Effect of sublethal concentrations of the bioinsecticide spinosyn treatment of Trichoplusia ni eggs on the caterpillar and its parasitoid, Trichogramma brassicae.

BACKGROUND: Integrated Pest Management (IPM) seeks to combine multiple management strategies for optimal pest control. One method that is successfully employed in IPM is the use of beneficial organisms. However, in severe circumstances when pest insects exceed threshold limits, insecticides may still need to be implemented. Thus, understanding the effects of insecticides on biocontrol agents, such as parasitoid wasps, is paramount to ensure sustainable agroecosystems. Sublethal effects of the bioinsecticide spinosyn, a mixture of the bacterial Saccharopolyspora spinosa (Mertz and Yao) fermentation products spinosyn A and D, on eggs of Trichoplusia ni (Hübner), a cruciferous crop pest, and its egg parasitoid Trichogramma brassicae (Bezdenko) was investigated. RESULTS: The LC50 for spinosyn A and D (dissolved in ethanol) on T. ni eggs is 54 ng mL-1. Transcriptomics on caterpillars (1st and 3rd instars) that hatched from eggs treated with sublethal concentrations of spinosyn identified the upregulation of several genes encoding proteins that may be involved in insecticide resistance including detoxification enzymes, such as cytochrome P450s, glutathione S-transferases and esterases. Sublethal T. ni egg treatments did not affect parasitoid emergence, however, there was a marked increase in the size of T. brassicae hind tibia and wings that emerged from spinosyn-treated eggs. CONCLUSIONS: For the caterpillar, treatment of eggs with sublethal concentrations of spinosyn may induce insecticide resistance mechanisms. For the parasitoids, their increased size when reared in spinosyn-treated eggs suggests that the emerged wasps may have higher performance. © 2024 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Contrasting reproductive traits of competing parasitoids facilitate coexistence on a shared host pest in a biological control perspective.

BACKGROUND: Interspecific competition in insect parasitoids is an important ecological phenomenon that has relevant implications for biological pest control. To date, interspecific intrinsic (=larval) competition has been intensively studied, while investigations on extrinsic (=adult) competition have often lagged behind. In this study we examined the role played by parasitoid reproductive traits and host clutch size on the outcome of extrinsic competition between Trissolcus basalis (Wollaston) and Ooencyrtus telenomicida (Vassiliev), two egg parasitoids of the pest Nezara viridula (L). Laboratory experiments were conducted by allowing both parasitoid species to exploit an egg mass made of 10, 20, 30, or 40 hosts through single or simultaneous releases. Furthermore, under field conditions, egg masses consisting of 10 or 40 hosts were exposed in a tomato crop in order to validate laboratory investigation. RESULTS: The results show that the egg mass size is an important predictor of extrinsic competition in our study system as a higher proportion of T. basalis emerged from large egg masses, while O. telenomicida dominated in small egg masses. Analysis of reproductive traits of parasitoid species indicates that T. basalis has superior abilities in host exploitation compared with O. telenomicida. CONCLUSIONS: We found that contrasting reproductive traits of two competing egg parasitoid species facilitate coexistence on a shared stink bug host. This work also highlights the importance to consider extrinsic competitive interactions between parasitoid species in a biological control perspective. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

The effect of temperature on host patch exploitation by an egg parasitoid.

The effect of temperature during host patch exploitation by parasitoids remains poorly understood, despite its importance on female reproductive success. Under laboratory conditions, we explored the behaviour of Anaphes listronoti, an egg parasitoid of the carrot weevil, Listronotus oregonensis, when foraging on a host patch at five temperatures. Temperature had a strong effect on the female tendency to exploit the patch: A. listronoti females parasitized more eggs at intermediate temperature (20 to 30°C) compared to those foraging at the extreme of the range (15.9°C and 32.8°C). However, there was no difference in offspring sex-ratio and clutch size between temperature treatments. Mechanisms of host acceptance within a patch differed between temperatures, especially at 32.8°C where females used ovipositor insertion rather than antennal contact to assess whether a host was already parasitized or not, suggesting that host handling and chemical cues detection were probably constrained at high temperature. Females spent less time on the host patch with increasing temperatures, but temperature had no effect on patch-leaving rules. Our results show that foraging A. listronoti females behave better than expected at sub-optimal temperatures, but worse than expected at supra-optimal temperatures. This could impair parasitoid performance under ongoing climate change.

