Journal of Pest Science

Published by Springer Nature
Online ISSN: 1612-4766
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  • Huifang GuoHuifang Guo
  • Yufeng QuYufeng Qu
  • Shuai SunShuai Sun
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  • Ary A. HoffmannAry A. Hoffmann
Current approaches to controlling plant viral diseases mainly focus on plant resistance, whereas suppression of viruses in vector species could provide an important alternative approach. Here we identified the therapeutic compound, gossypol, as capable of clearing Tomato yellow leaf curl virus (TYLCV) from its vector Bemisia tabaci (whitefly). Our initial field surveys showed that no whiteflies identified from cotton carried TYLCV, in contrast to a high incidence of this virus in whiteflies from other crops including tomato, cucumber and sweet potato. We found that when whiteflies were transferred from tomato or cucumber to cotton, there was a sharp reduction in the number of viruliferous whiteflies. When the whiteflies fed on cotton or ingested the metabolite, gossypol, derived from cotton, there was a sharp decrease in the incidence and abundance of TYLCV carried by the whiteflies. Gossypol degraded the coat protein and viral genome of TYLCV both in vitro and in vivo. Laboratory and field trials all showed that gossypol decreased TYLCV disease severity and had therapeutic efficacy on the disease. Our findings point to the possibility of identifying virus-therapeutic compounds by initially screening viruses in vectors derived from different crop plants.
First-year phenotypic response to the artificial selection of aggressiveness. The red line corresponds to the aggressive line and the blue line to the docile line. The black-dashed line corresponds to the mean aggressiveness value of the initial population. Vertical lines correspond to standard error. Letter a and b refer to the moment where statistical differences appeared between the lines. Artificial selection was conducted at the generation 0 and 1
Second-year phenotypic response to the artificial selection of aggressiveness. The red line corresponds to the aggressive line, the blue line to the docile line, and the green to the non-selected line. The black dashed line corresponds to the mean aggressiveness value of the initial population. Vertical lines correspond to standard error. Letter a, b and c refer to the moment where statistical differences appeared between the lines. Artificial selection was conducted at the generation 0, 2 and 4
In agroecosystems, omnivorous predators are recognized as potential biological control agents because of the numerous pest species they prey on. Nonetheless, it could be possible to enhance their efficiency through artificial selection on traits of economical or ecological relevance. Aggressiveness, which defines the readiness of an individual to display agonistic actions toward other individuals, is expected to be related to zoophagy, diet preferences and to a higher attack rate. The study aimed to assess the aggressiveness degree of the damsel bug, Nabis americoferus, and to estimate its heritability. We hypothesized that a high aggressiveness degree can be selected, and that males are more aggressive than females. Using artificial selection, we reared two separate populations, each composed of nine genetically isolated lines characterized by their different aggressiveness degree (aggressive, docile and non-selected). After three generations, we had efficiently selected aggressive behavior. The realized heritability was 0.16 and 0.27 for aggressiveness and docility in the first population. It was 0.25 and 0.23 for the second population. Males were more aggressive than females only for the second population. The potential of these individuals as biological control agents and the ecological consequences of aggressiveness are discussed.
Number of feces with presence of OBs (± SE) obtained from males and females of E. varians that consumed virus-infected second instars of S. exigua. For each post-infection time, the comparisons of sexes were t = 0.72, df = 18, p = 0.482; t =  −0.42, df = 18, p = 0.68; and t = 0.65, df = 18, p = 0.53 for 24, 48, and 72 h post-infected larvae consumption, respectively
Proportion of virus-induced mortality (± SE) of second instar S. exigua in bioassays of feces of E. varians adults containing OBs of the SeSIN6 isolate at three collection times. Data of both E. varians sexes and collection times followed by the same letter are not significantly different (GLM and LSD test; p > 0.05)
The interaction between the mirid predator Engytatus varians (Distant) and a Mexican isolate (SeSIN6) of Spodoptera exigua multiple nucleopolyhedrovirus (SeMNPV) was examined under laboratory conditions. In a choice test, E. varians females and males demonstrated no preference for virus-infected Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) second instar compared with non-infected at two different post-inoculation times (48 and 72 h). Similarly, prey search time (5–6 h) did not differ significantly for each type of prey. Bioassays were performed to confirm the viability of occlusion bodies (OBs) from predator’s faces collected at 48, 96, and 144 h after exposure to virus-infected S. exigua larvae. The proportion of larval mortality was between 0.20 and 0.62 across all times and both E. varians sexes. Another experiment was performed to evaluate the dispersal of SeSIN6 OBs by physical contact with E. varians adults on tomato (Solanum lycopersicum Miller) leaflets treated with the pathogen. Engytatus varians adults were exposed to OB-treated tomato leaflets during 24 or 48 h using a clip cage. After each exposure time, these adults were removed and placed on clean uncontaminated leaflets for periods of 4–48 h. These leaflets were then exposed to groups of S. exigua second instars in clip cages. The proportion of virus-induced larval mortality of S. exigua (ranging from 0.45 to 1.0) was significantly affected by the duration of exposure of E. varians adults on OB-treated or untreated tomato leaflets. Our results reveal the potential of E. varians as an agent for the dispersal of SeMNPV OBs.
Age-stage-specific survival rate (sxj) of Spodoptera frugiperda reared on the five host plants
Food utilization efficiency parameters for Spodoptera frugiperda third-instar larvae feeding on wheat, maize, pea, faba bean, and alfalfa leaves. A food consumption (FC), B approximate digestibility (AD), C relative consumption rate (RCR), D efficiency of conversion of ingested food (ECI), E relative growth rate (RGR), and F efficiency of conversion of digested food (ECD). Boxplots indicate median (middle line), 25th, 75th quartiles (box), and maximum and minimum values (whiskers). Different letters on the boxplots represent significant differences determined by Kruskal–Wallis nonparametric tests (P < 0.05)
Number of eggs laid by Spodoptera frugiperda female adults on wheat, maize, pea, faba bean, alfalfa plants, and inner cage walls in the choice (Kruskal–Wallis nonparametric, P < 0.05) (A–D) and no-choice tests (Wilcoxon nonparametric, *P < 0.05; ns P > 0.05) (E–I). Boxplots indicate median (middle line), 25th, 75th quartiles (box), and maximum and minimum values (whiskers)
Feeding preference (%) of the (A) first-instar and (B) third-instar larvae of Spodoptera frugiperda for leaves of the wheat versus maize, wheat versus pea, wheat versus faba bean, and wheat versus alfalfa combinations. Numbers on the right side of the bar charts represent the P value determined by Wilcoxon nonparametric tests for the paired samples. P values less than 0.05 were considered statistically significant
Illustration of the potential push–pull strategy for the management of Spodoptera frugiperda in wheat-based intercropping systems, based on the results of this study
The fall armyworm, Spodoptera frugiperda, is one of the most notorious insect pests, and a major threat to maize (Zea mays) and other important crops, such as wheat (Triticum aestivum). Although the push–pull strategy based on intercropping has been reported to effectively prevent damage caused to maize, the potential of wheat-based intercropping systems for S. frugiperda management has rarely been assessed. In this study, the offspring performance, oviposition, and feeding preferences of S. frugiperda on four commonly planted crops—maize, pea (Pisum sativum), faba bean (Vicia faba), and alfalfa (Medicago sativa)—in wheat-based intercropping system were investigated to evaluate the roles of those host plants in the pest management. The results showed that S. frugiperda larvae performed poorly on pea and faba bean plants, as indicated by the longest duration for larval developmental, total pre-oviposition period, and mean generation time as well as the lowest pupal weight and larval survival rate. Lower offspring performance on pea and faba bean leaves coincided with lower efficiency of larval consumption. Preference tests revealed that female adults and larvae exhibited a stronger oviposition on, and feeding preference for maize than wheat, whereas no-preference was observed for faba bean plants. This study revealed the adaptability of S. frugiperda and its preference for wheat and its four common intercropped host plants and provided an insight into the management of S. frugiperda through the establishment of a push–pull strategy in wheat-based intercropping systems.
Immature survival (mean ± SE) of P. ubiquitus and H. anconai on three diets (T. angustifolia pollen, A. lycopersici and A. lycopersici + pollen) on tomato leaf disks at 25 ± 0.5 °C and 65 ± 5% RH. Different letters above bars indicate significant differences among treatments (contrasts after GLM, p < 0.05)
Effect of P. ubiquitus without a or with b pollen and H. anconai without c or with d pollen on the population dynamics of A. lycopersici (mean number of tomato russet mite (TRM) eggs and immatures ± SE) over a five-days period at 25 ± 0.5 °C and 65 ± 5% RH on tomato leaf disks. Different lowercase and uppercase letters denote significant differences among TRM eggs and TRM immatures treatments, respectively (contrasts after GLM, p < 0.05)
Total number of A. lycopersici adults killed (mean ± SE) over a five-day period by P. ubiquitus and H. anconai on tomato leaf disk with tomato russet mites alone (A. lycopersici) or in combination with T. angustifolia pollen (A. lycopersici + pollen) at 25 ± 0.5 °C and 65 ± 5% RH. Different letters denote significant differences among treatments (contrasts after GLM, p < 0.05)
Total number of eggs (mean ± SE) laid over a five-days period by P. ubiquitus and H. anconai on tomato disks when fed with tomato russet mite alone (A. lycopersici) or in combination with T. angustifolia pollen (A. lycopersici + pollen) at 25 ± 0.5 °C and 65 ± 5% RH. Different letters denote significant differences among treatments (contrasts after GLM, p < 0.05)
Two iolinid predatory mites were studied in the laboratory as potential biological control agents of the tomato russet mite, Aculops lycopersici (Acari: Eriophyidae). The development, reproduction and predation capacity of Pronematus ubiquitus and Homeopronematus anconai (Acari: Iolinidae) on A. lycopersici were investigated. Developmental time from egg to adult at 25 °C averaged 9.59, 9.31 and 9.52 days for P. ubiquitus on A. lycopersici, A. lycopersici and Typha angustifolia pollen, and pollen only, respectively. H. anconai required 11.18, 10.39 and 11.90 days to complete development on the respective diets. Survival of the immature stages exceeded 83% on all diets for both iolinids. In experimental arenas, both predators caused a substantial reduction of the immature population development of A. lycopersici. The number of tomato russet mite offspring was reduced by 78% and 57% by P. ubiquitus and H. anconai, respectively. The addition of pollen to the arena lowered this population reduction to 35% and 27% for the respective predators. However, supplementing a diet of tomato russet mites with pollen significantly increased the fecundity of both predatory mites from 14–15 to 24–25 eggs over a five-day period. The results suggest that both P. ubiquitus and H. anconai have good potential to suppress A. lycopersici populations and that T. angustifolia pollen can support population establishment of the predators. Overall, P. ubiquitus developed faster on the three diets tested and suppressed A. lycopersici stronger as compared to H. anconai, with or without pollen as a supplementary food source.
The use of CRISPR/Cas9 system in model insects has facilitated functional genomics studies. However, this system has not been applied to many pest insects. Here, we report on the establishment of multiple transgenic CRISPR/Cas9-based genome editing methods in a global agricultural pest, the fall armyworm (FAW), Spodoptera frugiperda. To identify fluorescent proteins suitable for screening for transgenic FAW, nine transgenic lines expressing genes coding for fluorescent proteins under the control of different promoters were produced and evaluated. The enhanced green fluorescent protein and a red fluorescent protein, tdTomato genes driven by the hr5ie1 promoter were found to be suitable for the identification of transgenic FAW. Multiple lines of transgenic FAW expressing Cas9 were generated and microinjection of sgRNAs into the embryos of these lines failed to induce target gene knockout. To overcome this problem, sgRNAs were expressed in FAW using U6-sgRNA and U6-tRNA-sgRNA systems, U6-tRNA-sgRNA system was found to be more efficient than U6-sgRNA system. Expression of Cas9 and sgRNAs in the same transgenic animal or in two separate strains followed by crossing them to bring Cas9 and sgRNA together resulted in an efficient knockout of target genes. The multiple transgenic CRISPR/Cas9-based genome editing methods developed provide invaluable tools for gene editing and functional genomics studies in this global pest and other lepidopteran pests.
