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.     

The reproductive capability of Ooencyrtus kuvanae reared on eggs of the factitious host Antheraea pernyi

Ooencyrtus kuvanae is a key egg parasitoid of Lymantria dispar (L.), an important defoliating pest in China and North America. We have developed mass rearing techniques for O. kuvanae and in this study compared the reproductive capacity of O. kuvanae when it was previously reared on the natural host, L. dispar or the factitious host, Antheraea pernyi Guerin‐Meneville. There was no significant difference in the oviposition period or total number of eggs laid between L. dispar‐reared and A. pernyi‐reared females. However, the mean number of offspring successfully emerging from those eggs was significantly larger from the A. pernyi‐reared females compared with L. dispar‐reared females. From this, we can conclude that, with respect to reproductive capability, eggs of A. pernyi are suitable factitious hosts for mass rearing of O. kuvanae.     

Genetic variation and the performance of a mass‐reared parasitoid,Trichogramma pretiosum (Hymenoptera: Trichogrammatidae), in laboratory trials

During mass rearing, adaptation of biological control agents to the rearing environment is a potential problem. Using the parasitoid wasp Trichogramma pretiosum, the performance of 26 highly inbred lines, five composite ‘populations’ (created from the inbred lines) and one insectary‐reared population was compared using fertility life tables. Of the composite populations, three were created with maximal and identical genetic variation as a mixture of all 26 inbred lines, but these were then reared for a different number of generations (2, 6 or 17) before their performance was measured. The remaining two composite populations were created based on the performance of the individual inbred lines: one was a combination of two inbred lines with a high intrinsic rate of natural increase (rm), ‘high rm’; and the other was a combination of two lines with a ‘low rm’. High and low rm populations were reared for two generations prior to testing. Parameters measured were fertility, longevity and sex ratio. We found no difference between the maximally variable population reared for two generations and the ‘high rm’ population (rm = 0.285 and 0.282, respectively). ‘Low rm’ was the population with the lower performance (rm = 0.255). Genetically variable population reared for two generations for 48 h produced significantly more offspring than the populations reared for 6 and 17 generations. Hybrid population derived from the high‐rm lines did significantly better than that derived from the low‐rm lines. Low‐performance populations become more male based than high performance at 48 h. The potential benefits to improve population's performance using inbred lines for mass rearing are discussed.     

Does rearing an aphid parasitoid on one host affect its ability to parasitize another species?

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Effect of exposure time on mass‐rearing production of the olive fruit fly parasitoid,Psyttalia lounsburyi (Hymenoptera: Braconidae)

Classical biological control programmes rely on mass production of high‐quality beneficial insects for subsequent releases into the field. Psyttalia lounsburyi (Silvestri) (Hymenoptera: Braconidae) is a koinobiont larval–pupal endoparasitoid of tephritid flies that is being reared to support a classical biological control programme for olive fruit fly in California. The mass‐rearing system for a P. lounsburyi colony, initiated with insects originally collected in Kenya, was evaluated with the goal of increasing production, while at the same time reducing time requirements for rearing in a quarantine facility. We tested the effect of exposure time of a factitious host Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), on parasitization, adult production, superparasitism, and sex ratio of P. lounsburyi and survival of the host. Parasitization rates were highest (31%) at 3‐ and 4‐hr exposure times, while adult production (i.e., emergence of wasp progeny) was highest (16%) at the 2‐hr exposure time. Superparasitism over the course of the study was 1.5% and did not appear to be a factor affecting parasitoid production. The sex ratio of wasp progeny was male‐biased and did not vary significantly over different exposure times. The rate of stings on host larvae increased with exposure time and was consistent with decreases in pupal eclosion from larvae and emergence rate of adult flies. When compared to current rearing procedures, the 2‐hr exposure time resulted in an overall 2.8‐fold increase in P. lounsburyi production when standardized for time.     

