Superparasitism in mass reared Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae)

Superparasitism frequency and its effects on the quality of mass-reared Diachasmimorpha longicaudata (Ashmead) parasitoids were investigated under laboratory conditions. Percentage of adult emergence, sex ratio, survival, fecundity and flight ability of adult parasitoids that emerged from Anastrepha ludens (Loew) pupae with different levels of superparasitism were determined. A high prevalence of superparasitism was observed. The number of scars per pupa, produced by insertion of the parasitoid ovipositor, ranged from 1 to 30, with an average (±SD) of 8.3 ± 6.2. Adult parasitoid emergence decreased as the level of superparasitism increased. However, the fraction of females rose with increasing superparasitism and the flight ability was lower in adults emerging from pupae with only one scar, compared with adults emerging from superparasitized hosts. Female longevity and fecundity were not affected by superparasitism. Our results support the hypothesis that superparasitism in D. longicaudata might be adaptive, since adults emerging from hosts with moderate levels of superparasitism showed the highest percentage of emergence and there were no significant differences in the other quality control parameters tested. Our findings are relevant to the mass rearing process, where the ratio of hosts to parasitoids can be optimized as well as the distribution of eggs deposited in host larvae. This contributes to efficient mass rearing methods for augmentative biological control programs.     

Effect of temperature on immature development and longevity of two introduced opiine parasitoids on Bactrocera invadens

Temperature‐dependent development, parasitism and longevity of the braconid parasitoids, Fopius arisanus Sonan and Diachasmimorpha longicaudata Ashmed on Bactorcera invadens Drew Tsuruta & White, was evaluated across five constant temperatures (15, 20, 25, 30 and 35°C). Developmental rate decreased linearly with increasing temperature for both the parasitoid species. Linear and Brière‐2 nonlinear models were used to determine the lower temperature threshold at which the developmental rate (1/D) approached zero. For F. arisanus, lower thresholds to complete development estimated with the linear and nonlinear models were 10.1 and 6.9°C, respectively. The total degree‐days (DD) required to complete the development estimated by the linear model for F. arisanus was 360. In D. longicaudata, the linear and nonlinear models estimated lower thresholds of 10.4 and 7.3°C, respectively, and the total DD estimated was 282. In F. arisanus, percentage parasitism differed significantly across all temperatures tested and was highest at 25°C (71.1 ± 2.5) and lowest at 15°C (46.4 ± 1.4). Parasitoid progeny sex ratio was female biased at all temperatures except at 20°C. In D. longicaudata, percentage parasitism was highest at 20°C (52.2 ± 4.0) and lowest at 15°C (27.7 ± 2.5). Parasitoid progeny sex ratio was female biased and similar for all temperatures. Adult longevity of both parasitoids was shortest at 35°C and longest at 15°C, and females lived significantly longer than males at all temperatures tested. Our findings provide some guidance for future mass rearing and field releases of the two parasitoids for the management of B. invadens in Africa.     

Female pupae of the genetic sexing strain “Tap-7” of Anastrepha ludens as hosts of Coptera haywardi

Female black pupae from the Anastrepha ludens genetic sexing strain Tapachula-7 were evaluated as hosts for Coptera haywardi. We studied the host acceptance and the effects of age, irradiation and automated mechanical separation of black pupae on the emergence, survival, fecundity and flight ability of parasitoid C. haywardi adults. Our results indicated that black pupae are viable hosts for C. haywardi. Adult emergence was greater when the exposed pupae were three and five days old. The impact that occurred during mechanical separation reduced emergence by 16 %. The tested irradiation doses (25, 35 and 45 Gy) did not significantly affect adult emergence. No significant differences in longevity, fecundity or flight ability were observed between parasitoids that emerged from the Tapachula-7 black pupae and those that emerged from the standard mass-reared strain.     

