Fitness-related changes in laboratory populations of the egg parasitoid <Emphasis Type="Italic">Trichogramma galloi</Emphasis> and the implications of rearing on factitious hosts

In this study, we used the specialist egg parasitoid Trichogramma galloi Zucchi, 1988 (Hymenoptera: Trichogrammatidae) to test whether development over multiple generations on a factitious host would later influence performance on the target pest. We also investigated possible adaptations to laboratory rearing conditions by monitoring over 50 and 46 generations life history traits of T. galloi populations maintained on the natural [Diatraea saccharalis (Fabr., 1794) (Lepidoptera: Crambidae)] and factitious host [Ephestia kuehniella (Zeller, 1879) (Lepidoptera: Pyralidae)], respectively. We detected a possible sign of adaptation to rearing conditions in early generations on the emergence of the population maintained on the natural host. We also verified a reduction in fecundity and emergence of parasitoids maintained on the factitious host when fitness was evaluated on the natural host, confirming the prediction that the use of factitious hosts can lower fitness on the target pest. The importance of these results for the effectiveness of biological control programs is discussed.     

Host suitability of the Mediterranean flour moth for rearing <Emphasis Type="Italic">Meteorus pulchricornis</Emphasis> (Hymenoptera: Braconidae), a polyphagous endoparasitoid of pest lepidopteran larvae

We investigated the host suitability of the Mediterranean flour moth Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) for a polyphagous koinobiont endoparasitoid Meteorus pulchricornis (Wesmael) (Hymenoptera: Braconidae), a common natural enemy of various pest lepidopteran larvae. The estimated probability of adult wasp emergence was 80% or higher when eggs were laid in nearly fully grown larvae of E. kuehniella (fresh weight, >?20.0 mg). The body size of emerged adult wasps increased with the initial weight of the host larvae at oviposition. The fresh weight of adult wasps reared on E. kuehniella was approximately 60% of that when reared on a natural host Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae), and the lifetime fecundity of wasps reared on E. kuehniella was approximately half of that when reared on S. litura. Ephestia kuehniella was shown to be a positive host candidate for the mass rearing of M. pulchricornis, but further investigation is needed to increase the body size of wasps for more practical use of this species as a biocontrol agent.     

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.     

Putative Host Volatiles Used by <Emphasis Type="Italic">Habrobracon hebetor</Emphasis> (Hymenoptera: Braconidae) to Locate Larvae of <Emphasis Type="Italic">Plodia interpunctella</Emphasis> (Lepidoptera: Pyralidae)

Indianmeal moth, Plodia interpunctella (Hubner) (Lepidoptera: Pyralidae), is a post-harvest pest of grains, milled and processed food, processing plants, warehouses and bakeries. The parasitoid, Habrobracon hebetor (Say) is among the most important natural enemies of Pyralidae infesting stored grains and grain products. Many parasitoids use semiochemicals originating from their hosts, or host’s habitat as cues to locate hosts, hosts’ food or habitat. The authors used Y-tube and four-way olfactometers to assay responses to stimuli with the moth host and thereby understand the role of host-associated semiochemicals in host location by H. hebetor. Responses of mated parasitoid females were assayed to the following stimuli: P. interpunctella sex pheromone, female adults, larvae, or hexane extracts of residue of the rearing medium. Generally, host-related odor sources generated stimuli that elicited better responses than those to blank controls. Previous exposure to odor sources from the host shortened latency periods and response times compared to naïve females. Odors emanating from live moth larvae elicited the strongest responses. When responses from the four odor sources were compared in a four-way olfactometer, it was confirmed that volatiles from larval moths elicited the strongest attraction to the parasitoid. The involvement of host-specific chemical cues in both long and short range host location by female parasitoid is discussed.     

Sugar as nutritional supplement for the zoophytophagous predator Nesidiocoris tenuis

Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) is a zoophytophagous predator widely used in integrated pest management programs in both greenhouse and open-field tomato crops. Mass rearing of N. tenuis is greatly dependent on Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs as food source. Moreover, the addition of this factitious prey after the inoculative releases of N. tenuis under field conditions is recommended to facilitate establishment of this mirid. However, E. kuehniella eggs are expensive and availability is limited. One possible strategy to reduce the amount of E. kuehniella eggs needed is the provision of sugar. In this work, the effect of sucrose as nutritional supplement on selected life-history traits of N. tenuis was studied. The addition of sucrose (0.5 M) ad libitum to a diet of E. kuehniella eggs significantly increased the progeny of N. tenuis and did not affect survival of nymphs nor developmental time. Moreover, addition of sucrose significantly reduced the number of E. kuehniella eggs consumed. These results may have practical implications of interest in mass rearing systems of N. tenuis and its management in fields and greenhouses as a part of biological control programs.     

