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The identification of Trichogramma (Hymenoptera: Trichogrammatidae) species is problematic due to their small size and lack of distinct morphological characters. In this study, we combined morphological characters of the male genitalia and molecular methods using the mitochondrial cytochrome oxidase I (COI) gene as a molecular marker to identify eight species from 16 geographic populations: T. evanescens Westwood, T. cacoeciae Marchal, T. ostriniae Pang et Chen, T. chilonis Ishii, T. japonicum Ashmead, T. brassicae Bezdenko, T. bilingensis He et Pang, and T. dendrolimi Matsumura. We developed a polymerase chain reaction–restriction fragment length polymorphism (PCR–RFLP) method targeting the mitochondrial COI to distinguish the eight Trichogramma species using three restriction enzymes. We further analyzed 109 COI fragments from 18 Trichogramma species and found that the PCR–RFLP method could distinguish both intra- and inter-specific genetic variation among most of the species using four additional restriction enzymes.

The age ofTrichogrammaparasitoids could influence biological traits which are of great importance for effectiveness of mass rearing systems. Recent studies demonstrated thatTrichogramma ostriniae(TO) could parasitizeAntheraea pernyieggs through multiparasitism along with other Trichogrammaspecies, although few adults could emerge successfully. It is important to characterize the factors modulating the performance of TO onA. pernyieggs, notably in order to try enhancing its quantitative emergence through multiparasitism for further use in biological control. In this context, irrespective of host age, we tested different ages of TO females (from 0.5-day- to 6-day-old postemergence) in multiparasitism withTrichogramma chilonis(TC) onA. pernyieggs. The results of the present study confirmed that TO parasitism onA. pernyieggs was largely age dependent. Higher percentage of multiparasitism and higher number of emerged TO adults were recorded in the treatment where 3-day-old TO females were used for parasitization with TC onA. pernyihost. In addition, we also tested different female ratios of bothTrichogramma species to find out an optimal ratio for use in mass production. The highest percentage of multiparasitism, emergence and optimum emerged number of TO (perA. pernyiegg) was observed with the ratio 3:2 (TO:TC) per 1 host egg. This study demonstrated that the age of TO females can significantly affect their performance in multiparasitism of largeA. pernyieggs. These results prompt for more research in order to develop an effective multiparasitism-based production of TO at the industrial scale.

Trichogramma spp. (Hymenoptera: Trichogrammatidae) are generalist egg parasitoids widely used as biological control agents, yet with limited efficacy against Tuta absoluta (Meyrick; Lepidoptera: Gelechiidae), a key pest of tomato. Olfactory cues related to the host-plant complex influence the searching behavior in parasitoids. Studies have shown that female Trichogramma spp. can learn odor cues affecting their preference. We assessed if learning increases the response to tomato odor and whether it improves the parasitism rate of Trichogramma achaeae , Trichogramma evanescens, and Trichogramma dendrolimi . The parasitoids were either naive, reared for one generation on T.   absoluta eggs, or conditioned associatively with an oviposition experience on a factitious host in the presence of tomato odor. Subsequently, their arrestment response (searching time) to T.   absoluta -infested tomato leaves was observed in a static four-chamber olfactometer. Rearing the parasitoids on T.   absoluta increased the arrestment time of T.   dendrolimi strongly and that of T.   evanescens slightly but not that of T.   achaeae . In contrast, oviposition experience on a factitious host with the tomato odor (leaves or extract) increased the searching time of T.   achaeae and T.   evanescens strongly but did not improve the response of T.   dendrolimi. Concerning parasitism improvement, only T.   achaeae showed an increased parasitism rate after associative learning. Hence, the learning capacity of T.   achaeae should be further explored to improve its biological control efficacy against T.   absoluta .

Egg batches of Spodoptera moths are protected by scales deposited by females around and/or over eggs as a physical defense. These scales may affect the parasitism of some parasitoids, rendering biocontrol of Spodoptera eggs ineffective. In this study, we investigated the daily oviposition pattern of moths and the dynamics of egg mass scales of three Spodoptera species and examined the fitnesses of three potential egg parasitoid species to different egg mass scale thicknesses. The observations revealed that the three Spodoptera species share similar scale dynamics. From initial oviposition, S. exigua egg batches maintained a relatively high level of scale thickness (> 134.7 mu m) for 2 days and S. frugiperda and S. litura for 3 days (> 105.9 mu m, > 161.2 mu m, respectively). During this period, the scales effectively hindered parasitism by Trichogramma species (parasitized 0.4%-14.9% eggs). Thereafter, the thickness of the scales decreased daily. The scales of the three Spodoptera species were all relatively thin (< 20.0 mu m) after oviposition for 8 days, and subsequently, Trichogramma parasitized eggs more actively (parasitized up to 33.4%-36.5% eggs). Relatively, Trichogramma dendrolimi on S. frugiperda eggs, and Trichogramma chilonis on S. exigua eggs had higher parasitism. Meanwhile, Telenomus remus maintained a very stable and better performance than Trichogramma on Spodoptera species eggs with different scale thicknesses (parasitized 100% egg masses and 46.2%-60.0% eggs), which demonstrated its excellent potential as a Spodoptera species biocontrol agent. The findings elucidate the effect of egg mass scale thickness on effective parasitism by these egg parasitoid species and provide baseline information for the mixed use of Te. remus and Trichogramma against Spodoptera species.

