Biology and distribution of microbe-associated thelytokous populations of aphid parasitoids (Hym., Braconidae, Aphidiinae)

Abstract: Some phenomena of the biology and ecology of the microbe ( Wolbachia )-associated thelytokous populations of aphid parasitoids are presented for the first time. Thelytokous virgin females were found to refuse the mating attempts by males of biparental populations, although males occurred quite rarely among the offspring. The host range was found to be about identical in conspecific biparental and thelytokous populations, whereas the association of solely biparental populations with a certain host group might be considered as a marker of the presence of sibling species in the area. The relative frequency of conspecific biparental and thelytokous populations varied, depending upon the area and host species. The microbe-induced thelytokous populations were confirmed in three species of the genus Lysiphlebus Foerst. ( Lysiphlebus cardui Marsh., Lysiphlebus confusus Tremblay and Eady, Lysiphlebus fabarum Marsh.) and probably some other, as yet undescribed, species only in the West Palearctic subregion, whereas the other known congeneric species in the subregion as well as in the Nearctic and the Neotropical regions were determined as strictly biparental species. Microbe-induced thelytokous populations did not change due to host species alternation and/or distribution area (purposeful introductions as biocontrol agents).     

Overwintering strategies and cold hardiness of two aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae)

The role of winter diapause in two aphid parasitoid species, Aphidius ervi Haliday and Aphidius rhopalosiphi DeStefani-Peres (Hymenoptera: Braconidae: Aphidiinae), in host synchronization and the induction of cold hardiness was investigated. Parasitoids were reared during three successive generations on Sitobion avenae Fabricius, at 15 degrees C under a photoperiod of 9 h light 15 h dark. Although these conditions are known to be strongly diapause inducing, neither parasitoids showed an incidence of diapause above 65% over the three generations; the rest of the population underwent quiescence. In both parasitoid species, diapausing mummies exhibited greater cold hardiness than non-diapausing mummies, resulting in significantly lower supercooling points (SCP) and in a higher survival rate during long-term exposures at 0 and -10 degrees C. The induction of increased cold hardiness in parasitoids was thus associated with the diapause state. SCPs of third instar larvae of S. avenae were similar to those of non-diapausing mummies of both parasitoid species, but significantly higher than those of diapausing mummies. The effect of winter climate on the stability of the host-parasitoid interaction is discussed.     

A comparison of techniques used to study the morphology of final instar larvae of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae)

Abstract. The morphology of the head sclerites of final instar larvae of aphid parasitoids prepared from cast larval skins and excised heads of whole larvae are compared, using both optical and scanning electron microscopy. Remarkable differences in the apparent shape of head sclerites, particularly mandibles, were found. Some of these differences are probably due to a consistent dorso-ventral flattening of the head during moulting, observed in cast skin preparations, whereas excised heads tend to flatten antero-posteriorly. The importance of these findings for understanding the three-dimensional shape of final instar mandibles and for the study of larval morphology and taxonomy of Hymenoptera is discussed     

Aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) in cultivated and non-cultivated areas of Markazi Province, Iran

The fauna of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae), as well as their diversity and tritrophic (parasitoid-host aphid-host plant) associations in cultivated and non-cultivated areas of Markazi province, was studied during 2004–2009. Thirty species of Aphidiinae belonging to 9 genera were identified. There are presented, in total, 73 associations with 32 host aphids occurring on 42 host plants. Five parasitoid-aphid associations are newly recorded from Iran. Lysiphlebus cardui (Marshall) is newly recorded for the fauna of Iran. Lysiphlebus fabarum (Marshall) and Diaeretiella rapae (M’Intosh) were the most abundant species in non-cultivated (72.96%) and cultivated (41.17%) areas, respectively. In the non-cultivated areas, L. fabarum was found on eight aphid species, while in cultivated areas it was only found on Aphis craccivora Koch. In cultivated areas, Sitobion avenae (F.) has the greatest diversity of parasitoids (Shanon-Weiner H = 0.875) whereas in non-cultivated areas the greatest diversity of parasitoids was recorded upon Acyrthosiphon pisum (Harris) (Shanon-Weiner H = 1.149). Significant differences were found between diversity of two ecosystems based on the overall diversity indices. Both species diversity and evenness were greater in cultivated ecosystems. The results are discussed in relation to the over-all parasitoid-aphid-plant associations in the area.     

