The effects of periodic warming on the survival and fecundity of Diadromus pulchellus during long-term storage

Biological control strategies capitalise on natural mechanisms such as predation and parasitism to reduce the need for chemical applications to control insect pests. In Canada, the parasitic wasp Diadromus pulchellus Wesmael (Hymenoptera: Ichneumonidae) is being investigated for its use in the biological control of an invasive crop pest, the leek moth, Acrolepiopsis assectella (Zeller) (Lepidoptera: Acrolepiidae). Large numbers of insects will be needed for releases to ensure that populations of D. pulchellus establish quickly and impact leek moth populations. Since the current culture is not producing the number of insects required for large-scale releases, the accumulation and storage of D. pulchellus might be a viable option to obtain ideal numbers. Currently, little is known about the optimal conditions for the long-term storage and release of D. pulchellus, which overwinter in nature as adults. Using insects from the active culture, the effect of intermittent, short-term warming on cold-stored adults was evaluated for survivorship and fecundity. In accordance with previous findings, females survived cold storage more readily than males. However, the warming regimes employed had no significant impacts on overall survivorship. Cold-stored females had reduced fecundity compared to females maintained in the culture, though no significant differences were noted between the treatments. In addition, the offspring sex-ratio for all treatments was male skewed. Thus, the warming procedures utilised provided no advantages over current techniques for the long-term storage of D. pulchellus intended for release.     

Biology of Tetrastichus howardi (Olliff) (Hymenoptera: Eulophidae): A facultative Hyperparasitoid of stem borers

The biology of the parasitoid Tetrastichus howardi, which was introduced from the Philippines into South Africa for the biological control of the stem borer Chilo partellus, was studied in the laboratory. On average, a T. howardi female produced 101 progeny (92% females) which developed in 4.3 hosts. The upper threshold temperature for development was around 33°C, the minimum threshold was calculated as 12.8°C and the thermal constant as 239.8 day‐degrees. With hosts, females lived 23.6 and males 16.7 days. T. howardi was found to be a facultative hyperparasitoid with a very wide host range. As a primary parasitoid, it developed in pupae of various Lepidoptera as well as Coleoptera and Hymenoptera and as a hyperparasitoid in dipteran and hymenopteran parasitoids. A linear relation was found between the number of emergent parasitoids and the volume of the host from which they emerged. Preference tests indicated that T. howardi preferred to parasitize the phytophagous insects C. partellus and Heliothis armigera, over their parasitoids Xanthopimpla stemmator and Palexorista laxa. The host selection of inexperienced T. howardi females was different from the experienced parasitoids. When given a choice, females showed preference for the host species they were allowed to parasitize previously and the host species from which they had been reared. The use of facultative hyperparasitoids in biological control in general and against stem borers in South Africa in particular is discussed.     

Effects of floral resources on the efficacy of a primary parasitoid and a facultative hyperparasitoid

Resources added to agroecosystems to enhance biological control are potentially available to multiple members of the resident insect community—not only the biological control agents for which the resources are intended. Many studies have examined the effects of sugar feeding on the efficacy of biological control agents. However, such information is lacking for other, interacting species such as facultative hyperparasitoids, which may contribute to pest suppression but can also interfere with introduced biological control agents. Under greenhouse conditions, we tested the direct effects of sugar and nectar provisioning on the longevity, host‐killing impact and offspring production of two pupal parasitoids associated with leek moth, Acrolepiopsis assectella: the introduced biological control agent, Diadromus pulchellus, and the native facultative hyperparasitoid, Conura albifrons. Adding sucrose, buckwheat or a combination of buckwheat and common vetch to a sugar‐deprived system (potted leek plants in cages) increased parasitoid longevity and resulted in higher leek moth parasitism and mortality compared to water or common vetch treatments. However, the two parasitoid species exhibited a distinct temporal response to the treatments, likely influenced by differences in their life histories. This study provides insight into how integrating conservation biological control techniques could affect the success of a classical biological control programme.     