Mortality fecundity and longevity of parasitoids of the spotted tentiform leafminer,Phyllonorycter blancardella [Lep.: Gracillariidae] at constant temperatures in the laboratory

The results of laboratory tests showed that mortality of adult eulophids, primarily,Sympiesis sericeicornis (Nees),S. marylandensis Girault andPnigalio flavipes (Ashmead), was significantly (P<0.05) lower than that of adultPholetesor ornigis (Weed) when exposed to temperatures between 20° and 36°C for 48 h. However, adultP. ornigis lived longer than those of the eulophids at 15°C, but were shorter liver at 33°C. The fecundity ofP. ornigis was little affected at temperatures of 15°, 20°, 24° and 33°C. Exposure of adultP. ornigis to 30°C for 16 h resulted in reduced longevity of both sexes but did not affect fecundity or the proportion of females ovipositing. Mortality of pupae of the eulophids was significantly lower than that of pupae ofP. ornigis at temperatures of 20°, 30° and 33°C. The sex ratio of surviving adults was not affected by temperature.      

Effect of cold storage of pupae parasitoid wasp,Habrobracon hebetor (Say) (Hymenoptera: Braconidae), on its efficiency

Cold storage is an appropriate way to extend the life of natural enemies such as insect parasitoids. Identification of risk factors for use in biological control and replacing it instead of chemical control is important, and therefore wasp species of genus Bracon have been used for controlling various pests in the past and present. The aim of this study was to determine the optimum temperature and time of storage of parasitoids pupae, Habrobracon hebetor (Say) in cold conditions. After in vitro rearing of the insect, the pupae of H. hebetor at the temperatures of 12, 9 and 4?°C for a period of six weeks in five replicates were stored. After these times, the effect of storage on the percentage of emerged adults and the longevity of male and female adults was evaluated on a weekly basis. The results of the survey conducted at 12?°C showed that the percentage of adults emerged from the first week has dropped by almost half. H. hebetor pupae could be stored for a week at 9?°C. At 4?°C, a significant reduction was caused in the efficacy of the stored pupae and is not recommended.     

Effects of high temperature shocks on the development and biology ofTrichogramma brassicae [Hym.: Trichogrammatidae]

Trichogramma brassicae Bezdenko is used throughout Europe as an effective biological control agent against the European corn borer (Ostrinia nubilalis Hübner). However, in certain climatic regions, the biological control exerted by this parasitoid is less effective. High temperatures inside the released capsules are suspected to have a negative influence on the parasitoids. To simulate these adverse conditions, we applied heat shocks (35°C and 44°C) for 6 hours to pupae ofTrichogramma brassicae at two periods: white pupae and melanized pupae. The results showed the susceptibility of both the white pupae and melanized pupae, especially at 44°C. At this temperature, the adults (G₀ generation) derived from pupae treated at any age showed reduced longevity and fecundity. Moreover, those descended from treated melanized pupae showed an emergence rate lower than that of the control. These effects reduced to half and more the parasitic efficiency of the G₀ generation. For the progeny (G₁ generation), we observed a decrease of the female ratio: 38% for the progeny of adults derived from treated melanized pupae; 88% for the progeny of those derived from treated white pupae. In that condition, the G₁ generation, almost totally male, could not have any parasitic activity.     

Effect of low temperature on emergence, fecundity, longevity and host-feeding by Trichogramma brassicae

The occurrence of sub-optimal temperatures during development of immature parasitoids can have important consequences on adult fitness. We investigated the impact of different regimes of low temperature on emergence, differential mortality, longevity and fecundity in Trichogramma brassicae Bezdenko (Hymenoptera: Trichogrammatidae). The host-feeding behaviour of adult females was also measured as an indicator of energy reserve at emergence. Acclimation of 30 days at 10 °C or 24 days at 13 °C allowed T. brassicae immatures to develop with a lower mortality than those exposed directly at 5 °C. Longevity and fecundity of females decreased at a lower rate with acclimation at 10 °C suggesting that acclimation at 13 °C may have depleted the energy reserves of individuals more than acclimation at 10 °C. Short photoperiod exposure during the maternal generation had no effect on progeny’s fitness. We found no difference among the treatments in females’ host-feeding behaviours, in differential mortality at emergence, in female’s mobility and in F1 sex ratio.     