Background Fall armyworm, Spodoptera frugiperda , is a highly invasive pest of maize and other crops worldwide. It has recently been detected in Europe, and it is urgent to test and develop new sustainable control methods adapted to the European context and market. Trichogramma spp. are egg parasitoids that are sometimes used as biological control agent against S. frugiperda in other continents. However, a major issue using Trichogramma spp. against this pest is that females cannot reach all eggs in an egg mass, which is usually composed of one to three layers of eggs, often covered with scales and hair. Three European Trichogramma species were tested for their ability to parasitize egg masses with one to three layers and with or without hair and scale cover. Methods Trichogramma brassicae , T. dendrolimi and T. cacoeciae were offered five types of S. frugiperda egg masses: one-layer without hair; one-layer with hair; two-layers without hair; two-layers with hair; three-layers with hair. For each treatment, an egg mass laid on paper was placed in a small vial saturated with females, to be sure that all reachable eggs would be parasitized. For each egg mass, the number of eggs in each layer was counted. Fifteen replicates were made per treatment, as well as 10 control vials without Trichogramma sp. Parasitism rates were calculated for each egg mass. Results There were significant differences in the ability of parasitoid species to oviposit through hair and scales and to reach the lower egg layers. Trichogramma dendrolimi was the most efficient species and T. cacoeciae the least. Depending on the number of egg layers and hair and scales, parasitism rates by T. brassicae , T. dendrolimi and T. cacoeciae varied between 99 and 41%, 100 and 43% and 100 and 28%, respectively. Conclusions The assays confirmed that Trichogramma females cannot easily oviposit through thick layers of hair and scales but overall parasitism rates were higher than found previously. Important variations between species were found, and more Trichogramma sp. and other local natural enemies should be tested pre-emptively before S. frugiperda has invaded Europe.

Selecting the candidate agents or species is a fundamental step in developing effective biological control programs. However, no attempts have been made to evaluate the efficacy of Trichogramma Westwood (Hymenoptera: Trichogrammatidae) strains against the Asian corn borer, Ostrinia furnacalis Guenée (Lepidoptera: Crambidae) in Myanmar. In this study, Trichogramma strains were investigated through a series of glass tube bioassays and under a semifield condition. Ostrinia furnacalis or Corcyra cephalonica egg preferences were compared among six strains of Trichogramma ostriniae, three of Trichogramma chilonis, and four of Trichogramma dendrolimi using a choice-test assay design. Significant differences were observed at the inter- and intraspecific levels. Four strains of T. ostriniae and two of T. dendrolimi showed a strong preference for O. furnacalis eggs, while two strains of T. chilonis and one T. dendrolimi strain preferred Corcyra cephalonica Stainton (Lepidoptera: Pyralidae) eggs. The remaining strains showed no preference. Eleven strains were examined on O. furnacalis eggs only, wherein parasitism, sex ratio, and total progeny per female were highest for two strains of T. ostriniae (respectively: 67.6 ± 3.0%, 82.7 ± 2.3%, 49.6 ± 2.8, and 67.6 ± 3.6%, 90.0 ± 2.4%, 42.7 ± 2.6), and one strain of T. dendrolimi (65.2 ± 3.2%, 84.7 ± 2.6%, 46.3 ± 2.8). Parasitism and searching capacity were evaluated for the three, best performing strains in cages containing maize plants. One T. ostriniae from Southern Shan State, Myanmar parasitized ∼81% of egg masses, and should be considered a candidate biological control agent against O. furnacalis in Myanmar. Graphical Abstract

Trichogramma wasps are commonly used as biocontrol agents to manage lepidopteran rice pests in rice fields. However, lepidopteran pests synergistically occur with rice planthoppers which are not targeted by Trichogramma. The use of Trichogramma parasitoids in field-based pest control efforts is greatly affected by the application of insecticides targeting planthoppers. As such, insecticide-resistant strains of Trichogramma are urgently needed for the incorporation of these beneficial natural enemies into integrated pest management programs in rice agroecosystems. In the present study, Trichogramma japonicum Ahmead (Hymenoptera: Trichogrammitidae) and Trichogramma chilonis Ishii (Hymenoptera:Trichogrammitidae) were treated with sublethal doses of four insecticides which target rice planthoppers, to generate tolerant strains in the laboratory. The resistance rate of T. japonicum to imidacloprid was the highest (17.8-folds) after 10 successive treatments and experienced 2.5, 4.72, and 7.41-fold increases in tolerance to thiamethoxam, buprofezin, and nitenpyram, respectively. Tolerance of T. chilonis to imidacloprid, thiamethoxam, buprofezin, and nitenpyram were 8.8, 6.9, 4.43, and 5.67-fold greater, respectively. The emergence and deformity (without spreading wings or short wings) rates of T. japonicum and T. chilonis gradually recovered with an increased exposure time of treatments. The fecundity of T. japonicum treated with thiamethoxam was significantly higher than that of the control and T. chilonis treated with thiamethoxam and nitenpyra. Our results demonstrate that screening for insecticide-tolerant/resistant Trichogramma strains was feasible, especially in the pairing of T. japonicum and imidacloprid, which could provide a valuable biological control tool that can be combined with traditional chemical control strategies for use in IPM of rice agroecosystems.

