Biological Control 62 (2012) Contents lists available at SciVerse ScienceDirect. Biological Control

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1 Biological 62 (2012) Contents lists available at SciVerse ScienceDirect Biological journal homepage: Effect of Binodoxys communis parasitism on flight behavior of the soybean aphid, Aphis glycines Ying Zhang a, Kris A.G. Wyckhuys b, Mark K. Asplen c, George E. Heimpel c, Kongming Wu a, a State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing , PR China b International Center for Tropical Agriculture CIAT, Cali, Colombia c Department of Entomology, University of Minnesota, 1980 Folwell Avenue, St. Paul, MN 55108, USA highlights " Parasitized L3 alatoids were significantly less likely to fully develop wings than were parasitized L4 alatoids. " Timing of parasitism is critical for alate-mediated movement of immature Binodoxys communis. " Parasitized L4 nymphal instar aphids engaged in long-distance flights in flight-mill assays. " Aphis glycines flight did not have any measurable effect on the development of B. communis. graphical abstract article info abstract Article history: Received 5 May 2011 Accepted 3 March 2012 Available online 10 March 2012 Keywords: Aphis glycines Binodoxys communis Wing development Parasitoid dispersal Phoresy Biological control Many aphid species possess wingless (apterous) and winged (alate) stages, both of which can harbor parasitoids at various developmental stages. Winged aphids bearing parasitoid eggs or young larvae can potentially still engage in long-distance flights and thereby facilitate parasitoid dispersal, which has important implications for biological control of aphids by parasitoids. In this study, we determined the effect of parasitism by Binodoxys communis (Hymenoptera: Braconidae) on wing development and flight of the summer alate stage of the soybean aphid, Aphis glycines (Hemiptera: Aphididae), and quantified the effect of aphid flight duration on subsequent B. communis development. Parasitism by B. communis was allowed at alatoid 3rd (L3) and 4th instar (L4) nymphal stages of A. glycines and subsequent aphid flight was measured using a computer-monitored flight mill. Only 25% of aphids parasitized as L3 alatoid nymphs produced normal winged adults, compared to 100% of L4 alatoids. While flight performance of aphids that had been parasitized as 4th-instar alatoid nymphs 24 or 48 h prior to testing was similar to that of unparasitized alates of identical age, it declined sharply for alates that had been parasitized as 4th-instar alatoid nymphs 72 and 96 h prior to testing. Parasitoid larval and pupal development times, percent mummification and adult emergence rates did not differ between treatments in which aphids had flown over varying durations. Our results have implications for natural biological control of A. glycines in Asia and classical biological control of the soybean aphid in North America. Ó 2012 Elsevier Inc. All rights reserved. 1. Introduction The transport of insect parasitoids and pathogens by their hosts is known from a number of taxa, including aphids (e.g., Buschman Corresponding author. Fax: addresses: wkm@caascose.net.cn, kmwu@ippcaas.cn (K. Wu). and Whitcomb, 1980; Vorley and Wratten, 1987; Orr, 1988; Arakaki et al., 1996; Rauwald and Ives, 2001; Feng et al., 2004, 2007; Eng et al., 2005; Fatouros et al., 2005; Campos-Herrera et al., 2006; Chen and Feng, 2006; Chen et al., 2008; Zhang et al., 2009b). The dispersal of parasitoids within their aphid hosts likely aids to track populations of their hosts (Rauwald and Ives, 2001), but may also hinder the establishment of introduced parasitoids /$ - see front matter Ó 2012 Elsevier Inc. All rights reserved.