Visual summary of the experimental procedure. Grapevine inflorescences from the Geisenheim VineyardFACE were incorporated into artificial diet. Lobesia botrana larvae were raised on the respective diets and stanrard artificial diet as control. Eggs produced by the respective adults were then parasitized by Trichogramma cacoeciae
Size of eggs (length in mm) laid by Lobesia botrana adults that were raised on standard artificial diet (SAD) or grapevine-based artificial diet (GAD) containing inflorescences of the cultivar Riesling or Cabernet Sauvignon, cultivated at ambient (ca. 400 ppm) or elevated (ca. 480 ppm) CO2 concentrations in the Geisenheim VineyardFACE. Identical letters indicate that no significant differences were detected (GLM, Tukey contrasts; N = 600)
Lobesia botrana larval emergence rate from eggs A without or B with parasitoids present. Eggs were produced after feeding on standard artificial diet (SAD) or grapevine-based artificial diet (GAD) containing inflorescences of the cultivar Riesling or Cabernet Sauvignon, cultivated at ambient (ca. 400 ppm) or elevated (ca. 480 ppm) CO2 concentrations in the Geisenheim VineyardFACE. Identical letters indicate that no significant differences were detected. ns: not significant (GLM, Tukey contrasts; N = 80)
Parasitism rate A and emergence rate B of Trichogramma cacoeciae on Lobesia botrana eggs produced after larval feeding on standard artificial diet (SAD) or grapevine-based artificial diet (GAD) containing inflorescences of the cultivar Riesling or Cabernet Sauvignon, cultivated at ambient (ca. 400 ppm) or elevated (ca. 480 ppm) CO2 concentrations in the Geisenheim VineyardFACE. Different letters indicate that significant differences were detected (GLM, Tukey contrasts; N = 80)
Size of Lobesia botrana eggs (length in mm), parasitized or not parasitized by Trichogramma cacoeciae, that were produced after larval feeding on either A grapevine-based artificial diet containing inflorescences from the Geisenheim VineyardFACE (data were pooled over the two cultivars and CO2 concentrations) or on B standard artificial diet. For details on diets, see Table 1. Different letters indicate that significant differences were detected. (GLM, Tukey contrasts; on grapevine-containing diet: eggs parasitized = 465, not parasitized = 1965, on standard artificial diet: eggs parasitized = 381, not parasitized = 740)
Climate change can affect biological pest control by altering trophic interactions. Elevated carbon dioxide (CO2) concentrations can reduce host plant quality and, in turn, alter herbivore and natural enemy preference and performance. Using the Geisenheim VineyardFACE (free-air carbon dioxide enrichment) facility, we studied plant- and herbivore-mediated bottom-up effects of elevated CO2 concentration on the European grapevine moth, Lobesia botrana, and the parasitoid Trichogramma cacoeciae. Grapevine inflorescences of two cultivars cultivated at ambient or elevated CO2 (aCO2 and eCO2: 400 and 480 ppm) in the VineyardFACE were incorporated into L. botrana artificial diet. Eggs laid by the respective adults were parasitized by T. cacoeciae. Egg size and emergence rate of L. botrana as well as parasitism rate, parasitoid emergence rate and egg size preference of T. cacoeciae were evaluated. We observed an indirect grapevine cultivar-dependent bottom-up effect of CO2 on both herbivore and egg parasitoid. Compared to aCO2, eCO2 resulted in larger host eggs and higher parasitism rates regarding Riesling-feeding but not regarding Cabernet Sauvignon-feeding L. botrana larvae. Parasitoid emergence rate was higher when L. botrana had fed on Riesling compared to Cabernet Sauvignon-diet. Egg size preference depended on the host’s diet: T. cacoeciae preferred larger L. botrana eggs when the larvae had fed on grapevine-containing diet but not when they fed on standard artificial diet. Our results highlight the importance of the host’s diet for the parasitoid’s preference and performance. They furthermore suggest that the future efficiency of L. botrana-biocontrol by T. cacoeciae will not decrease under elevated CO2 concentrations.
Functional response on different prey (rows) offered to one female from different Orius laevigatus selected and reference populations (columns). The data points and solid fitted lines represent the number of prey killed and the predictions of the Holling’s (1959) model, respectively
Augmentative biological control in protected crops relies mainly on omnivorous predators. Their performance as biological control agents (BCA) depends on several characteristics of the species, which in turn may differ among strains within a species. We have recently reported the achievement of two Orius laevigatus (Hemiptera: Anthocoridae) strains showing a significant larger body size or better fitness when feeding on pollen, two characteristics having a key impact on field performance. However, selection towards a specific trait might result in trade-offs, such as reduced predation capacity, which may impair control efficiency. Therefore, the predation capacity of these selected populations was tested in laboratory as a first step prior to its field use. Functional response to different densities of Frankliniella occidentalis (Thysanoptera: Thripidae) (adults and larvae) and Myzus persicae (Hemiptera: Aphididae) (nymphs) were studied in the large-sized and pollen-tolerant O. laevigatus strains in comparison with commercial and wild populations. A type-II functional response was observed regardless of the population. Body size was significantly related to thrips but not to aphid predation. The large-sized strain showed a superior predation capacity, both on thrips larvae and especially on adult thrips, although not on aphids. Therefore, the larger body size of the selected strain may increase its effectiveness as BCA of thrips. Regarding the pollen-tolerant strain, no trade-offs were observed in predation rates on adults or larvae of thrips, but it showed higher predation capacity on aphid nymphs, suggesting an expanded prey range. Implications of such enhanced biocontrol services on crop protection are also discussed.
Effect of ethanol concentration (A) and ambrosia beetle species (B) on total number of entry holes per potted tree. Ad = Anisandrus dispar; Xs = Xyleborinus saxesenii; Xc = Xylosandrus crassiusculus; Xg = Xylosandrus germanus. Means with the same letter are not significantly different using Tukey’s HSD test
Effect of ethanol concentration on the number of entry holes per potted tree by A. dispar (A), X. saxesenii (B), X. crassiusculus (C), and X. germanus (D). Means with the same letter are not significantly different using Tukey’s HSD test
Effect of ethanol concentration on the number of galleries bored with and without offspring per potted tree for A. dispar (A), X. saxesenii (B), X. crassiusculus (C), and X. germanus (D). Means with the same letter are not significantly different using Tukey’s HSD test
Effect of ethanol concentration on the mean amount of sawdust and offspring produced per caged female in A. dispar (A, B), X. saxesenii (C, D), X. crassiusculus (E, F), and X. germanus (G, H). Means with the same letter are not significantly different using the pairwise Wilcoxon test
Total number of galleries recorded per each class considered in this study and total number of larvae, pupae and adults (not counting the foundress) obtained for each beetle species. The latter values represent the sum of offspring emerged and found within the gallery
Ambrosia beetles (Coleoptera; Curculionidae; Scolytinae and Platypodinae) can cause severe damage to trees growing in plant nurseries, orchards and natural forests. Ethanol is emitted by stressed trees and represents an important cue used by ambrosia beetles to locate suitable hosts to infest. Ethanol also favors the growth of ambrosia beetles' nutritional fungal symbionts and suppresses the growth of antagonistic fungi. An optimal concentration of ethanol in host tissues might maximize fungal growth and offspring production, but it is unclear if this optimal concentration varies among ambrosia beetle species. To investigate this mechanism, we injected five different concentrations of aqueous ethanol solution (5%, 25%, 50%, 75% and 90%) into the stems of container-grown oak trees, Quercus robur L. Modified Falcon tube chambers were used to confine four species of field-collected ambrosia beetles to the injected stems, namely, Anisandrus dispar, Xyleborinus saxesenii, Xylosandrus germanus, and Xylosandrus crassiusculus. Incidence of boring, ejected sawdust, gallery development , and offspring production were then quantified. The incidence of boring generally increased with increasing ethanol concentration for all four Scolytinae species tested. Ejected sawdust and offspring production increased with increasing ethanol concentration up to 90% for A. dispar and X. saxesenii; by contrast, an increasing trend up to 75% ethanol followed by a decrease at 90% ethanol was associated with X. germanus and X. crassiusculus. Our study highlights the key role of ethanol for ambrosia beetles, and showed that the optimal concentration maximizing colonization and offspring production can vary among species.
Oviposition by surviving females every three days after emergence by Nesidiocoris tenuis on Verbena × hybrida (V-F, verbena with flowers; V-FL, verbena without flowers) and on Scaevola aemula (S-F, scaevola with flowers; S-FL, scaevola without flowers) with and without flowers. Number of oviposited eggs was estimated from the number of hatched nymphs
Female survival of Nesidiocoris tenuis of every 3 days after emergence on Verbena × hybrida and on Scaevola aemula with and without flowers. Legends for different lines are as in Fig. 1
Amount of the three types of sugars included in the nectar of ten flowers sampled for Verbena × hybrida (verbena) and Scaevola aemula (scaevola). Statistical significance is shown (Mann–Whitney U test): *** indicates P < 0.001
Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) is a zoophytophagous mirid that can also feed on the plants upon which its prey lives. It is a generalist predator feeding on whiteflies, thrips, aphids, and other pests. The use of alternative plants as banker plants is recommended to aid the establishment of released natural enemies in greenhouses. If N. tenuis populations reproduce only on banker plants, the use of alternative hosts or prey to rear N. tenuis will be unnecessary, which makes the banker plant system easier to manage. Verbena × hybrida Voss (Lamiales: Verbenaceae) cv. Tapien and Scaevola aemula R. Br. (Asterales: Goodeniaceae) are recommended banker plants in Japan. This study examined the development, survival, and oviposition of N. tenuis on these two plant species in the laboratory, with and without flowers. N. tenuis performed similarly on both plants. The intrinsic rate of increase was slightly higher on Verbena × hybrida than S. aemula. The sugars in water samples collected from flowers of both plant species were analyzed using high-performance liquid chromatography. Fructose and glucose were detected in Verbena × hybrida, while fructose, glucose, and sucrose were detected in S. aemula. The total amount of sugars per ten flowers was much higher in Verbena × hybrida. These sugars, possibly derived from floral nectars, are considered as nutrients promoting the reproduction of N. tenuis, in addition to pollen. Verbena × hybrida and S. aemula both facilitate N. tenuis reproduction and can be used as banker plants.
(A) Number of mirids per tomato plant + SE in greenhouses compartments with four different treatments: (1) B. tabaci releases -Control; (2) B. tabaci + D. argensis releases; (3) B. tabaci + D. argensis + calabash as companion plant; and (4) B. tabaci + N. tenuis releases. (B) Number of D. argensis per plant + SE in calabash
(A) Number of mirids per tomato leaf + SE in greenhouses compartments with four different treatments: (1) B. tabaci releases -Control; (2) B. tabaci + D. argensis releases; (3) B. tabaci + D. argensis + calabash as companion plant; and (4) B. tabaci + N. tenuis releases. (B) Number of D. argensis per leaf + SE in calabash
(A) Proportion of aborted flowers + SE in tomato plants in greenhouses compartments with four different treatments: (1) B. tabaci releases -Control; (2) B. tabaci + D. argensis releases; (3) B. tabaci + D. argensis + calabash as companion plant; and (4) B. tabaci + N. tenuis releases. (B) Number of necrotic rings per tomato leaf + SE in the same four treatments as in graph A
(A) Number of whitefly nymphs per tomato leaf + SE in greenhouses compartments with four different treatments: (1) B. tabaci releases -Control; (2) B. tabaci + D. argensis releases; (3) B. tabaci + D. argensis + calabash as companion plant; and (4) B. tabaci + N. tenuis releases. (B) Number of whitefly adults per tomato leaf + SE in the same four treatments as in graph A
Number of whitefly nymphs and adults per leaf + SE in calabash plants
The plant matrix influences the performance of omnivorous mirids as biocontrol agents and increasing plant diversity has been hypothesised to enhance pest control. This research aimed to determine the effect of using calabash, Lagenaria siceraria, as a companion plant on the population dynamics and whitefly control efficacy of Dicyphus argensis in tomato greenhouses. The response of D. argensis was also compared with that of Nesidiocoris tenuis. Four treatments were assayed in a complete randomised block design with three replicates each: (1) Bemisia tabaci, (2) B. tabaci + D. argensis, (3) B. tabaci + D. argensis + calabash and (4) B. tabaci + N. tenuis. Calabash harboured high populations of D. argensis, but its abundance on tomato plants was significantly lower in the presence of calabash than in its absence, and in both treatments, it reached lower numbers than N. tenuis. Dicyphus argensis reduced the whitefly density on tomato plants relative to the compartments with no mirids, but the whitefly density was higher in the presence of companion plants, and N. tenuis was more effective in reducing whitefly populations. Calabash served as a host for the multiplication of whitefly and increased the pest density on tomato. In this research, increasing plant diversity in crops did not enhance pest control because: (1) the aggregation of D. argensis in calabash reduced its abundance in tomato plants; (2) the pest populations multiplied. This contrasts with the diversity hypothesis and confirms the importance of the plant context for predatory dicyphines.
