Bidirectional movement of aphid parasitoids (Braconidae: Aphidiinae) between crops and non-crop plants in agroecosystems of central Argentina

The movement of predators and parasitoids between natural and cultivated habitats is a common process in agroecosystems, which may be affected by different biotic and abiotic factors, mostly related to the availability of resources. Here, through a broad approach, we aimed to obtain an overview of factors affecting the bidirectional movement of aphid parasitoids (Braconidae: Aphidiinae) across cultivated habitats and their natural vegetated borders. Using bidirectional flight traps, we measured the number of parasitoids moving from borders to crops and vice versa, in fields of three common crop species (alfalfa, oat and wheat) in the Pampean region, Santa Fe, Argentina. The effects of the abundance of aphid prey, abundance and richness of flowers in both habitats, as well as temperature and wind speed on parasitoid movement, were assessed through generalized mixed models, considering sampling date and field as random factors. The relationship between parasitism percentages and parasitoid movement from the borders to the crops was explored separately for three pest aphid species: Aphis craccivora Koch, Rhopalosiphum padi (L.) and Schizaphis graminum (Rondani). Overall, we found a prevalence of parasitoids moving in the border-crop direction, mainly in wheat and alfalfa crops. Aphid abundance in the arrival habitat affected parasitoid movement in both directions. A link between parasitoid movement and parasitism percentages was observed for the aphid species S. graminum in wheat, suggesting a beneficial role of natural vegetation in pest control.     

Spatially aggregated parasitism on pea aphids, Acyrthosiphon pisum, caused by random foraging behavior of the parasitoid Aphidius ervi

We investigated the role of the foraging behavior of the parasitoid wasp Aphidius ervi in producing nonrandom spatial patterns of parasitism among pea aphids, Acyrthosiphon pisum . We measured spatial variability in percent parasitism by determining the number of aphids and percent parasitism in 40 sampling plots (0.65-m2 circles) located within a homogeneous alfalfa field. In one replicate of this experiment, mean parasitism of aphids was 18.7%, and percent parasitism showed density-independent aggregation (i.e., greater than random variability in percent parasitism among sampling plots). In the other replicate, mean parasitism was 56.3%, and percent parasitism was not aggregated among plots. We used a combination of field observations of parasitoid foraging and mathematical models to explore these results. In particular, we asked whether the presence or absence of density-independent aggregation at different mean percent parasitism can be explained even if parasitoids forage randomly, without changing their behavior in response to encounters with aphids. Observations show that parasitoids tend to move short distances between nearby alfalfa stems (mean=10.8 cm), and the turning angle between successively visited stems was uniformly distributed. We incorporated this behavior into both simulation and analytical models of parasitoid foraging. The models show the same pattern as that observed in the field: parasitism is aggregated in a density-independent fashion when mean percent parasitism is low but not when mean percent parasitism is high. Therefore, density-independent aggregation in percent parasitism does not necessarily imply behavioral responses of parasitoids to host encounters and previously parasitized hosts.     

Effect of <Emphasis Type="Italic">Diachasmimorpha longicaudata</Emphasis> releases on the native parasitoid guild attacking <Emphasis Type="Italic">Anastrepha</Emphasis> spp. larvae in disturbed zones of Chiapas,Mexico

We evaluated the effect of augmentative releases of Diachasmimorpha longicaudata (Ashmead), on the native parasitoid guild of Anastrepha spp. over a two year period in zones adjacent to mango commercial orchards in Chiapas, Mexico. We chose two 15 ha working zones, 15 km apart, harbouring fruit fly hosts of varying densities without chemical control. In 2013, parasitoids were released in zone “A” while zone “B” served as control. In 2014 zones were exchanged. As expected, releases of D. longicaudata significantly increased total parasitism, from around 0.5–5% to over 22%, but annual parasitism by native parasitoids was only significantly affected in zone “A”. The numbers of native parasitoids were higher in zone “A” in both years, and diversity (H′) was not affected by D. longicaudata releases in both zones. Our results suggest that releases of D. longicaudata affect the relative abundance but not the species richness of native parasitoids.     

