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Impact of Rag1 Aphid Resistant Soybeans on Binodoxys Communis (Hymenoptera: Braconidae), a Parasitoid of Soybean Aphid (Hemiptera: Aphididae)

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Impact of Rag1 Aphid Resistant Soybeans on Binodoxys Communis (Hymenoptera: Braconidae), a Parasitoid of Soybean Aphid (Hemiptera: Aphididae) BIOLOGICAL CONTROLÐPARASITOIDS AND PREDATORS Impact of Rag1 Aphid Resistant Soybeans on Binodoxys communis (Hymenoptera: Braconidae), a Parasitoid of Soybean Aphid (Hemiptera: Aphididae) KIRAN GHISING,1 JASON P. HARMON,1 PATRICK B. BEAUZAY,1 DEIRDRE A. PRISCHMANN-VOLDSETH,1 TED C. HELMS,2 PAUL J. ODE,3 1,4 AND JANET J. KNODEL Downloaded from https://academic.oup.com/ee/article/41/2/282/483303 by guest on 27 September 2021 Environ. Entomol. 41(2): 282Ð288 (2012); DOI: http://dx.doi.org/10.1603/EN11196 ABSTRACT Multiple strategies are being developed for pest management of the soybean aphid, Aphis glycines Matsumura; however, there has been little published research thus far to determine how such strategies may inßuence each other, thereby complicating their potential effectiveness. A susceptible soybean (Glycine max L.) variety without the Rag1 gene and a near isogenic resistant soybean variety with the Rag1 gene were evaluated in the laboratory for their effects on the Þtness of the soybean aphid parasitoid, Binodoxys communis (Gahan). The presence or absence of the Rag1 gene was veriÞed by quantifying soybean aphid growth. To test for Þtness effects, parasitoids were allowed to attack soybean aphids on either a susceptible or resistant plant for 24 h and then aphids were kept on the same plant throughout parasitoid development. Parasitoid Þtness was measured by mummy and adult parasitoid production, adult parasitoid emergence, development time, and adult size. Parasitoids that attacked soybean aphids on susceptible plants produced more mummies, more adult parasitoids, and had a higher emergence rate compared with those on resistant plants. Adult parasitoids that emerged from resistant plants took 1 d longer and were smaller compared with those from susceptible plants. This study suggests that biological control by B. communis may be compro- mised when host plant resistance is widely used for pest management of soybean aphids. KEY WORDS soybean, Aphis glycines, host-plant resistance, Binodoxys communis, biological control A primary concept underlying integrated pest man- fecting the quantity and quality of the herbivores that agement (IPM) is the use of multiple pest control natural enemies rely on to reproduce (Ode 2006). strategies (Allen and Rajotte 1990, Kogan 1998). Two Parasitoids may be particularly susceptible, as host common strategies are deploying host plants resistant plant resistance can affect host quality, which in turn to herbivores and promoting biological control agents impacts the survival of immature parasitoids, devel- that can also help control herbivores (Smith 2005). opment time, and ultimately adult Þtness (Barbosa et Combining these two strategies can result in enhanced al. 1982, Duffey and Bloem 1986, van Emden 1995). herbivore suppression compared with using either Moreover, parasitoid foraging behavior can be inßu- method alone; however, in some cases one strategy enced by morphological and chemical attributes of can negatively inßuence the other (Beddington et al. resistant plants, ultimately undermining their ability 1978, Auclair 1989, Harrewijn and Minks 1989, Bottrell to control herbivore populations (Gould et al. 1991, et al. 1998, Dogramaci et al. 2005). Turlings and Benrey 1998, Hare 1992, Ode 2006). Resistant plants often have chemicals and morpho- Since its Þrst detection in North America in 2000, logical characteristics that make them less attractive to the soybean aphid, Aphis glycines Matsumura herbivorous insects (antixenosis, nonpreference) or (Hemiptera: Aphididae), has spread throughout soy- negatively inßuence pest fecundity, survival, or de- bean-growing regions in the north central United velopment time (antibiosis) (Painter 1958, Smith States and some Canadian provinces where it is con- 2005). However, these same attributes can directly or sidered one of the most economically important pests indirectly impact higher trophic levels, often by af- of soybean (Alleman et al. 2002, Venette and Ragsdale 2004). Besides causing direct damage to plants, soy- 1 Department of Entomology, North Dakota State University, bean aphids can vector several viral diseases and ex- Fargo, ND 58108. crete honeydew, promoting a fungus known as sooty 2 Department of Plant Sciences, North Dakota State University, mold that disrupts photosynthesis (Guo and Zhang Fargo, ND 58108. 