Development of buprofezin resistance in BPH populations in China from 1996 to 2020
Genetics of buprofezin resistance in BPH
Genetics and mapping of buprofezin resistance in BPH
Location of the chs mutation and positive correlation of mutation frequency and resistance ratio
Fitness analysis and locomotion of adults among different Drosophila lines
Development of insecticide resistance in insect populations is a major challenge to sustainable agriculture and food security worldwide. Buprofezin, one of the commonly used chitin synthesis inhibitors, has severely declined its control efficacy against the brown planthopper (BPH, Nilaparvata lugens), a devastating rice insect species. To date, however, mechanism of buprofezin resistance in target pests remains elusive. We conducted a long-term (25 years from 1996 to 2020) and large geographical scale (11 provinces and cities in China) resistance monitoring program for buprofezin in BPH, a notorious pest of rice crop in East and Southeast Asia. BPH rapidly developed resistance with > 1,000-fold resistance being detected in nearly all the field populations after 2015. Using the bulk segregant mapping method, we uncovered a novel mutation (G932C) in chs1 gene encoding chitin synthase 1 from a near isogeneic buprofezin-resistant (> 10,000-fold) strain harboring recessive, monogenic resistance. Using CRISPR/Cas9-based genome-modified Drosophila melanogaster possessing the same mutation as a model, we found that the G932C mutation was not only responsible for buprofezin resistance but also conferred a cross-resistance to cyromazine, an insect molting disruptor, on which the mode of action is largely unknown. Taken together, our study for the first time revealed the molecular mechanism conferring buprofezin resistance in BPH and implicated that cyromazine also targets chitin biosynthesis to confer its toxicity.
The oviposition behavior of Orius sauteri on leaves of tomato (a), cucumber (b), and cowpea (c) plants. The images were captured at 50X magnification under a digital microscope (VHX-6000, Keyence, Japan)
Survival rate of Frankliniella occidentalis (a, b, and c) and Bemisia tabaci (d, e, and f) at 24 and 48 h on three plant species inoculated with Orius sauteri. Data in the figure are means ± SE. Significant differences based on Student’s t-test are marked with asterisks (*P < 0.05; **P < 0.01; ns, not significant)
Number of F1 nymphs of Frankliniella occidentalis (a) and the number of eggs of Bemisia tabaci (b) reared on three plant species inoculated with Orius sauteri. Data in the figure are means ± SE. Significant differences based on Student’s t-test are marked with asterisks (*P < 0.05; **P < 0.01; ***P < 0.001; ns, not significant)
Oviposition number, F1 nymph number, and hatching rate of Orius sauteri on three plant species. (a) Number of eggs of O. sauteri within each plant and each pest treatment combination. (b) Number of F1 nymphs of O. sauteri within each plant and each pest treatment combination. (c) Hatching rate of O. sauteri within each plant and each pest treatment combination. Data in the figure are means ± SE. Different letters indicate significant differences (P < 0.05)
Exploring the interactions between host plants, herbivores, and natural enemies is an important experimental approach for enhancing biological control. Induced plant defense responses following infestation by herbivores enable plants to minimize damage. Orius sauteri (Poppius), an important generalist predator, has been widely used as a biological control agent for suppressing many agricultural pests on agronomic and horticultural crops. Because this predator oviposits and feeds on plant tissue, in this work we hypothesized that these behaviors can induce defenses that modulate the subsequent pest attack. For this, we explored the fitness parameters of two key pests, the western flower thrips Frankliniella occidentalis (Pergande) and the tobacco whitefly Bemisia tabaci (Gennadius), on three different O. sauteri-pre-inoculated plant species, tomato, cucumber, and cowpea when compared to non-pre-inoculated plants. Pre-inoculation of O. sauteri on these three plant species decreased the performance of both herbivore pests but to differing degrees. The survival of F. occidentalis on tomato and B. tabaci on cowpea was significantly reduced on O. sauteri-pre-inoculated plants compared to non-inoculated plants. The reproduction of B. tabaci on tomato, cucumber, and cowpea was decreased in varying degrees by the pre-release of O. sauteri, whereas in the case of F. occidentalis the reproduction was only reduced on tomato and cucumber pre-inoculated plants. These results further enhance our knowledge of ecological relationships between natural enemies and herbivores and provide the context for the early release of natural enemies to control pests.
Synthetic pesticides used to control Solenopsis invicta Buren (Hymenoptera: Formicidae) can negatively affect human and environmental health due to non-target toxicity and long-lasting residues. Plant essential oils may have lower human health impacts and environmental toxicity. They can be an excellent source of pesticides because of their exceptional repellency and insecticidal properties. In this study, we used the fumigation method to study the insecticidal properties of essential oils from the bark and leaves of Cinnamomum loureirii Nees on S. invicta at different concentrations and fumigation time. The fumigation time with C. loureirii essential oils was positively correlated with the knockdown and mortality of S. invicta and negatively correlated with the grasping. The essential oils at 320 µg/cm³ had a noticeable fumigation effect. The insecticidal effect of the essential oils extracted from C. loureirii leaves was significantly stronger than that from the bark at effective concentrations. Cinnamyl acetate, an abundant component in leaf essential oils, plays a vital role in increasing the insecticidal effect of trans-cinnamaldehyde. The treatment of the mixed trans-cinnamaldehyde and cinnamyl acetate in a 2:1 ratio had the best insecticidal effect (at 50 and 25 µg/cm³, respectively) and more apparent electroantennogram change than the individual compounds. Essential oils caused disorganization and shedding of the antennae morphology and receptors that led to the death of S. invicta. This study provides a basis for developing and utilizing cinnamon leaf oil as a new environment-friendly insecticide resource to control S. invicta. Graphical abstract
Entomologists have often used computational modeling to study the dynamics of insects in agricultural landscapes. Recently, important issues such as the movement of adults and immatures associated with insect resistance to GMO (genetically modifed organism) crops have been addressed using computational models. We developed an individual-based model using the cellular automata approach (CA) to investigate how an intercropping system composed of maize engineered with Bacillus thuringiensis (Bt) gene, refuge areas (non-Bt maize), and grasses combined with of-season periods might infuence the evolution of resistance in Spodoptera frugiperda (Lepidoptera: Noctuidae), one of the leading agricultural pests targeted by GMOs. We designed the Bt and non-Bt plants in two diferent arrangements: (a) a seed mixture and (b) strips rows, adding grasses in areas adjacent to the feld. We added the seasonal planting dynamics (crop season and of-season), to evaluate a total of six agricultural scenarios. We followed a crop calendar from the United States to create simulations close to agricultural practice. The results showed that the frequency of the resistance allele was strongly related to the landscape arrangements and their dynamics. Since the adult insects are mobile, the seed-mixture scenario increased the frequency of the resistance the most (95.86%), followed by strips (82.10%), without grass felds. The maize harvest made it possible to reduce the frequency of resistance allele below 1%. Based on our results, we can expect that the maintenance of pasture areas, for instance next to the corn crops, will act as a reservoir of susceptible insects during of-season periods.
Cowpea ( Vigna unguiculata ) is one of the most important crops in semiarid areas of the world, where it thrives in hot, dry conditions. While cowpea is able to withstand abiotic stresses, it suffers serious losses from biotic antagonists, including infestation by the cowpea aphid ( Aphis craccivora ). Cowpea aphid infestations are highly destructive, especially on young plants. However, it is unclear whether cowpea aphid damage is the result of aphids having phytotoxic effects on their hosts, or simple density effects. To better understand cowpea aphid damage and the potential for resistance traits to mitigate aphid impacts, we evaluated phenotypic changes in cowpea in response to variable aphid densities and systemic versus local infestations. Low aphid densities induced leaf distortions and pseudogalling, suggesting that cowpea aphids are phytotoxic to cowpea. Resistance to the cowpea aphid has been previously identified in an African cowpea germplasm, and near isogenic lines (NILs) containing resistance quantitative trait loci (QTL) were generated in the California blackeye cultivar background. Using a series of performance assays, we determined that resistance conferred by the two QTL counteracts aphid phytotoxicity and severely limits aphid growth and fecundity. Using choice assays, a preference by cowpea aphids for the susceptible NIL was observed. Electrical penetration graph analysis revealed that the resistance phenotype includes weak surface level deterrence and strong phloem-based resistance that manifests during the sap ingestion phase. Our study provides evidence of phytotoxic traits in A. craccivora while identifying a viable means of counteracting aphid damage and reproductive potential through resistance.
Log dose-response of ACP adults treated by topical application for a 2-Methoxy-4-propylphenol 2M4P, b Sucrose fatty acid ester SFAE, c Pyrethrum extract and d Fenpropathrin. Mortality was measured at 1 h, 24 h and 48 h after treatment. Each point represents the mean (± SE) mortality measured at each concentration in at least 3 independently-conducted bioassays. The apparent ‘recovery’ of insects after 1 h counts, which was consistent between bioassays, particularly for pyrethrum and fenpropathrin, was due to the deviation of % mortality from a combination of affected and dead insects. At 24 h, many of the affected insects had recovered from the initial knockdown. The dotted line on each graph represents the 50% mortality level. The legend shown in figure 1a applies to all graphs.
Box and whiskers graph showing ACP mortality caused by four treatments at different times after treatment (DAT). Adult mortality was measured on lemon plants. Different letters between treatments on each assessment day are significantly different (P < 0.05) according to Friedman’s tests.
The Asian citrus psyllid (ACP), Diaphorina citri, Kuwayama (Hemiptera: Liviidae), is the vector of Candidatus Liberibacter asiaticus and Ca. Liberibacter americanus, both associated with Huanglongbing, the most destructive disease of citrus worldwide. ACP control mainly depends on the use of synthetic insecticides. However, the dependence on and overuse of synthetic insecticides can lead to insecticide resistance, adverse environmental effects. Due to this, as well as consumer demand for organic food and changing regulations, there is an urgent need to develop additional and more sustainable methods of control. Fatty acid-based and phenolic biopesticides derived from lignocellulosic biomass could be safe and inexpensive alternatives to synthetic insecticides. Thus, the objective of this work was to study the toxicity of two novel, naturally derived molecules—sucrose fatty acid ester (SFAE) and 2-methoxy-4-propylphenol (2M4P)—to ACP, and compare them with fenpropathrin and pyrethrum extract. Mortality of adult psyllids (3-7 days old) exposed to SFAE, 2M4P, the pyrethrum extract and fenpropathrin in topical application bioassays were compared at 1, 24 and 48 h post-treatment at different doses. Mortality of adults exposed to SFAE, 2M4P and the pyrethrum extract were also compared in whole plant assays under greenhouse conditions. In the topical bioassays all compounds worked rapidly against ACP, with the natural and synthetic pyrethroids showing significantly more toxicity than SFAE and 2M4P. Under greenhouse conditions, mortality caused by 2M4P was the highest, followed by the pyrethrum extract. Mortality caused by SFAE was not significantly different when compared to the control.
