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Megacopta cribraria. (A) M. cribraria damage in soybean. (B) Close-up of M. cribraria clustering on a soybean plant. (C) M. cribraria adult. (D) M. cribararia nymph. (E) adult on egg mass. (F) detail of egg mass.
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The kudzu bug, Megacopta cribraria (F.) (Heteroptera: Plataspidae), is an invasive insect pest introduced from Asia in 2009 that poses a threat to soybeans (Glycine max [L.] Merr. [Fabales: Fabaceae]) and other legume crops in the United States. Initially discovered in Georgia, M. cribraria rapidly expanded across the southeast until 2014 when a si...
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Phonoctonus lutescens which is a predator of Dysdercus voëlkeri (Schmidt, 1932) is present in cotton fields at the same time as its prey, D. voëlkeri. The objective of this study was to see which of the biological control or chemical control programs spares and maintains the potentially beneficial insects, especially P. lutescens. This study was co...
The kudzu bug, Megacopta cribraria (F.) (Heteroptera: Plataspidae), is an invasive insect pest introduced from Asia in 2009 that poses a threat to soybeans (Glycine max [L.] Merr. [Fabales: Fabaceae]) and other legume crops in the United States. Initially discovered in Georgia, M. cribraria rapidly expanded across the southeast until 2014 when a si...
Citations
... In the past decade, two egg parasitoids of M. cribraria, Paratelenomus saccharalis Dodd (Hymenoptera: Platygastridae) and Ooencyrtus nezarae Ishii (Hymenoptera: Encyrtidae), were discovered in the United States. Although parasitism of M. cribraria by O. nezarae and P. saccharalis is known [6,7], there are gaps in knowledge about the biology of both parasitoids in the United States. Given the ubiquity of parasitoids and their importance in influencing the abundance and dynamics of their hosts [8], it is essential to investigate the factors that affect their performance. ...
... All parasitoid colonies and experiments were conducted in these containers and incubated at 25 ± 1 • C, 14:10 (L:D) h, and 75 ± 5% RH photoperiod to maximize possible emergence [27,28]. Ooencyrtus nezarae and P. saccharalis were distinguished following the characteristics provided by Gardner et al. [6] and Ademokoya et al. [7], respectively, and were separated into different rearing cups. Colonies of the wasps were reared by providing adults with a honey solution (70% honey to 30% water, v/v) and allowing them to oviposit into ≤24 h old M. cribraria eggs. ...
Simple Summary
This research investigated the reproductive characteristics of two egg parasitoids, Paratelenomus saccharalis and Ooencyrtus nezarae, which target Megacoptera cribraria eggs. We evaluated the impact of different food sources, host egg-to-adult parasitoid ratios, and host exposure times on the number and sex ratio of the parasitoid offspring. The findings showed that a honey solution was the preferred dietary source for O. nezarae. Furthermore, a 21:7 host-to-parasitoid ratio yielded the highest and predominantly female offspring for both parasitoids; a host exposure time of three to five days optimized parasitism by O. nezarae, whereas a one-day exposure time optimized parasitism by or P. saccharalis. These findings contribute to our understanding of the biology of both newly discovered egg parasitoids.
Abstract
Parasitoids forage for hosts in dynamic ecosystems and generally have a short period of time to access hosts. The current study examined the optimal reproductive attributes of two egg parasitoids, Paratelenomus saccharalis Dodd (Hymenoptera: Platygastridae) and Ooencyrtus nezarae Ishii (Hymenoptera: Encyrtidae), of the kudzu bug, Megacopta cribraria Fabricius (Hemiptera: Plataspidae). The proportion of O. nezarae and P. saccharalis adult offspring that emerged from M. cribraria eggs and the sex ratio of the parasitoid offspring were compared among treatments for the effects of different adult parasitoid food sources, host egg-to-adult parasitoid ratios, and host exposure times. Our results suggest that honey solution as a food source, a 21:7 host-to-parasitoid ratio, and three-to-five days of exposure time optimized the production of female O. nezarae offspring. For P. saccharalis, honey solution as a food source, a 21:7 host-to-parasitoid ratio, and one day were optimal for maximizing female offspring production. These findings provide new information about the biology of these egg parasitoids.
