pupal parasitoid Fopius (+ Biosteres) arisanus (Sonan) (+Opius oophilus Fullaway) (Hymenoptera: Braconidae) and Ceratitis capitata (Wiedemann)(Diptera: Tephritidae) to assess the totalimpact of the parasitoid on the survival ofthis host. We tried to discover the factorsdetermining host suitability, measure actualpercent parasitism, and quantify host mortalityby parasitization. Research was carried outapplying dechorionation treatment, anon-destructive procedure that makes hosteggshells transparent to microscopicobservation, without interfering withdevelopment. We found that percent parasitismobserved at the egg stage did not correspond tothat detectable for emerging adults. In fact,parasitized host eggs were subject to a highermortality than non-parasitized ones. Moreover,a certain percentage of the parasitoid eggs didnot develop to the adult stage. Results fromour study allowed us to measure the percentmortality by parasitization per parasitizedegg. Furthermore, we analyzed the mortalityfactors due to parasitization acting during thehost egg stage. Most of them had never beenevidenced before and may help to explain thisphenomenon. In particular, we found that theage of the host eggs exposed to parasitoidsplays a fundamental role in the mortality byparasitization and that F. arisanusparasitizes C. capitata eggs moreefficiently close to the time of eclosion.     

Effects of parasitization or injection of parasitoid-derived factors from the endoparasitic wasp Glyptapanteles porthetriae (Hym., Braconidae) on the development of the larval host, Lymantria dispar (Lep., Lymantriidae)

Second instar larvae of Lymantria dispar were parasitized or injected with parasitoid-derived factors such as venom, calyx fluid or parasitoid eggs from Glyptapanteles porthetriae . Growth and development of the host larvae were affected in all different groups compared to control larvae of the same age, injected with Ringer solution. The greatest impact on host growth and on the duration of the 3rd instar was caused by injecting parasitoid eggs. Treated larvae showed melanized capsules or nodules in the hemocoel. While the wasp age had no effect on parasitization efficiency or on the percentage of melanized particles in the hemocoel, significantly more encapsulations were found in larvae parasitized by old wasps as opposed to young wasps. Superparasitization (double or quadruple oviposition) increased the parasitization efficiency markedly. While none of the control larvae showed melanized particles, in the groups of single and superparasitized (2× and 4×) hosts a high percentage of melanized particles (capsules and nodules) occurred.     

Does superparasitism improve host suitability for parasitoid development? A case study in the Microplitis rufiventris-Spodoptera littoralis system

Superparasitism refers to the oviposition behavior of parasitoid females who lay their eggs in an already parasitized host. Recent studies have shown that allocation of additional eggs to an already parasitized host may be beneficial under certain conditions. In the present work, mortality of Microplitis rufiventris wasps was significantly influenced by both host instar of Spodoptera littoralis larvae at parasitism and level of parasitism. In single parasitization, all host instars (first through sixth) were not equally suitable. Percentage of emergence success of wasp larvae was very high in parasitized first through third (highly suitable hosts), fell to 60% in the fourth instar (moderate suitable) and sharply decreased in the penultimate (5th) instars (marginally suitable). Singly parasitized sixth (last) instar hosts produced no wasp larvae (entirely unsuitable), pupated and eclosed to apparently normal adult moths. The scenario was different under superparasitism, whereas supernumerary individuals in the highly suitable hosts were almost always killed as first instars, superparasitization in unsuitable hosts (4th through 6th) had significant increase in number of emergence success of wasp larvae. Also, significantly greater number of parasitoid larvae successfully developed in unsuitable hosts containing three wasp eggs than counterparts containing two wasp eggs. Moreover, the development of surplus wasp larvae was siblicidal in earlier instars and nonsiblicidal gregarious one in the penultimate and last “sixth” instars. It is suggested that the optimal way for M. rufiventris to deal with high quality hosts (early instars) is to lay a single egg, while the optimal way to deal with low quality hosts (late instars) might be to superparasitize these hosts.     

