Unparasitized Pupae Research Articles

Native generalist natural enemies and an introduced specialist parasitoid together control an invasive forest insect.

Specialized natural enemies have long been used to implement the biological control of invasive insects. Although research tracking populations following biological control introductions has traditionally focused on the impact of the introduced agent, recent studies and reviews have reflected an appreciation of the complex interactions of the introduced specialist agents with native generalist natural enemies. These interactions can be neutral, antagonistic, or complementary. Here we studied the invasive defoliator winter moth (Operophtera brumata) in the Northeast USA to investigate the role of native, generalist pupal predators along with the introduced, host-specific parasitoid Cyzenis albicans. Prior research in Canada has shown that predation of winter moth pupae from native generalists increased after C. albicans was established as a biological control agent. To explain this phenomenon, the following hypotheses were suggested: (H1 ) parasitoids suppress the winter moth population to a density that can be maintained by generalist predators, (H2 ) unparasitized pupae are preferred by predators and therefore experience higher mortality rates, or (H3 ) C. albicans sustains higher predator populations throughout the year more effectively than winter moth alone. We tested these hypotheses by deploying winter moth pupae over 6 years spanning 2005 to 2017 and by modeling pupal predation rates as a function of winter moth density and C. albicans establishment. We also compared predation rates of unparasitized and parasitized pupae and considered additional mortality by a native pupal parasitoid. We found support for the first hypothesis; we detected both temporal and spatial density dependence, but only in the latter years of the study when winter moth densities were low. We found no evidence for the latter two hypotheses. Our findings suggest that pupal predators have a regulatory effect on winter moth populations only after populations have been reduced, presumably by the introduction of the host-specific parasitoid C. albicans.

Host availability affects the interaction between pupal parasitoid Coptera haywardi (Hymenoptera: Diiapridae) and larval-pupal parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae).

The use of multiple species in biological control programmes is controversial when interactions among them are not fully understood. We determined the response of the pupal parasitoid Coptera haywardi (Oglobin) to different availability of Anastrepha ludens (Loew) pupae previously parasitized or not by larval-pupal Diachasmimorpha longicaudata (Ashmead). The two types of pupae were exposed at different ages and proportions to different numbers of C. haywardi females for 48 h. The performance of C. haywardi adults emerging from parasitized and unparasitized pupae was measured. Coptera haywardi prefers to attack unparasitized A. ludens pupae rather than pupae parasitized by D. longicaudata. However, when the availability of unparasitized pupae was low or the number of foraging females was high, C. haywardi competed against early immature stages of the D. longicaudata, or hyperparasitized, feeding directly on the advanced-immature developmental stages of the early acting species. Adults of C. haywardi emerging as hyperparasitoids were no different in size, fecundity and longevity from those emerging as primary parasitoids. Our data suggest that simultaneous use of these species in augmentative biological control projects may be feasible but should be carefully planned in order to avoid any detrimental effect of its interaction.

Searching Ability of Pupal Parasitoid, Dirhinus giffardii (Silvestri) on Bactrocera zonata (Saunders) at Various Depths of Plant Debris

The present study was carried out to determine the searching ability of pupal parasitoid, Dirhinus giffardii of Bactrocera zonata in the Bio Control Research Laboratory, | department of Entomology, SAU, Tandojam, at temperature 27 ± 1ºC and 60 ± 5% relative humidity. Adults of fruit fly were fed with water, sugar and needo milk powder, whereas, Dirhinus giffardii were fed with honey and water solution. Ten days old D. giffardies were used against 20 pupae of Bactrocera zonata in the experiment and data recorded on parasitized pupae and un-parasitized pupae after 24, 48, 72 and 96 hours. The results in all treatments indicates that highest parasitized pupae were at peak level of (16.66) after 72 hours age of pupae on the depth of 0 cm in plant debris followed by 4 cm depth (16.33), whereas lowest parasitized pupae were recorded at 5cm depth (13.66) after 72 hours of age inside plant debris. Likewise, the highest un-parasitized pupae were at peak level of (14.00) after 24 hours of age of pupae on the depth of 3cm in plant debris followed by 1cm depth (13.00), whereas lowest un parasitized pupae were recorded at 4cm depth (11.66) after 24 hours of age inside plant debris. The analysis of variance indicated that there wasno significant difference among the parasitized and unparasitized pupae of flies in the different depths of plant debris and age intervals (P