... A GenBank BLAST of our COI sequences resulted in Ooencyrtus plautus Huang & Noyes (assuming correct identification), from a recently published complete mitochondrial genome study [33] as the top hit. The following 10 similar sequences are as follows: two of Ooencyrtus nezarae from [34], five of Metaphycus flavus, and three of Encyrtidae sp. or Hymenoptera sp. The last three sequences (KJ208550.1, ...
A new species of encyrtid wasp, Ooencyrtus pitosina Polaszek, Noyes & Fusu sp. n., (Hymenoptera: Encyrtidae: Encyrtinae) is described as a gregarious parasitoid in the eggs of the endemic Samoan swallowtail butterfly Papilio godeffroyi (Lepidoptera: Papilionidae) in the Samoan archipelago. It is described here because it is an important natural enemy of this butterfly, and to facilitate identification for future work with this parasitoid and its host.
... Parasitoid species may rely on shared subaeneuus Westwood (Hemiptera: Plataspidae), which was reported in Miami, Florida in 2020 [35]. Ooencyrtus nezarae is a generalist egg parasitoid reported to attack M. cribraria, and pentatomids that occur in Asia, Africa, Australia, and Europe [28,36,37], and in 2016 was first reported in Alabama [38]. Ooencyrtus nezarae is a gregarious parasitoid in eggs of larger hosts, but in eggs of Megacopta spp., it is usually a solitary parasitoid [39]. ...
... In their native range of southeast Asia, P. saccharalis and O. nezarae have been reported to parasitize M. cribraria eggs at rates of 100% and 76.9%, respectively [28,29]. In Alabama, P. saccharalis and O. nezarae have been observed parasitizing kudzu bug eggs in the same soybean field with rates ranging from 42-95% and 82.8-100%, respectively [38], but competition between O. nezarae and P. saccharalis has not been studied in this region. During a three-year field study (2018)(2019)(2020) in central Alabama, the number of P. saccharalis fell sharply. ...
... A decline of P. saccharalis (specialist species) is concerning because this may disrupt the biocontrol of M. cribraria. One potential explanation is the arrival of O. nezarae in 2016 in Alabama [38]. Research is needed to understand how competitive interaction between these two parasitoid species impacts host suppression, and whether competitive interference may disrupt biocontrol. ...
The present study investigated egg parasitoid interspecific interactions between a generalist, Ooencyrtus nezarae Ishii (Hymenoptera: Encyrtidae) and a specialist, Paratelenomus saccharalis Dodd (Hymenoptera: Platygastridae) in a laboratory setting using kudzu bug (Megacopta cribraria Fabricius, (Hemiptera: Plataspidae)) eggs as their shared host. Three experiments were conducted to evaluate the emergence of wasps from parasitized hosts after the simultaneous and sequential release of wasps, monitor aggressive behavior of P. saccharalis, and quantify intraguild predation of O. nezarae larvae on heterospecific P. saccharalis larvae. Results showed that total host egg parasitism was higher when both wasps were released simultaneously than if wasps were released sequentially. Ooencyrtus nezarae produced more total offspring than P. saccharalis in all sequential/simultaneous treatments but produced male offspring in most cases. In the aggressive behavioral experiment, specialist, P. saccharalis used head butting to fight O. nezarae, but no other aggressions were observed. In an experiment examining intraguild predation, O. nezarae was able to develop in host eggs parasitized by P. saccharalis four days earlier, acting as a superior larval competitor. These findings shed light on the potential interspecific interactions between O. nezarae and P. saccharalis, which may determine their relative abundance and influence their compatibility in kudzu bug biological control programs.