Telenomus nizwaensis (Hymenoptera: Scelionidae), an important egg parasitoid of the pomegranate butterfly Deudorix livia Klug (Lepidoptera: Lycaenidae) in Oman.

The pomegranate butterfly Deudorix (= Virachola) livia is the major pest of pomegranate, a crop of economic importance, in Oman. A species of parasitoid wasp in the hymenopteran family Scelionidae is responsible for high levels of mortality of its eggs. This wasp is described herein as Telenomus nizwaensis Polaszek sp. n., based on morphology and DNA sequence data. T. nizwaensis is currently known only from D. livia, which is also a pest of economic importance on other crops in North Africa, the Arabian Peninsula, and the Mediterranean. We summarise current knowledge of T. nizwaensis life-history and its potential to provide biological pest control.

High Egg Reduction Rate but poor clearance of Circulating Cathodic Antigen three weeks after Praziquantel treatment among school children on Ijinga Island, north-western Tanzania.

Traditionally, efficacy of Praziquantel (PZQ) is monitored using Parasitological Cure Rates and Egg Reduction Rates applying Kato Katz (KK) technique. This parasitological technique has a number of limitations. Recently, the Point-of-Care Circulating Cathodic Antigen (POC-CCA) rapid test which is a highly sensitive technique, has emerged as a promising candidate to be used for evaluating the efficacy of PZQ. A prospective longitudinal study was conducted among 399 school children aged 7-17 years on Ijinga Island, north-western Tanzania. At baseline and three weeks after treatment, stool and urine samples were collected from participating school children and screened for S. mansoni infection using the KK technique as well as POC-CCA test. All S. mansoni infected children at baseline were treated with 40mg/kg of PZQ and followed up after three weeks. At baseline, the overall prevalence of S. mansoni infection was 56.6% (95%CI: 51.7-61.4) and 99.7% (95%CI: 98.2-99.9) (considering trace as positive) using KK technique and POC-CCA test, respectively. Three weeks after treatment, the prevalence of S. mansoni was 0.92% using the KK technique and 97.7% when applying the POC-CCA test. The parasitological cure rates based on KK technique and POC-CCA were 99.1% (95%CI: 97.5-99.8) and 2.3% (95%CI: 1.2-4.5). Egg Reduction Rate was 99.1%. Based on WHO guidelines using the KK technique, at three weeks point, the efficacy of PZQ is satisfactory. However, the assessment of the efficacy of PZQ using POC-CCA tests needs further evaluation.

An Integrative Taxonomy of a New Species of Trichogramma Westwood (Hymenoptera: Trichogrammatidae) with High Reproductive Capacity.

A new species of Trichogramma Westwood (Hymenoptera: Trichogrammatidae) is described: Trichogramma foersteri sp. nov. Takahashi from eggs of Anticarsia gemmatalis Hübner, (Lepidoptera: Erebidae) a major soybean defoliating pest. The parasitoid was collected in São José dos Pinhais, Paraná State, Brazil, and molecular and morphological characters were used to confirm the identity of the new species. Preliminary biological data are provided to demonstrate its high capacity of parasitism. The new species is a potential candidate as a biological control agent against some lepidopteran-pests.

Effect of crop residue management on damage by Diatraea saccharalis (Lepidoptera: Crambidae), its egg parasitoids and the ants associated with sugarcane.