Trans‐generational effects of maternal rearing density on offspring development time in a parasitoid wasp

Maternal pre‐reproductive experience can impose phenotypic changes on offspring traits. These modifications may result from physiological constraints, although they can also increase the adaptation of offspring to their anticipated environment. Distinguishing between the two interpretations is often difficult. The effects of virgin female rearing density on their longevity and the characteristics of their male offspring are explored in the polyembryonic parasitoid wasp Copidosoma koehleri (Blanchard) (Encyrtidae: Hymenoptera). High rearing density may adversely affect maternal physiology or, alternatively, act as a cue for anticipated competition during the lives of the mothers and their offspring. Male offspring of group‐reared females reach pupation significantly sooner than male offspring of females reared alone. This accelerated development may provide an advantage when competition from superparasitising individuals is expected. The lifespan of high‐density females is longer than that of singly‐reared females, and their male offspring survive longer, suggesting that crowded rearing does not reduce the fitness of females or offspring. The shortened development time of male offspring may reflect an adaptive epigenetic response to predicted competitive conditions.     

Pre‐release host range determination of the parasitoid Allotropa burrelli for the biocontrol of Pseudococcus comstocki in France

We performed “no‐choice” tests to study the host range of the parasitoid Allotropa burrelli (Muesebeck) (Hymenoptera: Platygastridae) for use against the Comstock mealybug, Pseudococcus comstocki (Kuwana) (Hemiptera: Pseudococcidae), in Southern France. We tested three Pseudococcidae species as potential non‐target hosts: two species from the same genus (Pseudococcus longispinus and Pseudococcus viburni) and Planococcus citri. Allotropa burrelli did not parasitize any of the non‐target mealybug species tested. No attempt of oviposition was recorded for the three species tested during the first 20 min of parasitoid release and no parasitism occurred in 6–8 hr of exposure of the mealybugs to the parasitoid.     

Genetic rescue in a severely inbred wolf population

Natural populations are becoming increasingly fragmented which is expected to affect their viability due to inbreeding depression, reduced genetic diversity and increased sensitivity to demographic and environmental stochasticity. In small and highly inbred populations, the introduction of only a few immigrants may increase vital rates significantly. However, very few studies have quantified the long‐term success of immigrants and inbred individuals in natural populations. Following an episode of natural immigration to the isolated, severely inbred Scandinavian wolf (Canis lupus) population, we demonstrate significantly higher pairing and breeding success for offspring to immigrants compared to offspring from native, inbred pairs. We argue that inbreeding depression is the underlying mechanism for the profound difference in breeding success. Highly inbred wolves may have lower survival during natal dispersal as well as competitive disadvantage to find a partner. Our study is one of the first to quantify and compare the reproductive success of first‐generation offspring from migrants vs. native, inbred individuals in a natural population. Indeed, our data demonstrate the profound impact single immigrants can have in small, inbred populations, and represent one of very few documented cases of genetic rescue in a population of large carnivores.     

Determination of the optimal parasitoid‐to‐host ratio for efficient mass‐rearing of the parasitoid,Sclerodermus pupariae (Hymenoptera: Bethylidae)

Sclerodermus pupariae Yang et Yao (Hymenoptera: Bethylidae) is used as a potential biocontrol agent for several buprestid and cerambycid larvae. This study aimed to enhance the efficiency of mass‐rearing of this parasitoid by investigating the fitness gain of this bethylid wasp, including the proportion of successful parasitism and development, brood size, sex ratio, proportion of winged female offspring, body size and longevity of female offspring, under eight different maternal parasitoid density treatments using Thyestilla gebleri Faldermann as host in the laboratory. The results indicated that the foundress densities did not affect the parasitism or emergence rate of this parasitoid. Brood size of the parasitoids increased significantly when the number of maternal wasps ranged from one to four. However, further increases in foundress number did not affect the parasitoid brood size. The sex ratios of S. pupariae were always female‐biased. The proportions of male in the progeny colonies were <10% throughout all experimental treatments. The percentage of winged female progeny was not significantly influenced by the density of adult maternal parasitoids. Body sizes of parasitoids significantly declined with increasing maternal parasitoid densities. Although the parasitoid body size reduced when maternal wasp number was higher, it could be compromised by the relatively higher number of female offspring produced. Further, more than 70% of the parasitoids remained alive when they were stored at 12°C for four months throughout the experiments. These findings suggest that exposure of four female wasps to a single host larva would result in the highest fitness of S. pupariae. Our findings might provide a new approach to enhance the efficiency of mass‐rearing of this bethylid wasp.     