Diachasmimorpha longicaudata and D. kraussii (Hymenoptera: Braconidae), potential parasitoids of the olive fruit fly

The olive fruit fly, Bactrocera oleae (Tephritidae), is a significant threat to California's olive industry. As part of a classical biological control program started in 2002, the parasitoids Diachasmimorpha kraussii and D. longicaudata (Hymenoptera: Braconidae) were imported to California from laboratory colonies in Hawaii. Studies on their biology and behavior as parasitoids of the olive fruit fly were conducted in quarantine. Both species tend to oviposit into 2nd and young 3rd instars, with the offspring completing development in the flies’ puparia. Most eggs are deposited in the first two weeks of adult life. Observed lifetime fecundity was low, possibly as a consequence of the relatively poor quality of the harvested olives used as a host substrate. Both pre-imaginal development and adult longevity were limited at constant temperatures above 30°C, which may indicate that these species will have difficulty establishing in the warmest regions of California.     

Side-effects of organic and synthetic pesticides on cold-stored diapausing prepupae of <Emphasis Type="Italic">Trichogramma cordubensis</Emphasis>

The side-effects of three insecticides (deltamethrin, lambda-cyhalothrin and Bacillus thuringiensis Berliner) and one fungicide (basic copper sulphate) were tested on cold-stored diapausing prepupae of Trichogramma cordubensis Vargas and Cabello (Hymenoptera: Trichogrammatidae). Pesticides were directly sprayed on parasitized host eggs (being the diapausing parasitoids in the prepupal stage) after cold storage (3°C) for three different periods (60, 120 and 180 days). Regardless of the period of cold storage, both pyrethroids reduced the emergence rates of T. cordubensis (both <25%) compared to the control (emergence varied from 83% to 89%). The most toxic pyrethroid was lambda-cyhalothrin; Trichogramma cordubensis adult emergence varied from 7% to 15%. Lambda-cyhalothrin also negatively affected the longevity and fecundity of parasitoids cold stored for 60 days. Bacillus thuringiensis Berliner subsp. kurstaki and basic copper sulphate had little or no adverse effect on emergence rates (generally >80%), longevity nor fecundity of T. cordubensis, indicating that these pesticides could be successfully integrated into pest management programs using wasps that were cold stored under diapause. Such integration would be valuable to pest management programs by reducing the costs of T. cordubensis mass rearing and by allowing producers to stockpile parasitoids for release in the growing season. However, since the emergence rate, longevity and fecundity of T. cordubensis generally decreased with increasing duration in cold storage, wasps to be used in integrated pest management programs should only be stored at 3°C for 60 days maximum. Handling Editor: Sam Cook.     

Age-specific fecundity and life table of Trissolcus semistriatus, an egg parasitoid of the sunn pest Eurygaster integriceps

The effects of temperature on age‐specific fecundity and life table parameters of the egg parasitoid Trissolcus semistriatus (Nees, 1834) (Hymenoptera: Scelionidae) were examined under four constant temperature conditions (17, 20, 26 and 32°C), using eggs of the sunn pest Eurygaster integriceps Puton, 1881 (Hemiptera: Scutelleridae), an important pest of wheat, as hosts. The intrinsic rate of increase increased linearly, while the mean generation time and the doubling time decreased with increases in temperature. The net reproductive rate, however, varied without clear correlation with temperature. Fecundity tended to be higher at higher temperatures. The total number of eggs per female was estimated as 52.0 and 116.4 eggs, respectively, at 17°C and 32°C, with the highest fecundity rate during the first day of oviposition. The oviposition rate fluctuated from 4.4 to 14.3 eggs per day. Oviposition and postoviposition periods and longevity decreased when temperature increased. Maximum longevity for females was 21.6 days at 20°C, and female parasitoids lived longer than males at all temperatures. The development period ranged from 7.1 days (32°C) to 35.6 days (17°C) for males and from 8.4 days (32°C) to 37.2 days (17°C) for females. The development of female T. semistriatus required 166.7 degree‐days (DD) above a theoretical threshold of 11.8°C and the development of males required 142.9 DD above 13.1°C. The numbers of generations per year for female and male T. semistriatus, given the temperature in Tekirdag, Turkey, were estimated to be 9.0 and 8.8, respectively. The potential of the egg parasitoid for the control of E. integriceps is discussed.     