... In those locations, parasitism was observed from May to October at levels ranging from 22.4% to 76.9% [8,13]. Ooencyrtus sp. is widely distributed in Korea, Japan, China, Brazil, and Thailand [14,15], and is also reported in North America [16]. ...
... Unlike P. saccharalis, O. nezarae parasitizes eggs of 13 hemipteran species [15], including Pentatomidae, Coreidae, and Alydidae [16]. Parasitism of M. cirbraria on kudzu and catnip (Nepeta cataria) by O. nezarae was first reported in Florida by Diedrick et al. [17] ( Figure 1). ...
... The ratio of Ooencyrtus was higher in July than in August which differs from results in Japan [27]. The work by Ademokoya et al. [16] did not compare populations, but it seems clear that the Alabama and Florida populations are not as established as those in Asia, and it will be interesting to follow the coexistence of the two parasitoids. While Ooencyrtus parasitizing kudzu bugs represents one more possible biological control agent, it is a generalist predator, and more research is needed to evaluate its importance in Florida. ...
Megacopta cribraria (Fabricius) (Hemiptera: Plataspidae), commonly called the kudzu bug, is a pest of concern in many soybean and legume-producing states. It was first detected in the United States in 2009. In the southeastern United States, M. cribraria reduced crop yields by 47% in untreated soybean fields. Paratelenomus saccharalis (Dodd) (Hymenoptera: Platygastridae) is a known parasitoid of the kudzu bug, and a potential biological control agent. This study was comprised of three phases: (1) Preliminary assessment of the presence of the kudzu bug and its parasites in north Florida and south Georgia. (2) Measurements of the levels of parasitism in 12 sites selected from the preliminary evaluation to compare population dynamics in two growing seasons in agricultural, forested, and urban areas. (3) Laboratory studies to measure parasitism after 21 days in controlled environments. The preliminary assessment showed that in both 2016 and 2017, P. saccharalis emerged from eggs of M. cribraria collected in Leon and Gadsden County. Additionally, parasitism was recorded for the recently discovered egg parasitoid in north Florida, Ooencyrtus nezarae (Ishii) (Hymenoptera: Encyrtidae). In the assessment of parasitism in the field, differences were observed in the average level of parasitism within the urban and forest area in both years, and in the agricultural area for 2017. Between-group comparisons indicated significant differences between the average parasitism levels in agricultural, urban, and forested areas in 2016; in 2017, the differences between the areas were not significant. In the laboratory, after 21 days of observation, an average of 77.4% of freshly laid and 61.6% of cooled eggs were parasitized by P. saccharalis, and adult parasitoids emerged. There was a significant difference in the emergence of freshly laid eggs over cooled eggs. This study suggests that both P. saccharalis and O. nezarae exert some levels of natural control of the kudzu bug in the field and may be useful as biological control agents in an integrated pest management program.
... Trissolcus hyalinipennis Rajmohana and Narendran-a parasitoid of Bagrada hilaris (Burmeister)-is another adventive species that has been discovered in the US [106]. Other discoveries of adventive stink bug egg parasitoids include Gryon aetherium Talamas [107], Psix striaticeps (Dodd) [108], and Ooencyrtus nezarae Ishii [109]. However, it should be noted that O. nezarae is a generalist that parasitizes several heteropteran families, including Pentatomidae [109][110][111][112][113][114], in other parts of the world. ...
... Other discoveries of adventive stink bug egg parasitoids include Gryon aetherium Talamas [107], Psix striaticeps (Dodd) [108], and Ooencyrtus nezarae Ishii [109]. However, it should be noted that O. nezarae is a generalist that parasitizes several heteropteran families, including Pentatomidae [109][110][111][112][113][114], in other parts of the world. Among the pentatomids parasitized by O. nezarae are Piezodorus hybneri (Gmelin), Eysarcoris guttiger (Thunberg) [110,112], N. viridula [37,115], Euschistus sp., Acrosternum sp., Edessa sp., and Thyanta sp. ...