Exotic natural enemies that are imported to control a target pest may attack non-target species or disrupt the performance of other natural enemies of the target that are already present. We evaluate possible interactions between three parasitoid species, the native Telenomus nizwaensis and the imported Trichogramma brassicae and Trichogramma evanescens , when presented with Deudorix livia host eggs under high-density laboratory conditions. Deudorix livia is a butterfly which is an economically damaging pest in the Omani pomegranate agro-ecosystem. Most (73.5% overall) of the observed parasitism was by T. nizwaensis. It performed best when presented with host eggs in the absence of either of the Trichogramma species. These imported species thus have some potential to disrupt suppression of the pest by the indigenous natural enemy under lower-density conditions in the field, and neither of them achieved high parasitism rates themselves (laboratory conditions: T. brassicae  = 12.5%; T. evanescens  = 18.5%; with no evidence for any parasitism of field-collected eggs). Future efforts in this agro-ecosystem would best be directed towards encouraging T. nizwaensis, rather than towards importation of Trichogramma . Screening for negative effects of natural enemies on the pest suppression provided by other natural enemies is recommended.

Trichogramma parasitoids are important biological control agents for insect pest management. However, efficient means for mass production of Trichogramma parasitoids are needed, particularly for T. ostriniae, which often fail to form emergence holes on host eggs of Chinese oak silkworm, Antheraea pernyi, because of the hard chorion. In the present study, we evaluated the possibilities to enhance adult emergence of T. ostriniae by utilizing emergence holes made by T. dendrolimi during multiparasitism on host eggs of A. pernyi and other biological parameters such as pre-emergence time, parasitism rate, and emergence rate of the two parasitoids, which were also evaluated between the two parasitism regimes of multi- and monoparasitism. Our data showed that multiparasitism on host eggs of A. pernyi significantly facilitated the emergence of adult T. ostriniae. Generally, both Trichogramma species favored parasitizing A. pernyi eggs, with multiple parasitoid adults emerged per host egg. The overall performance of T. dendrolimi was similar between the two parasitism regimes, although a significantly higher number of unemerged adults were found in the multiparasitized eggs than in the monoparasitized. For T. ostriniae, significantly more adults emerged, and a higher emergence rate was recorded on host eggs multiparasitized with T. dendrolimi than that on monoparasitized. Furthermore, significantly fewer unemerged adults were found in multi- than monoparasitized host eggs. The results of this study provided useful information on the feasibility of mass production of T. ostriniae via multiparasitism with T. dendrolimi on large eggs of A. pernyi.

Pod borers are economically important soybean pests in temperate and tropical regions. However, the biological control of these pests using their natural insect enemies has been poorly studied to date. Indigenous natural populations of three Trichogramma (Hymenoptera: Trichogrammatidae) species, Trichogramma chilonis Ishii, Trichogramma ostriniae Pang & Chen, and Trichogramma leucaniae Pang & Chen, were collected from Leguminivora glycinivorella (Matsumura) (Lepidoptera: Tortricidae) eggs in soybean fields in China. In this study, we compare the parasitic capacities and suitabilities of three indigenous Trichogramma species on L. glycinivorella eggs at various ages. Host eggs of all ages were accepted by T. chilonis, T. ostriniae, and T. leucaniae. T. chilonis tended to parasitize 0–2-d-old eggs more than 3–4-d-old eggs. There were no significant differences in parasitism between the 0–2-d-old eggs and the 1–4-d-old eggs for T. ostriniae and T. leucaniae. For eggs at various ages, T. chilonis parasitized the smallest number of eggs, while T. leucaniae and T. ostriniae exhibited similar parasitic capacities. With 0-d-old host eggs, T. ostriniae developed over the longest time period (8.7 d), and T. leucaniae produced the most female progeny (87.9%). Both T. leucaniae and T. ostriniae had similar developmental times, survival rates and percentages of female progeny with 1–3-d-old eggs. These results show that T. leucaniae can parasitize host eggs at varying ages with the best development and suggest that it may be a valuable biological control agent for soybean pod borers.