Parasitoid–Pathogen–Pest Interactions of Chelonus insularis, Campoletis sonorensis, and a Nucleopolyhedrovirus in Spodoptera frugiperda Larvae

In this study we examined interactions between two solitary endoparasitoids, the braconid Chelonus insularis and the ichneumonid Campoletis sonorensis, and a multiple-enveloped nucleopolyhedrovirus infecting Spodoptera frugiperda larvae. We examined whether ovipositing females minimize interference by discriminating amongst hosts and examined the outcome of within-host competition between parasitoid species and between the parasitoids and the virus. The egg–larval parasitoid Ch. insularis did not discriminate between virus-contaminated and uncontaminated S. frugiperda eggs; all S. frugiperda larvae that emerged from surface-contaminated eggs died of viral infection prior to parasitoid emergence. The larval parasitoid C. sonorensis also failed to discriminate between healthy and virus-infected S. frugiperda larvae or between larvae unparasitized or parasitized by Ch. insularis. Host larvae parasitized in the egg stage by Ch. insularis were suitable for the development of C. sonorensis when they were multiparasitized by C. sonorensis as first, second, third, and fourth instars, whereas emergence of Ch. insularis was dramatically reduced (by 85 to 100%) in multiparasitized hosts. Nonspecific host mortality was significantly higher in multiparasitized hosts than in singly parasitized hosts. The development time and sex ratio of C. sonorensis in multiparasitized host larvae were unaffected by the presence of Ch. insularis larval stages. Both Ch. insularis parasitized and nonparasitized larvae of the same instar (second, third, or fourth instars) had a similar quantitative response to a challenge of virus inoculum. All host larvae that ingested a lethal dose of virus were unsuitable for Ch. insularis development. In contrast, C. sonorensis did not survive in hosts that ingested a lethal virus dose immediately after parasitism, but parasitoid survival was possible with a 2-day delay between parasitism and viral infection and the percentage of parasitoid emergence increased significantly as the interval between parasitism and viral infection increased. The development time of C. sonorensis was significantly reduced in virus-infected hosts compared to conspecifics that developed in healthy hosts. C. sonorensis females that oviposited in virus-infected hosts did not transmit the virus to healthy hosts that were parasitized subsequently. Field applications of virus for biocontrol of S. frugiperda may lead to substantial mortality of immature parasitoids, although field experiments have not yet demonstrated such an effect.     

Intrinsic competition between the parasitoids Eretmocerus mundus and Encarsia formosa in Bemisia tabaci

Immature stages of Eretmocerus mundus Mercet and Encarsia formosa Gahan (both Hymenoptera: Aphelinidae) compete in larvae of their host, Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Laboratory tests were carried out on excised tree tobacco leaves, exposing B. tabaci nymphs to one of the parasitoid species alone or to both species, one after the other, to obtain multi‐parasitization. Parasitization by E. mundus and E. formosa was allowed on specific host stages in order to obtain interactions between different immature stages of the two parasitoids (eggs, and first, second, and third instars). The outcome from each multi‐parasitization treatment was verified by analysing data on parasitoid adult emergence. Observations under a stereomicroscope and dissections of multi‐parasitized hosts were also performed in order to demonstrate any factors potentially determining the outcome of competition. Eretmocerus mundus clearly prevailed over E. formosa when multi‐parasitism occurred. A higher percentage of adults emerging from multi‐parasitized hosts belonged to this parasitoid species (68.0–88.9% depending on the treatment). The lowest percent emergence by E. mundus (68.0%) and total percent emergence of parasitoid adults (52.2%) were obtained when E. mundus first instars interacted with hosts parasitized by E. formosa third instars. Observations and dissections showed that first‐instar E. mundus induced mortality in E. formosa immatures at penetration into the hosts, although they encountered greater difficulty in exploiting hosts inside which E. formosa had reached the third stage of development. In contrast, development of E. formosa immatures was not immediately inhibited if parasitization took place on hosts inside which E. mundus larvae had already penetrated. In this case, however, E. mundus also prevailed over E. formosa (72.5% of the emerged adults). Implications for the use of these parasitoid species against B. tabaci in biological control programmes are discussed.     