Polypeptides of Acrolepiopsis assectella cocoon (Lepidoptera: Yponomeutoidea): an external host-acceptance kairomone for the parasitoid Diadromus pulchellus (Hymenoptera: Ichneumonidae)

Contact kairomones are essential for host-acceptance behaviour by female parasitoids. In the solitary endoparasitoid wasp, Diadromus pulchellus, this behaviour depends mainly on compound(s) in the cocoon of their host, Acrolepiopsis assectella pupae. Extracts of empty cocoons and polypeptides extracted from cocoons were tested in acceptance behaviour assays using cotton fibre lures bearing extracts. Extractions with solvents of increasing polarity indicated that the active compounds were polar, while SDS-PAGE showed that four glycopolypeptides contained enough information to trigger host-acceptance behaviour in female wasps. This kairomonal activity was found to be due to the protein moieties, and was independent of any glycosylation. These four glycopolypeptides might be two variants of two soluble sericin-like polypeptides differing in their degree of glycosylation.     

颈双缘姬蜂寄生引起小菜蛾蛹脂肪体形态和超微结构的变化

采用光学和电子显微镜观察了颈双缘姬蜂Diadromus collaris（膜翅目： 姬蜂科）寄生后小菜蛾Plutella xylostella（鳞翅目：菜蛾科）蛹脂肪体形态、超微结构和脂肪细胞的变化。结果表明： 被寄生72 h后小菜蛾蛹脂肪体结构松散,细胞游离,细胞膜破裂;细胞内营养物质开始被动地消耗;细胞器数量减少,细胞核内染色质状态发生变化。这些现象说明寄生对寄主的脂肪体结构及脂肪细胞产生了明显的影响,这有利于为幼蜂的发育提供营养。     

Viability of diploid males in the parasitic wasp,Diadromus pulchellus (Hym.: Ichneumonidae)

In the HymenopteraDiadromus pulchellus diploid males have been observed in samples collected in the wild and bred in the laboratory. Using a yellow body color mutant strain, a protocol of crosses, involving inbred individuals, allows the routine production of such diploid males. These males result from the development of fertilized ova and emerge normally. Their preimaginal viability is similar to those of other individuals, and their imaginal viability does not differ from that of haploid males. Diploid males present normal external morphology and neither mosaicism nor intersexuality was observed. However, they are bigger than haploid males and have head size and wing length similar to those of females. The significance of diploid male viability in hymenopteran populations is discussed.     

The effect of mating behaviour on progeny sex ratio of Mastrus ridens (Hymenoptera: Ichneumonidae), a biological control agent of codling moth

Mastrus ridens (Horstmann) (Hymenoptera: Ichneumonidae) was imported into quarantine as a potential biocontrol agent for codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae). Mating behaviour of the parasitoid and its effect on progeny sex ratio (as a proportion of males) were studied to help sustain the laboratory culture. Both females and males were reproductively active soon after emergence. Unmated females produced only male progeny, confirming males developed from unfertilized eggs. The proportion of males in a progeny was independent of the copulation period (24–40 s) of the parents. The progeny sex ratios from three parent ratios (f:m 2:1, 1:1 and 1:2) were not significantly different. Females effectively mated only once but males mated frequently in their lifetime. The progeny sex ratios from single females with a known single mating and possible multiple matings (through exposure to two males for 18 days) were not significantly different. However, when males copulated with five virgin females in sequence over a 2 h period, the fifth female produced more males than the preceding four, presumably due to sperm depletion. Results of this study provide data on progeny sex allocation of M. ridens that help to prevent the development of a male-biased sex ratio that could threaten the maintenance of the culture over time.     

Aphanogmus sp. (Hymenoptera: Ceraphronidae): a hyperparasitoid of the coffee berry borer parasitoid Prorops nasuta (Hymenoptera: Bethylidae) in Kenya

This is the first report of a hyperparasitoid of Prorops nasuta, a primary parasitoid of the coffee berry borer. Aphanogmus sp. is a gregarious ectoparasitoid of larval and pupal stages of P. nasuta, which was found in coffee berry samples collected on the ground of an organic coffee plantation in Western Kenya. The hyperparasitoid shows a clear pattern of emergence from year to year, following its host. Aphanogmus sp. parasitizes around 10% of P. nasuta immature stages under field conditions.     