Functional responses of aphid parasitoids,Aphidius colemani (Hymenoptera: Braconidae) and Aphelinus asychis (Hymenoptera: Aphelinidae)

We evaluated the functional responses of two aphid parasitoids: Aphidius colemani on the green peach aphid Myzus persicae (Hemiptera: Aphididae), and Aphelinus asychis on M. persicae and the potato aphid, Macrosiphum euphorbiae (Hemiptera: Aphididae). Parasitoid oviposition occurred at host densities of 5, 10, 20, 30, 50, 80 or 100 aphids for A. colemani and 5, 10, 20, 30 or 50 aphids for A. asychis. More M. persicae were parasitized by A. colemani than by A. asychis at an aphid density of 50. Among the three types of functional response, type III best described the parasitoid response to the host densities both in A. colemani and A. asychis. The estimated handling time was shorter for A. colemani than for A. asychis (0.017 and 0.043 d, respectively). The proportion of aphids that were parasitized exhibited the same characteristic curve among the three host-parasitoid combinations: a wave form that appeared to be a composite of a decelerating (as in type II) response at low host density and an accelerating-and-decelerating (as in type III) response at medium to high host density. We hypothesize that the novel host species (and its host plant), density-dependent superparasitism, and/or density-dependent host-killing may have induced the modified type III response.     

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.     

A Molecular Phylogeny of the Aphidiinae (Hymenoptera: Braconidae)

Phylogenetic relationships within the Aphidiinae, and between this and other subfamilies of Braconidae (Hymenoptera), were investigated using sequence data from three genes: elongation factor-1α, cytochrome b, and the second expansion segment of the 28S ribosomal subunit. Variation in both protein-coding genes was characterized by a high level of homoplasy, but analysis of the expansion segment—robust over a range of alignment methods and parameters—resolved some of the older divergences. Parsimony analysis of the combined data suggests the following tribal relationships: (Ephedrini + (Praini + (Aphidiini + Trioxini))). In addition, the cyclostome subfamilies were found to form a clade separate from the Aphidiinae, but relationships between the Aphidiinae and the noncyclostome braconids could not be resolved. The inferred phylogeny also supported a secondary loss of internal pupation within the Praini and a polyphyletic origin of endoparasitism within the Braconidae.     

Density-dependent parasitism of cowpea aphid,Aphis craccivora by Lysiphlebus fabarum,Binodoxys acalephae,and Aphidius matricariae (Hymenoptera: Braconidae: Aphidiinae)

Biological control, as a major component of pest management strategies, uses natural biological agents to reduce pest populations. Studying the interaction among Aphis craccivora and its parasitoids including, Lysiphlebus fabarum, Binodoxys acalephae, and Aphidius matricariae in 2016 and 2017 in Tehran Parke-Shahr, showed positive, significant correlations in all cases between the densities of three parasitoid species and that of aphid nymphs and adults. The density of the parasitoids increased by increasing the density of the aphids. The parasitoids showed aggregative behavior in response to different densities of the host. There was a positive density-dependent correlation between the density of A. craccivora and rate of parasitism. Parasitism rates of nymphs and adult aphids by L. fabarum, B. acalephae, and A. matricariae increased or decreased along with decline or increase in the population of the aphid host. In 2016 spring, the highest rates of parasitism on aphid nymphs by L. fabarum, B. acalephae, and A. matricariae were 46.82, 23.09, and 17.16%, respectively. In 2017 spring, the highest rates of parasitism on aphid nymphs by L. fabarum, B. acalephae, and A. matricariae were 48.97, 21.77, and 15.06%, respectively. So, given the accordance between changes in aphid population and that of parasitoids, and parasitoids’ efficacy in Tehran’s polluted air, they can be used as biological agents in the management of A. craccivora population.     

Spatio-temporal variation of strawberry aphid populations and their parasitoids

Aphids are common herbivores in the strawberry crop that can reduce plant vigor and fruit quality and also transmit viruses. Aphid species prefer diverse plant organs, which represent particular habitats of different quality for aphids and for the development of natural enemies’ populations. Different habitat units (young leaves, mature leaves, buds, flowers) of strawberry were sampled fortnightly during all seasons. We identified seven aphid species, namely Chaetosiphon fragaefolii, Aphis gossypii, and Macrosiphum euphorbiae, the most abundant. During the autumn, C. fragaefolli and M. euphorbiae were scarce and A. gossypii was denser on mature leaves, while during summer M. euphorbiae was absent. During the winter, C. fragaefolii predominated on buds and young leaves, A. gossypii on flowers, and both species on mature leaves. During the spring, C. fragaefolii was even more abundant on buds, A. gossypii predominated on mature leaves, and the three species were equally abundant on flowers and young leaves. Parasitoids emerged from A. gossypii, M. euphorbiae and Myzus persicae, but not from C. fragaefolii. Three Aphidius and two Aphelinus species were recovered. All primary parasitoid species emerged from A. gossypii, and secondary parasitoids emerged only from this aphid. Aphis gossypii parasitism on mature leaves was markedly higher in winter and summer than in autumn and spring. Parasitism of A. gossypii was independent of its density, and the number of parasitized aphids was never higher than six. Our results contribute to define the most appropriate sample unit to estimate aphid density of different species and provide information about seasonal natural parasitism.     