Stink bugs comprise a significant and costly pest complex for numerous crops in the US, including row crops, vegetables, and tree fruits and nuts. Most management relies on the use of broad-spectrum and disruptive insecticides with high human and environmental risks associated with them. Growing concerns about pesticide resistance in stink bugs are forcing pest managers to explore safer and more sustainable options. Here, we review the diverse suite of natural enemies of stink bugs in the US, noting that the egg and the late nymphal and adult stages of stink bugs are the most commonly attacked by parasitoids, whereas eggs and young nymphs are the stages most commonly attacked by predators. The effectiveness of stink bugs’ natural enemies varies widely with stink bug species and habitats, influencing the biological control of stink bugs across crops. Historically, biological control of stink bugs has focused on introduction of exotic natural enemies against exotic stink bugs. Conservation and augmentation methods of biological control have received less attention in the US, although there may be good opportunities to utilize these approaches. We identify some considerations for the current and future use of biological control for stink bugs, including the potential for area-wide management approaches.
... Organic bean growers in the southeastern United States may have severely damaged or destroyed crops by and have limited control options for kudzu bugs [19]. Only a few natural enemies of kudzu bugs have been found in the United States [20][21][22][23]. The pathogenic fungus Beauveria bassiana (Bals.-Criv.) ...
This is the first study that examined and compared the survival, LC50, and RR50 estimates of Megacopta cribraria F. (Hemiptera: Plataspidae) nymphs and adults that were exposed to two native Beauveria bassiana isolates (Previously codified as NI8 and KUDSC strains) at four concentrations. The greatest reduction in survival and mortality was observed primarily on or after 10 d post-exposure to B. bassiana isolates. Survival of early instars (2nd, 3rd) were not affected by either strains or concentration at 3 d and 5 d post-exposure. Survival of later instars (5th) and adults was significantly reduced when exposed to the KUDSC strain at all concentrations. Comparison of dose–mortality values (LC50) using resistance ratios (RR50) were significantly different between life stages of the kudzu bug for both strains of B. bassiana. The LC50 values showed that kudzu bug adults are more susceptible than any other life stage when exposed to either strain. The KUDSC strain was more pathogenic than NI8 10 d after exposure, but NI8 exhibited significantly higher pathogenicity than KUDSC 20 d after exposure. Our results suggest potential field application of B. bassiana for kudzu bug control and their integration into pest management strategies to suppress them before they cause economic damage to soybean crops.
... The bean plataspid, Megacopta cribraria (Fabricius) (Hemiptera: Plataspidae), is an invasive pest of leguminous crops in the south-eastern United States that was eventually followed by two parasitoid wasps from its range in the eastern hemisphere, Paratelenomus saccharalis (Dodd) (Scelionidae) and Ooencyrtus nezarae Ishii (Encyrtidae). In North Central Florida, sentinel egg masses, intended to capture Paratelenomus saccharalis, instead yielded Ooencyrtus nezarae, which was previously known only from Alabama (Ademokoya et al. 2018). Two generations of O. nezarae were subsequently reared in the laboratory. ...
... Thus, egg parasitoids have the potential to arrive adventively in new areas. In addition to T. japonicus, three other species of hymenopteran egg parasitoid of pentatomoids have unexpectedly emerged in the United States within the last five years: T. hyalinipennis Rajmohana & Narendran, a parasitoid of Bagrada hilaris (Burmeister) (Pentatomidae), was discovered in California (Ganjisaffar et al. 2018); Paratelenomus saccharalis, a specialist egg parasitoid of Megacopta cribraria, was detected in Georgia and Florida (Gardner et al. 2013, Medal et al. 2015; and Ooencyrtus nezarae, a generalist egg parasitoid, was reared from M. cribraria in Alabama in 2016 (Ademokoya et al. 2018). ...