In the American continent, the sugarcane borer Diatraea saccharalis (F.) is the main pest in sugarcane producing areas. The objective of this study was to assess the effect of crop residue management on damage by D. saccharalis, its egg parasitoids and the ants associated with sugarcane. The study was carried out during 2011-2012, 2012-2013 and 2013-2014 crop cycles, in three commercial fields located in different regions of Tucumán state, Argentina. Two types of crop residue management (= treatments) were compared: conservation of trash at the soil surface (CT) and trash burning (TB). In 'trash conservation' treatment, crop residue was allowed to remain over the soil surface during the whole sugarcane growing season, while the second treatment consisted of complete burning of trash blanket approximately 2 weeks after harvest. The injury level was measured by recording the number of stalks bored and internodes bored. Parasitism was estimated by counting the total number of eggs and number of black eggs (which indicates the occurrence of egg parasitoids). Ants (Formicidae) richness was calculated by two estimators; abundance-based coverage estimator and incidence-based coverage estimator, using the non-parametric richness estimators: Chao 2 and Jackknife. Finally, the indicator value was estimated through the measurement of specificity and fidelity. In all the parameters studied no significant difference was found between TB and CT treatments.

Oviduct Fluke (Prosthogonimus macrorchis) Found Inside a Chicken Egg in North Carolina.

A video received by faculty at North Carolina State University's Prestage Department of Poultry Science revealed a live parasite inside a chicken egg. The parasite was identified as an oviduct fluke (Prosthogonimus macrorchis), a trematode with a three-host life cycle: the primary host, a galliform bird, then an aquatic snail, and finally a dragonfly larva or adult consumed by the infected bird. The egg was from a "backyard flock" with access to a watercourse. No other instances of this parasite were seen in eggs from the flock. The presence of this parasite inside an egg suggests that the worms had migrated above the shell gland in the oviduct to be incorporated inside the egg. Currently, the occurrence of an oviduct fluke inside an egg in the United States is rare. Such parasites are not found in eggs from caged layers because those birds do not have access to watercourses. This case reinforces the view that parasites requiring intermediate hosts may become more common in birds reared under free-range conditions.

Tachinobia repanda (Hymenoptera: Eulophidae) From Egg Sacs of a Colonial Spider, Cyrtophora moluccensis (Araneae: Araneidae) in Papua New Guinea.

We report the discovery of the wasp Tachinobia repanda Boucek collected from egg sacs of the colonial spider Cyrtophora moluccensis (Doleschall) in Morobe Province, Papua New Guinea (PNG) by Lubin, Y.D. in 1980. This is the first record of T. repanda from egg sacs of a colonial spider. The likely host of this eulophid wasp was the larvae of a sarcophagid fly that parasitizes the egg sacs of these spiders. The 67 T. repanda collected were all females and varied little in body size. We suggest that this species is a gregarious hyperparasitoid.

Interrelationships of vitelline and muscle cells within the vitelline follicles of the blood fluke Aporocotyle simplex (Digenea, Aporocotylidae) and morphological evidence for the modification of vitelline material for eggshell formation.

This study of the fish blood fluke Aporocotyle simplex represents the first detailed transmission electron microscopical (TEM) investigation of the vitellarium of an aporocotylid digenean blood fluke. It revealed some unusual characteristics in the cytoarchitecture of the vitelline follicles and demonstrated modifications of the vitelline granules for eggshell formation. The vitelline follicles consist of vitellocytes at different developmental stages surrounded by sarcoplasmic processes of myocytes which occur throughout each follicle. Sites of intimate contact occur between the vitellocytes and the myocytes. Individual vitelline globules (0.1-0.2 µm in diameter) accumulate in quite small clusters of 10-20 and have a dense, heterogeneous matrix possessing central and peripheral regions with a greater density. Modifications of the vitelline globules take place within the clusters and are first apparent when the vitellocytes reach the lumen of the vitelline duct and vitelline reservoir. Globules within the clusters become confluent, and, when the vitellocytes reach the lumen of the oviduct and proximal ootype, these consolidated clusters contain a shapeless, loosely packed, dense material which is released from the vitellocytes by exocytosis. This investigation has provided morphological evidence for shell formation from modified vitelline globules in the form of a discontinuous, thin layer (~ 0.07 µm in thickness) of electron-dense shell material around the fertilized ovum and associated vitellocytes in the proximal ootype. The eggshell of intra-uterine eggs acquires an additional thin, heterogeneous outer layer, increasing its thickness to ~ 0.1 µm. The cytoarchitecture of the vitellarium, modifications of the vitelline globules within the clusters and the structure of the eggshell of A. simplex may prove to be of value in studies examining relationships between the three distinct lineages of aporocotylid digeneans.

