Implementing Mass Rearing of Trissolcus japonicus (Hymenoptera: Scelionidae) on Cold-Stored Host Eggs

Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), a pest of Asian origin, has been causing severe damage to Italian agriculture. The application of classical biological control by the release of Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae), an exotic egg parasitoid, appears to be one promising solution. In Italy, releases of T. japonicus in the field were authorized in 2020. In this study, some parameters that could influence the rearing of T. japonicus in insectaries were investigated. A significantly higher production of progeny was observed on host eggs stored at 6 °C (86.5%) compared to −24 °C (48.8%) for up to two months prior to exposure to parasitism. There were no significant differences in progeny production from single females in a vial provided with only one egg mass (83.2%) or 10 females inside a cage with 6 egg masses (83.9%). The exposure of parasitoids to refrigerated (6 °C) egg masses of H. halys for 72 h led to a significantly higher production of progeny (62.1%) compared to shorter exposures for 48 (44.0%) or 24 h (37.1%). A decline in production of progeny by the same female was detected between the first (62.1%) and the second parasitization (41.3%). Adult parasitoids stored at 16 °C for up to 90 days had an 87.1% survival rate, but a significant decrease in progeny production was detected. These parameters could be adjusted when rearing T. japonicus for specific aims such as the production of individuals for field release or colony maintenance.

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Influence of Holding Conditions and Storage Duration of Halyomorpha halys (Hemiptera: Pentatomidae) Eggs on Adventive and Quarantine Populations of Trissolcus japonicus (Hymenoptera: Scelionidae) Behavior and Parasitism Success

Environmental Entomology ◽

10.1093/ee/nvaa183 ◽

2021 ◽

Author(s):

Dalton C Ludwick ◽

Layne B Leake ◽

William R Morrison ◽

Jesús R Lara ◽

Mark S Hoddle ◽

...

Keyword(s):

United States ◽

Classical Biological Control ◽

The United States ◽

Invasive Pest ◽

Egg Mass ◽

Halyomorpha Halys ◽

Storage Duration ◽

Egg Masses ◽

Trissolcus Japonicus ◽

And Storage

Abstract Halyomorpha halys (Stål) is an invasive pest in the United States and other countries. In its native range, H. halys eggs are parasitized by a co-evolved parasitoid, Trissolcus japonicus (Ashmead). In the United States, T. japonicus, a classical biological control candidate, is being redistributed in many states where adventive populations exist. To establish if H. halys egg holding conditions affect T. japonicus foraging behavior or successful parasitism, naïve, female parasitoids from an adventive population were allowed to forage in laboratory bioassay arenas with either fresh or frozen (−20 or −80°C) egg masses, the latter held for five durations ranging from 1 h to 112 d. Parasitoid movements were recorded for 1 h. Thereafter, parasitoids were transferred with the same egg mass for 23 h. Additionally, female parasitoids from a quarantine colony were exposed to: 1) pairs of fresh egg masses and egg masses frozen at −40°C (>24 h) or 2) a single fresh egg mass or egg mass frozen at −40°C (<1 h). All exposed egg masses were held to assess progeny emergence. In the foraging bioassay, holding temperature and storage duration appeared to influence host-finding and host quality. Egg masses held at −80°C and fresh egg masses resulted in significantly greater levels of parasitism and progeny emergence compared with eggs held at −20°C. No differences were recorded between egg masses held at −40°C for ≤1 h and fresh egg masses. These results will help refine methods for preparation of egg masses for sentinel monitoring and parasitoid mass rearing protocols.

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Integrative taxonomy and phylogeography of Telenomus remus (Scelionidae), with the first record of natural parasitism of Spodoptera spp. in Brazil

Scientific Reports ◽

10.1038/s41598-021-93510-3 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Ana P. G. S. Wengrat ◽

Aloisio Coelho Junior ◽

Jose R. P. Parra ◽

Tamara A. Takahashi ◽

Luis A. Foerster ◽

...