Rearing of five hymenopterous larval-prepupal (Braconidae, Figitidae) and three pupal (Diapriidae, Chalcidoidea, Eurytomidae) native parasitoids of the genus Anastrepha (Diptera: Tephritidae) on irradiated A. ludens larvae and pupae

The aim of this study was to ascertain if eight species of native larval-prepupal and pupal Anastrepha (Diptera: Tephritidae) parasitoids which have been recently domesticated and colonized (Aluja et al. in press) could be reared on irradiated larvae and pupae, and if such was the case, determine the optimal irradiation dose so that only adult parasitoids (not flies) would emerge. The species considered were: Doryctobracon crawfordi, Utetes anastrephae, Opius hirtus (all larval-prepupal braconids), Aganaspis pelleranoi, Odontosema anastrephae (both larval-prepupal figitids), Coptera haywardi, Eurytoma sivinskii and Dirhinus sp. (diapriid, eurytomid and chalcidoid pupal parasitoids). Eight-day-old A. ludens larvae or 3-day-old A. ludens pupae were irradiated with 0, 5, 10, 15, 20, 25, 30, 35, 40, 50, 60 and 70 Gy under free oxygen and then subjected to parasitoid attack. Emergence of the unparasitized host was completely halted at 20–25 Gy but such was not the case with the three braconid parasitoids that emerged even if subjected to doses as high as 70 Gy. In the case of the figitids, the emergence of the host and the parasitoids was completely halted at 20 and 25 Gy, respectively. Some parasitoid emergence was recorded at 5–15 Gy but at this irradiation dose, fly adults also emerged rendering the fly/parasitoid separation procedures impractical. Finally, in the case of the pupal parasitoids, A. ludens adults emerged from unparasitized pupae irradiated at 15 Gy. Beyond this dose, only parasitoids emerged. With the exception of the figitid larval-prepupal parasitoids, irradiation did not negatively affect adult longevity or fecundity. Our results show that parasitoid mass rearing with irradiated hosts is technically feasible.

Closely related parasitoids induce different pupation and foraging responses inDrosophilalarvae

Few examples exist where parasites manipulate host behaviour not to increase their transmission rate, but their own survival. Here we investigate fitness effects of parasitism byAsobaraspecies in relation to the pupation behaviour of the host,Drosophila melanogaster. We found thatAsobara citriparasitized larvae pupate higher in rearing jars compared to unparasitized controls, whileA. tabidapupated on or near the medium. No change in pupation site was found for three other species. A follow‐up experiment showed a non‐random distribution of parasitized and unparasitized pupae over the different jar parts. To test the adaptiveness of these findings, we performed pupal transfer experiments. Optimum pupation sites were found to be different between host individuals; wall individuals survived better than bottom individuals, but bottom individuals did worse at the wall. Two parasitoid species that alter pupation site significantly showed high rates of diapause at their ‘preferred’ pupation site. For one of them,A. citri, pupation occurred at the optimal site for highest survival (emergence plus diapause). From literature we know that pupation height and foraging activity are genetically positively linked. Therefore, we implement a short assay for rover/sitter behavioural expression by measuring distance travelled during foraging after parasitism. For one out of three species, foraging activity was reduced, suggesting that this species suppresses gene expression in theforpathway and thereby reduces pupation height. The parasitoid species used here, naturally inhabit widely different environments and our results are partly consistent with a role for ecology in shaping the direction of parasite‐induced changes to host pupation behaviour. More parasitoids are found on the wall of the rearing jar when they originate from dry climates, while parasitoids from wet climates pupate on the humid bottom.