Bacillus thuringiensis (Bt), an effective entomopathogen, has been widely used for pest control. However, insect resistance risk threatens the sustainable utility of Bt products. Previous findings suggest the interactions between gut microbiota and the host probably influence the evolution of insect resistance. To understand how the microbiota affects the development of insect resistance and manage the resistance, we characterized the gut microbiota of Chilo suppressalis from five Bt-resistant or Bt-susceptible strains by 16S rRNA sequencing. The diversity, richness, and composition of gut microbial community were analyzed among these five strains by alpha and beta analyses. Gut microbiota diversity was significantly higher in Bt-resistant (BJ1Ab-R and FZ1Ca-R) than that in Bt-susceptible strains (BJ-S and FZ-S). A significantly higher abundance of the genus Enterococcus were found in BJ-S- and FZ-S-susceptible strains than that in BJ1Ab-R- and FZ1Ca-R-resistant strains. The genus Bifidobacterium significantly dominated in the FZ1Ca-R-resistant strain, compared with the other four strains. Moreover, the gut microbial community displayed significantly more complex cooccurrence patterns in Bt-resistant than in Bt-susceptible strains by network analysis. Furthermore, the BJ-S, FZ-S and FZ1Ca-R strains had significantly reduced larval mortalities in bioassays with Bt toxin after larval pretreatment with antibiotics to remove gut bacteria. This study suggests that the gut microbiota participates in regulating the Bt-induced killing mechanism in C. suppressalis, and provides insights into the impact of Bt selective pressure on microbiome composition and potential insect resistance induced by microbiome alterations. Graphical abstract
Sampling localities of putative Planococcus ficus populations. Mealybugs were collected from 23 localities distributed along the 6 main vineyard regions in Egypt namely, Marsa Matrouh (MM), West of Nobaria (WN), Elbostan (EB), Menouf (MF), Elkhatatba (EK), and Giza (GZ)
Haplotype distribution and population structure in Planococcus populations from Egypt. A) Median-joining network showing the genetic distance and geographic distribution of the 19 haplotypes found in the present study. B) Main genetic barriers (i and ii, highlighted in red) obtained from the Monmonier’s maximum distance algorithm as implemented in BARRIER
Neighbor-Joining tree and histogram of genetic distances. A Phylogenetic tree revealing the genetic relationships between the 19 haplotypes found in this work and data from previous studies. B Genetic distance observed (i) Within species, (ii) Between species, and (iii) Between different groups of species. Note the presence of the so-called “Barcoding gap”
Adult female of Planococcus ficus (Signoret)
(Adapted from Cox 1989 and Ezzat and McConnell 1956)
Adult female of Planococcus vitis (Niedielski)
(Adapted from Ezzat and McConnell 1956)
Mealybugs (Hemiptera: Coccomorpha: Pseudococcidae) constitute important agricultural pests that often require control measures. Different mealybug taxa might, however, react differently to natural enemies and pesticides so that appropriate control measures against mealybugs rely heavily on the correct species identification. The mealybug Planococcus ficus (Signoret) is the most damaging scale insect infesting vineyards worldwide. Despite its economic impact, the taxonomic status of this mealybug species is still unclear, and recent studies suggest the possibility that P. ficus from eastern (i.e., Egypt) and western (i.e., France) Mediterranean regions may correspond in fact to two distinct species. The purpose of this work was to deepen our current knowledge of putative P. ficus from eastern Mediterranean using molecular tools and morphological analysis and test for the existence of cryptic species within P. ficus. Mealybug samples were collected from Egyptian vineyards to better characterize the genetic diversity and analyze the population structure of putative P. ficus along the eastern Mediterranean. We also estimated the phylogenetic relationships among the P. ficus complex haplotypes in different vineyard regions worldwide and analyzed the morphological characters of the different clades obtained. Morphological and molecular analyses confirmed the existence of two species: P. ficus (Signoret) s.str. and P. vitis (Niedielski), a species that was previously synonymized as P. ficus. These results have direct implications for pest management and could explain the lack of success in previous implementations of biological control programs against this pest in several vineyard regions.
Timeline for the assessments performed during the experiments in 2020 (second timeline) and 2021 (first timeline)
Total abundance (mean ± SE) of the different developmental stages of Nesidiocoris tenuis in the four experimental greenhouses 2020 (2020A and 2020B) and 2021 (2021A and 2021B)
Percentage (mean ± SE) of first to third instars of Nesidiocoris tenuis cultivar compared to the total population in the experimental greenhouse. Sample size n = 30 for each bar. Bars sharing the same letter are not statistically different at P > 0.05 (Pair-wise post hoc tests with package “Emmeans” in R)
Percentage (mean ± SE) of necrotic rings caused by Nesidiocoris tenuis per cultivar compared to the total number of necrotic rings in the experimental greenhouse. Sample size n = 30 for each bar. Columns sharing the same letter are not statistically different at P > 0.05 (Pair-wise post hoc tests with package “Emmeans” in R)
Flower abortion (percentage) per cultivar (Error bars indicate 95% confidence intervals) in the presence or absence (control) of Nesidiocoris tenuis. Sample size n = 2 in the control cages and n = 3 in the N. tenuis cages per bar. Asterisks above columns denote statistically significant differences at * = P < 0.05, ** = P < 0.01, *** = P < 0.001) (Pair-wise post hoc tests with package “Emmeans” in R)
The predatory bug Nesidiocoris tenuis (Hemiptera: Miridae) is the cornerstone of Integrated Pest Management (IPM) in greenhouse tomatoes in southern Europe. N. tenuis can also feed on the plant causing necrotic rings, flower abortion and punctured fruits. Thus, its role as biocontrol agent is controversial. Especially in Northern Europe, where N. tenuis has invaded recently, N. tenuis is considered a pest. Despite the importance of N. tenuis in Northern Europe, there is no information about the damage it may inflict on commercial tomato varieties. Thus, in this study, we evaluated the preference and plant damage caused by N. tenuis on twenty-one commercially available tomato cultivars. N. tenuis showed preference for certain tomato varieties. Higher N. tenuis populations on the plants resulted in more necrotic rings. A clearer distinction between the different tomato cultivars was the sensitivity for flower abortion. We observed that small fruit cultivars (cherry, plum) were more susceptible to suffering flower abortion compared to larger fruit-bearing cultivars (truss, beef) because of N. tenuis feeding. Interestingly, we identified tomato cultivars that supported high population densities of N. tenuis without suffering flower abortion. Analyses of plant nutrients suggest that the damage (percentage of necrotic rings) inflicted by N. tenuis was negatively associated with the amount of total sugars, sodium, chloride, sulphur and copper and positively associated with nutrients such as potassium, calcium, phosphorus and magnesium. The new insights provided herein about the interaction between N. tenuis and plant damage are relevant for growers, IPM consultants and plant breeders.
Halyomorpha halys (Stål, 1855), the brown marmorated stink bug (BMSB), is an invasive species that has become a key agricultural pest in its invaded range. Commercial traps available for BMSB monitoring rely on male produced aggregation pheromones as lure, with two possible shortcomings: trap spillover and low detection precision. In this study, we assessed if vibrational signals can increase the attractiveness of pheromone traps by testing the optimized vibration-based lure (Female Song 2, FS2) associated with a specifically designed trap (i.e., the vibrotrap). We evaluated the efficacy of this bimodal trap (i.e., pheromones + vibrations) on females, males and nymphs in controlled conditions (greenhouse) and in the field, in two sites at the margin of two commercial vineyards. In the field, bimodal vibrotraps were compared to three unimodal (i.e., only pheromone) trap types. Both experiments showed that the vibrotrap is highly attractive for BMSB, and the optimized FS2 signal significantly improved its effectiveness. Even though FS2 was selected to target males, the number of trapped females increased as well. Overall, the presented findings show a feasible improvement to future commercial BMSB traps through the synergic use of semiophysicals and semiochemicals. Further research is needed to evaluate the effectiveness of vibrotraps for both early detection and mass trapping.
Fall armyworm (FAW) Spodoptera frugiperda (J.E. Smith) is becoming an invasive pest globally, and it causes significant yield losses in sorghum (Sorghum bicolor (L.) Moench) and maize (Zea mays L.). In this study, we demonstrated that sorghum and maize flavonoids affect survival of FAW larvae. Larvae reared on an artificial diet supplemented with sorghum flavonoids showed significant mortality and decreased body weight. When sprayed on leaves of susceptible maize lines, flavonoid extract effectively reduced the growth and increased the mortality of FAW larvae. As FAW is a major pest of maize, we further investigated the larval mortality when reared on maize lines overproducing flavonoids compared to their near-isogenic wild-type lines. The detached leaf assays showed significantly high mortality of larvae that were fed on flavonoid producer lines compared to wild type. The peritrophic membrane that protects the midgut was severely damaged in larvae fed on leaves of flavonoid producer lines compared to wild type. The effectiveness of the flavonoids as feeding deterrents by endogenous expression and exogenous application demonstrates the eco-friendly potential for the management of FAW larvae.
Beekeepers have various options to control the parasitic mite Varroa destructor in honey bee colonies, but no empirical data are available on the methods they apply in practice. We surveyed 28,409 beekeepers maintaining 507,641 colonies in 30 European countries concerning Varroa control methods. The set of 19 different Varroa diagnosis and control measures was taken from the annual COLOSS questionnaire on honey bee colony losses. The most frequent activities were monitoring of Varroa infestations, drone brood removal, various oxalic acid applications and formic acid applications. Correspondence analysis and hierarchical clustering on principal components showed that six Varroa control options (not necessarily the most used ones) significantly contribute to defining three distinctive clusters of countries in terms of Varroa control in Europe. Cluster I (eight Western European countries) is characterized by use of amitraz strips. Cluster II comprises 15 countries from Scandinavia, the Baltics, and Central-Southern Europe. This cluster is characterized by long-term formic acid treatments. Cluster III is characterized by dominant usage of amitraz fumigation and formed by seven Eastern European countries. The median number of different treatments applied per beekeeper was lowest in cluster III. Based on estimation of colony numbers in included countries, we extrapolated the proportions of colonies treated with different methods in Europe. This suggests that circa 62% of colonies in Europe are treated with amitraz, followed by oxalic acid for the next largest percentage of colonies. We discuss possible factors determining the choice of Varroa control measures in the different clusters.
Oviposition preferences a the number of egg masses; b the number of eggs of Ostrinia furnacalis female moths for each maize plant in the control and Beauveria bassiana-inoculated treatments. Values are means ± S.E. (n = 10). Different small letters above bars indicate significant differences between the control and inoculated maize plants (p < 0.05)
Classification and proportion of total volatile compound profiles detected in maize plants in the control a and inoculated b treatments; and principal component analysis (PCA) among samples of maize plants between the control and inoculated treatments (c, n = 9)
Oviposition stimulation index (OSI) of Ostrinia furnacalis females in response to different chemical compounds. The OSI ranges from − 100 to 100, and when OSI = 0, this indicates that oviposition preference on the tested compound was equal to that of the control; when OSI < 0, this indicates that the tested chemical compound was a deterrent to oviposition; when OSI > 0, the chemical tested was an attractant for oviposition. Values are means ± SE, and number is sample size. Asterisk indicates significant differences in OSI between the treated (chemical compounds) and the control (Paraffin) using χ² tests (p < 0.05). *0.05 < p < 0.01; ***p < 0.001; ns, no significance
Insect offspring development on control and Beauveria bassiana-inoculated plants. a survival ratio of larvae, b pupation ratio, and c eclosion ratio. Values are means ± S.E. (n = 10). Different small letters above bars indicate significant differences between the control and inoculated treatments (p < 0.05)
The effects of Beauveria bassiana on properties of maize plants after inoculation. a plant height, b leaf length of plants, c leaf width of plants, d plant nitrogen content, and e plant carbon content. Values are means ± S.E. (n = 10). Different small letters above bars indicate significant differences between control plants and inoculated plants (p < 0.05)
Several species of entomopathogenic fungi (EPF), often considered as bioinsecticides, are able to colonize and establish a symbiotic relationship with plants as endophytes. Recent studies have demonstrated that insects feeding on endophytically colonized plants could have reduced survival. These newly emerging, but not yet fully understood, ecological roles suggest the possibility that EPF may affect preferences and performance of herbivorous insects. However, such plant-mediated effects and underlying mechanisms are largely unexplored. Here, we examined that the endophytic EPF, Beauveria bassiana, could affect oviposition selection and offspring fitness of Asian corn borer, Ostrinia furnacalis on maize, Zea mays. We observed that O. furnacalis females preferred to lay eggs on B. bassiana-inoculated maize plants. This was attributed to the changes in plant volatile profiles upon endophytic colonization by B. bassiana. Of these plant volatiles, we observed increased amounts of insect-preferred compounds, 2-ethyl-1-hexanol and 3-hexen-1-ol, and decreased amounts of non-preferred compounds β-caryophyllene, naphthalene and α-pinene. This finding suggests that B. bassiana-induced plant volatiles could modulate the interactions between plants and insects. However, fewer O. furnacalis larvae, pupae, and adults survived on the B. bassiana-colonized maize plants and this was correlated with lower plant nitrogen content in these plants. These results indicated that oviposition selection of O. furnacalis did not reflect the maximization of offspring fitness following maize inoculation with B. bassiana. We suggest that EPF-inoculated maize causes a detrimental attraction for O. furnacalis, which should be considered for potential application of “trap plants” when incorporating endophytic EPF within integrated pest management programs.