Introduction,establishment, and impact of Lathrolestes thomsoni (Hymenoptera: Ichneumonidae) for biological control of the ambermarked birch leafminer,Profenusa thomsoni (Hymenoptera: Tenthredinidae), in Alaska

The ambermarked birch leafminer, Profenusa thomsoni Konow (Hymenoptera: Tenthredinidae), was first discovered in Alaska in 1991 but was not correctly identified until 1996 when it invaded Anchorage and became a widespread and damaging pest to forest and urban birches. In 2003, the parasitoid wasp, Lathrolestes thomsoni Reshchikov (Hymenoptera: Ichneumonidae), was selected as a candidate for a classical biological control program against P. thomsoni. Parasitized leafminer larvae were collected from the Northwest Territories and Alberta, Canada, where it was previously introduced and causing injury to Betula spp., and transferred to Alaska in soil as pre-pupae for emergence. From 2004 to 2008, 3636 adult L. thomsoni adults were released in birch stands in Alaska. Parasitoids were later recovered at all six release sites in Anchorage and the Kenai Peninsula. While percent leaves mined declined by 30–40% at parasitoid release sites over the period of this study, a similar decline was also observed at paired, non-release long-term monitoring sites. Therefore, the decline in the pest density cannot be ascribed entirely to L. thomsoni.     

A large-scale rearing method for Peristenus digoneutis (Hymenoptera: Braconidae), a biological control agent of Lygus lineolaris (Hemiptera: Miridae)

Releases of Peristenus digoneutis against Lygus spp. in North America have been conducted for many years; however, no published procedures for mass production of the biological control agent were available. A laboratory rearing method was developed using Lygus lineolaris as the host to enhance establishment efforts and provide large numbers of wasps for inundative releases into high value fruit crops. Experiments were conducted to determine optimum host:parasitoid density and rearing temperature. The effects of nymph:wasp ratios and temperature on parasitism and wasp survival showed a 20:1 ratio at 20°C provided high parasitism (256 parasitized nymphs/wasp over lifetime) and excellent wasp survival of 27 days. Experiments on diapause-inducing conditions for P. digoneutis demonstrated that fluctuating temperatures of 23°C (day) and <16°C (night) and corresponding photo phases of 16 h light, for rearing parasitized nymphs, produced 100% diapausing parasitoids whereas non-diapausing parasitoids were only produced at more than 16 h light. Furthermore, parasitized Lygus nymphs need to be transferred to short day conditions no later than 10 days after parasitism to produce diapausing parasitoids. Critical life stages for exposure to conditions inducing diapause, the egg, first and second instar parasitoid larva, occurred from 0 to 10 days at 24°C constant temperature. Increased time in cold storage reduced the number of days to first emergence of parasitoids from diapausing cocoons when transferred to warm temperatures. The optimum storage time for diapausing P. digoneutis is between 25 and 44 weeks, depending upon the length of time that cocoons remain at warm conditions prior to chilling.     

Parasitisation of Tetrastichus brontispae (Hymenoptera: Eulophidae), a biological control agent of the coconut hispine beetle Brontispa longissima (Coleoptera: Chrysomelidae)

The gregarious endoparasitoids Tetrastichus brontispae Ferrière is one of the important natural enemies of the coconut hispine beetle Brontispa longissima (Gestro), a serious invasive pest on coconut palm plants (Cocos nucifera L.) in Southeast Asia. Development at different temperatures, effect of host and female ages, effect of food and oviposition frequency and superparasitism were investigated in the laboratory. Females were allowed only one attack against one host in all experiments. The wasp developed in a host between 19 and 30°C, whilst no wasp completed its immature development at 16 and 31°C. Host and female ages affected parasitisation. Parasitoid emergence was high on day 0 and day 1 pupal hosts, and younger females produced more offspring than older females. The longevity of the female was affected not only by food supply, but also by oviposition frequency. The female survived longer when oviposition frequency was low. However, the total number of hosts parasitised by the female during her lifetime did not differ at different oviposition frequencies. In superparasitism, although the percentage of adult emergence and body size of offspring decreased with an increasing number of attacks per host, a host parasitised by up to four females could produce parasitoid offspring.     