... Laboratory reared specimens were compared to descriptions in Ishii (1928), Zhang et al. (2005) and Ademokoya et al. (2018). The morphology of the specimens was consistent with the diagnoses given in these references (see Figs 1, 2, 3): frontovertex approximately 1/3 of head width; ocelli forming an obtuse triangle; posterior ocelli closer to compound eye than to occipital margin; mandible with crenulated truncation and distal tooth; stigmal vein of wings longer than postmarginal vein; linea calva open posteriorly; dark colouration on coxae, mesal femora, sub-basal tibiae and apical tarsi; the rest of the legs whitish-yellow; body dark with bluish metallic sheen; reticulation present on most of body; apex of scutellum smooth. ...
The adventive arrival of biological control agents circumvents the regulatory process by introducing exotic species to control invasive pests and is generally followed by post hoc risk evaluation. The bean plataspid, Megacopta cribraria (Fabricius) (Hemiptera: Plataspidae), is an invasive pest of leguminous crops in the south-eastern United States that was eventually followed by two parasitoid wasps from its range in the eastern hemisphere, Paratelenomus saccharalis (Dodd) (Scelionidae) and Ooencyrtus nezarae Ishii (Encyrtidae). In North Central Florida, sentinel egg masses, intended to capture Paratelenomus saccharalis , instead yielded Ooencyrtus nezarae , which was previously known only from Alabama (Ademokoya et al. 2018). Two generations of O. nezarae were subsequently reared in the laboratory. COI sequences from the Florida population of O. nezarae differed by 1.3% from the Alabama population and the presence of a different haplotype suggests the possibility of a separate introduction. Laboratory parasitism rates, sex ratios, morphology, molecular diagnosis and implications for agriculture are discussed.
... Kudzu bug eggs are attacked by at least two parasitoid wasp species: Paratelenomus saccharalis (Dodd) and Ooencyrtus nezarae Ishii. Neither were previously reported in the United States and both are thought to have arrived through the subsequent introduction of parasitized host eggs (Gardner et al. 2013;Dhammi et al. 2016;Ademokoya et al. 2018). Paratelenomus saccharalis and O. nezarae were first observed and identified from samples collected in Georgia in 2013 and Alabama in 2016, respectively (Gardner et al. 2013;Ademokoya et al. 2018). ...
... Neither were previously reported in the United States and both are thought to have arrived through the subsequent introduction of parasitized host eggs (Gardner et al. 2013;Dhammi et al. 2016;Ademokoya et al. 2018). Paratelenomus saccharalis and O. nezarae were first observed and identified from samples collected in Georgia in 2013 and Alabama in 2016, respectively (Gardner et al. 2013;Ademokoya et al. 2018). However, other wasps from the genus Ooencyrtus were collected in Virginia in 2015 and may be the same species (Dhammi et al. 2016; Ademokoya et al. . ...
... Examination of the map of kudzu bug spread ( Fig. 1) suggests that their spread rate has declined rapidly in the last few years, leading Ademokoya et al. (2018) to suggest that this may be a consequence of introduced parasitoids and other natural enemies. The fact that the parasitoids in this study were able to overtake the spreading kudzu bug populations (both surveyed frontline populations suffered parasitism), suggests that they are capable of dispersal distances comparable to or greater than their hosts. ...