Interspecific competition between Xanthopimpla stemmator Thunberg and Dentichasmias busseolae Heinrich (Hymenoptera: Ichneumonidae), pupal parasitoids attacking Chilo partellus (Lepidoptera: Crambidae) in East Africa

Abstract Interspecific competition between Xanthopimpla stemmator and Dentichasmias busseolae was studied using pupae of the invasive crambid stemborer Chilo partellus as the host. While X. stemmator is an old association, D. busseolae formed a relatively new association with C. partellus in East Africa. Two different time intervals between parasitism (0 and 48 h) and two parasitoid sequences [i.e., X. stemmator before D. busseolae (Xs–Db) and D. busseolae before X. stemmator (Db–Xs)] were chosen. In addition, the parasitoids’ performance on pupae in maize stems and ears was assessed. For both X . stemmator and D . busseolae , there was no difference in foraging time between unparasitized pupae and pupae previously parasitized by the other species, indicating that the two species were not capable of interspecific host discrimination. In the Xs–Db sequence, the time interval between parasitism did not have an influence on the percentage of pupae producing either parasitoid species. By contrast, in the Db–Xs sequence, the percentage of pupae producing X. stemmator was almost 8 times higher in the 0-h than the 48-h interval, while for D. busseolae it was the reverse. In the 0-h interval, X. stemmator outcompeted D. busseolae irrespective of whether it parasitized first or second, while in the 48-h interval, the parasitoid parasitizing first won. While D. busseolae successfully searched for and parasitized pupae in both stems and ears, parasitism of pupae in ears by X. stemmator was negligible. It was concluded that the two species could co-exist because they partly exploit different ecological niches.

Intraguild predation by the generalist predator Dicyphus hesperus on the parasitoid Encarsia formosa

Predation was measured in the laboratory by Dicyphus hesperus females on patches of greenhouse whitefly (Trialeurodes vaporariorum) pupae. The patches contained different proportions of unparasitized pupae and those parastisized as nymphs by Encarsia formosa. Dicyphus hesperus fed readily on parasitized pupae and the number of parasitized pupae consumed increased with the proportion available indicating a capacity for intraguild predation. However, D. hesperus females did not display a preference for feeding on parasitized pupae versus unparasitized pupae. Dicyphus hesperus adults were released at three densities into greenhouse enclosures containing tomato plants harbouring greenhouse whitefly and immature E. formosa. Numbers of killed and parasitized whitefly nymphs and pupae and the total number of healthy whitefly were compared among Dicyphus density treatments. On upper leaves, the amount of predation on whitefly nymphs was higher at the highest predator density than at the lower density or in enclosures where D. hesperus was not released. On lower leaves, the number of parasitized pupae was lowest with the highest predator density indicating a negative effect of intraguild predation by D. hesperus on E. formosa. Despite this, Dicyphus density did not affect the density of whitefly in the presence of E. formosa. The results are discussed as they relate to concurrent use of D. hesperus and E. formosa for regulation of greenhouse whitefly populations.

Discrimination of Self-Parasitized Hosts by the Pupal Parasitoid <I>Muscidifurax zaraptor</I> (Hymenoptera: Pteromalidae)

Abstract Females of Muscidifurax zaraptor Kogan & Legner, a solitary pupal parasitoid of house flies, Musca domestica L., discriminated between hosts previously parasitized by themselves and by conspecifics. When hosts were in short supply, females avoided self-superparasitism and laid eggs in hosts that had been previously parasitized by conspecifics. When females were given a choice to oviposit in unparasitized pupae and hosts previously parasitized by themselves and conspecifics, females avoided superparasitism. Superparasitism seems to be avoided by the use of short-term memory of the position of the pupae and the use of internal host cues. Females did not respond to external cues. The adaptive significance of superparasitism in M. zaraptor is discussed.