Polyandrous females found fitter populations

Multiple mating by females (polyandry) requires an evolutionary explanation, because it carries fitness costs in many species. When mated females disperse alone to a new habitat, their offspring may have no option but to mate with their siblings and incur inbreeding depression. However, some of the offspring of polyandrous females may only be half siblings, reducing inbreeding depression when isolated groups of siblings only have each other as mates. We investigated this putative benefit of polyandry over monandry by initiating multiple genetically isolated populations of Callosobruchus maculatus beetles, each founded by a single female, who received a complete ejaculate from either one or two males. The early generations had comparable fitness, but the F4 and F5 descendants of doubly inseminated females were more numerous and had higher egg‐to‐adult survival than the descendants of singly inseminated females. This fitness benefit was of similar magnitude whether beetles were reared on their standard food plant, or on a less favourable food source. Our results suggest that polyandrous females produce fitter descendants in inbred founder populations and therefore that polyandry may affect movement ecology and invasion biology.     

The more the merrier: Conspecific density improves performance of gregarious larvae and reduces susceptibility to a pupal parasitoid

Aggregation can confer advantages in animal foraging, defense, and thermoregulation. There is a tight connection between the evolution of insect sociality and a highly effective immune system, presumably to inhibit rapid disease spread in a crowded environment. This connection is less evident for animals that spend only part of their life cycle in a social environment, such as noneusocial gregarious insects. Our aim was to elucidate the effects of group living by the gregarious larvae of the Glanville fritillary butterfly with respect to individual performance, immunity, and susceptibility to a parasitoid. We were also interested in the role of family relative to common postdiapause environment in shaping life‐history traits. Larvae were reared at high or low density and then exposed to the pupal parasitoid wasp Pteromalus apum, either in presence or absence of a previous immune challenge that was used to measure the encapsulation immune response. Surviving adult butterflies were further tested for immunity. The wasp offspring from successfully parasitized butterfly pupae were counted and their brood sex ratios assessed. Larvae reared at high density grew larger and faster than those at low density. Despite high mortality due to parasitism, survival was greater among individuals with high pupal immunity in both density treatments. Moreover, butterfly pupae reared at high density were able to kill a larger fraction of individuals in the parasitoid broods, although this did not increase survival of the host. Finally, a larger proportion of variation observed in most of the traits was explained by butterfly family than by common postdiapause rearing environment, except for adult survival and immunity, for which this pattern was reversed. This gregarious butterfly clearly benefits from high conspecific density in terms of developmental performance and its ability to fight a parasitoid. These positive effects may be driven by cooperative interactions during feeding.     

Research and application of Chouioia cunea Yang (Hymenoptera: Eulophidae) in China

Chouioia cunea Yang (Hymenoptera: Eulophidae) is an effective parasitoid of many lepidopteran pests in China. Specifically, C. cunea has successfully suppressed populations of the fall webworm, Hyphantria cunea (Drury) (Lepidoptera: Arctiidae), an invasive and quarantined pest in China. Fall webworm biological control programmes in China have been aided by the development of artificial rearing technology for C. cunea. While researchers have determined some aspects of this parasitoid’s biology, such as fecundity and ratio of female offspring, as well as rearing methods, there was less information on the behavioural and ecological mechanisms by which C. cunea regulates host populations. Here, we review the research and application of C. cunea since it was first discovered in China.     