Timely detection of an invasion event, or a pest outbreak, is an extremely challenging operation of major importance for implementing management action toward eradication and/or containment. Fruit flies—FF—(Diptera: Tephritidae) comprise important invasive and quarantine species that threaten the world fruit and vegetables production. The current manuscript introduces a recently developed McPhail-type electronic trap (e-trap) and provides data on its field performance to surveil three major invasive FF (Ceratitis capitata, Bactrocera dorsalis and B. zonata). Using FF male lures, the e-trap attracts the flies and retains them on a sticky surface placed in the internal part of the trap. The e-trap captures frames of the trapped adults and automatically uploads the images to the remote server for identification conducted on a novel algorithm involving deep learning. Both the e-trap and the developed code were tested in the field in Greece, Austria, Italy, South Africa and Israel. The FF classification code was initially trained using a machine-learning algorithm and FF images derived from laboratory colonies of two of the species (C. capitata and B. zonata). Field tests were then conducted to investigate the electronic, communication and attractive performance of the e-trap, and the model accuracy to classify FFs. Our results demonstrated a relatively good communication, electronic performance and trapping efficacy of the e-trap. The classification model provided average precision results (93–95%) for the three target FFs from images uploaded remotely from e-traps deployed in field conditions. The developed and field tested e-trap system complies with the suggested attributes required for an advanced camera-based smart-trap.
Alpha diversity (number of observed ASVs) of bacterial a and fungal b communities associated with fruits and wild D. suzukii flies, arranged by fruit type and collection site. The richness of both bacterial and fungal communities across fruits and the emerging wild flies differed significantly (p-values < 0.1 and < 0.05, respectively)
Beta diversity of bacterial (a and b) and fungal (c and d) communities associated with fruits (triangles) and wild D. suzukii (dots). a PCoA of weighted UniFrac distance of bacterial communities differed significantly between fruits and flies (p-value = 0.001). b Individual facets of PCoA using weighted UniFrac for every fruit type in every collection site. c PCoA of Bray Curtis dissimilarity index for fungal communities, which differed significantly between fruits and flies (p-value = 0.021). d Individual facets of PCoA using Bray Curtis by fruit type in every collection site
Alpha and beta diversity (of bacterial communities across wild and lab-reared flies Alpha diversity (observed ASVs) of a) did not differ significantly between wild and lab-reared flies (p-value = 0.40). Beta diversity c) based on Weighted UniFrac distances for bacterial communities differs significantly between the lab-reared and wild flies (p-value = 0.001)
Top ten abundant bacteria across wild flies and their source fruits (a). Four core bacteria were observed across the wild flies (b). Top ten abundant bacteria across lab-reared flies and wild flies, which also comprised three of the core bacteria (c). Top ten abundant fungi across wild flies and their corresponding fruits (d)
The invasive fly Drosophila suzukii is a pest that can infest a diverse range of intact, ripening fruits, using its serrated ovipositor. This constitutes a different niche compared to the rotting fruits its ancestors use, especially because these intact fruits have limited quantities of microbes and soluble nutrients for the developing larvae. To investigate the potential role of microbial associations in the niche expansion of this invasive fly, we characterized the bacterial and fungal communities of D. suzukii and various wild fruits from which they developed. To assess cross-generational microbial associations, we also lab-reared fly populations and characterized their microbial communities. Diversity metrics of microbial communities differed significantly between flies and fruits. Different fruit types varied substantially in microbial composition, while flies showed relatively uniform bacterial communities, irrespective of the fruit source they developed on. After approximately ten generations of lab-rearing, bacterial communities still showed considerable overlap with those of wild flies. Fungal communities of flies and fruits showed larger resemblance, with a substantial overlap between wild flies and the fruits on which they had developed. Our study thus reports that the fungal community structure in these pests largely reflects those on the breeding substrates, while these flies might have formed more persistent associations with some bacteria and transmit these across generations.
Rising temperatures can enhance foraging activity and accelerate the encounter rate of different predators, which may increase their interference competition strengths. However, limited information is available on such effects of temperature, and on the consequences for their predation rates. We used a functional response approach to experimentally quantify the interspecific interference competition strength of two species of ladybirds, Harmonia axyridis and Propylea japonica (Coleoptera: Coccinellidae), toward their prey Myzus persicae (Hemiptera: Aphididae) at 23 and 33 °C, respectively. The results indicated that high temperature could cause P. japonica to be more active and interfere with H. axyridis more often, and strengthened the interference competition between these two predators. The functional response of H. axyridis was changed from type II in single H. axyridis treatment to type III in paired predator assays at 23 and 33 °C. Moreover, single H. axyridis consumed more aphids than H. axyridis in heterospecific predator trials at aphid densities below 50 and 35 at 23 and 33 °C treatments, respectively. For P. japonica, type II functional responses were detected in all assays. Additionally, when competing with H. axyridis, the predation rate of P. japonica at 23 °C was almost unchanged compared to that of single P. japonica, but fewer aphids were eaten compared with single P. japonica across all aphid densities at 33 °C. Thus, with interference competition, two predator species respond differently to temperature changes in terms of foraging efficiency, which may further affect the population adaptability and control efficiency of these two focal species.
Schematic representation of the aphid preference setup using an arena for dual choice bio-assays. The example shown here is the one involving a choice between a sweet pepper plant (P) alone and a sweet pepper plant associated with a geranium plant (P-G) (C modality)
Percentage of aphids making a choice between a sweet pepper (P) and A a geranium (G); B a brushed geranium (BG); C a sweet pepper associated with a geranium (P-G); D a sweet pepper associated with a brushed geranium (P-BG). n: total number of responding aphids (in brackets, the total number of tested aphids). * indicates a significant difference (*p ≤ 0.05; ***p ≤ 0.001; Chi-squared test). ns: non-significant
Total duration of phloem sap sustained ingestion by Myzus persicae on sweet pepper alone (P) or associated with geranium (P-G or P-BG). Different letters indicate significant differences
Principal component analysis (PCA) of geranium VOCs emissions following mechanical stimulation (n = 7)
Germacrone and β-elemenone emissions (µg L⁻¹ gDW⁻¹) (n = 7). The gray line links each indivual before and after treatment (paired T test)
The combination of a companion plant with a cultivated plant is considered an interesting strategy to reduce pest pressure and, hence, the use of pesticides. Although several plants from the Alliaceae and Lamiaceae families are known to be efficient companion plants against aphid pests, only a few plants of the Geraniaceae family have been studied so far. The aim of this work was to investigate the potential effects of Geranium macrorrhizum as a companion plant on the colonization of sweet pepper (Capsicum annuum, Solanaceae) by the green peach aphid (Myzus persicae). Aphid's orientation behavior, probing behavior and life history traits were assessed on sweet pepper using a host choice preference setup, Electrical Penetration Graph technique and clip-cage laboratory bioassays, respectively. The potential disturbance through mechanical stimulation of geranium leaves was also assessed. The composition of VOCs from G. macrorrhizum leaves was analyzed using SPME technic followed by GC-MS. This study revealed that G. macrorrhizum as a companion plant was intrinsically repellent but not enough to completely mask the attractive odor of the sweet pepper host plant. Moreover, G. macrorrhizum negatively impacted the probing behavior, fecundity and survival rate of M. persicae on sweet pepper. The effects were exacerbated when G. macrorrhizum leaves were mechanically stimulated. This could be due to the greater amount of the main VOCs germacrone and β-elemenone emitted by G. macrorrhizum following mechanical stimulation. Our results bring new insights into the use of novel companion plants to regulate aphid pest populations.
Root-knot nematodes (Meloidogyne spp.) are notorious plant-parasitic nematodes that affect agricultural crops. These obligate soil-dwelling parasites typically maneuver the host plant physiology by forming specialized feeding cells resulting in heavy yield losses. Scant management tools are available to effectively combat this pest. In an exploratory attempt of identifying new fungal biocontrol agent(s) for M. incognita from India, a Paecilomyces tenuis isolate from rhizosphere soil was found to incur > 90% mortality of the infective second-stage juveniles (J2s) at 24 h post-exposure to the fungal filtrate with about 87% parasitization. The fungal filtrate also significantly reduced the egg hatching and host-root penetration of M. incognita under in vitro and in vivo conditions revealing its effectiveness in curbing nematode pathogenicity with positive effects on plant growth. Chromatographic analyses revealed the presence of Huperzine A (433.56 mg L⁻¹) in the P. tenuis isolate. Besides, the isolate possessed acetylcholinesterase inhibition attribute with an IC50 of 2.85 ± 0.12 mg mL⁻¹ of the fungal filtrate. Further, GC-MS analysis revealed the production of other nematicidal compounds by the fungus including acetic acid. To conceptualize the mode of nematicidal action, RNA-Seq was done post-treatment of the M. incognita J2s and model worm Caenorhabditis elegans with fungal filtrate and pure Huperzine A. The transcriptomic profile unraveled the molecular intricacies underlying the nematicidal action affecting several biological pathways and developmental checkpoints of the nematode. Thus, the P. tenuis isolate offers significant potential to be used as a biocontrol agent against M. incognita along with its commercial use for Huperzine A production.
Schematic illustration of the whitefly life cycle and their control through conventional and new genomics tools. The image was created using BioRender (
RNAi-mediated control strategies. (a) Non-transformative RNAi-mediated approaches, (b) Transformative RNAi-mediated control. (c) The double-stranded RNA (dsRNA) of target genes is formed that induce RNAi machinery. Dicer (RNAse III enzyme) can chop down the dsRNA into 21–24 nucleotide small interfering RNAs (siRNAs). RISC (RNA inducing silencing complex) can bind with siRNAs, and the guide strand of siRNA helps RISC to target the messenger RNA (mRNA). The Argonaute protein (Argo) in RISC complex cleaves the target mRNA, and the cleaved target mRNA is amplified b RNA-dependent RNA polymerase (RdRp) to form dsRNAs that enter the RNAi pathway and amplify the signal. The image was created using Microsoft power point and BioRender (
Schematic illustration of microbiome-based whitefly management approaches. (a) Elimination and replacement of microbiome, (b) incompatible insect technique (IIT), (c) paratransgenesis, (d) microbial insecticides and plant-incorporated protectants, (e) beneficial microbes for mass-reared insects for autocidal programs, (f) semiochemicals produced by microbes. The image was created using BioRender (
Mode of inheritance of gene drive altered gene as compared to Mendelian inheritance. Gene drive element including Cas9 is inserted at a targeted position on the chromosome. Once, active inside the cell Cas9 generates a cut and copies itself on the opposite homologous chromosome, thus converting heterozygote into homozygotes. Dissemination of gene drive altered gene in the entire insect population. Standard Mendelian inheritance and gene drive-based Super-Mendelian inheritance where theoretically any gene drive construct is able to overtake an insect population in few generations. The image was created using BioRender (
Bemisia tabaci species complex (whitefly) is one of the most dangerous pests that destroy many important crops worldwide. It causes damage to the host plant by feeding on phloem sap as well as transmitting a wide range of devastating plant viruses (especially begomoviruses) that cause severe epidemics on crops. To fend off the menace, modern genomic-based strategies have been adapted to minimize the crop losses due to this destructive pest. Genetic engineering techniques, e.g., transgenics and RNA interference (RNAi) have shown promising results in controlling B. tabaci in plants; however, these techniques often face challenges due to the concerns about GMOs in food crops. With the enhanced knowledge about B. tabaci genomics, new technologies, e.g., manipulation of microbiota or CRISPR-based genome editing have shown promising results in several insect pests and could have an instrumental role in controlling agricultural pests including whitefly. Genome editing is an eco-friendly approach that can be employed to suppress or even destroy the target species. In this review, we have discussed B. tabaci as a pest and advancement in control strategies of B. tabaci. Various potential targets for genome editing have also been discussed that could be used in gene-editing technologies for the efficient management of B. tabaci and the viruses it transmits. Finally, we also outlined the future perspective and effective use of genome editing technology in developing CRISPR-based gene drive for whitefly population modification, suppression, and eradication.