Rapid cold-hardening response in Ophraella communa LeSage (Coleoptera: Chrysomelidae), a biological control agent of Ambrosia artemisiifolia L.

In China, an unintentionally introduced beetle Ophraella communa shows good control efficiency against invasive common ragweed, Ambrosia artemisiifolia. With the aim of understanding the capacity of O. communa to overcome sub-zero low temperature rapidly, the longevity, survival and fecundity of the beetle adults were studied at conditions of different rapid cold-hardening in the laboratory. The results showed that approximately 20% female or male individuals still survive at ?12°C for 2 h, thus the discriminating temperature for rapid cold-hardening of both female and male beetles is ?12°C. The survival, longevity and fecundity of adult beetles were significantly affected by rapid cold-hardening treatments. Compared to the control, the survival rates of adult beetles experiencing 2 h of rapid cold-hardening at 2, 5 and 8°C prior to exposure to its discriminating temperature (?12°C) were significantly increased. Adult longevity and fecundity were significantly higher after pre-treatment at 2, 5 and 8°C for 2 h than those of the control. Both longest longevity and maximum fecundity of adult beetles were observed at the rapid cold-hardening of 2°C. Our experiment implies that the cold-tolerance ability of O. communa can be rapidly increased after rapid cold-hardening treatments, which reveals an important ecological significance for population establishment and expansion of O. communa in the invaded areas of common ragweed.     

Effect of temperature on reproduction and parasitism of the egg parasitoid,Anastatus orientalis (Hymenoptera: Eupelmidae)

Anastatus orientalis is a solitary endoparasitoid of Lycorma delicatula (Hemiptera: Fulgoridae) eggs. We investigated the development, longevity, fecundity, and sex ratio of A. orientalis on different temperatures to establish the optimal temperature condition for laboratory mass rearing. There were significant differences in its development and longevity between 15 °C and the rest of temperature conditions (20, 25, and 30 °C), among which were no significant differences. The average number of eggs laid by A. orientalis was higher at 20 and 25 °C, but there was no statistically significant difference in its fecundity between the two temperatures. More females emerged at 15 and 20 °C than higher temperatures.Parasitisms of A. orientalis varied with host egg ages and densities. Even in 14 day old eggs of L. delicatula, parasitoids successfully emerged from 92.3% of the parasitized eggs. On the other hand, parasitism was lowest (13.8%) on just before hatching eggs. Parasitism was negatively dependent on host density.Oviposition behavior for A. orientalis primarily occurred at 1400–1600 h, not at 2400–0800 h. The majority of this parasitoid's emergence occurred at 0800–1000 h, largely before noon. These results may be useful for controlling the adequate time for supplying host eggs and release density of this parasitoid as well as for potentially predicting the accurate time for securing parasitoid adults in laboratory mass rearing of A. orientalis.     

Effects of high temperatures recorded during diapause completion ofTrichogramma brassicae prepupae (Hym.: Trichogrammatidae), on the treated generation and its progeny

Trichogramma brassicae Bezdenko (Hym., Trichogrammatidae) is a parasitoid used for controlling the European corn borer,Ostrinia nubilalis Hübner (Lep., Pyralidae). In parts of south-eastern France, the parasitoids may be placed under a shelter when they are in the prepupal stage for diapause termination, before they are released among the crops. High temperatures (31°C–32°C) can occur during this period. Prepupae were exposed to one or two high temperature shocks at 32°C in the laboratory, and the effects of these shocks were then recorded on a number of biological parameters of the parasitoids belonging to the experimental generation Go and to the progeny generation G1. The emergence rate of Go individuals was highly affected, even when the prepupae had been exposed to a single shock. This decreased the number of parasitoids, in addition to reducing the fecundity of the females. The temperature shocks also affected the emergence rate of generation G₁. No changes were observed regarding the other parameters (minimum duration of final pupal development, longevity, proportion of females). A temperature shock, even a short-lasting low amplitude one, may thus have strong implications on the efficiency of the parasitoids.     