EFFECT OF PARASITIZATION BY THE PUPAL ENDOPARISITOID, PTEROMALUS PUPARUM (HYMENOPTERA: PTEROMALIDAE) ON HUMORAL IMMUNE REACTIONS OF PIERIS RAPAE (LEPIDOPETERA: PIERIDAE)*

Abstract Studies on the effect of parasitization by the endoparasitoid on host humoral immune reactions are carried out with the pupal endoparisitic wasp, Pteromalus puparum, and its host, Pieris rapae. Phenoloxidase (PO) activity of parasitized hosts hemolymph increased significantly at 12 h, day four and day five after parasitization. Hem‐agglutination activity of parasitized hosts hemolymph was always higher than that of wounded and unparasitized ones. Moreover, antibacterial activity of parasitized hosts hemolymph became more and more stronger, whilst wounded and unparasitized pupae only owned a weak antibacterial activity. It suggested that activities of humoral immune factors of Pieris rapae could be influenced to some degrees by P. puparum.

The Bionomics ofCoptera Haywardi(Ogloblin) (Hymenoptera: Diapriidae) and Other Pupal Parasitoids of Tephritid Fruit Flies (Diptera)

Abstract The endoparasitoidCoptera haywardi(Ogloblin) (Diapriidae) was discovered in Mexico attacking the pupae of the Mexican fruit fly,Anastrepha ludens(Loew). Typically, parasitoids of Diptera Cychlorrhapha pupae develop as ectoparasitoids and are generalists that attack hosts in a number of families. Aspects of the bionomics ofC. haywardiwere compared to those of two chalcidoid ectoparasitoids,Dirhinus himalayanusWestwood andSpalangia geminaBoucek.C. haywardideveloped in three genera of Tephritidae, but not in species of other families. The two species of chalcidoids developed in all the calypterate and acalypterate hosts to which they were exposed. In an olfactometerC. haywardipreferredAnastrepha suspensa(Loew) pupae, while the chalcidoids preferred the pupae ofMusca domestica L.This preference inS. geminawas diminished in insects that had been reared onA. suspensa. C. haywardioviposited in theA. suspensapupae that had been previously parasitized by the braconidDiachasmimorpha longicaudata(Ashmead). However, it completed development only in unparasitized pupae. Mortality of the primary parasitoid due toD. himalayanuswas approximately two-thirds the mortality inflicted on the host fly.S. geminadid not discriminate between parasitized and unparasitized pupae ofA. suspensaand developed in both.C. haywardiappears to have a more restricted host range relative to chalcidoid pupal parasitoids and this may be due to its endoparasitic development.

Biological Control of Greenhouse Whitefly with the ParasitoidEncarsia formosaon Tomato: An Individual-Based Simulation Approach

Biological control strategies of greenhouse whitefly with the parasitoidEncarsia formosawere studied with a simulation model of the parasitoid–host interaction in a crop. The model is based on developmental biology of both insect species and on the searching and parasitization behavior of individual parasitoids, in relationship to host plant characteristics and greenhouse climate. The model includes stochasticity and a spatial structure which is based on location coordinates of plants and leaves. The simulated population increase of greenhouse whitefly in the absence or presence of parasitoids agreed well with observed populations in a tomato crop. Whiteflies were suppressed rather than regulated by the parasitoids at extremely low densities (<0.3 unparasitized pupae per plant), but did not become extinct. The percentage of black pupae fluctuated between 40 and 70%. According to the model, the parasitoid adults reached high densities of 7.4 per plant, but due to the low whitefly density not more than 1% of the parasitoids were searching on infested leaflets. The degree of whitefly control was strongly affected by variation in giving up time (GUT) of the parasitoids. When variation in GUT was excluded in the model, the whitefly population became almost extinct. Other important parameters of the parasitoid which strongly influenced the level of control were the walking speed and walking activity, the probability of oviposition after encountering a host, the ratio of search times on both leaf sides, and the longevity. The combined effect of these important attributes of a parasitoid can be tested with the model. When comparing successes ofE. formosaon different crops, attention should be focused on the same parameters plus the whitefly development duration and the number, size, and production of leaves in the canopy. The model can be used to evaluate a number of release strategies on several crops and under various greenhouse climate conditions.