Effects of pupal treatment with Proteus® and Metarhizium anisopliae sensu lato on functional response of Habrobracon hebetor parasitising Helicoverpa armigera in an enclosed experiment system

The ectoparasitoid wasp, Habrobracon hebetor Say (Hymenoptera: Braconidae) is a valuable biocontrol agent attacking larval stages of many lepidopteran pests including Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). The possibility of combined application of this parasitoid wasp with other biological control agents and chemical insecticides is necessary for the success of an Integrated Pest Management (IPM) programme. One of the most important behaviours of a parasitoid refers to the number of hosts attacked by per parasitoid as a function of host density. In this research, the single and joint effects of the insecticide, Proteus® and the entomopathogenic fungus, Metarhizium anisopliae sensu lato (Metsch.) Sorokin (Hypocreales: Clavicipitaceae) (isolate M14) were studied on the functional response of H. hebetor. Newly mated females (<24?h) from treated pupae of H. hebetor were used to study the functional response of this parasitoid wasp to different densities of H. armigera larvae. A type II functional response was observed in all treatments. The results revealed that control and Proteus® treatments developed the lowest (0.5599?±?0.0373?h) and the highest (0.5709?±?0.0443?h) handling time, respectively. The most and the least values of attack rate were observed in control (0.0996?±?0.0164?h^?1) and Proteus® (0.0776?±?0.0119?h^?1) treatments, respectively. The maximum theoretical parasitism rate (T/T_h) was estimated to be 42.86 for female control wasps. After conducting field experiments on functional response along with life table parameters, M. anisopliae sensu lato (isolate M14) may be used as a compatible biocontrol agent with H. hebetor in IPM programmes of H. armigera.     

Seasonal parasitism and biological characteristics of Habrobracon hebetor (Hymenoptera: Braconidae) – a potential larval ectoparasitoid of Helicoverpa armigera (Lepidoptera: Noctuidae) in a chickpea ecosystem

Seasonal parasitism of Habrobracon hebetor (Say) on Helicoverpa armigera (Hübner) in chickpea was studied for three consecutive years. Parasitism by H. hebetor on larvae of H. armigera reached 12.3%. The parasitoid maintained reproductive activity on H. armigera from February to April coinciding with pod formation and maturation stages of the crop. In laboratory assays, we investigated the suitability of larval instars of H. armigera to the parasitoid H. hebetor. This parasitoid attacked third to sixth instars, though fourth and fifth instar larvae were found most suitable with 100% parasitism and development to adults. Parasitoid developmental time was longest in fifth instar (9.1 days) compared to other instars (8.1–8.9 days). Fifth instar larvae resulted in highest numbers of cocoons and adult emergence. In addition, suitability of seven lepidopteran species to H. hebetor was investigated. Corcyra cephalonica, Galleria mellonella and H. armigera were the most suitable hosts with 100% parasitism and development to adults. It was followed by Maruca vitrata and Autographa nigrisigna with 60–76.7% and 40–70% parasitism and parasitoid developmental success, respectively. Though there was 23.3% parasitism, there was no parasitoid development in Spodoptera litura. No parasitism was recorded in Spilarctia obliqua. Development of H. hebetor was most rapid in C. cephalonica (8.7 days), and longest in G. mellonella (9.3 days). Parasitoids that developed on these hosts resulted in highest numbers of cocoons and adult emergence. The parasitoid could be exploited for the biological control of H. armigera in a chickpea ecosystem.     

Development and reproduction of Geocoris varius (Hemiptera: Geocoridae) on two types of artificial diet

Biological control using the polyphagous predator big-eyed bug Geocoris varius (Uhler) (Hemiptera: Geocoridae) is currently being investigated in Japan. However, the production costs of G. varius are relatively high because the eggs of Ephestia kuehniella Zeller (Lepidoptera; Pyralidae) are used as the major food source for mass rearing. Development time and reproductive fitness were therefore examined for G. varius fed two types of artificial diet based on liver and ground pork. The diets were administered either by wrapping in Parafilm^® or by presenting the food in lyophilized form. The results were compared with those obtained by rearing G. varius on E. kuehniella eggs. Although development time of Geocoris varius fed the artificial diets was significantly delayed compared with G. varius fed on E. kuehniella eggs, delays are slight and not serious for mass rearing projects. The findings suggested that both artificial diets could be used to reduce the costs associated with mass rearing of G. varius.     