Close‐kin mating,but not inbred parents,reduces hatching rates and offspring quality in a threatened tortoise

Inbreeding depression, the reduction in fitness due to mating of related individuals, is of particular conservation concern in species with small, isolated populations. Although inbreeding depression is widespread in natural populations, long‐lived species may be buffered from its effects during population declines due to long generation times and thus are less likely to have evolved mechanisms of inbreeding avoidance than species with shorter generation times. However, empirical evidence of the consequences of inbreeding in threatened, long‐lived species is limited. In this study, we leverage a well‐studied population of gopher tortoises, Gopherus polyphemus, to examine the role of inbreeding depression and the potential for behavioural inbreeding avoidance in a natural population of a long‐lived species. We tested the hypothesis that increased parental inbreeding leads to reduced hatching rates and offspring quality. Additionally, we tested for evidence of inbreeding avoidance. We found that high parental relatedness results in offspring with lower quality and that high parental relatedness is correlated with reduced hatching success. However, we found that hatching success and offspring quality increase with maternal inbreeding, likely due to highly inbred females mating with more distantly related males. We did not find evidence for inbreeding avoidance in males and outbred females, suggesting sex‐specific evolutionary trade‐offs may have driven the evolution of mating behaviour. Our results demonstrate inbreeding depression in a long‐lived species and that the evolution of inbreeding avoidance is shaped by multiple selective forces.     

Optimal biological parameters for rearing Ooencyrtus pityocampae on the new laboratory host Philosamia ricini

Biological control programmes involving Ooencyrtus pityocampae Mercet (Hymenoptera: Encyrtidae) have proved effective at reducing the damage caused by the pine processionary Thaumetopoea pityocampa Denis & Schiffermüller (Lepidoptera: Thaumatopoeidae). In this study, the biological variables that influence the parasitism of O. pityocampae on the new laboratory host Philosamia ricini Danovan (Lepidoptera: Saturniidae) have been investigated. Laboratory experiments were conducted under the conditions of 25 ± 1°C, 65 ± 5% R.H (relative humidity) and a photoperiod of 16 : 8 h (L : D = light : dark). The host egg age and parasitoid age are often regarded as being key factors influencing the emergence rate of O. pityocampae. The optimal age of host eggs for parasitization was 1–2 days, and the emergence rate was highest with 5‐day‐old female parasitoids. Thus, our results define the optimal conditions for the effective and economic rearing of parasitoids as follows: one 5‐day‐old female parasitoid per 50 (1–2)‐day‐old host eggs. The development time of O. pityocampae ranged between 19.5 and 22.6 days. Parasitoids that were exposed to bio‐honey survived 10.5 times longer than those that did not receive supplemental food. O. pityocampae was reared for more than nine generations on the eggs of P. ricini. Consequently, P. ricini has been found as a suitable new laboratory host for the mass rearing of O. pityocampae for the use of biological control programmes against T. pityocampa in future.     

Offering honey containing a selective insecticide as food for pests and parasitoids: another effective use

We investigated the effects of the presence of a selective insecticide, pyridalyl, in aqueous solutions of honey as food for adults of diamondback moth (DBM) Plutella xylostella (L.) and its larval parasitoid Cotesia vestalis (Halliday) on their performances. We used a commercial formulation of pyridalyl which contained 10% pyridalyl. Survival times of DBMs reared with honey solution with pyridalyl at 10 000‐fold dilution were not significantly different from those of DBMs reared with pure honey solution. However, at 1000‐fold and 100‐fold dilutions of pyridalyl in honey solution, survival times were significantly shorter than those with honey solution alone. By contrast, survival times of C. vestalis reared with honey solution with pyridalyl at 1000‐fold and 100‐fold dilution were not significantly different from those of C. vestalis reared with pure honey solution. Offering honey solution with pyridalyl at 100‐fold dilution to C. vestalis did not affect its parasitization ability or offspring sex ratio. The novel aspects of the use of selective pesticides to control DBMs using C. vestalis are discussed.     