Insect‐crop interactions in a diversified cropping system: parasitism by Aleochara bilineata and Trybliographa rapae of the cabbage root fly, Delia radicum, on cabbage in the presence of white clover

AbstractParasitism of the cabbage root fly, Delia radicum (L.) by the staphylinid Aleochara bilineata Gyllenhal and the cynipid Trybliographa rapae Westwood was examined in a cabbage monoculture and a mixed stand of cabbage undersown with white clover. Number of overwintering cabbage root fly pupae per plant was consistently reduced in the mixed stand, and the incidence of plants attacked by cabbage root fly was either reduced or not different in the mixed stand compared to cabbage monoculture. For both parasitoids, the probability of D. radicum attacked plants having at least one parasitized pupa increased with density of cabbage root fly pupae around the plant. For A. bilineata, this positive relation between presence of parasitism and host density was consistently stronger in cabbage monoculture than in cabbage undersown with clover. Location of a host plant by T. rapae was not consistently affected by the presence of clover. D. radicum attacked plants situated in the cabbage and clover mixture were found by T. rapae as easily as in cabbage monoculture. Overall, the ‘total risk of parasitism’ for a cabbage root fly pupa by A. bilineata was reduced in the mixed stand compared to the cabbage monoculture, whereas the risk of parasitism by T. rapae was not consistently affected by clover. For both parasitoids, intensity of parasitism showed a variable relationship with host density on individual plants attacked by the cabbage root fly. Overall, in spite of consistently lower total density of pupae in the mixed cabbage – clover than in cabbage monoculture, the density of unparasitized pupae was reduced by the presence of non‐host plants only in two of the four experiments. The results emphasize the need to include not only herbivore and crop, but also other plant species as well as natural enemies when evaluating management methods.

After the Decline: What Maintains Low Winter Moth Density after Successful Biological Control?

Life-table data for winter moth are analysed for an 8-year period following introduction of parasitoids for biological control in British Columbia, Canada. Winter moth density declined in 1984, and has remained low since 1985 at an average density of approximately 1.20 adults per m 2 . Introduced parasitoids contributed to mortality during the decline, and have a weak, delayed density-dependent effect at the new low density. Mortality of unparasitized pupae in the soil (primarily by predation) is strongly, and directly density-dependent at the new low density, and is the factor which is most strongly regulatory. Analysis indicates that the strong regulation of winter moth numbers by generalist predators allows parasitism levels to vary greatly after suppression without the eruption of winter moth populations; if parasitism were absent, winter moth populations would erupt to pre-biocontrol levels

Assessment of Potential Methods of Measuring Parasitism by Brachymeria intermedia (Nees) (Hymenoptera: Chalcididae) of Pupae of the Gypsy Moth

This study was conducted to assess potential biases associated with three methods of calculating percentage parasitism of gypsy moth, Lymanttia dispar (L.), pupae by Brachymeria intermedia(Nees). We determined the timing of four processes: (1) recruitment of gypsy moth (host) larvae to the pupal stage, (2) recruitment (oviposition) of B. intermedia to its immature stage, (3) losses of hosts from the pupal stage because of mortality or adult emergence, and (4) losses of immature B. intermedia because of mortality or adult emergence. B. intermedia emerged after most unparasitized pupae had died or after moths had emerged. As a result, the proportion of pupae in samples that were parasitized increased with time. Sample percentage parasitism peaked late in the season and overestimated levels of stage-specific parasitism. Parasitism extended the residence time of parasitized pupae, with the result that they were available to predators for a longer period of time than un parasitized pupae and suffered a higher level of predation. Examination of pupal exuviae at the end of the season, therefore, underestimated the effect of B. intermedia. No biases were observed that affected estimation of percentage parasitism through the direct measurement of host and parasitoid recruitment. Of the three methods studied (percentage parasitism in samples, examination of exuviae, and measurement of recruitment), direct measurement of host and parasitoid recruitment appears to be the best method for measuring the effect of B. intermedia on L. dispar.