A laboratory comparison of four Trichogramma species (Hymenoptera: Trichogrammatidae) as potential biocontrol agents for the carob moth,Ectomyelois ceratoniae (Lepidoptera: Pyralidae)

Four Trichogramma species were recovered in the field from eggs of carob moth, Ectomyelois ceratoniae (Lepidoptera: Pyralidae). The oviposition rates of Trichogramma oleae, Trichogramma cacoeciae, Trichogramma evanescens and Trichogramma bourarachae were compared when presented either E. ceratoniae or Ephestia kuehniella (Lepidoptera: Pyralidae). T. oleae and T. bourarachae did not parasitise either species of Lepidoptera.     

Augmentative on-farm delivery methods for the parasitoid Habrobracon hebetor Say (Hymenoptera: Braconidae) to control the millet head miner Heliocheilus albipunctella (de Joannis) (Lepidoptera: Noctuidae) in Burkina Faso and Niger

Augmentative on-farm delivery methods for the parasitoid Habrobracon hebetor (Say) (Hymenoptera: Braconidae) to control the millet head miner (MHM) Heliocheilus albipunctella (de Joannis) (Lepidoptera: Noctuidae) were investigated in Burkina Faso from 2011 to 2012 and in Niger in 2012. Our findings indicate that 7 cm × 10 cm jute bags containing 50 g of millet grains, 30 g of millet flour, 25 Corcyra cephalonica larvae and two mated H. hebetor females are the most effective option for on-farm delivery of the parasitoid. The parasitoid progeny started emerging from the bags eight days after confinement and 57–71 parasitoid adults emerged from each bag. Using the methods we developed, over 90 % parasitism of MHM larvae was achieved in millet farms. The implications of these findings for a large extension of MHM biocontrol program are discussed.     

Continuous rearing on Ephestia kuehniella reshaped quality of the parasitoid wasp Trichogramma brassicae (Hymenoptera: Trichogrammatidae)

Continuous mass rearing of Trichogramma brassicae (Bezdenko) at commercial mass-rearing insectaries may affect both quality and performance of natural enemies. In the present study, we studied the quality and performance of a colony of T. brassicae reared for over 45 generations (G) on Ephestia kuehniella Zeller using two-sex life table parameters and parasitism capacity. Our results revealed that although different generations showed no significant difference in terms of female longevity or total life span until G35, G5 and G10 had the highest values of fecundity, gross reproductive rate (GRR), net reproductive rate (R₀), intrinsic rate of natural increase (r), and finite rate of increase (λ). No significant difference in male adult longevity was found among different generations. The longest and shortest mean generation times (T) were found in G10 (13.65 ± 2.31 d) and G45 (13.25 ± 3.37 d), respectively. The finite rate of parasitism (ω) ranged from 0.355 ± 2.332 host/parasitoid/day in G5 to 0.242 ± 0.017 host/parasitoid/day in G45. However, ω did not show any significant difference until G20. These results indicate that T. brassicae wasps held under continuous laboratory rearing declined in quality after 20 generations, and therefore periodical rejuvenation of the colony by adding feral parasitoids is strongly recommended.     

A semi-artificial rearing system for the specialist predatory ladybird Cryptolaemus montrouzieri

In the present study a semi-artificial rearing system for the Australian ladybird Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae), a specialist predator of mealybugs, was developed. In a first step, a rearing system using eggs of the Mediterranean flour moth Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) as a food and synthetic polyester wadding as an oviposition substrate was compared with a natural rearing system using the citrus mealybug, Planococcus citri (Risso) (Hemiptera: Pseudococcidae), as to its effects on the predator’s developmental and reproductive parameters. In a second series of experiments the performance of C. montrouzieri on bee pollen or on a mixture of E. kuehniella eggs and bee pollen was assessed. E. kuehniella eggs proved to be a suitable food to support larval development of the predator. Ladybird larvae reared on flour moth eggs developed two days faster and weighed approximately 10 % more than their counterparts reared on mealybugs. Despite a prolongation of the preoviposition period with ca. eight days and a decrease in egg hatch by about 10 %, C. montrouzieri females fed moth eggs accepted the synthetic wadding as an oviposition substrate and deposited the same number of eggs their counterparts maintained on mealybugs. A mixture of E. kuehniella eggs with pollen yielded similar developmental and reproductive rates as E. kuehniella eggs alone, but a diet of bee pollen alone was not adequate for the predator. Our findings indicate the potential of a rearing system using E. kuehniella eggs as a factitious food and synthetic wadding as an artificial oviposition substrate for the mass production of C. montrouzieri.     