Molecular and light microscopy evidence for the transfer of Myxobolus honghuensis from Carassius auratus gibelio broodfish to progeny.

Myxozoans usually have a complex life cycle involving indirect transmission between vertebrate and invertebrate hosts. The vertical transmission of these parasites in vertebrate hosts has not been documented so far. Here, we assessed whether the myxozoan parasite Myxobolus honghuensis is vertically transmitted in naturally infected allogynogenetic gibel carp Carassius auratus gibelio (Bloch). M. honghuensis infection of broodfish, fertilized eggs and laboratory-cultured progeny was monitored in 2018 and 2019. The presporogonic stage was microscopically observed in the pharynx of broodfish and their progeny. In situ hybridization confirmed the presence of M. honghuensis presporogonic stage in the pharynx of broodfish and progeny. Nested PCR results showed that M. honghuensis was present in tissues and eggs of broodfish, fertilized eggs and their corresponding progeny. The sequences obtained from broodfish and progeny showed 98.0-99.8% similarity with ITS-5.8S rDNA of M. honghuensis. This study provides molecular and light microscopy evidence for the transfer of M. honghuensis from broodfish to progeny via the eggs, but it is insufficient to assert that M. honghuensis can transmit vertically in naturally infected allogynogenetic gibel carp. This is the first record about vertical transfer of myxozoan in the vertebrate host.

Susceptibility of the floodwater mosquito Aedes albifasciatus from eggs of different dormancy times to the nematode parasite Strelkovimermis spiculatus.

This study aimed to evaluate the effects of egg dormancy times on susceptibility of larvae of the floodwater mosquito Aedes albifasciatus (Diptera: Culicidae) to parasitism by their natural enemy Strelkovimermis spiculatus (Nematoda: Mermithidae) and on their life history traits. Aedes albifasciatus eggs stored for 2, 4, 6, 8 and 10 months were hatched, and the larvae either exposed to S. spiculatus (treatment group) or not exposed (control group). Egg dormancy time had a negative effect on the retention of parasites, but no effect on the prevalence and intensity of parasitism or the melanization of nematodes. The survival to adulthood of control individuals decreased as dormancy time increased, whereas that of exposed individuals that remained uninfected was constant and low. A trend towards increasing development times with longer dormancy times was detected in the control group, but not in the exposed noninfected group. The results suggest nonconsumptive effects of parasites in exposed but not infected larvae from eggs with short dormancy times. In contrast, the relatively low fitness of larvae from eggs with long dormancy times regardless of their contact with the nematodes may be the result of the nutritional deprivation during the egg stage.

How to escape from insect egg parasitoids: a review of potential factors explaining parasitoid absence across the Insecta.

The egg is the first life stage directly exposed to the environment in oviparous animals, including many vertebrates and most arthropods. Eggs are vulnerable and prone to mortality risks. In arthropods, one of the most common egg mortality factors is attack from parasitoids. Yet, parasitoids that attack the egg stage are absent in more than half of all insect (sub)orders. In this review, we explore possible causes explaining why eggs of some insect taxa are not parasitized. Many insect (sub)orders that are not attacked by egg parasitoids lack herbivorous species, with some notable exceptions. Factors we consider to have led to escape from egg parasitism are parental egg care, rapid egg development, small egg size, hiding eggs, by e.g. placing them into the soil, applying egg coatings or having thick chorions preventing egg penetration, eusociality, and egg cannibalism. A quantitative network analysis of host-parasitoid associations shows that the five most-speciose genera of egg parasitoids display patterns of specificity with respect to certain insect orders, especially Lepidoptera and Hemiptera, largely including herbivorous species that deposit their eggs on plants. Finally, we discuss the many counteradaptations that particularly herbivorous species have developed to lower the risk of attack by egg parasitoids.