Effect of cold storage of adult Trichogramma brassicae,T. cacoeciae and T. evanescens (Hym.: Trichogrammatidae)

Abstract

Trichogramma cacoeciae Marchall, T. brassicae Bezdenko and T. evanescens Westwood could be useful in biological control programmes of agricultural insect pest. The possibility of storing adult Trighogramma species at low temperatures, and the effect of such storage on the quality of the parasitoids and its fecundity were studied. Trighogramma cacoeciae, T. brassicae and T. evanescens adults were stored for 1, 2, 3, 4 and 5 days at 4 ± 1°C in a refrigerator, 60 – 70%RH and full darkness. Storage at 4 ± 1°C reduced fecundity and longevity of female parasitoids.     

Thermotolerance and rapid cold hardening ameliorate the negative effects of brief exposures to high or low temperatures on fecundity in the flesh fly, Sarcophaga crassipalpis

Although the immediate effects of temperature stress are well documented, the longer‐term effects of such stresses are more poorly known. In these experiments, we investigate the effects of suboptimal and supraoptimal temperatures during pharate adult development on fecundity in the flesh fly, Sarcophaga crassipalpis Macquart. A 1 h cold shock at ?10°C during the red‐eye pharate adult stage decreases the fecundity of both sexes. Induction of rapid cold hardening by pre‐treatment at 0°C for 2 h partially prevents reproductive impairment. Heat shock of pharate adults for 1 h at 45°C also reduces fecundity in both sexes, but inducing thermotolerance by pre‐treatment at 40°C for 2 h affords protection only to females. Males heat shocked at 45°C or first pre‐treated at 40°C consistently fail to transfer sperm to the females. The injury inflicted on males by heat shock is most pronounced when the stress is administered to pharate adults or adults; wandering larvae and true pupae are unaffected. The implications of these data for naturally occurring populations are discussed.     

Parasitism and oviposition of Melittobia acasta on Bombus terrestris: Impact of larval overwintering and host status on pupation and adult emergence

Melittobia acasta (Walker) are microhymenopteran ectoparasitoids of the pupae and prepupae of the commercially‐used pollinator bumblebee species Bombus terrestris L. The female parasitoids puncture the host cuticle with their sting and feed oozing hemolymph. This study shows that M. acasta parasitize 100% pupae and 84% prepupae of B. terrestris but are ineffective on the larvae of the bees. The female parasitoids lay a significantly higher number of eggs on pupae (67.7 ± 16.2 female^?1) compared to prepupae (20.5 ± 14.5 female^?1). The parasitoids differ in their choice for oviposition sites and fecundity on different locations of B. terrestris pupae, and they show most preference for oviposition (32%) as well as fecundity (34.9 ± 15.1 female^?1) on the petiole of the host. Larvae of the parasitoids overwinter at low temperatures but larval overwintering duration and post‐diapause rearing on original or new hosts do not affect their pupation and adult emergence. Larvae have a higher percentage of pupation (88.0–94.4%) and adult emergence (84.4–92.9%) both on the original and the new host, thus indicate that the parasitoids are highly capable of reproduction in B. terrestris colonies.     

Recurrent warming to improve cold storage of Trichogrammatids (Hymenoptera: Trichogrammatidae)

Cold storage can be used to slow development, facilitate accumulation of the organisms and accommodate fluctuating demand for augmentative biological control agents. Previous research suggested the possibility of improving cold storage of Trichogrammatids by recurrent warming, so we subjected Trichogramma ostriniae juveniles within Ephestia kuehniella host eggs to either 2°C constant or to 2°C with twice-weekly recurrent warming for 3 h to 20°C. Parasitoid subsamples were allowed to mature for 1–9 days before placement in cold storage for up to 8 weeks. Parasitism by parentals, progeny emergence and fecundity and longevity of progeny were measured weekly for 8 weeks. Relative to constant 2°C, recurrent warming generally improved emergence, fecundity and longevity, and all the response variables were affected by the interaction of temperature regimen, parasitoid maturity class, and cold storage duration. This implies the utility of recurrent warming to improve egg parasitoid performance and for extending the duration of cold storage.     