Effect of temperature on the reproductive biology of Peristenus spretus (Hymenoptera: Braconidae), a biological control agent of the plant bug Apolygus lucorum (Hemiptera: Miridae)

Peristenus spretus Chen et van Achterberg (Hymenoptera: Braconidae), a parasitoid of the plant bug Apolygus lucorum (Hemiptera: Miridae), has been studied for use in augmentative biological control in China. Under laboratory conditions, we explored the development, survival, age-specific and potential lifetime fecundity, oviposition period and progeny sex ratio of P. spretus reared at six constant temperatures (15°C, 19°C, 23°C, 27°C, 31°C, 35°C) on the second instar nymphs of A. lucorum. At 15°C, male and female P. spretus took 48.7 ± 0.3 and 52.5 ± 0.3 days to complete their immature development, while developmental time was reduced by more than half at 23°C and 27°C. The parasitoid can only develop to the larval stage at 31°C and neither larva nor pupa survived at 35°C. The estimated lower developmental threshold of the immature stage was 7.3°C. When parasitoid adults were exposed at 15°C, females laid 90% of their eggs at first 19 days of oviposition and had an extended reproductive life. In contrast, females held at 27°C laid most of their eggs (90%) in their first of 10 days of oviposition and had shorter longevity. The highest potential lifetime fecundity of P. spretus was 671.2 ± 34.7 SE eggs produced over 23.4 ± 1.4 SE days at 23°C. At 15°C, 19°C and 23°C, sex ratios of reared parasitoids were male-biased, but at 27°C there was no male bias.     

Selecting the right parasitoid for the environment in classical biological control programmes: the case of Diadegma semiclausum (Hymenoptera: Ichneumonidae) and Plutella xylostella (Lepidoptera: Plutellidae) in the Kofele highland of Ethiopia

The careful selection of parasitoids with a track record of success in similar environmental conditions may increase the likelihood of effective biocontrol. Diamondback moth (DBM) population and level of parasitism were assessed for three years prior to the release of Diadegma semiclausum (Hellén) in June 2008. Thereafter, the DBM population and severity of crop damage and the occurrence of D. semiclausum and indigenous DBM parasitoids were monitored by monthly surveys during the main production season of June to December for three years. Before release, DBM numbers fluctuated between 4.2 and 11.2 per plant and parasitism ranged between 6.5 and 24.7%. DBM density declined to 2.8, 0.9 and 0.7 per plant whilst parasitism levels increased successively to 21, 39 and 38% in 2008, 2009 and 2010, respectively. A significant shift in parasitoid guild was observed after D. semiclausum release: it comprised 18.6, 80.3 and 88.6% of total parasitism in the first, second and third year, respectively. The decline of DBM density following the release of the introduced parasitoid and its establishment will ensure production of Brassica spp. without pesticide use against DBM in the affected area.     

Potential non-target impact of Microctonus aethiopoides Loan (Hymenoptera: Braconidae) on Cleopus japonicus Wingelmüller (Coleoptera: Curculionidae), a biocontrol agent for putative release to control the butterfly bush Buddleja davidii Franchet in New Zealand