Mechanism and consequences for avoidance of superparasitism in the solitary parasitoid Cotesia vestalis.

A parasitoid's decision to reject or accept a potential host is fundamental to its fitness. Superparasitism, in which more than one egg of a given parasitoid species can deposit in a single host, is usually considered sub-optimal in systems where the host is able to support the development of only a single parasitoid. It follows that selection pressure may drive the capacity for parasitoids to recognize parasitized hosts, especially if there is a fitness cost of superparasitism. Here, we used microsatellite studies of two distinct populations of Cotesia vestalis to demonstrate that an egg laid into a diamondback moth (Plutella xylostella) larva that was parasitized by a conspecific parasitoid 10 min, 2 or 6 h previously was as likely to develop and emerge successfully as was the first-laid egg. Consistent with this, a naive parasitoid encountering its first host was equally likely to accept a healthy larva as one parasitized 10 min prior, though handling time of parasitized hosts was extended. For second and third host encounters, parasitized hosts were less readily accepted than healthy larvae. If 12 h elapsed between parasitism events, the second-laid egg was much less likely to develop. Discrimination between parasitized and healthy hosts was evident when females were allowed physical contact with hosts, and healthy hosts were rendered less acceptable by manual injection of parasitoid venom into their hemolymph. Collectively, these results show a limited capacity to discriminate parasitized from healthy larvae despite a viability cost associated with failing to avoid superparasitism.

Biological characteristics of Trissolcus urichi (Crawford) (Hymenoptera: Scelionidae) on Euschistus heros (Fabricius) and Dichelops melacanthus (Dallas) (Hemiptera: Pentatomidae) Eggs.

Species of the genus Trissolcus are effective as egg parasitoids of Euschistus heros and can potentially be used in a multispecies pest management approach. However, in order to successfully use those biocontrol agents in the field, previous detailed knowledge about their life history are necessary. Therefore, we evaluate some biological characteristics of Trissolcus urichi on Euschistus heros and Dichelops melacanthus eggs. Three independent experiments were performed: (1) T. urichi host preference between E. heros and D. melacanthus eggs. (2) T. urichi eggs-adult period (days), number of parasitized eggs in 24 h, emergence rate (%) and sex ratio of the parasitoid in E. heros and D. melacanthus eggs. (3) Morphometric characteristics of T. urichi grown on E. heros and D. melacanthus eggs. Trissolcus urichi preferred to parasitize E. heros eggs, exhibiting a higher number of parasitized eggs, higher rate of emergence (%) and faster development, as well as producing progeny of larger size than the parasitoids emerged from eggs of D. melacanthus in relation to body length, wing length and width. Thus, it can be concluded that T. urichi had better performance on E. heros eggs, although the parasitoid had also acceptable parasitism capacity and development in D. melacanthus eggs.

Epidemiology of Polypodium hydriforme in American Paddlefish.

Polypodium hydriforme is a parasitic cnidarian that develops within the eggs of acipenseriform fish in the Old and New Worlds. Currently regarded as monotypic, P. hydriforme has been studied largely in the context of caviar production in Russian sturgeon species. We report the first robust epidemiological study of P. hydriforme in North American acipenseriform fish. We sampled infection prevalences (in 2017 and 2018) and intensities (in 2017) during annual surveys of American Paddlefish, Polyodon spathula, caught during spawning migration in north-eastern Oklahoma. Egg masses were characterized for the presence and intensity of P. hydriforme infection. Prevalences were similar in 2017 and 2018 (49% and 45%, respectively). Generally, a small number of eggs were infected per egg mass, but a few were heavily infected. Longer, heavier and older fish are more likely to be infected and to harbour more severe infections. In addition, infection is linked to decreases in roe fat weight independently of fish length, weight, age or roe weight. Infection thus diminishes Paddlefish energy reserves (roe fat) which could in turn impact host fitness. Our results raise questions about the impacts of infection on caviar production and Paddlefish conservation and suggest insights on infection dynamics and parasite strategies.