Keyword(s):

Biological Control ◽

Mitochondrial Gene ◽

First Record ◽

Mass Rearing ◽

Classical Biological Control ◽

Egg Parasitoid ◽

Integrative Approach ◽

Agricultural Pests ◽

Telenomus Remus ◽

Natural Parasitism

AbstractThe egg parasitoid Telenomus remus (Hymenoptera: Scelionidae) has been investigated for classical and applied biological control of noctuid pests, especially Spodoptera (Lepidoptera: Noctuidae) species. Although T. remus was introduced into Brazil over three decades ago for classical biological control of S. frugiperda, this wasp has not been recorded as established in corn or soybean crops. We used an integrative approach to identify T. remus, combining a taxonomic key based on the male genitalia with DNA barcoding, using a cytochrome c oxidase subunit I mitochondrial gene fragment. This is the first report of natural parasitism of T. remus on S. frugiperda and S. cosmioides eggs at two locations in Brazil. We also confirmed that the T. remus lineage in Brazil derives from a strain in Venezuela (originally from Papua New Guinea and introduced into the Americas, Africa, and Asia). The occurrence of T. remus parasitizing S. frugiperda and S. cosmioides eggs in field conditions, not associated with inundative releases, suggests that the species has managed to establish itself in the field in Brazil. This opens possibilities for future biological control programs, since T. remus shows good potential for mass rearing and egg parasitism of important agricultural pests such as Spodoptera species.

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Rearing Trissolcus japonicus and Trissolcus mitsukurii for Biological Control of Halyomorpha halys

Insects ◽

10.3390/insects11110787 ◽

2020 ◽

Vol 11 (11) ◽

pp. 787

Author(s):

Giuseppino Sabbatini-Peverieri ◽

Christine Dieckhoff ◽

Lucrezia Giovannini ◽

Leonardo Marianelli ◽

Pio Federico Roversi ◽

...

Keyword(s):

Biological Control ◽

Control Method ◽

Egg Parasitoids ◽

Halyomorpha Halys ◽

Progeny Production ◽

Asian Origin ◽

Frequent Use ◽

Trissolcus Japonicus ◽

Cumulative Curves

Halyomorpha halys is a severe agricultural pest of Asian origin that has invaded many countries throughout the world. Pesticides are currently the favored control methods, but as a consequence of their frequent use, often disrupt Integrated Pest Management. Biological control with egg parasitoids is seen as the most promising control method over the long-term. Knowledge of the reproductive biology under laboratory conditions of the most effective candidates (Trissolcus japonicus and Trissolcus mitsukurii) for optimizing production for field releases is strongly needed. Rearing of these egg parasitoids was tested by offering three different host supply regimes using new emerged females and aged, host-deprived females in different combinations. Results showed a mean progeny per female ranging from 80 to 85 specimens for T. japonicus and from 63 to 83 for T. mitsukurii. Sex ratios were strongly female biased in all combinations and emergence rates exceeded 94% overall. Cumulative curves showed that longer parasitization periods beyond 10–14 days (under the adopted rearing regimes) will not lead to a significantly increase in progeny production. However, ageing females accumulate eggs in their ovaries that can be quickly laid if a sufficient number of host eggs are supplied, thus optimizing host resources. Our data showed that offering H. halys egg masses to host-deprived female Trissolcus once a week for three weeks allowed its eggs to accumulate in the ovary, providing the greatest number of offspring within a three week span.

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Trissolcus japonicus (Hymenoptera: Scelionidae) Causes Low Levels of Parasitism in Three North American Pentatomids Under Field Conditions

Journal of Insect Science ◽

10.1093/jisesa/iez074 ◽

2019 ◽

Vol 19 (4) ◽

Cited By ~ 8

Author(s):

Joshua M Milnes ◽

Elizabeth H Beers

Keyword(s):

North American ◽

Native Species ◽

Classical Biological Control ◽

The United States ◽

Host Finding ◽

Pest Species ◽

Case Scenario ◽

Worst Case ◽

Egg Masses ◽

Trissolcus Japonicus

Abstract Trissolcus japonicus (Ashmead), an Asian parasitoid of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), was first detected in North America in 2014. Although testing in quarantine facilities as a candidate for classical biological control is ongoing, adventive populations have appeared in multiple sites in the United States, Canada, and Europe. Extensive laboratory testing of T. japonicus against other North American pentatomids and H. halys has revealed a higher rate of parasitism of H. halys, but not complete host specificity. However, laboratory tests are necessarily artificial, in which many host finding and acceptance cues may be circumvented. We offered sentinel egg masses of three native pentatomid (Hemiptera: Pentatomidae) pest species (Chinavia hilaris (Say), Euschistus conspersus Uhler, and Chlorochroa ligata (Say)) in a field paired-host assay in an area with a well-established adventive population of T. japonicus near Vancouver, WA. Overall, 67% of the H. halys egg masses were parasitized by T. japonicus during the 2-yr study. Despite the ‘worst case’ scenario for a field test (close proximity of the paired egg masses), the rate of parasitism (% eggs producing adult wasps) on all three native species was significantly less (0.4–8%) than that on H. halys eggs (77%). The levels of successful parasitism of T. japonicus of the three species are C. hilaris > E. conspersus > C. ligata. The potential impact of T. japonicus on these pentatomids is probably minimal.