Bioactivity of botanical insecticides at different life stages of arbovirus vectors
Mosquitoes (Diptera: Culicidae) are insect vectors of epidemiologically important arboviruses owing to their behavior, physiology, morphology, and proximity to humans, which require incisive strategies to contain their spread. The failure of current arbovirus management plans and lack of fully effective treatments suggest that vector control by botanical insecticides could be an effective and safe strategy. Botanical insecticides are obtained from renewable sources and have complex chemical compositions, different modes of action, and selective toxicity for target organisms. In this review, we present the main control strategies for insects belonging to the genera Aedes, Culex, and Anopheles and discuss the possibility of using botanical insecticides in the integrated management of vectors. Numerous botanical insecticide formulations are presented, and their potential modes of action during the immature stages include damage to the egg exocorionic network and abnormal disruption of embryos, which result from deficiencies in egg chitinization, impairment of larval morphology, and inhibition or differential expression of enzymes, promoting changes in the digestive tract epithelium and reduced larval mobility, and impairment of external surfaces or the respiratory system of pupae, altering pupal swimming patterns. In adult insects, botanical insecticides can promote incomplete ecdysis, in addition to dysfunction of olfactory receptors, food traffic, and reproductive function. Thus, broad-spectrum botanical insecticides can be used to control the different stages of insect development. The contributions of nanotechnology to vector control should be further explored to enhance the insecticidal activity and stability of botanical insecticides under different conditions.
Emergence time of the F0T. remus after cold storage with 14 different treatments
Survival curves of the female F0T. remus after cold storage with 14 different treatments
Number of eggs parasitized in the first five days by females of the F0 generation after cold storage with 14 different treatments. Values are expressed as means ± SE. Different lowercase letters above the bars indicate significant differences (Tukey’s test, P < 0.05)
Emergence percentage (a) and percentage of females (b) of the F1 generation. Values are expressed as means ± SE. Different lowercase letters above the bars indicate significant differences (Tukey’s test, P < 0.05)
Telenomus remus (Nixon) is a promising egg parasitoid for the management of Spodoptera frugiperda (J. E. Smith). This species has been successfully reared on alternative hosts under laboratory conditions. However, the production of biocontrol agents is often out of sync with the demands in the field. Appropriate cold storage techniques can drastically prolong their shelf-life to synchronize the release schedule with field needs and reduce production costs. Past studies on the cold storage of T. remus only focused on certain developmental stages, but not all stages. Here, we comprehensively evaluated the impacts of storage temperature (8, 11, and 14 °C) and duration (7, 14, 21, 28, and 35 days) on the maternal emergence and offspring fitness of T. remus stored at different developmental stages (first instar larvae, second instar larvae, prepupae, and pupae) using Spodoptera litura (Fabricius) eggs as alternative hosts. For each developmental stage, emergence percentage and parasitism capacity of parents all decreased with increased storage duration and decreased storage temperature. Maternal female longevity, offspring emergence percentage and percentage of females were barely affected by cold storage. We concluded that storage of the first instar larvae at 14 °C for 21 days was the optimum storage scheme for T. remus. Our findings can be directly used as guidance in mass production and storage of this parasitoid.
Diurnal insects can select suitable oviposition sites by discriminating plant coloration. The long wavelength sensitive opsin (LW) gene is mainly for discriminating long wavelengths of colors in diurnal insects. However, the affection of coloration on oviposition selection and the roles of LW gene in nocturnal insects are unclear. Here, the questions were explored in Helicoverpa armigera (Lepidoptera, Noctuidae) using CRISPR/Cas9 gene editing technology and experiments of oviposition selection under different coloration backgrounds. To different brightness (achromatic white, grey, black), wild moths preferred to oviposit on higher-brightness background, while the LW mutant had no preference. To different colors, wild moths had no oviposition preference, while the LW mutant significantly reduced oviposition on long-wavelengths of colors (red, orange, yellow, and green) compared to blue and violet. When both brightness (white) and color (orange and green) cues were presented for oviposition, wild moths were more attracted to brightness than color, while LW mutant had no significant preference. For the coloration of young and old leaves, wild moths preferred to oviposit on coloration of young leaves that had a brighter light green, while LW mutant had no preference. Electroretinogram recordings showed that the responses of moths to different bright light or different color light were significantly decreased after knockout of LW, especially to the long-wavelengths. These results suggest that brightness is a more reliable cue rather than color for oviposition selection of nocturnal moth H. armigera in changing microhabitats and LW mediates the recognition of different brightness and long wavelengths.
Average oviposition rate (± s.e.) of T. evansi populations on plants exposed to different concentrations of cadmium (a to f; N=7-10 plants per concentration, each tested with 3-5 spider mites per population) and on artificial diets containing different concentrations of cadmium (g to l; N=6 arenas per concentration, each tested with 10 spider mites)
Average oviposition rate (± s.e.) of T. urticae populations on plants exposed to different concentrations of cadmium (a to e; N=7-10 plants per concentration, each tested with 3-5 spider mites) and on artificial diets containing different concentrations of cadmium (f to j; N=6 arenas per concentration, each tested with 10 spider mites)
Some plants are able to accumulate on their leaves metals taken from the soil, using this as a defence against herbivorous arthropods. However, herbivore response to metal accumulation in plants is known to be variable. While some species and taxonomic groups are less affected than others, hormetic effects have also been observed in spider mites, herbivorous crop pests. Still, knowledge on the range and causes of intraspecific variation in the response of herbivores to metal accumulation is lacking. Here, using two species of spider mites, Tetranychus urticae and Tetranychus evansi, we tested the variation in 17 populations in response to cadmium-accumulating tomato plants and the drivers of such variation. We observed a nonlinear, hormetic response of mites to plants with cadmium in some, but not all, populations. The same pattern was recaptured in artificial diets with different concentrations of cadmium but not in artificial diets with sugars, which change in the plant in response to cadmium. This indicates that herbivores on metal-accumulating plants respond to metals, not to the variations in leaf carbohydrates. Therefore, metals exert different effects on herbivores according to the amount accumulated, but independently of other studied plant traits. This knowledge is key to the understanding of the mechanisms underlying herbivore responses to metal-based plant defences and to pesticides containing heavy metals. Additionally, our findings draw attention to the need of considering intraspecific variation and nonlinearities when studying the effects of metals and other contaminants on herbivorous arthropods.
Observed (red asterisks) and simulated (blue line) adult population dynamics of Spodoptera frugiperda within the area of current distribution in North America: (left) Southern Florida, Miami Dade County, and (right) Northern Florida, Alachua County
Heat map showing the predicted distribution and the yearly average abundance of adult individuals of Spodoptera frugiperda per trap per week under the median-case assessment scenario
Heat maps showing the predicted distribution and the yearly average abundance of adult individuals of Spodoptera frugiperda per trap per week under the best-case A and worst-case B assessment scenarios
Simulated (blue line) population dynamics of adults of Spodoptera frugiperda along a south–north latitudinal gradient within the area of potential establishment in Europe, in A Cyprus, B Southern France, and C Atlantic coast of Portugal
Population dynamics of adults of Spodoptera frugiperda simulating an inoculum of 5 adults at the 90th, (green line), 150th (blue line), and 210th (red line) day of the year in (upper left corner) Rădoiești (Southern Romania), (upper right corner) Ghedi (Southern Italy), (lower left corner) Ouarville (Northern France) and (lower right corner) Engelsberg (Germany)
The fall armyworm, Spodoptera frugiperda (J.E. Smith), is an invasive pest threatening crop production and food security worldwide. High concerns are linked to the potential establishment of the species in Europe. The high migratory capacity of S. frugiperda causes concerns about the potential impacts of transient populations invading new areas from suitable hotspots. In the present work, we developed and used a physiologically-based demographic model to quantitatively assess the risks of S. frugiperda in Europe. The risks were assessed considering a best-, a median-, and a worst-case scenario. The Mediterranean coastal areas of Southern Europe resulted particularly suitable for the establishment of the species, with suitable areas reaching even higher latitudes, in the worst-case scenario. In Europe, up to four generations per year were predicted. The predicted yearly average number of moths per trap per week (± standard deviation) was 5 (± 4), 17 (± 5), and 139 (± 22) in the best, median-, and worst-case assessment scenarios, respectively. Model results showed that Southern and Central Europe up to the 48th parallel north might be exposed to the risk of transient populations. Depending on the latitude and on the period of arrival of the propagule, 1–2 transient generations per year might be expected. The model can be used to define strategies for reducing the risks of establishment of the pest at the country level. Predictions on the dynamics and phenology of the pest can also be used to support its management at the local level.
Variation in leaf structural traits in two cultivars (Q—drought-susceptible Quintus, S—drought-tolerant Septima) of T. aestivum under drought stress. Vertical bars represent the s.e. estimated by linear models. a Trichome length. b Trichome density. c Stomata density. d Cuticle thickness. All values are available in Supplementary Materials: Table S1
Variation in morphophysiological traits in two cultivars of T. aestivum under drought stress and aphid infestation. Vertical bars represent the s.e. estimated by mixed-effects models. a Biomass. b Leaf length. cΨπ100\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\varPsi }_{\pi 100}$$\end{document}. All values are available in Supplementary Materials: Table S2
Life table and population growth parameters for Metopolophium dirhodum reared on two cultivars of T. aestivum. Vertical bars represent the s.e. estimated with 100,000 bootstraps. Cultivars assigned with the same letters did not differ significantly from each other (the paired bootstrap test). The values ± s.e. of all parameters can be found in the Supplementary Materials: Table S3
Population projection (log10[n + 1]) for M. dirhodum reared on two cultivars of T. aestivum (Q—drought-susceptible Quintus, S—drought-tolerant Septima) under three water supply scenarios (soil water capacity of 70, 50 or 40%). The projection is based on the age-stage, two-sex life table theory. a The predicted course of population growth on the two cultivars and three levels of humidity. The relationships between time for d ≥ 35 (after the stable age-stage distribution was reached, dashed vertical line) and the population sizes for the individual cultivars are as follows. Q40: (log10[n + 1]) = 0.5660 + 0.1080d; Q50: (log10[n + 1]) = 0.5082 + 0.1022d; Q70: (log10[n + 1]) = 0.5393 + 0.1150d; S40: (log10[n + 1]) = 0.5699 + 0.1108d; S50: (log10[n + 1]) = 0.6132 + 0.1014d; S70: (log10[n + 1]) = 0.5565 + 0.1124d. b Projected population size ± 95% confidence intervals after 35 d
Relationships between the reproductive rate (R0) of M. dirhodum and a plant aboveground biomass, b trichome density and cΨπ100\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${\varPsi }_{\pi 100}$$\end{document}. Lines indicate significant relationships according to linear regression models
Drought affects both crops and their pests, but the effect of the interaction between drought and pests on crops has not been sufficiently understood. The aim of this work is to determine (i) the response of spring wheat (Triticum aestivum) to three watering regimes (soil water capacity of 70, 50 and 40%) and aphid (Metopolophium dirhodum) infestation, and (ii) how drought affect aphid population growth. Seedlings of one drought-susceptible (Quintus) and one drought-tolerant (Septima) cultivar were used, and changes in leaf structural and morphophysiological traits were measured. The age-stage, two-sex life table approach was used to determine aphid population growth. The plant stress and plant vigour hypotheses in this system were tested by analysing correlations between leaf traits and aphid life table parameters. Drought stress negatively affected parameters related to plant vigour (reduced biomass, decrease in Ψπ100 and increased resource allocation in structural defence trichomes) regardless of the stress tolerance of the cultivar, although the level of stress was generally greater in Quintus than in Septima. Plants perceived the stress caused by the aphids as significant only under high drought stress, as the physiological response of increasing growth and osmolyte accumulation was triggered under these conditions. This response also benefited the aphids; hence, the population growth of the aphids was most severely affected under moderate drought stress. The reproductive rate was negatively affected by trichome density and positively affected by leaf biomass and Ψπ100; these findings provide support for the plant vigour hypothesis for the spring wheat seedling–rose-grain aphid study system.
