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Comparative Study of Egg Parasitism by Gryon Pennsylvanicum (Hymenoptera: Scelionidae) on Two Squash Bug Species Anasa Tristis A

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Comparative Study of Egg Parasitism by Gryon Pennsylvanicum (Hymenoptera: Scelionidae) on Two Squash Bug Species Anasa Tristis A Environmental Entomology, 47(6), 2018, 1451–1458 doi: 10.1093/ee/nvy145 Advance Access Publication Date: 25 September 2018 Biological Control - Parasitoids and Predators Research Comparative Study of Egg Parasitism by Gryon pennsylvanicum (Hymenoptera: Scelionidae) on Two Squash Bug Species Anasa tristis and Anasa armigera (Hemiptera: Coreidae) Mary L. Cornelius,1,3 Jing S. Hu,1 and Bryan T. Vinyard2 Downloaded from https://academic.oup.com/ee/article/47/6/1451/5106965 by guest on 29 September 2021 1Invasive Insect Biocontrol and Behavior Laboratory, USDA Agricultural Research Service, Beltsville Agricultural Research Center, Beltsville, MD 20705, 2Statistics Group, USDA Agricultural Research Service, Northeast Area Office, Beltsville, MD 20705, and 3Corresponding author, e-mail: [email protected] Subject Editor: Zsofia Szendrei Received 11 May 2018; Editorial decision 30 August 2018 Abstract This study evaluated how the size of the egg mass and the parasitoids prior exposure to eggs influenced parasitism rates by Gryon pennsylvanicum Ashmead (Hymenoptera: Scelionidae) on egg masses of two squash bug species, Anasa tristis DeGeer and Anasa armigera Say (Hemiptera: Coreidae). G. pennsylvanicum is the primary egg parasitoid of A. tristis. There were no published reports available on egg parasitism of A. armigera. In choice tests, there was no difference in host acceptance by G. pennsylvanicum of egg masses of the two squash bug species. In no-choice tests, overall parasitism rates were significantly higher onA. armigera egg masses than on A. tristis egg masses. Naive parasitoids had significantly higher parasitism rates than experienced parasitoids on egg masses of both squash bug species. In a comparison of parasitism rates of field-collected and laboratory-testedA. tristis egg masses of different sizes, parasitism rates were similar in the field and in the laboratory, with the exception of egg masses with > 25 eggs. Only 17.9% of eggs were parasitized in the laboratory, compared with 36.4% in the field. Results of this study indicate that transient egg limitation prevents G. pennsylvanicum from ovipositing in every available host egg in large squash bug egg masses. The low parasitism rate of G. pennsylvanicum on large egg masses may limit its effectiveness as a biological control agent of squash bugs. Key words: oviposition behavior, egg load, egg limitation, biological control, natural enemies The squash bug Anasa tristis DeGeer (Hemiptera: Coreidae) is Several studies have examined the development, and survival of a serious pest of cucurbit crops causing plant wilt and acting as a A. tristis on different cucurbit species. Bonjour and Fargo (1989) found vector of a bacterial infection, cucurbit yellow vine disease, which that survival to the adult stage was significantly higher on cultivars of can devastate cucurbit crops (Doughty et al. 2016). Squash bugs Cucurbita pepo L. (Cucurbitales: Cucurbitacaeae), cv. pepo (70.0%), overwinter as adults in crop residue or other debris and emerge in cv. melopepo (49.0%), than on watermelon, Citrullus lanatus (Thunb.) the spring. After emergence, adults search for cucurbit plants. Once Matsum. & Nakai (Cucurbitales: Cucurbitaceae) (14.4%), cucum- plants are located, they feed and mate. Females begin depositing ber, Cucumis sativus L. (Cucurbitales: Cucurbitaceae) (0.3%), and eggs on the host plant within 7–10 d of emergence (Nechols 1987). muskmelon, Cucumis melo L. (Cucurbitales: Cucurbitaceae) (0%). Squash bugs complete their entire lifecycle within 6–8 wk (Beard Other studies have demonstrated that Cucurbita moschata 1940). Depending on location, squash bugs can have one to three Dusch (Cucurbitales: Cucurbitaceae). is more resistant to A. tristis than generations per year. In Virginia, there are one to two generations C. pepo (Novero et al. 1962, Vogt and Nechols 1993a). Additionally, with new adults emerging in late July to early August and entering A. tristis nymphs were not able to develop successfully on cucumber diapause in late September to early October (Doughty et al. 2016). (Cook and Neal 1999) and were more likely to oviposit on C. pepo The horned squash bug, Anasa armigera Say (Hemiptera: Coreidae), than on cucumber (Cornelius 2018). In contrast, A. armigera was is considered to be a minor pest of cucurbit crops (Drake and Harris reared successfully on both cucumber and C. pepo and females were 1926, Britton 1937, Gould 1944). There are no published reports on equally likely to oviposit on either host plant, regardless of which spe- the phenology of A. armigera. cies they were reared on (Cornelius 2018). Published by Oxford University Press on behalf of Entomological Society of America 2018. This work is written by (a) US Government employee(s) and is in the public domain in the US. 1451 1452 Environmental Entomology, 2018, Vol. 47, No. 6 There is a