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3.5 SUPPRESSION OF SPRUCE BUDWORM POPULATIONS BY TRICHOGRAMMA MINUTUM RILEY, 1982–1986

Memoirs of the Entomological Society of Canada ◽

10.4039/entm122153056-1 ◽

1990 ◽

Vol 122 (S153) ◽

pp. 56-81 ◽

Cited By ~ 4

Author(s):

S.M. Smith ◽

D.R. Wallace ◽

G. Howse ◽

J. Meating

Keyword(s):

Choristoneura Fumiferana ◽

Host Density ◽

Spruce Budworm ◽

Mass Rearing ◽

Egg Parasitoid ◽

Curvilinear Relationship ◽

Egg Masses ◽

Trichogramma Minutum ◽

Egg Parasitism ◽

Release Timing

AbstractThe ability of the egg parasitoid, Trichogramma minutum Riley, to suppress outbreak populations of the spruce budworm, Choristoneura fumiferana (Clemens), was studied annually near Hearst, Ont., from 1982 through 1986. Timing of broadcast parasitoid-releases was linked to spruce budworm moth emergence and oviposition. These phenological relationships were predicted from a regression based on larval development at least 2 weeks before expected emergence; this allowed sufficient time to regulate (program) parasitoid emergence during mass-rearing. Emergence of caged spruce budworm adults was used to monitor moth eclosion in the field. Pheromone traps provided daily information on the activity of male moths and helped to synchronize the parasitoid releases with spruce budworm oviposition. Information on parasitoid activity was obtained from sentinel (laboratory-reared) and naturally occurring spruce budworm egg masses. A curvilinear relationship between the rate of parasitoid release and parasitism of sentinel egg masses was developed. Two parasitoid releases, 1 week apart, early in the oviposition period of spruce budworm, significantly increased parasitism of host eggs by 14–83% and reduced larval populations correspondingly from 42 to 82%. Single releases were less effective and increased parasitism by 0.3–52% (single ground release, 1986). Two parasitoid releases, combined with a spring application of Bacillus thuringiensis Berliner to larval populations, was the most effective strategy and resulted in 83% egg parasitism and 93% larval reduction. Release rates greater than 12–16 × 106 ♀ ♀ T. minutum per hectare were not warranted based on impact and costs. The effects of release timing, weather, host density, and parasitoid quality on the future successful use of T. minutum are discussed.

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REPRODUCTIVE BIOLOGY AND BEHAVIOR OF TELENOMUS CALVUS (HYMENOPTERA: SCELIONIDAE), A PHORETIC EGG PARASITOID OF PODISUS MACULIVENTRIS (HEMIPTERA: PENTATOMIDAE)

The Canadian Entomologist ◽

10.4039/ent1181063-10 ◽

1986 ◽

Vol 118 (10) ◽

pp. 1063-1072 ◽

Cited By ~ 37

Author(s):

D.B. Orr ◽

J.S. Russin ◽

D.J. Boethel

Keyword(s):

Adult Emergence ◽

Intrinsic Rate ◽

Egg Parasitoid ◽

Natural Increase ◽

Egg Mass ◽

Podisus Maculiventris ◽

Progeny Production ◽

Female Progeny ◽

The Mean ◽

And Behavior

AbstractThe behavior, reproductive capability, and longevity of Telenomus calvus Johnson, a phoretic egg parasitoid of the spined soldier bug, Podisus maculiventris (Say), were examined in the laboratory. Telenomus calvus females were observed at 25 different locations on hosts’ bodies; preferred sites were pronota and femora. Attachment to hosts was facilitated by greatly enlarged arolia. Parasitoids dismounted from hosts at the time of oviposition to parasitize egg masses. Production of female progeny by parasitoids in phoretic association with hosts peaked on the 1st day after adult emergence, then declined steadily until day 6; male progeny production remained relatively low and constant over the same period. The mean (± SE) number of progeny produced by T. calvus females was 22.4 ± 3.0. Such a small egg complement enabled most females not in phoretic association, and presented with a fresh egg mass daily, to oviposit all or nearly all of their eggs in the first host egg mass encountered. The intrinsic rate of natural increase for T. calvus in phoretic association was estimated as 0.149 ♀ ♀−1 day−1, resulting in a doubling time of 4.65 days. Longevity on non-ovipositing females with access to honey was 33.7 ± 1.1 days, but declined sharply to 5.7 ± 0.4 days when in phoretic association with hosts. Pre-imaginal development of T. calvus was restricted to host eggs that were ≤12h old, despite continued observed oviposition attempts in older host masses. These results are discussed with regard to the biology of T. calvus as a phoretic parasitoid and to its importance as a parasitoid of P. maculiventris in Louisiana.