Host location and discrimination mediated through olfactory stimuli in two species of Encyrtidae

The role of olfactory stimuli in host detection and evaluation was studied in two encyrtid Hymenoptera. The first, Epidinocarsis lopezi De Santis, is a monophagous parasitoid of the cassava mealybug Phenacoccus manihoti Matile-Ferrero, itself feeding exclusively on cassava, Manihot esculenta Crantz. The second, Leptomastix dactylopii Howard, is a monophagous parasitoid of the Citrus mealybug, Planococcus citri Risso, but this latter is highly polyphagous. The behaviour of females of both parasitoids (attaction and locomotion) was compared in a tubular olfactometer for the odours of their respective hosts on cassava and poinsettia. Tests were made using: 1) healthy host-plant alone; 2) host-plant infested with unparasitized mealybugs; 3) unparasitized mealybugs only; 4) host-plant infested with parasitized mealybugs and 5) parasitized mealybugs only. Only E. lopezi was attracted by the odour of the host-plant alone, but both species were attracted by the odour of an infested host-plant and that of unparasitized mealybugs. The odour of parasitized mealybugs, alone or on host-plant, induced an undirected activity. The attraction of E. lopezi to the odour of the host-plant alone could be linked to the monophagous diet of its host, whereas the attraction of the two species of parasitoids to the odours of infested host-plants and unparasitized mealybugs could be due to the fact that both parasitoids are specialists. The behavioural response of both species to the odour of parasitized mealybugs revealed a new aspect in host discrimination: the identification of parasitized hosts could be partly mediated through olfactory stimuli, and not only through gustatory stimuli.     

Phenology of Parasetigena silvestris (Diptera: Tachinidae), gypsy moth (Lymantria dispar) (Lepidoptera: Lymantriidae) larval parasitoid and its efficiency for parasitisation

Parasetigena silvestris is a univoltine, solitary, larval endoparasitoid which lays its eggs on the surface of gypsy moth larvae. Field collection of the host larvae (2nd through 5th instar) from an artificially established gypsy moth population were made to compare stage specific parasitism between larvae without and with P. silvestris tachinid eggs. The tachinid oviposition rate detected was highest in second instar larvae, and then decreased as larvae developed toward full maturity. The opposite was true for tachinid parasitoid emergence which had no emergence from second through third host instar larvae. Fourth instar gypsy moth larvae, however, experienced significantly higher parasitism by P. silvestris in the larvae with eggs than those without the eggs. The braconid wasp Cotesia melanoscelus caused significantly higher parasitism in early instar larvae with P. silvestris eggs than in those without the eggs. The tachinid prefers to lay more eggs on parasitised larvae by the braconid even though the braconid is a superior competitor to the fly during multiparasitism. Factors influencing parasitism rates by P. silvestris such as host-parasitoid synchronisation and the multiparasitism interaction with C. melanoscelus are discussed.     

Developmental interactions between the army wormLeucania separata [Lep.: Noctuidae] and its parasiteApanteles ruficrus [Hym.: Braconidae]

The developmental interactions between the gregarious endoparasitoidApanteles ruficrus Hal. and the army worm,Leucania separata Walker were investigated. The parasitoid preferred young host larvae and developed in 9.5 days irrespective of host age at the time of parasitization. The growth of parasitized host larvae were depressed. The net maximum weight of the host larva was positively correlated with the number of parasitoid eggs laid when the 2nd instar was parasitized. And when parasitizing in 2nd instar, the weight of parasitoid was negatively correlated with the number of eggs laid. The parasitoid has an ability to regulate the size of the host and the parasitoid itself according to the number of eggs laid when the host larva is very small.     

Interaction between MbMNPV and the braconid parasitoid Habrobracon hebetor (Hym., Braconidae) on larvae of beet armyworm,Spodoptera exigua (Lep., Noctuidae)

The survival of a braconid parasitoid Habrobracon hebetor was investigated on nucleopolyhedrovirus (NPV)-infected Spodoptera exigua larvae. The second-instar larvae were exposed to 30, 51.4 and 180 PIB/mm² of Mamestra brassicae NPV (MbMNPV) as under-LD₅₀, LD₅₀ and over-LD₅₀ values, respectively. They were accessible to be parasitized by H. hebetor after 24, 48 and 72 h post-treatment. Infection of the larvae with MbNPV was deleterious to the survival and parasitism of H. hebetor. The survival of H. hebetor in MbNPV-infected S. exigua larvae was dependent on the interval between viral infection and parasitization, as well as on the treatment dose of MbMNPV; very few adults of parasitoid emerged from infected hosts when host larvae were exposed to 180 PIB/mm² of MbNPV on 72-h interval treatment. The inoculation dose of MbNPV and the timing of parasitoid release had significant effect on the development of H. hebetor on virus-infected hosts. Field applications of virus for biocontrol of S. exigua may lead to substantial mortality of immature parasitoids.