Ultrastructure of the natural and factitious host eggs of Trichogramma galloi Zucchi and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae)

The surface and structure of the chorion of eggs of Diatraea saccharalis (F.) (Lepidoptera: Crambidae), Anticarsia gemmatalis (Huebner), Heliothis virescens F., Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae), Sitotroga cerealella (Oliver) (Lepidoptera: Gelechiidae), Ephestia kuehniella Zeller and Corcyra cephalonica Stainton (Lepidoptera: Pyralidae), that are hosts of Trichogramma galloi Zucchi and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) were studied on SEM and TEM. Other characteristics of these eggs, such as changes in their color during embryonic development, size and volume were also recorded. Sculpturing and texture of the surface of the chorion greatly varied among the species studied, as well as the number of layers of the chorion and their thickness. Eggs of the factitious hosts were among the smallest and their volume was very close to each other. All these characteristics would provide basic information for a better understanding of the host selection behavior and are useful for the development of a suitable artificial host egg for the in vitro rearing of these egg parasitoids.     

Costs and benefits of host feeding in the parasitoid wasp Trichogramma turkestanica

Females of the parasitoid wasp Trichogramma turkestanica Meyer (Hymenoptera: Trichogrammatidae) generally host feed after ovipositing on the first egg of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) they encounter. We measured the impact of host feeding on the fecundity and longevity of females, in absence of host or food, and on the fitness of their progeny. We also determined if the frequency of host feeding is influenced by the humidity level at which T. turkestanica females developed. Host feeding increased egg production by 70% but decreased female longevity. This impact of host feeding on the longevity of females is probably due to the allocation of carbohydrates to egg production at the expense of somatic maintenance. Humidity did not influence the occurrence or duration of host feeding. The size of individuals developing in eggs on which females host fed was smaller, indicating that their fitness was affected.     

Potential for lab rearing of <Emphasis Type="Italic">Apanteles taragamae</Emphasis>, the larval endoparasitoid of coconut pest <Emphasis Type="Italic">Opisina arenosella</Emphasis>, on the rice moth <Emphasis Type="Italic">Corcyra cephalonica</Emphasis>

A lab rearing technique was standardised for Apanteles taragamae Viereck (Hymenoptera: Braconidae), the early larval parasitoid of the coconut leaf-eating caterpillar, Opisina arenosella Walker on the alternate host Corcyra cephalonica Stainton (Lepidoptera: Pyralidae). The parasitoid took 23.3 ± 3.2 days to complete the egg to adult period. Adult longevity for males and females was 15.3 ± 4.6 and 13.8 ± 4.6 days respectively. Fecundity was 14.8 ± 4.3 eggs per female. The percentage parasitism was 60.6 ± 5.7 on the alternative host C. cephalonica and 64.6 ± 5.5 on the natural host O. arenosella. Eight- to ten-day-old caterpillars were the ideal stage of C. cephalonica for rearing A. taragamae. The results indicated the amenability of rearing A. taragamae on C. cephalonica in the laboratory.     

Is the parasitization capacity of Trichogramma cordubensis influenced by the age of the females?

We investigated the parasitization capacity of Trichogramma cordubensis Vargas & Cabello (Hymenoptera: Trichogrammatidae) females aged 24 h, 48 h, 72 h, 96 h, 120 h, and 144 h, using Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs as hosts. Wasps were held without hosts during the period of ageing, therefore being increasingly time-limited with respect to parasitization as they got older. The total number of parasitized hosts decreased as the age of the parasitoid increased. However, the proportion of lifetime parasitism carried out on the first day increased with wasp age, up to 120-h old females. These results show that the parasitization capacity of ageing T. cordubensis females changes as they become time-limited. The consequences of such changes for biological control programs are discussed.     

Consequences of mixed species infestation on the searching behavior and parasitism success of a larval parasitoid

When two herbivore pest species are potential hosts of a single parasitoid species, two questions arise. Firstly, which host is preferable for mass rearing in terms of later parasitoid performance, and secondly, how do parasitoids perform in mixed herbivore situations after colony establishment? We tested Hyssopus pallidus, a gregarious parasitoid of two major pests of apple, Cydia (Grapholita) molesta and Cydia pomonella, before and after landing on apples infested by one of the two Cydia species. Pre-alighting host preference was tested in a Y-tube olfactometer setup, and parasitism success in a contact bioassay. To gain information on parasitoid performance throughout the growing season, different fruit growth stages were used. Irrespective of the host they had developed on, the parasitoids showed similar olfactory preferences when given a dual choice between infested and healthy fruits, and they did not discriminate between fruits infested by C. molesta and C. pomonella. Responsiveness was generally high, especially late in the season close to harvest. Both hosts are parasitized regardless of the host the parasitoid female had developed on, and no differences in parasitism rates or number of offspring were noted for the two hosts offered. Results were consistent for all apple growth stages tested. In conclusion, mass rearing of this parasitoid can be carried out on either host, without limiting the future efficacy of the bio-control agent. Similarly, established colonies are expected to develop further on both hosts without any bias in host preference.     