Quality of different aphids species as hosts for the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae)

The suitability of Macrosiphum euphorbiae (Thomas), Aulacorthum solani (Kaltenbach) and Acyrthosiphon kondoi Shinji (Hemiptera: Aphididae) as hosts for the aphid parasitoid Aphidius ervi Haliday was evaluated by assessing host size, host preference, and host quality. Tests were carried out in an environmental chamber at 22±1oC, 70±10% RH and 12h photophase. Replicates (11) consisted of one 24h-old mated female of A. ervi without a previous oviposition experience. Female was released into a Petri dish (5 cm) with 20 2nd and 3rd instars of one of each aphid species tested on a leaf disc of the host plant onto a 1% water-agar layer. Parasitoid emergency was lower in A. kondoi (78.7%) compared to M. euphorbiae (92.2%) and A. solani (91.7%). Acyrthosiphon kondoi (0.36 mm) was the smallest host. The parasitoid showed preference (74.0% parasitism) for M. euphorbiae, the largest host (hind tibia length=0.73 mm), which in turn yielded larger A. ervi females (0.75 mm).     

Three new records of the subfamily Aphidiinae (Hymenoptera: Braconidae) from Korea

Three species of the Aphidiinae (Hymenoptera: Braconidae) are reported for the first time in Korea: Aphidius rhopalosiphi de Stefani-Perez, 1902, Aphidius uzbekistanicus Luzhetzki, 1960 and Lysiphlebus orientalis Starý and Rakhshani, 2010. Their diagnosis, photographs and host list are included.     

Host quality of different aphid species for rearing Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae)

This study aimed to evaluate the quality of the aphid Myzus persicae (Sulzer), Lipaphis erysimi (Kaltenbach) and Brevicoryne brassicae (L.) as hosts for the parasitoid Diaeretiella rapae (McIntosh). Parasitization by D. rapae was higher on M. persicae than on L. erysimi and B. brassicae. The time of development of D. rapae from egg to mummy or egg to adult male or female were shorter on M. persicae than on L. erysimi and B. brassicae. Moreover, D. rapae showed no significant differences in the emergence rate, sex ratio and longevity when reared on the three aphid species. Myzus persicae was the largest aphid host, with B. brassicae and L. erysimi being of intermediate and of small size, respectively. Diaeretiella rapae reared on M. persicae was larger than when reared on L. erysimi and B. brassicae, and females of D. rapae were significantly larger than males on M. persicae, but males of D. rapae were larger than females when reared on L. erysimi. No difference in size was detected between males and females in parasitoids reared on B. brassicae. Among the aphid species studied, M. persicae was found to be the most suitable to D. rapae.     

Diversity of Natural Enemies of Aphids Belonging to Aphidiinae (Hymenoptera: Braconidae) in India

An inventory of the biodiversity of aphidiine parasitoids (Hymenoptera: Braconidae) associated with aphids in India showed 123 species under 23 genera to be intensively and extensively exercising natural control. The inventory has been reinforced with all associated details, mainly zoogeographical distribution, parasitism potential attributes and other such relative details from primary sources so as to make it serve as an important startup tool for planning any IPM strategy, involving biocontrol of aphids.     

Toxicity of spinosad in protein bait to three economically important tephritid fruit fly species (Diptera: Tephritidae) and their parasitoids (Hymenoptera: Braconidae)