Abstract  Cleopus japonicus Wingelmüller (Coleoptera: Curculionidae) is being considered for release to control buddleia Buddleja davidii in New Zealand. As part of the pre-release testing, Moroccan and Irish biotypes of the solitary endoparasitoid Microctonus aethiopoides Loan (Hymenoptera: Braconidae) were evaluated for potential non-target impacts on adult C. japonicus should release occur. Laboratory experiments evaluated both the behavioural and physiological suitability of C. japonicus to both biotypes of the parasitoid. Parasitoid behavioural attraction was assessed using the pathenogenic bacterium Serratia marcescens (Enterobactereaceae), as an indicator of ovipositor penetration. Physiological suitability was assessed by comparing parasitism of C. japonicus with the natural hosts of the respective parasitoid biotypes. The parasitoid-bacteria study showed that C. japonicus was behaviourally acceptable to both Moroccan and Irish M. aethiopoides , with the two experiments producing 34% and 8% mortality, respectively. Cleopus japonicus did not support development of either Moroccan or Irish M. aethiopoides biotypes. None of the weevils dissected at the end of the experiment contained immature parasitoids. Comparison between unexposed and parasitoid-exposed C. japonicus found no difference in premature mortality during the experiment nor in the number of fully reproductive females at its conclusion. The results of this study predict that should C. japonicus be released, the potential impact of M. aethiopoides on field populations will be negligible.     

Mass production of Diglyphus isaea (Hymenoptera: Eulophidae), a biological control agent of a Korean population of potato leaf miner Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae)

The potato leaf miner, Liriomyza huidobrensis (Blanchard), is an important pest of potato throughout the world, including Korea. A method was developed for mass rearing the parasitoid Diglyphus isaea (Walker) using faba bean, Vicia faba L. (Fabaceae), as the host‐plant and L. huidobrensis as the insect host. Faba bean plants were planted in pots and maintained in a greenhouse for about 15 d. Pots were then exposed to adult leaf miners in oviposition cages for 4 h. Plants containing late second to early third instar larvae were exposed to adult D. isaea in parasitoid cages for 24 h. The leaf area per pot after 15 d was 597.9 cm², which produced 103.33 larvae per pot. The number of adult parasitoids emerging per pot was 72.5; about 41% of these were female. The daily cost of parasitoid production was USD20.95 per 1000 individual parasitoids. The methodology developed for D. isaea could be used to rear other ectoparasitoids such as Hemiptarsenus spp. and Pnigalio sp. with different insect hosts like L. trifolii. This is why this mass‐rearing information is important for securing test insect materials for ecological and biological study of Liriomyza species, and also for developing a biological control for Liriomyza species other than L. huidobrensis by mass production of associated natural enemies. We are facing rapid agro‐ecosystem changes including pest systems. Continuous monitoring of Liriomyza in solanaceous crops is needed.     

Laboratory evaluation of Orthocentrus brachycerus (Hymenoptera: Ichneumonidae), as a potential biological control agent in mushroom cultivation

Fungus gnats in the genus Neoempheria Osten Sacken (Diptera: Mycetophilidae) are serious pests of the shiitake mushroom, Lentinula edodes (Berk.) Sing. (Agaricales: Omphalotaceae), a prize edible. Recently, we found that the parasitoid wasp Orthocentrus brachycerus Humala & Lee, 2020 (Hymenoptera: Ichneumonidae) attacks larvae of Neoempheria. We have shown in previous research that O. brachycerus suppresses population growth of Neoempheria in simulated cultivation conditions, and thus shows potential for use as a biological control agent. However, the behavioural and ecological aspects of this wasp have not been studied. Here, under controlled laboratory conditions, we investigated the fecundity, longevity and host stage specificity of O. brachycerus against Neoempheria larvae. We found that O. brachycerus are prolific throughout their life cycle. On average, female O. brachycerus made over 140 attempts to parasitize pest larvae, and over 90% of Neoempheria larvae were parasitized or died before emergence. Parasitoid females kept at 20°C survived for an average of 15.4 ± 3.58 days, and some females survived >30 days. Females continued to oviposit eggs throughout their life cycle and parasitized all stages of host larvae, but not eggs. These observations indicate that O. brachycerus may be effective for control of Neoempheria larvae in shiitake cultivation facilities. These results provide a basis for establishing a protocol for using O. brachycerus in mushroom cultivation.     