need to evaluate the effectiveness of biological con- on wild A. tristis egg masses collected in squash fields. Field-collected trol as a strategy for controlling pests in squash fields. The market A. tristis egg masses ranged in size from 1 to 44 eggs per egg mass with for organically grown produce is increasing (National Agricultural a mean (± SE) of 15.15 ± 0.69 eggs per egg mass (Cornelius et al. 2016). Statistics Service [NASS] 2010). In addition, squash bugs are difficult In parasitized egg masses with > 20 eggs, parasitoids never parasitized to control with insecticides (Nechols 1987, Olson et al. 1996). Egg 100% of the eggs in the egg mass, whereas they parasitized 100% of parasitoids can be effective biological control agents due to their the eggs in egg masses with ≤ 10 eggs 68% of the time. The inability of ability to prevent emergence of the pest, their relative host specificity, G. pennsylvanicum to successfully parasitize every egg in large squash and their high degree of host searching efficiency. bug egg masses limits its efficiency as a biological control agent. Gryon pennsylvanicum Ashmead (Hymenoptera: Scelionidae) is The lower rates of parasitism on larger egg masses could be the primary egg parasitoid of the squash bug, A. tristis (Olson related to transient egg limitation. Female parasitoids are expected et al. 1996, Cornelius et al. 2016, Doughty et al. 2016, Wilson and to maximize lifetime fecundity by balancing the risk of egg and time Kuhar 2017). It accounted for over 98% of parasitism in field sur- limitation (Rosenheim 1996, 1999; Rosenheim et al. 2008). For syn- veys conducted in Maryland and Virginia (Cornelius et al. 2016, ovigenic parasitoids, transient egg limitation can occur if the deple- Wilson and Kuhar 2017). Between June and September in 2013 tion of eggs exceeds the rate of egg maturation. If female parasitoids and 2014, G. pennsylvanicum emerged from 55.7% of squash bug deplete their supply of mature eggs before ovipositing in every host Downloaded from https://academic.oup.com/ee/article/47/6/1451/5106965 by guest on 29 September 2021 eggs in squash fields at the Beltsville Agricultural Research Center egg available, they must halt oviposition until they can replenish their in Maryland, with a peak emergence rate of 72.8% in the last week egg loads. Females in environments with a high host density may of July (Cornelius et al. 2016). In 2014 and 2015, over 50% of experience oviposition-mediated egg limitation (Rosenheim et al. squash bug eggs collected in Virginia were parasitized by G. penn- 2000). Egg limitation is mediated by egg maturation, oviposition, egg sylvanicum (Wilson and Kuhar 2017). These results indicate that resorption, and the factors influencing these processes (Casas et al. G. pennsylvanicum could be effective for suppressing squash bug 2009, Richard and Casas 2012). For instance, females of the soy- populations in commercial squash fields in Virginia and Maryland. bean aphid parasitoid Binodoxys communis (Gahan) (Hymenoptera: Currently, G. pennsylvanicum is being considered as a clas- Braconidae), were able to avoid egg limitation and maintain constant sical biological control agent of the invasive Western conifer seed egg loads throughout the day (Dieckhoff et al. 2014). bug Leptoglossus occidentalis Heidemann (Hemiptera: Coreidae) The objective of this study was to evaluate the oviposition in Europe (Sabbatini Peverieri et al. 2012, Peverieri et al. 2013, behavior of G. pennsylvanicum towards egg masses of different Roversi et al. 2014). When host egg age ranged from < 24 h old sizes to determine how many eggs a female will parasitize within to a day before hatching, parasitism rates on L. occidentalis eggs a 24-h period. Also, parasitism rates by naive parasitoids with no were not affected by age of the eggs (Peverieri et al. 2013). Because prior exposure to eggs were compared with parasitism rates by G. pennsylvanicum had high fecundity and long-lived adults, it was experienced parasitoids that had been previously exposed to eggs. considered to be a good candidate for classical biological control Parasitism rates with naive and experienced parasitoids were com- (Sabbatini Peverieri et al. 2012). pared because experienced parasitoids were likely to have a lower In a comparative study of G. pennsylvanicum with three species egg load due to their prior exposure to eggs. Because previous of Ooencyrtus, G. pennyslvanicum had the highest fecundity, net research determined that no oocyte resorption occurred for 3-d-old reproductive rate, and intrinsic rate of increase at 27°C of the four host-deprived G. pennsylvanicum (Vogt and Nechols 1993b), naive parasitoid species tested. Female G. pennsylvanicum had a mean (± 1–3-d-old females were expected to have their full egg loads. SD) fecundity of 80.7 ± 36 A. tristis eggs over a mean (± SD) ovi- In addition, this study evaluated the efficacy of parasitoids on positional period of 22.0 ± 6.7 d and their progeny had a percent eggs of A. armigera in both no-choice and choice tests. There are survivorship of 86% (Nechols et al. 1989). The daily number of no published reports concerning the natural enemies of A.
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