Interactions between an eucoilid [Hymenoptera] and a staphylinid [Coleoptera] parasitoid of the cabbage root fly

The interaction betweenTrybliographa rapae andAleochara bilineata, 2 parasitoids of the cabbage root fly, is discussed. Larvae ofA. bilineata could not differentiate between cabbage root fly pupae containingT. rapae in its endoparasitic state and unparasitized pupae but could recognize pupae containingT. rapae once the latter had reached its ectoparasitic state. Attack byA. bilineata whileT. rapae was still in its endoparasitic state usually resulted in the staphylinid killing the eucoilid. IfT. rapae had reached the ectoparasitic state before the host pupa was attacked byA. bilineata larvae the eucoilid survived attack by the beetle larva. Multiparasitism, however, resulted in increased levels of mortality of both parasitoid populations.

Competitive Parasitism of House Fly Pupae (Diptera: Muscidae) by Muscidifurax Zaraptor and Urolepis Rufipes (Hymenoptera: Pteromalidae)1

Muscidifurax zaraptor was more efficient at parasitizing house fly pupae than was Urolepis rufipes. Both wasp species preferred to oviposit on unparasitized pupae. Ovipositional restraints of M. zaraptor broke down at high parasitoid-to-host ratios; superparasitism caused a reduction in parasitoid emergence and in the percentage of females that emerged. Under competitive conditions, reductions in parasitoid emergence occurred for both species, but M. zaraptor dominated and showed greater discrimination between species.

OVIPOSITION RESTRAINT OFNASONIA VITRIPENNIS(HYMENOPTERA: PTEROMALIDAE) ON HOSTS PARASITIZED BY OTHER HYMENOPTEROUS SPECIES

AbstractFemales ofNasonia vitripennis(Walk.) (Hymenoptera: Pteromalidae) discriminate between unparasitized housefly pupae (Musca domesticaL.) and those parasitized by eitherMuscidifurax raptorG. &amp; S. orSpalangia cameroniPerk. (Hymenoptera: Pteromalidae) and lay fewer eggs on parasitized hosts. Oviposirion restraint is more pronounced towards hosts attacked byM.raptorthan towards those attacked byS.cameroni, but less than that exhibited towards pupae previously parasitized byN.vitripennis. Damage to the fly pupae, from piercing by the female’s ovipositor and probably also from a "venom" injected by the female, is responsible for inter- as well as ultra-specific discrimination and restraint.

Discrimination Between Parasitized and Unparasitized House Fly Pupae by Females of Nasonia vitripennis (Walk.) (Hymenoptera: Pteromalidae)

AbstractFemales of Nasonia vitripennis (Walk.) (Hymenoptera: Pteromalidae) laid fewer eggs on parasitized than on unparasitized pupae of the house fly, Musca domestica L. Chemical and/or physical conditions of parasitized pupae are detected by the female’s ovipositor, causing this restraint. These conditions may in part result from the host’s death, caused by earlier parasitization, but other factors are also involved. These may include venom injected by the female parasite before she lays, and internal injury to the host resulting from insertion of the parasite’s ovipositor. The female parasite does not discriminate because of physical or chemical traces on the surface of parasitized puparia, of eggs or a surface wound on the pupa, or of absence of heart beat in the pupa.