1989, Clark and Perry 2002). Insecticide applications 3 Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO 80523. are a common and effective method of soybean aphid 4 Corresponding author, e-mail: [email protected]. control, although drawbacks associated with broad- 0046-225X/12/0282Ð0288$04.00/0 ᭧ 2012 Entomological Society of America April 2012 GHISING ET AL.: IMPACT OF Rag1 APHID RESISTANT SOYBEANS ON B. communis 283 spectrum pesticide use, such as insecticide resistance, Soybean aphid colonies were reared and maintained nontarget effects, and environmental contamination on the susceptible soybean variety, RG607RR. All col- make alternative management strategies desirable onies and experiments were held at 25 Ϯ 5ЊC, 60Ð80% (ffrench-Constant et al. 2004, Heimpel et al. 2004, RH, and 16L:8D photoperiod. Ragsdale et al. 2007). Classical biological control and The B. communis colony (Harbin strain) was initi- host plant resistance are two nonchemical approaches ated in winter 2009 and maintained for several gen- that are currently being explored for soybean aphid erations in the laboratory from the soybean aphid management (Heimpel et al. 2004, Hill et al. 2004b, colony. The colony was started from 30 mummies Wyckhuys et al. 2009). obtained from Dr. George E. Heimpel, University of Classical biological control using parasitoids from Minnesota, St. Paul, MN. This parasitoid colony was Asia is believed to be an important option for man- originally established from 7 males and 33 females of agement of soybean aphids for two reasons. First, parasitized A. glycines near Harbin and Suihua county soybean aphids are kept below economically damag- of Heilongjiang province, China in late August 2002 Downloaded from https://academic.oup.com/ee/article/41/2/282/483303 by guest on 27 September 2021 ing population levels in Asia through natural control (Wyckhuys et al. 2007a). Specimens of soybean aphids with both insect predators and parasitoids (Wu et al. and B. communis were deposited in the North Dakota 2004). Second, parasitism levels in Asia are often Insect Reference Collection at North Dakota State Ͼ10%, while in North America they are typically be- University in Fargo. low 1% (Heimpel et al. 2010, Lui et al. 2004). Binodoxys Experiments were performed with young, naõ¨ve fe- communis (Gahan) (Hymenoptera: Braconidae) is a male parasitoids from the colony. To obtain each of monophagous aphid parasitoid wasp that has been these parasitoids, one B. communis mummy from the collected from eastern Asia, and recently released in colony was kept in a clear gelatin capsule (size 0) the United States on a limited scale for experimental nested within a 1.5 ml micro centrifuge tube until adult purposes (Wyckhuys et al. 2007b). Because of its high emergence. Once adults emerged, pairs of male and prey speciÞcity, B. communis is thought to be more female adults were isolated in separate glass vials with effective than other biocontrol agents at maintaining plaster of Paris at the bottom to maintain moisture. A soybean aphid populations at low levels (Desneux et mixture of honey and water (4:1) was soaked in cotton al. 2009, Wyckhuys et al. 2007b). balls (size 5) as a feeding supplement. Parasitoids were Plant resistance to the soybean aphid has been ad- given the opportunity to mate for 24 h and then fe- vanced with the discovery of resistance in cultivars males were transferred to an experimental plant. Fe- like ÔDowlingÕ and ÔJackson,Õ which show resistance to male parasitoids in the experiment were naõ¨ve with the soybean aphid (Hill et al. 2004a). Resistance in respect to hosts, and were Ϸ1Ð2 d old at the start of the Dowling is conferred by a single dominant gene, Rag1, experiment. which limits soybean aphid colonization and nega- Plant Varieties. Two soybean varieties were used as tively affects their fecundity, survival, longevity, and treatments: a susceptible variety without the Rag1 development (Li et al. 2004, Hill et al. 2006). Rag1 is gene, RG607RR, and a near isogenic resistant variety currently being bred into commercial soybean lines. with the Rag1 gene (provided by T. Helms, North Despite the potential associated with each of these Dakota State University, Fargo, ND). The source control strategies, there has been little work investi- of the Rag1 gene used for the experiment was gating their effects on each other. LDXG04018Ð3 (provided by B. Diers, University of Our overall research objective was to evaluate the Illinois, Urbana-Champaign, IL), which was devel- development and Þtness of B. communis when exposed oped by crossing Dwight X (Loda X Dowling) (T. to soybean aphids on a near isogenic resistant soybean Helms, personal communication). The resistant line is variety with the Rag1 gene compared with a suscep- a BC3F3-derived line (using RG607RR as the recur- tible soybean variety without the Rag1 gene. We Þrst rent parent) that carries the Rag1 gene. For our ex- conÞrmed that our experimental varieties differed in periment, the presence of the Rag1 gene in the resis- their resistance to soybean aphid by measuring the tant soybean variety was conÞrmed by performing an growth rate of aphid populations reared on resistant aphid growth rate experiment (see Aphid Growth). In and susceptible soybean plant varieties and by assay- addition, individual plants used in the experiment ing for the Rag1 gene. We then assessed effects of the were tested for the allelic state of the Rag1 gene using Rag1 gene on the parasitoid by allowing parasitoids to the simple sequence repeat marker Satt435 and elec- attack and develop on soybean aphids reared on either trophoresis of the polymerase chain reaction (PCR) the resistant or susceptible plants. We measured para- product according to the methods of Kim and Diers sitoid Þtness by determining the total number of (2009).
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