The feeding toxicity of the natural insecticide spinosad in Provesta protein bait was evaluated for three economically important fruit fly species, the Mediterranean fruit fly, Ceratitis capitata (Wiedemann); the melon fly, Bactrocera cucurbitae Coquillett; and the oriental fruit fly, Bactrocera dorsalis Hendel. Both females and males were evaluated. Spinosad was remarkably similar in toxicity to all three fruit fly species. Male C. capitata (24 h LC50 values and 95% fiducial limits = 2.8 [2.60-3.0] mg/liter spinosad) were significantly, although only slightly more susceptible to spinosadthan females (4.2 [3.8-4.6] mg/liter). Male (5.5 [4.7-6.6] mg/liter) andfemale (4.3 [3.7-4.9] mg/liter) B. cucurbitae were equally susceptible to spinosad. Female (3.3 [3.1-3.6] mg/liter) and male (3.1 [2.9-3.3] mg/liter) B. dorsalis also were equally susceptible to spinosad. Provesta bait containing spinosad also was evaluated against two parasitoids of tephritid fruit flies, Fopius arisanus (Sonan) and Pysttalia fletcheri (Silvestri). These parasitoids did not feed on the bait, so a contact toxicity test was conducted. Significant amounts of mortality were found only after exposure of parasitoids to spinosad-coated glass vials with concentrations > or =500 mg/liter spinosad. Parasitoids were less susceptible than fruit flies to such a degree that use of spinosad in bait spray should be compatible with these parasitoid species. Because the fruit flies tested in this study were so susceptible to spinosad, this product seems to be promising as a bait spray additive and a replacement for malathion for control of these species.     

Evolutionary relationships of wing venation and wing size and shape in Aphidiinae (Hymenoptera: Braconidae)

We explored evolutionary changes in wing venation and wing size and shape in Aphidiinae, one of the well-known groups of parasitic wasps from the family Braconidae. Forewings of 53 species from 12 genera were examined, for which a molecular phylogeny was constructed on the basis of the mitochondrial barcoding gene COI. By covering all types of wing venation within the subfamily Aphidiinae and by using landmark-based geometric morphometrics and phylogenetic comparative methods, we tested whether evolutionary changes in wing shape correlate to the changes in wing venation and if both changes relate to wing size. The relationship between wing morphology and host specificity has been also investigated. We found that six types of wing venation, with different degree of vein reduction, could be recognized. Wing venation type is largely genus specific, except in the case of maximal reduction of wing venation which could be found across examined Aphidiinae taxa. The reconstruction of evolutionary changes in wing venation indicates that evolutionary changes in wing shape are related to the changes in wing size, indicating that miniaturization play a role in evolution of wing morphology while host specialization does not affect the wing shape within the subfamily Aphidiinae.     

Interference competition between Aphidius matricariae and Praon volucre (Hymenoptera: Braconidae) attacking two common aphid species

Interference competition is a common phenomenon that occurs among adult females of different species to gain the highest food resources at the same time. In this research, extrinsic competition between Aphidius matricariae and Praon volucre on different densities and stages of two important pests of greenhouse crops in the world, Aphis gossypii and Myzus persicae, were investigated. The results of this study showed that total percentage parasitism of second, third and fourth nymphal instars of A. gossypii and M. persicae by A. matricariae, and P. volucre were affected by extrinsic competition. A combination of A. matricariae and P. volucre on A. gossypii had a negative effect on performance of these parasitoids. Although extrinsic competition reduced the efficiency of A. matricariae and P. volucre on M. persicae, total parasitism of M. persicae by A. matricariae and P. volucre (combination of two parasitoids) increased compared to A. matricariae or P. volucre acting alone. Also the results indicated that the extrinsic competition between A. matricariae and P. volucre on both A. gossypii and M. persicae was apparently more intense when presented with 25 hosts compared to 50 and 100 hosts. The results of this research show important information to determine an appropriate combination of these two parasitoid wasps for biological control of A. gossypii and M. persicae in greenhouses.     

Molecular identification of Aphidius transcaspicus (Hymenoptera: Braconidae: Aphidiinae), a closely associated species of Aphidius colemani,in Korea

Aphidius colemani (Braconidae: Aphidiinae) is an endoparasitoid and one of the most commercially used parasitoids for the control of various pest aphids. However, species identification of A. colemani is difficult because of the high degree of morphological similarity with closely associated species, such as A. transcaspicus and A. platensis. Recently, we identified a large-scale emergence of parasitoids from mummies of Rhopalosiphum maidis on barley banker plants in Yecheon County, Korea. The morphological characteristics of the forewing, petiole, and antenna indicated that our specimen is A. transcaspicus. The partial nucleotide sequence analysis of the mitochondrial cytochrome oxidase subunit I (COI) gene showed that it is 100% identical to Japanese specimens and 1.69% variable to Greek specimens. Analysis of the phylogenetic tree, haplotypes, and amino acid sequence of the COI gene, as well as the internal transcribed spacer 2 (ITS2) of the nuclear ribosomal DNA region, indicated that A. transcaspicus is closer to A. platensis than A. colemani, and Korean and Japanese populations were mostly diversified groups at the intraspecific level. This study provides important information to elucidate the genetic variation in A. transcaspicus and the relationships between closely related species within the A. colemani group.