Effects of cold storage on life-history traits of Aphidius matricariae

Aphidius matricariae Haliday (Hymenoptera: Braconidae) is a polyphagous solitary endoparasitoid, attacking more than 40 species of aphids. This parasitoid is an important commercial product of many companies that produce biological control agents. Storage at low temperature increases the shelf life of many biocontrol agents, allowing companies to provide a steady and sufficient supply of insects for biocontrol programs. In the current study, the effects of cold storage of 1-day-old host mummies with A. matricariae for various time periods (5, 10, 15, 20, and 30 days) at 5 °C on the parasitoid’s key life-history traits were investigated. Parameters assessed after storage included adult emergence rate, offspring sex ratio, adult longevity, oviposition period, fecundity, and life-table parameters (R₀, r, λ, T, and DT). Our results showed that the mummies of A. matricariae could be stored at 5 °C for 5 days without loss of quality and for 10–15 days with minimal reduction in quality (e.g., some reduction in adult longevity and R₀). If parasitoids were stored for >15 days, quality was more strongly affected. In conclusion, A. matricariae pupae could be stored at 5 °C for up to 15 days without significant negative post-storage effects on fitness of the parasitoid. These results could be used to improve the planning of mass rearing and mass release of A. matricariae in augmentative biological control programs.     

Influence of larval rearing temperature on the quality of cold‐stored Oomyzus sokolowskii Kurdjumov (Hymenoptera: Eulophidae)

Oomyzus sokolowskii, an important parasitoid of Plutella xylostella, has great potential for use in biological control. Storage at suboptimal temperature is valuable for increasing the shelf‐life of insect parasitoids. In this study, O. sokolowskii larvae were reared at 30/25, 25/25 and 25/20°C light/dark (65 ± 5% RH, 16 : 8 h L : D) until pupation. The pupae were then cold‐stored at 4 ± 1°C (60 ± 5% RH, full darkness). The pupae were removed out from the storage at 10, 20, 30 and 40 days after storage (DAS) and maintained at 25 ± 2°C until adults emerged or pupae died. Quality of the emerging adults and their F₁ offspring were assessed. Incidence of parasitism by O. sokolowskii was higher at 30/25°C than at 25/20°C. Cold storage of O. sokolowskii pupae greatly affected the fitness of the parasitoid: adult emergence rates were lower in the 40 DAS treatment than in other treatments; when O. sokolowskii larvae developed at 25/25°C, female proportions of the emerged adults were lower in the 40 DAS treatment than in the 0 and 10 DAS treatments. Larval rearing temperature mildly affected the adult emergence rate, post‐storage developmental time and female proportion with a few exceptions. Number of parasitoids emerged per host pupa, and incidence of parasitism by the females were neither affected by larval rearing temperature nor cold storage duration. Trans‐generational effects on F₁ offspring were evident in adult emergence rate, egg‐adult developmental time and female proportion which were negatively affected by long duration of storage (40 days), but not by larval rearing temperature with a few exceptions. In conclusion, O. sokolowskii pupae could be stored at 4°C for up to 30 days without significant fitness loss.     

Effects of temperature on the fecundity and longevity of Zeugodacus cucurbitae (Coquillet) (Diptera: Tephritidae) on artificial diet

The melon fruit fly, Zeugodacus cucurbitae (Coquillett), is an important polyphagous pest that damages to various agricultural crops, whose distribution has become global as a result of human activity. In this study, we investigated the fecundity, pre-oviposition and oviposition periods, and the longevity of adult Z. cucurbitae at various constant temperatures ranging from 15 to 35.2°C. One newly emerged one virgin female and two males of Z. cucurbitae were used, and the longevity of both sexes and the fecundity of the females were examined daily. The longevity of female Z. cucurbitae ranged from 183.8 days at 15.0°C to 30.8 days at 35.2°C, and the maximum fecundity per female was 1204 eggs at 24.5°C. The lower development threshold (LDT) and thermal constant (K) of females were estimated as 14.8°C and 781.13 degree-days, respectively. Female reproduction was modeled using a two-phase oviposition model. Oviposition was estimated using females in the oviposition phase, which had a complete pre-oviposition phase. The oviposition model consisted of two reproductive components (total fecundity and age-specific cumulative oviposition rate during oviposition) and a survival component (age-specific survival rate). The daily egg production of Z. cucurbitae was estimated in relation to adult age and temperature.