Kairomones from Euschistus heros egg masses and their potential use for Telenomus podisi parasitism improvement.

Telenomus podisi Ashmead (Hymenoptera: Scelionidae) is the most important egg parasitoid of Euschistus heros (Fabricius) (Hemiptera: Pentatomidae), and its successful parasitism is related to their searching ability to find suitable hosts under a complex chemical environment using host-reliable cues. Thus, the objective of this study was to elucidate chemical substances on the external layer of E. heros eggs and report its potential kairomonal activity on T. podisi. We tested female wasps in olfactometer system to synthetic compounds obtained from a chemical identification of E. heros egg masses. The synthetic blend was also evaluated in parasitism tests under laboratory and semi-field conditions. We identified 31 substances from egg surface extracts, including monoterpenes, aldehydes and alkanes. Among those compounds, a synthetic solution including camphene, ß-pinene, limonene and benzaldehyde-induced chemotaxic behaviour on the wasps and increased the parasitism on E. heros eggs, either in laboratory or semi-field test, suggesting its potential use to T. podisi manipulation and parasitism improvement.

Side effects of chlorantraniliprole, phosalone and spinosad on the egg parasitoid, Trichogramma brassicae.

The combined use of chemicals and biological control is not always a successful strategy owing to the potential side effects on biocontrol agents. Lethal and sublethal effects of three commonly used insecticides were assessed on adult and immature stages of the egg parasitoid Trichogramma brassicae Bezdenko (Hymenoptera: Trichogrammatidae). Recommended field concentrations of chlorantraniliprole, phosalone and spinosad caused mortality on preimaginal stages by 24, 87, and 98%, respectively. Lethal effects on parasitoid adults exposed to the insecticide dry residues were estimated as median lethal concentrations (LC50) that were 13.28, 0.25, and 0.03 µg a.i. ml-1 for chlorantraniliprole, phosalone, and spinosad, respectively. The effect of a low lethal concentration (LC30) of the compounds was evaluated on various adult biological traits, such as longevity, fecundity, emergence rate and other life table parameters. All compounds caused detrimental effects on all the estimated demographical indexes. Chlorantraniliprole affected the net reproductive rate, mean generation time and doubling time in comparison to the control; while, phosalone and spinosad adversely affected all assessed parameters. Phosalone and spinosad significantly reduced gross reproductive rate, net reproductive rate, intrinsic rate of increase, finite rate of increase, mean generation time and doubling time and reduced longevity, fecundity, emergence rate related to other biological parameters in comparison with control. The results suggest that all compounds are not fully compatible with the activity of T. brassicae, and that the inclusion of chlorantraniprole, spinosad and phosalone into Integrated Pest Management (IPM) involving this parasitoid has to be avoided. Nevertheless, further studies in open field conditions and on a multiple generation scale are necessary for providing a more definitive conclusion on the IPM suitability of the three tested insectcides.

Suitability of Chinese oak silkworm eggs for the multigenerational rearing of the parasitoid Trichogramma leucaniae.

Trichogramma leucaniae is believed to be an efficient biological control agent for controlling the soybean pod borer [SPB; Leguminivora glycinivorella]. The large eggs of Chinese oak silkworm, Antheraea pernyi, are one of the best alternative host for mass production of Trichogramma. However, they are considered poor host for the growth and development of T. leucaniae. Here, we determine the feasibility of successive rearings of T. leucaniae on the large eggs for eight generations and evaluated their capacity of parasitizing SPB eggs of different ages. In the first four generations, the suitability of T. leucaniae reared on large eggs exhibited a significant increasing tendency and then decreased with the successive generations thereafter. The percentage of parasitized eggs and number of emerged adults per egg were increased from 40.0% and 10.8 adults/egg in F1 generation to 86.7% and 36.4 adults/egg in F4 generation respectively. In addition, T. leucaniae reared on A. pernyi for four generations significantly parasitized more SPB eggs regardless of egg age compared with those reared on Corcyra cephalonica eggs. These results provided useful information on the feasibility of mass production of T. leucaniae by reared for successive generations on A. pernyi large eggs.