In search of secondary plants to enhance the efficiency of cabbage seed weevil management

The infestation rate and parasitoid communities of Ceutorhynchus obstrictus (Marsham) (Coleoptera: Curculionidae) were assessed on seven spring sown brassicaceous plant species to find potential secondary plants that might help increase the parasitism rates of this serious oilseed pest. Over the three-year study, the average infestation rate of pods by C. obstrictus remained below 10 % for each plant species. Despite the low pest abundance, C. obstrictus was parasitized by hymenopteran parasitoids on all plant species, except on Eruca vesicaria subsp. sativa ((Mill.) Thell.). Parasitism rates were remarkably high: between 33.7 and 70.8 % on average and peaked at 94.7 % on Raphanus sativus (L.) var. oleiformis (Pers.). Not only was the parasitism rate high on R. sativus, but it also had a different parasitoid species composition consisting mainly of egg parasitoids (Mymaridae), while on the other plant species larval parasitoids (Pteromalidae) dominated. These findings are important for planning new sustainable pest management approaches.     

Effect of host feeding on life history traits of <Emphasis Type="Italic">Tamarixia radiata</Emphasis>, parasitoid of the Asian citrus psyllid, <Emphasis Type="Italic">Diaphorina citri</Emphasis>

The parasitoid Tamarixia radiata (Hymenoptera: Eulophidae) is being used for the biological control of the Asian citrus psyllid (ACP), Diaphorina citri (Hemiptera: Liviidae). The parasitoid is strongly synovigenic, as it is born with very few mature eggs. Synovigenic insects need to feed on host haemolymph to mature additional eggs, and are able to resorb mature eggs to allocate resources toward maintenance. We investigated the effect of host feeding on parasitism, longevity and egg load dynamics, and estimated egg maturation and resorption rates. Although host feeding does not increase survival or longevity, it results in increased parasitization rates when parasitoids are seven days old, and that a single host meal leads to an average gain of three eggs. We discuss the importance of these data to predict the foraging and parasitization behavior of T. radiata in the field, and to potentially improve current efforts to control ACP.     

Effects of Botanical Insecticides on Hymenopteran Parasitoids: a Meta-analysis Approach

Botanical insecticides (BIs) are considered a valuable alternative for plant protection in sustainable agriculture. The use of both BIs and parasitoids are presumed to be mutually compatible pest management practices. However, there is controversy on this subject, as various studies have reported lethal and sublethal effects of BIs on hymenopteran parasitoids. To shed new light on this controversy, a meta-analytic approach of the effects of BIs on adult mortality, parasitism, and parasitoid emergence under laboratory conditions was performed. We show that BIs increased mortality, decreased parasitism, and decreased parasitoid emergence. Botanical insecticides derived from Nicotiana tabacum and Caceolaria andina were particulary lethal. Most of the parasitoid groups showed susceptibility to BIs, but the families Scelionidae and Ichneumonidae were not significantly affected. The negative effects of BIs were seen regardless of the type of exposure (topical, ingestion, or residual). In conclusion, this meta-analysis showed that under laboratory conditions, exposure of hymenopteran parasitoids to BIs had significant negative effects on adult mortality, parasitism, and parasitoid emergence.     

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.     

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.     

Density-dependent foraging behaviors in a parasitoid lead to density-dependent parasitism of its host

Empirical studies of spatial heterogeneity in parasitism by insect parasitoids have focused largely on patterns, while the many possible underlying mechanisms have been little studied in the field. We conducted experimental and observational studies on Tachinomyia similis (Diptera: Tachinidae) attacking western tussock moths (Orgyia vetusta; Lepidoptera: Lymantriidae) on lupine bushes at Bodega Bay, Calif., USA. We examined several foraging behaviors that have been hypothesized to create density-dependent variation in parasitism rates, including spatial aggregation of parasitoids to high host density, mutual interference among searching parasitoids and decelerating functional responses of the parasitoid. At the spatial scale of individual bushes, we detected both aggregation to a high density and a decelerating functional response. The resulting spatial pattern of parasitism was best fit by two models; one included an effect of parasitoid aggregation and the other included an effect of aggregation and a decelerating functional response. Most of the variation in parasitism was not correlated with density of O. vetusta.     