Incest versus abstinence: reproductive trade‐offs between mate limitation and progeny fitness in a self‐incompatible invasive plant

Plant mating systems represent an evolutionary and ecological trade‐off between reproductive assurance through selfing and maximizing progeny fitness through outbreeding. However, many plants with sporophytic self‐incompatibility systems exhibit dominance interactions at the S‐locus that allow biparental inbreeding, thereby facilitating mating between individuals that share alleles at the S‐locus. We investigated this trade‐off by estimating mate availability and biparental inbreeding depression in wild radish from five different populations across Australia. We found dominance interactions among S‐alleles increased mate availability relative to estimates based on individuals that did not share S‐alleles. Twelve of the sixteen fitness variables were significantly reduced by inbreeding. For all the three life‐history phases evaluated, self‐fertilized offspring suffered a greater than 50% reduction in fitness, while full‐sib and half‐sib offspring suffered a less than 50% reduction in fitness. Theory indicates that fitness costs greater than 50% can result in an evolutionary trajectory toward a stable state of self‐incompatibility (SI). This study suggests that dominance interactions at the S‐locus provide a possible third stable state between SI and SC where biparental inbreeding increases mate availability with relatively minor fitness costs. This strategy allows weeds to establish in new environments while maintaining a functional SI system.     

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.     

Continuous rearing of the predatory anthocorid Orius laevigatus without plant materials

The omnivorous anthocorid predator Orius laevigatus is an economically important biological control agent of several small arthropod pests including the western flower thrips Frankliniella occidentalis. Mass rearing systems for Orius bugs typically make use of plant materials such as bean pods as an oviposition substrate and moisture source. Omission of plant materials from the mass rearing system of these beneficial arthropods could drastically improve the cost‐effectiveness of their production and thus stimulate their use in augmentative biological control. This study investigated the effect of a plantless rearing system, using wax paper as a walking substrate, water encapsulated in Parafilm domes, and an artificial oviposition substrate made of Parafilm and moist cotton wool, on the developmental and reproductive fitness of O. laevigatus. Plantless rearing during four generations resulted in females with an 11% lower body weight and a pre‐oviposition period that was prolonged by 29%. However, other biological parameters were not negatively affected by the absence of plants. In addition, plantless‐reared females had similar predation rates on F. occidentalis larvae as their peers maintained on plants. Our study indicates that the omission of plant material from the production cycle of O. laevigatus is possible when Ephestia kuehniella eggs are provided as a nutritionally optimal food source.     

Invertebrate predation of 15N-marked prey in semi-field wheat enclosures

One of the most famous examples of successful, classical biological control in Japan is the introduction of the parasitoids Coccobius fulvus and Aphytis yanonensis against the citrus pest arrowhead scale Unaspis yanonensis. Together, they comprise a host‐parasitoid system that has been demonstrated to be stable. To test the conventional theory that successful biological control of pests occurs through the establishment of a low stable equilibrium, brought about by the density‐dependent responses of natural enemies to the pest species, sampling was carried out at five sites in the field during 2000 and 2001 to examine the relationship between the rate of parasitism by C. fulvus and the density of its host. The data were analysed using three statistical techniques at nine spatial scales. Contrary to conventional theoretical predictions, each method of analysis detected very little density‐dependence at any spatial level in this study. Parasitoid aggregations independent of host density were not sufficient to stabilise host–parasitoid interactions. Our results suggest that neither spatial density‐dependent nor density‐independent parasitism is necessary for successful biological control, or for the stability of the host–parasitoid system. We propose an alternative mechanism: a spatial refuge induced by parasitoid introduction may stabilise a system.     

Inbreeding variability and population structure in the invasive haplodiploid palm‐seed borer (Coccotrypes dactyliperda)

We investigated the mating system and population genetic structure of the invasive haplodiploid palm‐seed borer Coccotrypes dactyliperda in California. We focused on whether these primarily inbreeding beetles have a ‘mixed‐breeding’ system that includes occasional outbreeding, and whether local inbreeding coefficients (F_IS) varied with dominant environmental factors. We also analysed the genetic structure of C. dactyliperda populations across local and regional scales. Based on the analysis of genetic variation at seven microsatellite loci in 1034 individual beetles from 59 populations, we found both high rates of inbreeding and plentiful evidence of mixed‐breeding. F_IS ranged from ?0.56 to 0.90, the highest variability reported within any animal species. There was a negative correlation between F_IS and latitude, suggesting that some latitude‐associated factor affecting mating decisions influenced inbreeding rates. Multiple regressions suggested that precipitation, but not temperature, may be an important correlate. Finally, we found highly significant genetic differentiation among sites, even over short geographic distances (< 1000 m).