Schematic model of the function of the organs and feeding activity of the Asopinae zoophytophagous that involves the ingestion, extra-oral, and complete digestion during the injection of venoms/digestive proteins to cause death and prey consumption
Model of three-trophic level interaction with cultivated plants, insect pests, and zoophytophagous Asopinae in the agroecosystem. Feeding activities of food (prey and plant) consumption vary according to prey availability
The use of predatory Hemiptera (Pentatomidae: Asopinae) in agroecosystems has increased considerably in the last decades. All Asopinae representatives are obligate predatory stink bugs but they are classified as zoophytophagous because they feed on prey and occasionally feed on plants. They prey on wide variety of insects including the agricultural pests Coleoptera, Diptera, and Lepidoptera. Despite the predatory potential of Asopinae, their use and establishment in the agroecosystems have some restrictions, yet. Here, the aim is to review the advances in biology, feeding strategies, and biological control for using Asopinae species with zoophytophagous-predatory habits (SZP) in the agroecosystems. We discuss four different approaches that can improve the worldwide effectiveness and popularization of SZPs representatives as biocontrol agents in crops,(i) feeding strategies, ingestion, and digestion;(ii) diets for survival during prey shortage;(iii) adaptation of species for biological control in crops; (iv) use of Asopinae in integrated pest management programs.
Reproductive Interference occurs when interactions between individuals from different species disrupt reproductive processes, resulting in a fitness cost to one or both parties involved. It is typically observed between individuals of closely related species, often upon secondary contact. In both vertebrates and invertebrates, Reproductive Interference is frequently referred to as ‘Satyrisation’. It can manifest in various ways, ranging from blocking or reducing the efficacy of mating signals, through to negative effects of heterospecific copulations and the production of sterile or infertile hybrid offspring. The negative fitness effects of Satyrisation in reciprocal matings between species are often asymmetric and it is this aspect, which is most relevant to, and can offer utility in, pest management. In this review, we focus on Satyrisation and outline the mechanisms through which it can operate. We illustrate this by using test cases, and we consider the underlying reasons why the reproductive interactions that comprise Satyrisation occur. We synthesise the key factors affecting the expression of Satyrisation and explore how they have potential utility in developing new routes for the management and control of harmful insects. We consider how Satyrisation might interact with other control mechanisms, and conclude by outlining a framework for its use in control, highlighting some of the important next steps .
Surface treatment is commonly used in controlling the red imported fire ants, Solenopsis invicta Buren. In the present study, the behavioral responses of S. invicta workers to surfaces treated with insecticides were investigated. Toxicological tests showed that beta-cypermethrin had the highest contact toxicity (with the lowest LC 50 value) among nine tested insecticides, followed by thiamethoxam, fipronil, indoxacarb, chlorfenapyr, spinetoram, rotenone, avermectin, and chlorantraniliprole. In the laboratory, surfaces treated with beta-cypermethrin or rotenone significantly reduced the number of foraging ants. In addition, S. invicta workers transported significantly more particles (measured in weight and/or covered area) onto surfaces treated with fipronil (50, 500, and 5000 µg/mL), rotenone (5000 µg/mL), or avermectin (5000 µg/mL) compared with the controls. Similarly, these insecticides significantly triggered the particle-covering behavior of ants in the field. We hypothesized that such behaviors would reduce the contact toxicity of insecticides against S. invicta. When the surfaces treated with fipronil or rotenone (500 or 5000 µg/mL) were artificiality covered with particles, S. invicta had significantly higher LT50 values compared with insecticide-treated surfaces without particles. This study provides the first evidence that S. invicta workers can perform particle-covering behavior to reduce the toxicity of certain insecticides, which constitutes a unique insecticide-resistance strategy in ants.
Effects of maize genotype × Si interaction on the relative consumption rate (RCR) of Spodoptera frugiperda larvae. Different uppercase letters for the effect between genotypes and lowercase letters for the effect between Si treatments denote significant differences (P < 0.05)
Effects of the Si × herbivory interaction on concentration of hydrogen peroxide (H2O2). Different uppercase letters for the effect between Si treatments and lowercase letters for the effect between herbivory treatments denote significant differences (P < 0.05)
Effects of Si × herbivory interaction on Si concentration in the shoot of plants. Different uppercase letters for the effect between Si treatments and lowercase letters for the effect between herbivory treatments denote significant differences (P < 0.05)
a Effects of the Si × herbivory interaction on the injury score of Spodoptera frugiperda larvae in maize genotypes. b Effect of maize genotype on the injury score of Spodoptera frugiperda larvae. a Different uppercase letters for the effect between Si treatments and lowercase letters for the effect between herbivory treatments denote significant differences (P < 0.05); b Different lowercase letters between genotypes denote significant differences (P < 0.05)
a Effects of maize genotype × herbivory by S. frugiperda interaction on shoot dry mass of plants; b Effects of maize genotype × Si interaction on relative chlorophyll index before infestation; c Effects of maize genotype × Si interaction on plant height before infestation.; d Effects of maize genotype on plant height after infestation. a Different uppercase letters for the effect between genotypes and lowercase letters for the effect of herbivory treatments denote significant differences (P < 0.05); b Different uppercase letters for the effect between genotypes and lowercase letters for the effect of Si treatments denote significant differences (P < 0.05); c Different uppercase letters for the effect between genotypes and lowercase letters for the effect of Si treatments denote significant differences (P < 0.05); d Different lowercase letters between genotypes denote significant differences (P < 0.05)
Fall armyworm (FAW) Spodoptera frugiperda is considered the main defoliating insect pest of maize in many countries. Silicon (Si) applied to plants has been shown to increase the resistance to insects, especially in grasses such as maize. This study characterized the effects of Si fertilization regarding priming, induced resistance, and tolerance to FAW in a landrace variety and hybrid of maize. Si was applied in soil of potted-plants as H4SiO4 at 2 t ha⁻¹ when maize plants were at V2 stage, and when they reached V3 two FAW neonates were placed in the plant’s whorls to cause herbivory. FAW performance was evaluated on excised leaf sections in the laboratory and on plants with larvae infesting V4-stage plants in the greenhouse. Concentrations of H2O2, malondialdehyde, and Si, and the activities of antioxidant enzymes were recorded and correlated to Si-based responses on plant growth, and FAW injury and performance. As main results, there was reduced FAW injury and larval weight gain in Si-treated plants subjected to herbivory. Greater root dry mass was observed in the landrace variety with Si and without herbivory. Landrace plants showed higher shoot weights than the hybrid under FAW infestation. Si-fertilized plants showed higher H2O2 concentrations. The highest peroxidase activities occurred in Si-treated plants without herbivory, and the catalase and superoxide dismutase activities were highest in Si-treated plants without herbivory or herbivory-injured plants without Si. In conclusion, Si-based defense in maize to FAW involve mixed effects of priming and tolerance, and were more pronounced in the landrace variety.
Evolutionary relationships of strain KMS-6 among closely related Bacillus species. The phylogenetic tree was constructed with MegaX using the maximum likelihood method
In vitro effect of different concentrations (% v/v) of B. altitudinis KMS-6 fermentation supernatant on hatching of M. javanica eggs at different time intervals
In vitro effect of different concentrations (% v/v) of B. altitudinis KMS-6 fermentation supernatant on M. javanica J2s mortality, at 24 h and 48 h of incubation
Roots of eggplant grown in the greenhouse. a untreated roots (Control). b roots treated with Bacillus altitudinis KMS-6, after 45 days
Root-knot nematodes are among the most dangerous plant pathogens. Biological control is a safer and effective way to manage such pests. In this context, bacterial strain KMS-6 was isolated from nematode-affected soil of the research field, CCS HAU, Hisar. It was subjected to morphological and biochemical characterization. The bacterium produced 14.02 ± 0.03 µg/ml of IAA and showed a cyanogenic activity. KMS-6 was identified based on 16S rRNA gene sequence analysis as Bacillus altitudinis (accession no. MT626660). In vitro experiments with fermentation supernatants of KMS-6 resulted in potential hatching inhibition and up to 86% J2s mortality of M. javanica. The bacterium significantly suppressed root-knot nematode infestations in greenhouse and field experiments. During the greenhouse experiment on eggplant, KMS-6 inoculation resulted in a 76% reduction in eggs, 80% reduction in galls, reducing the final nematode population up to 92% compared to control. All trials were significantly more effective than the chemical treatment as well. Also, an enhancement in plant growth was observed in KMS-6 inoculated plants with the highest plant height, maximum fresh and dry weight of root and shoot. Similar results were seen in trials conducted on eggplant (2018) and cucumber (2019) crops in nematode-infested fields. KMS-6 inoculation reduced nematode infestation more effectively than control and carbofuran treatments. The yield was significantly improved in the KMS-6 treatment. Data suggest that B. altitudinis KMS-6 could be an effective biological control agent with plant-growth enhancing properties against root-knot nematodes and a potent alternative to chemical nematicides.
The indirect effect of seminatural habitats on pest suppression has been widely studied in agricultural landscapes. By contrast, the role of crop diversity on pest suppression by predators has seldom been explored, particularly using molecular gut-content analysis (MGCA). In addition, differences between early- and late-season effects of landscape complexity on pest control, crucial to ensure season-long control, have received little attention. During 2014 and 2015, we investigated the effect of agricultural landscape complexity and crop diversity on cereal leaf beetle (CLB, Oulema melanoplus) predation early in the season using sentinel egg cards and late in the season by assessing larval predation using MGCA. Early-season CLB egg predation and late-season abundance of Nabis americoferus and coccinellids in wheat fields were positively correlated with amount of woodland habitat in these landscapes. Contrary to our predictions, crop diversity had negative associations with the late-season frequency of larval predation and the abundance of N. americoferus. Predator diversity and the abundance of Hippodamia lady beetles had negative associations with CLB abundance, highlighting the significant contribution of some generalist predators to CLB suppression. Our results suggest that the proportion of woodland and a few major crops (e.g., canola and non-cereal crops), rather than crop diversity, are associated with higher predation at different temporal scales. Overall, our results suggest that a habitat management strategy could be implemented to adjust the crop rotation regime to add the right kind of crop diversity in the landscape to support the natural control of CLB.