Egg Parasitoid Complex of the Corn Leafhopper, <Emphasis Type="Italic">Dalbulus maidis</Emphasis> (DeLong) (Hemiptera: Cicadellidae), in Argentina

The corn leafhopper, Dalbulus maidis (DeLong), is the most important leafhopper pest of maize, Zea mays, in the Americas. A survey of the diversity of its egg parasitoids was carried out in northwestern Argentina. During summer from 2004 to 2007, the samples were collected, using sentinel eggs of D. maidis on corn leaves, exposed in 48 cornfields. Sixteen species belonging to four families of Chalcidoidea (Hymenoptera) were identified. Among the parasitoid groups, Trichogrammatidae was the most represented family with eight species, followed by Mymaridae with six species. The mymarid Anagrus incarnatus Haliday and the trichogrammatid Pseudoligosita longifrangiata (Viggiani) were the most abundant and frequent parasitoids. The mean percentage of parasitism of D. maidis eggs was 16.4% and varied greatly among the sites, ranging from 0 to 56.7%; generally, it was higher in Yungas and lower in Monte province sites. The species richness was higher in the localities within the Yungas, with 13 parasitoid species, of which two species were dominant, comprising 83.6% of the collected individuals. Monte was the province that showed the highest diversity index (H´ = 1.62). In addition, we present information on the distribution, known host associations of each parasitoid species and an identification key to all species of egg parasitoids of D. maidis in Argentina.     

Aggregation and the Coexistence of Competing Parasitoid Species

In nature, many insect species are attacked by more than one specialized species of parasitoid. We examine whether parasitoid aggregation among patches containing hosts can promote the coexistence of specialized parasitoids on the same host species. We construct models to analyze the effects of three types of parasitoid aggregation: direct density-dependent, inverse density-dependent, and density-independent aggregation. All three types of aggregation may facilitate coexistence, provided the parasitoid species show behavioral differences that produce different patterns of aggregation. By deriving general conditions of coexistence of parasitoids, we show that all three types of aggregation act to facilitate coexistence in the same way—by increasing the covariance between the distributions of susceptible hosts and the least common parasitoid. Although they act in the same way, in general the effect of density-independent aggregation in facilitating coexistence is greater than either direct or inverse density-dependent aggregation. This suggests that density-independent aggregation may have the greatest potential to facilitate the coexistence of specialize parasitoids using the same host.     

Predators and parasitoids of the harlequin ladybird, <Emphasis Type="Italic">Harmonia axyridis</Emphasis>, in its native range and invaded areas

The harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae) has rapidly spread in several continents over the past 30 years and is considered an invasive alien species. The success of H. axyridis as an invader is often attributed to weak control by natural enemies. In this paper, we provide an overview of current knowledge on predators and parasitoids of H. axyridis. The common feature of predators and parasitoids is that they directly kill exploited organisms. Currently available data show that H. axyridis, displaying a variety of chemical, mechanical, and microbiological anti-predator defenses, is usually avoided by predators. However, some birds and invertebrates can eat this ladybird without harmful consequences. The primary defenses of H. axyridis against parasitoids include immune response and physiological and nutritional unsuitability for parasitoid development. These defenses are probably relatively efficient against most ladybird parasitoids, but not against flies of the genus Phalacrotophora. The latter are idiobiont parasitoids and hence can evade the host’s immune response. Indeed, rates of parasitism of H. axyridis by Phalacrotophora in the Palaearctic region (both in the native range in Asia and in Europe) are relatively high. While strong evidence for enemy release on the invasive populations of H. axyridis is lacking, several cases of parasitoid acquisition have been recorded in Europe, North America, and South America. We conclude that enemy release cannot be excluded as a possible mechanism contributing to the spread and increase of H. axyridis in the early stages of invasion, but adaptation of parasitoids may lead to novel associations which might offset previous effects of enemy release. However, further work is required to elucidate the population-level effects of such interactions.     

Spatio‐temporal variation in Helicoverpa egg parasitism by Trichogramma in a tropical Bt‐transgenic cotton landscape