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An effective cold storage method for stockpiling Halyomorpha halys eggs for field surveys and laboratory rearing of Trissolcus japonicus

10.1101/2020.04.30.071183 ◽

2020 ◽

Cited By ~ 2

Author(s):

Warren H. L. Wong ◽

Matt A. Walz ◽

Angela B. Oscienny ◽

Jade L. Sherwood ◽

Paul K. Abram

Keyword(s):

Current Method ◽

Field Studies ◽

Egg Parasitoid ◽

Halyomorpha Halys ◽

Stink Bug ◽

Time Activity ◽

Egg Masses ◽

Fitness Consequences ◽

Laboratory Colony ◽

Trissolcus Japonicus

AbstractAn effective stockpiling method for egg masses of the invasive brown marmorated stink bug (Halyomorpha halys [Stål]; Hemiptera: Pentatomidae) would be useful for rearing and field studies of its egg parasitoid Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae). The current method of stockpiling H. halys egg masses at sub-zero temperatures has lethal and sublethal fitness consequences for T. japonicus. We show that parasitoid emergence from egg masses refrigerated at 8°C for up to two months before parasitism is higher than from frozen egg masses and usually has minimal or no sublethal fitness effects (sex ratio, development time, activity, fecundity, longevity, and weight) on emerging T. japonicus. Only after two months of host egg refrigeration did the emergence of T. japonicus begin to decrease significantly (by 9.6% relative to untreated viable egg masses), whereas egg masses previously frozen at -80°C had a 58.8% reduction in parasitoid emergence after 14 days of storage. Refrigerated egg masses that were subsequently exposed to average field temperatures (warm: 22.9°C; cool: 13.2°C) were still suitable for T. japonicus parasitism after 7 days, while viable egg masses exposed to warm temperatures for 7 days before parasitism had 24.1% lower parasitoid emergence. Our results demonstrate that refrigeration at 8°C, while resulting in complete mortality of H. halys embryos after 10 days, are more suitable for T. japonicus parasitism than those stored at sub-zero temperatures. The quantity and quality of H. halys eggs that can be stockpiled with this method could facilitate T. japonicus laboratory colony maintenance, field monitoring, and releases.

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Integrating Trissolcus japonicus (Ashmead, 1904) (Hymenoptera: Scelionidae) into Management Programs for Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae) in Apple Orchards: Impact of Insecticide Applications and Spray Patterns

Insects ◽

10.3390/insects11120833 ◽

2020 ◽

Vol 11 (12) ◽

pp. 833

Author(s):

Dalton C. Ludwick ◽

Jessica Patterson ◽

Layne B. Leake ◽

Lee Carper ◽

Tracy C. Leskey

Keyword(s):

The United States ◽

Post Treatment ◽

Egg Mass ◽

Halyomorpha Halys ◽

Apple Orchards ◽

Specialty Crops ◽

Egg Masses ◽

Trissolcus Japonicus ◽

Application Techniques ◽

Pre Treatment

Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae) is an invasive species in the United States, where it has caused significant damage to specialty crops, including apples. While integrated pest management techniques have been developed for H. halys in apple, including spray application techniques, it is unknown how these techniques affect foraging, adventive Trissolcus japonicus (Ashmead, 1904) (Hymenoptera: Scelionidae), and its offspring. In this study, egg masses (unparasitized and 2 and 7 day parasitized pre-treatment) were placed in apple orchards in treated and untreated locations that received full block insecticide applications or reduced application techniques, including border row or alternate row middle applications. Bifenthrin, thiamethoxam + λ-cyhalothrin, clothianidin, and methomyl were evaluated. Egg masses were retrieved 24 h after spray applications. For 2 and 7 day parasitized pre-treatment, adult T. japonicus emergence was recorded from each egg mass. For unparasitized egg masses, T. japonicus females were given 24 h to forage and oviposit on post-treatment egg masses with female survivorship, and adult emergence from egg masses was recorded. Female survivorship was significantly lower on post-treatment egg masses retrieved from areas receiving bifenthrin applications. Emergence from post-treatment egg masses was affected by thiamethoxam + λ-cyhalothrin, bifenthrin, and methomyl in some treated areas, whereas less impact was observed on 2 and 7 day pre-treatment parasitized egg masses in general. These data provide further insights into H. halys management and the potential impact of T. japonicus in sprayed orchard agroecosystems.