2 Y. Zhang et al. / Biological 62 (2012) through enhanced Allee effects (Zhang et al., 2009b; Heimpel et al., 2010; Heimpel and Asplen, 2011). The prevalence of passive transport of parasitoids by alate aphids is mainly dependent upon three factors: (1) the ability of parasitoids to oviposit in alate and alatoid stages, (2) the suitability of these stages for parasitism, and (3) the flight behavior of winged aphids that contain parasitoid eggs or larvae. This latter point is especially relevant, since certain aphid parasitoids disrupt the formation of host wings and cause a lower incidence of flight (Christiansen-Weniger and Hardie, 1998, 2000; Rauwald and Ives, 2001; Demmon et al., 2004). Aphis glycines is a minor pest of soybeans in its native Asia, but has emerged as the most serious insect pest of soybeans in North America (Ragsdale et al., 2004, 2011; Wu et al., 2004; Rhainds et al., 2010). Although A. glycines was first reported in the North- Central United States in 2000, it had spread throughout 30 states of the USA and three Canadian provinces by 2009 (Venette and Ragsdale, 2004; Ragsdale et al., 2011). The impressive geographical spread of this species has been ascribed to a combination of passive and active flight (Venette and Ragsdale, 2004; Zhang et al., 2008). A. glycines is a typical heteroecious, holocyclic species in that it uses primary and secondary host plants during winter and summer, respectively, and produces sexual morphs and overwintering eggs (Ragsdale et al., 2004). Aphids produce both wingless (i.e., apterous) and winged (i.e., alate) morphs, with the latter moving between secondary hosts (i.e., soybean) during summer months and ensuring migration to primary hosts (typically shrubs in the genus Rhamnus) in the fall (Hodgson et al., 2005). Production of winged soybean aphids is likely triggered by photoperiod, although factors such as temperature, host plant quality, crowding and presence of natural enemies also play a role (Sutherland, 1967; Sloggett and Weisser, 2002; Hodgson et al., 2005). Flight mill assays showed that h old A. glycines alates exhibit a fairly strong flight propensity (Zhang et al., 2008, 2009a,b). Alates flew actively on flight mills for a maximum of 11.2 continuous hours (mean 4.3 h ± 0.5 SEM), which corresponded to a maximum displacement of 18.5 km (mean 5.1 km ± 0.7 SEM). Importation biological control is currently being attempted against Aphis glycines in North America (Heimpel et al., 2004, 2010; Hoelmer and Kirk, 2005). A number of Asian aphid parasitoids have been imported into quarantine in the United States, but to date only one has been released Binodoxys communis, a soybean aphid specialist collected in Northeastern China (Wyckhuys et al., 2008; Desneux et al., 2009b; Heimpel et al., 2010). This parasitoid was collected in an area of China that provided a good climate match to the North-Central United States. The Chinese strain of B. communis was released into North America began in The establishment and spread of this species may be influenced by its ability to attack alate and alatoid stages of its host and be transported to novel locations (Wyckhuys et al., 2008; Desneux et al., 2009a; Asplen et al., 2011). Previous work with B. communis suggests that (1) this parasitoid can complete development on alatoid nymphs and alate female aphids of both the summer and fall morphs, and (2) parasitized alatoid nymphs can develop into winged adults and later form parasitoid mummies (Wyckhuys et al., 2008; Asplen et al., 2011). These laboratory observations suggest that passive transport of B. communis by A. glycines may be possible, which may help explain observations in China indicating large numbers of parasitized aphids during the beginning of the colonization period on soybean (Liu et al., 2004; Hoelmer and Kirk, 2005). Recently, flight mill tests also showed that A. glycines parasitized by Aphelinus varipes as 4th-instar alatoid nymphs and alate adults engage in up to 4 h of active flight, covering an average estimated distance of 6 km during a single flight period (Zhang et al., 2009b). These studies also showed that parasitoids developed normally following flight within aphids. Here, we investigate the effects of parasitism by B. communis on the flight capacity of alate A. glycines using a laboratory flight mill (Zhang et al., 2008, 2009a,b). We first determined the effect of parasitism on aphid wing development. Next, we compared flight performance of alate A. glycines that were parasitized at different times during their development. 