Individuals at the frontlines of expanding populations tend to experience less parasitism than those in the core of their range. This reduction in parasitism may contribute to the rapid spread of invasive species because parasites could otherwise reduce host population growth. To better understand patterns of parasitism in the invasive population of the kudzu bug, Megacopta cribraria (F.), we examined how both the proportion of eggs parasitized and the incidence of parasitism—presence or absence of parasitism within a clutch of eggs—varied with distance from the kudzu bug’s site of introduction and with their density at two different spatial scales: at the level of sites (10–20 m²) and the level of the egg clutch (number of eggs in a clutch). Egg clutches were collected from populations along an east–west and a south-north transect of the U.S. invasion. We found that both metrics of parasitism declined with increasing host-density at the site level, which may be a general trend for the wind-dispersed parasites of invasive species. We also found that both metrics of parasitism declined with increasing distance from the site of introduction. However, since kudzu bug density tended to decrease across their invasion gradient and parasitism rates increased with decreasing kudzu bug density, the reductions in parasitism with increasing distance from site of introduction were not discernible if the effect of site-level density was not accounted for; leaving site-level density out of our models made it seem as though there was no distance effect. This finding complicates models that exhibit a “honeymoon phase”, where vanguard populations of the host suffer from little or no parasitism. In addition, we observed a small effect of clutch size on the incidence of parasitism, but no interaction among the spatial scales of density investigated. Our results underscore the importance of considering host density at different scales when seeking to understand trends in parasitism across a host’s invasive range.
The kudzu bug, Megacopta cribraria (Fabricius) (Hemiptera: Plataspidae), is a major economic pest of soybean in the southeastern United States. With climate warming, this pest is expected to move northward and cause additional crop damage. Parasitoid biocontrol is a potential method of integrated pest management for kudzu bug. Two species of egg parasitoid wasps have been observed emerging from kudzu bug egg masses in the southeastern United States: Paratelenomus saccharalis (Dodd) (Hymenoptera: Platygastridae) and Ooencyrtus nezarae (Ishii) (Hymenoptera: Encyrtidae). This paper used egg mass emergence data collected between 2018 and 2020 in Alabama soybean fields and compared the data to weather indices. Indices included the number of days with minimum temperatures below zero, accumulated rainfall (mm m−2), as well as species specific metrics of accumulated growing degree days, accumulated daily minimum temperature (°C), and accumulated daily maximum temperature (°C). Emergence of the generalist parasitoid, O. nezarae, was highly correlated with kudzu bug nymph abundance, accumulated degree day, accumulated daily temperatures, and precipitation. Ooencyrtus nezarae emergence was predicted in a stepwise regression equation by aggregated degree day and date of collection, which indicates that seasonality may be a predictor of its presence. In contrast, collections of the specialist parasitoid, P. saccharalis, were near-zero throughout the collection period, suggesting that this species may no longer be a usable biocontrol agent in the southeastern United States as a result of external limiting factors.
Ooencyrtus lucidus Triapitsyn & Ganjisaffar (Hymenoptera: Encyrtidae) was recently recovered from fresh sentinel eggs of Bagrada hilaris (Burmeister) (Hemiptera: Pentatomidae) in California. In the present study, life history traits of O. lucidus were studied at 26 ± 0.5 • C, 40 ± 10% RH, and a photoperiod of 14 L: 10 D hours. Results showed that 95.2% of the parasitized eggs yielded successful emergence of adults. The total immature developmental time was 14.27 and 13.95 days for females and males, respectively. The sex ratio of O. lucidus was 0.5 (females/offspring). Mated females laid on average 6.0 eggs per day and 222.7 eggs during their mean ovipositional period of 37.3 days. There was no significant difference in reproduction parameters between mated and non-mated females. The net reproductive rate (R 0) was 103.8 females/female/generation, the intrinsic rate of increase (r m) was 0.171 females/female/day, the finite rate of increase (λ) was 1.187 population multiplication/day, the mean generation time (T) was 27.1 days, and the doubling time (DT) was 4.0 days. The highest longevity was observed in mated and non-mated females fed with honey, and they lived for 70.8 and 70.1 days, respectively. Providing females with host eggs in addition to honey, reduced their longevity by 24% in mated and 28% in non-mated individuals. Non-mated females and males deprived of honey only lived for 3.5 and 2.5 days after emergence, respectively. Our results indicate that O. lucidus has sufficient life history traits to make it a promising egg parasitoid for the biological control of B. hilaris.