• 1 Understanding the spatio‐temporal dynamics of insects in agroecosystems is crucial when developing effective management strategies that emphasize the biological control of pests.
• 2 Wild populations of Trichogramma Westwood egg parasitoids are utilized for the biological suppression of the potentially resistant pest species Helicoverpa armigera (Hübner) in Bt‐transgenic cotton Gossypium hirsutum L. crops in the Ord River Irrigation Area (ORIA), Western Australia, Australia.
• 3 Extensive, spatially‐stratified sampling during a season of relatively high Trichogramma abundance found that spatial patterns of pest egg parasitism in the ORIA tend toward heterogeneity, and do not necessarily coincide with host spatio‐temporal dynamics. Both patterns of host egg density and mean rates of parasitism are not good indicators of parasitoid spatio‐temporal dynamics in ORIA cotton crops.
• 4 Parasitism rates can be significantly higher within the middle strata of the cotton plant canopy before complete canopy closure, despite a similar number of host eggs being available elsewhere in the plant.
• 5 Spatial variation in egg parasitism by Trichogramma in Bt‐transgenic cotton is evident at the between‐field, within‐field and within‐plant scale, and is not solely driven by host spatial dynamics. These factors should be considered when estimating Trichogramma impact on pest species during biological control and spatio‐temporal studies of host‐parasitoid interactions in general.

     

Relationship between oviposition,virulence gene expression and parasitism success in <Emphasis Type="Italic">Cotesia typhae</Emphasis> nov. sp. parasitoid strains

Studying mechanisms that drive host adaptation in parasitoids is crucial for the efficient use of parasitoids in biocontrol programs. Cotesia typhae nov. sp. (Fernández-Triana) (Hymenoptera: Braconidae) is a newly described parasitoid of the Mediterranean corn borer Sesamia nonagrioides (Lefebvre) (Lepidoptera: Noctuidae). Braconidae are known for their domesticated bracovirus, which is injected with eggs in the host larva to overcome its resistance. In this context, we compared reproductive success traits of four Kenyan strains of C. typhae on a French and a Kenyan populations of its host. Differences were found between the four strains and the two most contrasted ones were studied more thoroughly on the French host population. Parasitoid offspring size was correlated with parasitism success and the expression of bracovirus virulence genes (CrV1 and Cystatin) in the host larva after parasitism. Hybrids between these two parasitoid strains showed phenotype and gene expression profiles similar to the most successful parental strain, suggesting the involvement of dominant alleles in the reproductive traits. Ovary dissections revealed that the most successful strain injected more eggs in a single host larva than the less successful one, despite an equal initial ovocyte number in ovaries. It can be expected that the amount of viral particles increase with the number of eggs injected. The ability to bypass the resistance of the allopatric host may in consequence be related to the oviposition behaviour (eggs allocation). The influence of the number of injected eggs on parasitism success and on virulence gene expression was evaluated by oviposition interruption experiments.     

Effect of Bt maize on the plant-aphid–parasitoid tritrophic relationships

The effect of Bt maize on aphid parasitism and the aphid–parasitoid complex was measured in field conditions on three transgenic varieties, two derived from Event MON810 and one from Bt176, and their near-isogenics in a two-year study. No differences in aphid abundance were found between Bt maize varieties and their near-isogenics. Differences within Bt and within near-isogenic varieties were found, but only in one year. Differences in aphid abundance were probably better accounted for the variety background and year conditions than by the transgenesis or Event. Lysiphlebus testaceipes (Cresson), Lipolexis gracilis Förster (Hymenoptera, Braconidae, Aphidiinae) and Aphelinus sp. (Hymenoptera, Aphelinidae) were the prevalent parasitoids. Bt maize did not alter the aphid–parasitoid associations and had no effect on the aphid parasitism and hyperparasitism rates. The results suggest that Bt maize has no negative impact on second, third and fourth levels of the trophic relationships studied.     

Innate Olfactory Responses of <Emphasis Type="Italic">Asobara japonica</Emphasis> Toward Fruits Infested by the Invasive Spotted Wing Drosophila

Insect parasitoids are often manipulated to improve biological control programs for various arthropod pests. Volatile compounds can be a relevant cue used by most parasitoid hymenoptera for host or host microhabitat location. Here, we studied olfactory responses of the braconid Asobara japonica Belokobylskij, an Asiatic endoparasitoid of the invasive pest Drosophila suzukii (Matsumura), toward its host and host substrates. Adult A. japonica displayed an innate attraction to undescribed volatile cues from infested host fruits irrespectively of the juvenile rearing experience, i.e. they respond to a novel cue subsequently used for microhabitat selection. These data suggest that A. japonica parasitoids mass-reared on artificial diet and factitious host (D. melanogaster) can successfully locate their hosts. Naïve female parasitoids did not show a preference towards any of the tested host media. However, the enforced adult experience with the rearing host medium modified the olfactory preference patterns toward non-natal host fruits. These findings provide evidence of associative learning during the adult stage of A. japonica, and demonstrate its plasticity in exploiting the volatiles from various fruits infested by D. suzukii.     