Diversity and impact of herbivorous insects on Brazilian peppertree in Florida prior to release of exotic biological control agents

Brazilian peppertree, Schinus terebinthifolia Raddi (Anacardiaceae), is a South American plant that is highly invasive in Florida. The impact of insect herbivores on the performance of Brazilian peppertree was evaluated at two locations in Florida using an insecticide exclusion method. Although 38 species of insect herbivores were collected on the invasive tree, there were no differences in growth or reproductive output of insecticide protected and unprotected trees, providing evidence that insect feeding had no measurable impact on tree performance. The majority of insects collected on Brazilian peppertree were generalists, and several were serious agricultural pests.     

Role of Diadegma semiclausum (Hymenoptera: Ichneumonidae) in controlling Plutella xylostella (Lepidoptera: Plutellidae): Cage exclusion experiments and direct observation

We evaluated the role of the larval parasitoid, Diadegma semiclausum Hellén (Hymenoptera: Ichneumonidae), in controlling Plutella xylostella (L.) (Lepidoptera: Plutellidae) by cage exclusion experiments and direct field observation during the winter season in southern Queensland, Australia. The cage exclusion experiment involved uncaged, open cage and closed cage treatments. A higher percentage (54–83%) of P. xylostella larvae on sentinel plants were lost in the uncaged treatment than the closed (4–9%) or open cage treatments (11–29%). Of the larvae that remained in the uncaged treatment, 72–94% were parasitized by D. semiclausum, much higher than that in the open cage treatment (8–37% in first trial, and 38–63% in second trial). Direct observations showed a significant aggregation response of the field D. semiclausum populations to high host density plants in an experimental plot and to high host density plots that were artificially set-up near to the parasitoid source fields. The degree of aggregation varied in response to habitat quality of the parasitoid source field and scales of the manipulated host patches. As a result, density-dependence in the pattern of parasitism may depend on the relative degree of aggregation of the parasitoid population at a particular scale. A high degree of aggregation seems to be necessary to generate density-dependent parasitism by D. semiclausum. Integration of the cage exclusion experiment and direct observation demonstrated the active and dominant role of this parasitoid in controlling P. xylostella in the winter season. A biologically based IPM strategy, which incorporates the use of D. semiclausum with Bt, is suggested for the management of P. xylostella in seasons or regions with a mild temperature.     

Potential of a strain of the entomopathogenic fungus Beauveria bassiana (Hypocreales: Cordycipitaceae) as a biological control agent against western flower thrips,Frankliniella occidentalis (Thysanoptera: Thripidae)

Five Beauveria bassiana strains were evaluated for control of western flower thrips. Strain RSB was the most virulent, causing 69–96% mortality at concentrations of 1×10⁴–1×10⁷ conidia mL^?1, 10 days after inoculation of first instars. In greenhouse trials, RSB applied to broccoli foliage significantly reduced adult and larval populations.     

Adaptiveness of sex ratio control by the pupal parasitoid Itoplectis naranyae (Hymenoptera: Ichneumonidae) in response to host size

Adaptiveness of sex ratio control by the solitary parasitoid wasp Itoplectis naranyae (Hymenoptera: Ichneumonidae) in response to host size was studied, by examining whether differential effects of host size on the fitness of resulting wasps are to be found between males and females. The offspring sex ratio (male ratio) decreased with increasing host size. Larger hosts yielded larger wasps. Male larvae were less efficient in consuming larger hosts than female larvae. No significant interaction in development time was found between parasitoid sex and host size. Larger female wasps lived longer than smaller females, while longevity of male wasps did not increase with increasing wasp size. Smaller males were able to mate either with small or with large females, while larger males failed to mate with small females. Larger female wasps had a greater number of ovarioles and mature eggs at any one time than smaller females, although the number of eggs produced per host-feeding was not influenced by female wasps. Thus, the differential effect of host size on the fitness of males and females exists in I. naranyae. The basic assumption of the host-size model was therefore satisfied, demonstrating that sex ratio control by I. naranyae in response to host size is adaptive.