Preference of P. persimilis for the volatiles from clean plants (white bars) or plants previously exposed to M. pygmaeus (grey bars); Each bar represents the result of a separate replicate, each with new groups of plants and predatory mites. Numbers along the vertical axis give the identity of these groups of plants, most of which groups were also used for the experiments which results are shown in Fig. 2. Each bar represents the response of 20 predatory mites. NC indicates the number of predatory mites that did not respond. Per replicate, significant preference for one of the two volatiles is indicated by asterisks (*: P < 0.05; ***: P < 0.001)
Preference of P. persimilis for the volatiles emanating from two groups of plants: a plants previously exposed to M. pygmaeus for 4 days and subsequently infested with spider mites for 2 days (grey bars) vs. unexposed plants subsequently infested with spider mites for 2 days (white bars); b plants infested with spider mites for 2 days (white bars) vs plants infested with spider mites for 2 days (grey bars); c plants infested with spider mites for 6 days (white bars) vs plants infested with spider mites for 6 days and exposed to M. pygmaeus for the last 4 days (grey bars). Within each panel, each bar represents the result of a different replicate, each with new groups of plants and predatory mites. Results presented in a were obtained with the same groups of plants as in Fig. 1; they were first tested after exposure to the omnivore (Fig. 1), then infested with spider mites and tested again (a). Numbers along the vertical axis give the identity of these groups of plants. Results presented in b and c were also obtained with the same plants; they were first tested after infestation with spider mites (b), then exposed to the omnivore and tested again (c). Letters along the vertical axis give the identity of these groups of plants. Each bar represents the response of 20 predatory mites. NC indicates the number of predatory mites that did not respond
Preference of P. persimilis for the volatiles emanating from clean plants (white bars) and plants exposed to M. pygmaeus (grey bars), with a and without bM. pygmaeus present on the plants. Shown are average numbers (+ SE) of predators of 4 replicates (M. pygmaeus present) or 2 replicates (M. pygmaeus absent), each with new groups of plants and predators. See legend to Fig. 1 for more explanation
Preference of P. persimilis (mean + SE) for volatiles from clean plants (white bars) and from plants exposed to M. pygmaeus (grey bars). Shown are results of three groups of predatory mites with different experiences with volatile cues from plants exposed to M. pygmaeus: aP. persimilis without experience, starved for 1 h; bP. persimilis without experience, starved for 1 day; cP. persimilis experienced with the volatiles from plants with M. pygmaeus plus volatiles from M. pygmaeus in the absence of food for 1 day. Each bar represents the average of 4 (1 h naïve) or 5 replicates (1d naïve and 1d experienced), each with new groups of plants and predators. Different capital letters indicate significant differences among the three groups of P. persimilis (contrasts after GLM: P < 0.05). See legend to Fig. 1 for more explanation
Grouping of the three treatments as a function of two linear discriminants, based on the 16 selected volatile compounds (see text)
It has become clear that omnivorous predators can induce plant defences that affect the performance and host plant choice of herbivores. They are also known to induce the production of plant volatiles that can affect the behaviour of herbivores searching for plants. These volatiles may also affect the searching behaviour of other predators, which was investigated here. The predatory mite Phytoseiulus persimilis preferred plants previously exposed to the omnivorous mirid Macrolophus pygmaeus over clean plants. The mites were equally attracted to plants previously exposed to the omnivore and subsequently infested by spider mites (Tetranychus urticae, prey of the predatory mite and the omnivore) and plants infested with spider mites alone. Moreover, the mites were more attracted to plants infested with prey and subsequently exposed to the omnivore than plants infested with prey but not exposed to the omnivore. The predatory mites were also significantly more attracted to plants on which the omnivores were still present. Experience of the predatory mites with volatiles from plants previously exposed to the omnivore and without prey resulted in a loss of the preference for volatiles emitted by plants exposed to the omnivore. Analysis of the volatiles showed that plant exposure to omnivores induced qualitative and quantitative changes in the volatile blend. Together, these results suggest that omnivorous predators induce the production of plant volatiles that can interfere with the searching behaviour of other predators. The consequences of such interference for biological pest control remain to be investigated.
Total sugar, trehalose, glycerol, lipid, and proline content in adult Ophraella communa from two latitudes and their hybrids. a Total sugar; b trehalose; c glycerol; d lipid; and e proline. Data are showed as the mean ± SE. Bars marked with different lowercase letters with the same colour are significantly different between the same sex from two different latitudes, based on t-tests (P < 0.05). Bars marked with “*” are significantly different between hybrids and their parents of the same sex, based on t-tests (P < 0.05)
Relative expression of five identified genes responsible for cold tolerance in three-day-old adult female Ophraella communa from two latitudes and their hybrids. Panels depict the relative expression of: aTret1a; bTret1b; cTret1-2; dP5CS; and eGST. The relative expression levels are showed as the mean ± SE. Bars marked with different lowercase letters with the same colour are significantly different between females from the two latitudes, based on one-way ANOVA followed by an LSD test (P < 0.05). Bars marked with “*” are significantly different between hybrids and their parents of the same sex, based on one-way ANOVA followed by an LSD test (P < 0.05)
Effect of dsRNA on relative mRNA expression, bioassay results, and SCP. a–e Relative mRNA expression levels; f–h trehalose content; i proline content; j GST enzyme activity; and k–o effect of dsRNA on SCPs. Data are showed as the mean ± SE. Bars marked with “*” are significantly different based on one-way ANOVA followed by an LSD test (P < 0.05)
Low winter temperatures severely stress newly arriving insect species. Adaptive evolutionary changes in cold tolerance can facilitate their establishment in new environments. Ambrosia artemisiifolia, a noxious invasive plant, occurs throughout China. Ophraella communa, a biological control agent of A. artemisiifolia, mainly occurs in southern China. However, in 2012, it established populations in Beijing (39.98°N, 115.97°E) following introduction from Laibin (23.62°N, 109.37°E), implying cold adaptation. The mechanisms underlying its rapid evolution of cold tolerance remain unknown. We investigated the levels of cryoprotectants and energy reserves in adult O. communa from two latitudes. In high-latitude insects, we found high trehalose, proline, glycerol, total sugar, and lipid levels; five potential genes (Tret1a, Tret1b, Tret1-2, P5CS, and GST), responsible for regulating cold tolerance and involved in trehalose transport, proline biosynthesis, and glutathione S-transferase activation, were highly expressed. These hybridisation changes could facilitate cold temperature adaptation. We demonstrate the genetic basis underlying rapid adaptation of cold tolerance in O. communa, explaining its extension to higher latitudes. Thus, specialist herbivores can follow host plants by adapting to new temperature environments via rapid genetic evolution.
Assessment of foraging strategy for entomopathogenic nematodes (EPNs). Foraging Strategy was evaluated by a formula, number of EPN infective juveniles (IJs) finding an unrestrained Galleria mellonella larva (mobile) minus those finding a restrained one (non-mobile) divided by the total of them finding both types of host. The value closes to 1.0 called ambush, 0.0 called intermediate, and −1.0 called cruise. Sd: Steinernema diaprepesi; Sk: S. khuongi; Sc: S. carpocapsae. Points and error bars denote means and standard errors, respectively. Means that are significantly different in one-way ANOVA analysis are represented by asterisks (* and ** indicate P < 0.05 and P < 0.01, respectively)
Effects of entomopathogenic nematodes (EPNs) from different classifications of characteristics on their dispersal behavior. Differences of various (A) EPN species, (B) EPN genera and foraging strategy, and (C) EPN biomass in dispersal rates were evaluated. Hb: Heterorhabditis bacteriophora; Hf: H. floridensis; Hi: H. indica; Sc: Steinernema carpocapsae; Sd: S. diaprepesi; Sf: S. feltiae; Sg: S. glaseri; Sk: S. khuongi; Sr: S. riobrave. Bars and error bars denote means and standard errors, respectively. Means that are significantly different in one-way ANOVA analysis and Tukey’s HSD Test are represented by different lowercase (P < 0.05) or asterisks (*** indicates P < 0.001). Significant regression constant and slope were represented by asterisks (* and *** indicate P < 0.05 and P < 0.001, respectively)
Effect of mixed entomopathogenic nematode (EPN) species on dispersal behavior. (A) Dispersal rate of EPN infective juveniles (IJs) treated by single species or two combined species was evaluated. There was equivalent EPN biomass in all treatments. (B) Dispersing IJs were observed on water agar plate. Hi: Heterorhabditis indica; Sd: Steinernema diaprepesi; Sg: S. glaseri. Bars and error bars denote means and standard errors, respectively. Means that are significantly different in one-way ANOVA analysis and Tukey’s HSD Test are represented by different lowercase (P < 0.05)
Assessment of interaction between Steinernema diaprepesi and Heterorhabditis indica by insect mortality. Expected mortality (PE) = P0 + (1−P0) (P1) + (1−P0) (1−P1) (P2), where P0 is the mortality in the control, P1 is the mortality in treatment with S. diaprepesi alone, and P2 is the mortality in treatment with H. indica alone
Combinations of entomopathogenic nematode (EPN) species are sometimes more or less effective than individual species for the management of insect pests. We hypothesized that these outcomes are due in part to dispersal rates that differ when EPN species are conspecific or heterospecific. Dispersal rates of three heterorhabditid species, six steinernematid species, and mixtures of some were assessed using image analysis of nematodes on water agar. The dispersal rates between the genera differed significantly and were unrelated to the estimated body mass or the putative foraging strategy, including that of the recently named Steinernema khuongi, characterized here as a cruise forager (actively search for hosts). Heterorhabditis indica dispersed more rapidly on agar when combined with S. diaprepesi, but not with S. glaseri. The presence of S. diaprepesi in soil microcosms also increased the proximity of H. indica to Galleria mellonella host insects, while H. indica presence reduced the number of G. mellonella killed by S. diaprepesi. Nevertheless, increasing the H. indica dispersal rate did not increase its insecticidal effectiveness, likely due to competition with the more virulent S. diaprepesi. Rather, the effect of combining the species on the mortality of G. mellonella was additive. Our results suggest that interspecific EPN communication affects not only orientation but also dispersal rate, with potential impacts on biological control and the subsequent fitness of each species.
Silicon (Si) has a physical barrier effect on plant tissues, decreasing nematode infection in different crops. Notwithstanding, research on lettuce is lacking, especially regarding the chemical mechanisms of action of this beneficial element. This study evaluated the effect of Si supply on lettuce plants infested with 0, 6000, and 12,000 eggs and second stage juveniles of Meloidogyne incognita, both in the absence and in the presence of Si (2 mM) in the nutrient solution. Silicon increased phenolic compounds and ascorbic acid, reducing M. incognita population and decreasing oxidative stress. The element also increased chlorophyll content and the quantum efficiency of photosystem II (FV/FM), favoring lettuce growth and production. The use of Si decreased the number of nematodes and affected their reproduction, decreasing the number of eggs and galls on lettuce roots. This indicates that Si may serve as a sustainable alternative for the control of M. incognita. The benefit of using Si appears to be due to the combined effect chemical action from the increase in phenolic compounds and ascorbic acid in plant tissues, improving plant physiology. Graphical abstract
Silicon (Si) enhances rice resistance to various insect herbivores. However, the underlying mechanisms remain unclear. Whereas the salicylic acid (SA) signaling pathway plays a vital role in plant defense responses to sucking insects, its role in Si-enhanced rice resistance has not been investigated. Si transporter mutant OsLsi1 and mutants with antisense expression of ICS (as-ics) and NPR1 (as-npr1) in the SA pathway and their corresponding wild types (WT) were treated with and without Si to determine Si effects on rice resistance to brown planthopper (BPH), Nilaparvata lugens (Stål), as well as on SA accumulation, defense-related enzyme activity and gene expression. Si application significantly affected host preference of BPH, significantly reduced honeydew secretion and inhibited oviposition and hatch rate. Upon BPH infestation, SA content, transcript levels of BPH3, ICS1 and PAL4, and activities of POD, SOD, PPO and PAL were significantly higher in Si-treated than untreated plants. The defense responses were also faster. However, OsLsi1 mutant plants displayed higher susceptibility to BPH and minimal defense responses. Furthermore, simultaneous application of SA and Si in WT plants showed the highest resistance to BPH, but had no obvious effect on OsLsi1, antisense as-ics and as-npr1 plants. Our results suggest that Si enhances rice defense against the sucking insect BPH by defense priming and the Si-mediated priming involves SA signaling pathway.
Top-cited authors
Nicolas Desneux
  • INRA (French National Institute for Agricultural Research)
Antonio Biondi
  • University of Catania
Tim Haye
  • Centre for Agricultural Bioscience International
Vaughn Walton
  • Oregon State University
Xingeng Wang
  • United States Department of Agriculture