Dynamic host-feeding and oviposition behavior of an aphid parasitoid <Emphasis Type="Italic">Aphelinus asychis</Emphasis>

In order to maximize the lifetime reproductive success of parasitoids, they should be induced to dynamically accept individual hosts that have different suitability for oviposition. Parasitoids tend to exhibit higher host-selective behavior when their egg load is limited, and are less selective if they are facing time constraints. Here, we evaluated the effects of parasitoid age on egg load, fecundity and host instar preference of a honey-fed aphid parasitoid, Aphelinus asychis Walker (Hymenoptera: Aphelinidae). Host selective experiment was conducted to measure host-preference of honey-fed A. asychis females at different ages, using the second and fourth instars of the green peach aphid Myzus persicae as their hosts. The results showed that the choice of host-instar for oviposition was significantly influenced by the parasitoid age. Honey-fed parasitoids in the age groups of 1, 5, 10 and 20 days tended to parasitize predominantly second-instar aphids, whereas 15-days old parasitoids showed no significant preference of host instars. On the other hand, host-feeding preference was not affected by parasitoid age. Parasitoid females of all ages preferred younger aphids to older aphids. This result could help evaluate the effectiveness of A. asychis for biological control of M. persicae when they encountered mixed-instar aphids in the field. In addition, the results might be helpful in assessing the host killing effects of other host-feeding parasitoids.     

Optimized timing of parasitoid release: a mathematical model for biological control of <Emphasis Type="Italic">Drosophila suzukii</Emphasis>

We present a model for the population dynamics of the invasive fruit fly Drosophila suzukii and its pupal parasitoid Trichopria drosophilae. Seasonality of the environment is captured through a system of delay differential equations with variable delays. The model is used to explore optimal timing for releasing parasitoids in biological control programs. According to the results, releasing parasitoids is most effective between late spring and early summer when the host population begins to increase. A single parasitoid release event can be more efficient than multiple releases over a prolonged period, but multiple releases are more robust to suboptimal timing choices. The findings can be useful for optimizing parasitoid release and should be transferable for similar systems. More generally, the model is an example for stage-structured resource-consumer dynamics in a varying environment.     

Parasitism rates and parasitoid complexes of the wheat midges, <Emphasis Type="Italic">Sitodiplosis mosellana</Emphasis>, <Emphasis Type="Italic">Contarinia tritici</Emphasis> and <Emphasis Type="Italic">Haplodiplosis marginata</Emphasis>

Three species of cecidomyiid midges (Diptera: Cecidomyiidae), whose larvae overwinter in the soil, can cause significant yield losses on wheat in Europe: the orange wheat blossom midge, Sitodiplosis mosellana (Géhin), the yellow wheat blossom midge, Contarinia tritici (Kirby), and the saddle gall midge, Haplodiplosis marginata (von Roser). The biological control of wheat midges by their parasitoids can contribute to reduce the midge populations. Soil samples were collected in several fields in Belgium in 2012–2014 in order to characterize the parasitism rates and parasitoid complexes in overwintering larvae. The parasitism rates varied greatly between the sampled fields: 3–100, 0–100 and 2% for S. mosellana, H. marginata and C. tritici, respectively. The parasitism rate was not related to the larval density of wheat midge. The three wheat midges have totally distinct parasitoid complexes in Belgium. Eight species (Hymenoptera: Pteromalidae and Platygastridae) were found as parasitoid of S. mosellana: Macroglenes penetrans (Kirby), Amblypasis tritici (Walker), Euxestonotus error (Fitch), Euxestonutus sp. Fouts, Leptacis sp. Foerster, Platygaster gracilipes (Huggert), Platygaster nisus Walker, and Platygaster tuberosula (Kieffer). According to their abundance, M. penetrans, E. error and P. tuberosula appeared as the main parasitoids of S. mosellana in Belgium. For the two other wheat midges, only one species of the family Platygastridae was found for each midge: Platygaster equestris (Spittler) for H. marginata and Synopeas myles (Walker) for C. tritici.     

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.