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Effect of female weight on reproductive potential of the predator Brontocoris tabidus (Signoret, 1852) (Heteroptera: Pentatomidae)

Brazilian Archives of Biology and Technology ◽

10.1590/s1516-89132005000200017 ◽

2005 ◽

Vol 48 (2) ◽

pp. 295-301 ◽

Cited By ~ 9

Author(s):

Isaias Oliveira ◽

José Cola Zanuncio ◽

José Eduardo Serrão ◽

Teresinha Vinha Zanuncio ◽

Tobias Baruc Moreira Pinon ◽

...

Keyword(s):

Reproductive Potential ◽

Mass Rearing ◽

Adult Longevity ◽

Egg Mass ◽

Egg Masses ◽

Egg Incubation ◽

Males And Females ◽

Heteroptera Pentatomidae ◽

Female Weight ◽

Coleoptera Tenebrionidae

The objective of this work was to determine the fecundity of the predator Brontocoris tabidus (Signoret) (Heteroptera: Pentatomidae) females of two weight classes aiming to define, which one presented higher productivity in the laboratory. Males and females of B. tabidus were reared from nymphs fed with Tenebrio molitor L. (Coleoptera: Tenebrionidae) pupae in laboratory. Females of B. tabidus weighting 95 to 150 mg and those with 160 to 220 mg constituted two treatments. Oviposition period and numbers of egg masses, eggs and nymphs per female of B. tabidus were higher in the treatment with heavier females, while the periods of preoviposition, between egg mass laying, egg incubation and number of eggs per egg mass, besides the percentage of nymphs hatched and adult longevity were similar between treatments. Heavier females of B. tabidus presented better productivity and for this reason they should be used in programs of mass rearing this predator.

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Host Kairomones Influence Searching Behavior of Trissolcus japonicus (Hymenoptera: Scelionidae), a Parasitoid of Halyomorpha halys (Heteroptera: Pentatomidae)

Environmental Entomology ◽

10.1093/ee/nvz155 ◽

2019 ◽

Vol 49 (1) ◽

pp. 15-20 ◽

Cited By ~ 5

Author(s):

Sean M Boyle ◽

Donald C Weber ◽

Judith Hough-Goldstein ◽

Kim A Hoelmer

Keyword(s):

Host Range ◽

Classical Biological Control ◽

Egg Parasitoid ◽

Halyomorpha Halys ◽

Stink Bug ◽

Red Maple ◽

Classical Biocontrol ◽

Trissolcus Japonicus ◽

Walking Velocity ◽

Heteroptera Pentatomidae

Abstract The brown marmorated stink bug, Halyomorpha halys (Stål), is a highly polyphagous species native to Asia that has become a serious invasive agricultural and nuisance pest across North America and Europe. Classical biological control host range evaluations have revealed egg parasitoid Trissolcus japonicus (Ashmead) to be the primary candidate biocontrol agent for field release against H. halys. However, these evaluations only provide us with the physiological host range of T. japonicus. Other Trissolcus species have demonstrated that contact kairomones from different host species elicit varied responses in the parasitoids’ host foraging behaviors. To assess T. japonicus response to host kairomones, mated naive females were exposed to leaf surfaces contaminated with adult kairomones from its preferred host, H. halys, or from a native nontarget host, Podisus maculiventris (Say) (Heteroptera: Pentatomidae). Red maple, apple, and soybean were used as plant substrate treatments. The wasp’s residence time on the leaf surface, linear walking velocity, and angular walking velocity were observed and measured using Noldus EthoVision XT tracking software. Within each leaf treatment, T. japonicus displayed stronger behavioral responses on leaves contaminated with contact kairomones from H. halys. The parasitoid resided on H. halys contaminated leaves for approximately twice as a long as it did on P. maculiventris contaminated leaves. Further, both species’ kairomones elicited significant decreases in parasitoid walking velocity on all tested substrate types. Overall, our study suggests that kairomone-based behavioral studies can be used to further evaluate the host specificity of T. japonicus and can be an invaluable supplement to classical biocontrol host range testing regimes.

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