Host switching in a generalist parasitoid: contrasting transient and transgenerational costs associated with novel and original host species

Parasitoids face challenges by switching between host species that influence survival and fitness, determine their role in structuring communities, influence species invasions, and affect their importance as biocontrol agents. In the generalist parasitoid, Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae), we investigated the costs in encapsulation, survival, and body size on juveniles when adult parasitoids switched from their original host, Plodia interpunctella (Hübner) (Lepidotera, Pyralidae) to a novel host, Ephestia kuehniella (Zeller) (Lepidoptera, Pyralidae), over multiple generations. Switching had an initial survival cost for juvenile parasitoids in the novel host, but increased survival occurred within two generations. Conversely, mortality in the original host increased. Body size, a proxy for fecundity, also increased with the number of generations in the novel host species, reflecting adaptation or maternal effects due to the larger size of the novel host, and therefore greater resources available to the developing parasitoid. Switching to a novel host appears to have initial costs for a parasitoid, even when the novel host may be better quality, but the costs rapidly diminish. We predict that the net cost of switching to a novel host for parasitoids will be complex and will depend on the initial reduction in fitness from parasitizing a novel host versus local adaptations against parasitoids in the original host.     

Performance of Sclerodermus brevicornis,a parasitoid of invasive longhorn beetles,when reared on rice moth larvae

Biological control efficiency can be improved by developing effective mass‐rearing systems to produce large numbers of high‐quality parasitoids. This study explored an alternative host for rearing Sclerodermus brevicornis (Kieffer) (Hymenoptera: Bethylidae), a potential biocontrol agent for the suppression of exotic and invasive wood‐boring longhorn beetle (Coleoptera: Cerambycidae) populations in the European agroforestry ecosystems. We tested larvae of the rice moth, Corcyra cephalonica Stainton (Lepidoptera: Pyralidae), as host for the parasitoid. We quantified the probability and timing of host attack and parasitism as well as reproductive success, offspring production, and the characteristics of adult offspring. As S. brevicornis is a quasi‐social species (multiple females, communally produced offspring broods), we also explored the effects of varying the number of females to which individual hosts were presented, with the aim of determining the optimal female‐to‐host ratio. As time to host attack can be a limiting factor in S. brevicornis rearing protocols, we tested the use of adult females of another bethylid species, Goniozus legneri Gordh, to paralyse C. cephalonica larvae prior to presentation. We identified the conditions within our experiment that maximized offspring production per host and offspring production per adult female parasitoid. We found that C. cephalonica is suitable as a factitious host and, as it is considerably more straightforward for laboratory rearing than cerambycid species, it is a good candidate for adoption by future S. brevicornis mass‐rearing and release programmes.     

Existence of two strains of <Emphasis Type="Italic">Habrobracon hebetor</Emphasis> (Hymenoptera: Braconidae): a complex in Thailand and Japan

Habrobracon hebetor Say (Hymenoptera: Braconidae) is a cosmopolitan gregarious ectoparasitoid that attacks larvae of several species of Lepidoptera. Although there are two genetically different strains within H. hebetor, distribution of the strains has been poorly understood. In 2010, in Thailand, where H. hebetor has been known as a parasitoid of stored grain pests, it was found that H. hebetor attacked Opisina arenosella Walker (Lepidoptera: Oecophoridae), which is an invasive pest of coconut palm. For correct identification of this H. hebetor, we conducted DNA analysis and cross tests using populations collected from O. arenosella and stored grain pests in Thailand and populations in Japan known as H. hebetor. We obtained 413 bp of mitochondrial cytochrome oxidase I (COI) sequences and 414 bp of 16S rRNA gene sequences, and both indicated that there are two distinct clades within H. hebetor: one contains insects from Thailand, Spain, India, and Barbados; the other contains insects from Japan and the USA. There were no genetic differences or sexual isolation between Thai populations from different hosts. Our results also showed that populations in Thailand were sexually isolated from a H. hebetor population in Japan.