2. Materials and methods 2.1. Study insects A laboratory colony of A. glycines was initiated with individuals collected from a soybean field in Beijing, China in July The colony was maintained on soybean plants (variety: Zhonghuang 13) at 25 C, 75% RH and 16:8-h L:D. Soybeans were planted in potting soil in plastic containers (size: L W H = cm) and were transplanted as seedlings into 100 ml glass bottles filled with a nutrient solution (Wu and Liu, 1994). Plants were changed every three days. Aphids were reared under crowded conditions to induce alate production. Alatoid nymphs (i.e., nymphal instars with wingpads) were collected from aphid colonies, placed individually on a clean plant and checked for molting into the adult stage every 8 h. We considered the day of adult molt as day 0, and the time past this day reflected alate age (Liquido and Irwin, 1986). A laboratory colony of B. communis was initiated with 30 mummies collected from soybean fields in Langfang (Hebei province, China) during August This colony was maintained on A. glycines under controlled climatic conditions (25 C, 75% RH and 16:8- h L:D). Parasitoid mummies were transferred to 15 ml plastic tubes in which honey droplets were provided as food for emerging wasps. Two-day-old mated female wasps were used in the experiment, as pilot studies had indicated that wasps of this age were likely to attack and successfully parasitize various A. glycines developmental stages Influence of parasitism on A. glycines wing development We collected 40 individuals of either third (L3) or fourth (L4) instar alatoid nymphs from the aphid colony. We allowed one half of the individuals from both instars to be parasitized by B. communis, while the other half was left to develop normally (control). Parasitism of alatoid nymphs was confirmed through behavioral observation as follows. First, an A. glycines alatoid nymph was placed singly on a soybean leaf and allowed to settle for 2 min. A B. communis female was then gently introduced into a 1.8 cm-high and 0.7 cmwide gelatine dome, and the dome (with the parasitoid wasp) was placed over the aphid. Subsequent wasp behavior was recorded under a dissecting microscope (see Wu and Heimpel, 2007; Zhang et al., 2009b). An insertion of the ovipositor by B. communis into the aphid for more than 5 s without interruption indicated actual oviposition (Tang and Yokomir, 1996; Desneux et al., 2009a). Each individual wasp was not offered more than five aphids. Aphids were placed individually into 5 cm diam Petri dishes with a soybean leaflet on 1% agar (Liu et al., 2003). Dishes were kept at 25 C, 75% RH and 16:8-h L:D, with aphids checked daily for wing development and adult emergence. Upon mummy formation, aphids were scored as alate, apterous or intermediate morphs. Intermediate morphs were those in which wings were deformed or only partially formed (Christiansen-Weniger and Hardie, 1998, 2000) Effect of parasitism on soybean aphid flight Experiments were carried out at the Institute of Plant Protection (Chinese Academy of Agricultural Sciences, Beijing) using 32

3 12 Y. Zhang et al. / Biological 62 (2012) computer-monitored flight mills (see Zhang et al., 2008, 2009a,b). Each flight mill was composed of a 10 cm copper thread placed between two small magnets. Individual aphids were glued to the top surface of the copper thread with a droplet of 502 glue (Yuyao Kexing Adhesive Co., Zhejiang, China) applied to the ventral side of their abdomen. For each aphid, we recorded the time of flight initiation and cessation and the number of mill revolutions in consecutive 5-s intervals. Flights interrupted by a >1-min interval were considered separate flights. The number of mill revolutions over a given time period was used to compute flight distance, speed, and duration for each aphid (Cheng et al., 1997; Zhang et al., 2008, 2009a,b). All trials were done in a climate-controlled chamber at 25 C and 75% R.H. The flight assay started at the onset of the photophase (16:8 L:D). We characterized the effect of B. communis parasitism of alatoid A. glycines nymphs on flight performance of the subsequent alate stage at different times following parasitism. For this trial, in each treatment, we collected a total of 30 L4 alatoid nymphs. Half of the individuals were exposed to parasitism (see above), and subsequently reared to adult stage on soybean plants. The other half were left un-parasitized and reared on soybean. Flight was recorded for the winged stage at 24, 48, 72 and 96 h post-parasitism, with the (adult) age of tested individuals being 0 24 h, h, h, or h, respectively. The flight of the same-aged unparasitized alate were test as comparison. Flight of parasitized individuals of a given age was compared to that of un-parasitized ones of identical age. Flight performance was monitored over a 24 h period, and individuals within any given treatment were only tested once (at a specified age) Effect of soybean aphid flight on parasitoid development For this experiment, we subjected L4 alatoid nymphs to parasitism by B. communis (see above). Aphids were then held individually and checked for adult eclosion every 8 h. Parasitized alates that were h old were attached to the flight mill and allowed to engage in flights of 0, 0.5, 1, and 2 h. There were no less than 10 replicates per treatment. Next, aphids were removed from the apparatus by dipping their abdomen into water at ambient temperature to dissolve the glue (Feng et al., 2004). Live aphids without visible injury were placed individually into 5 cm diam Petri dishes with a soybean leaflet on 1% agar (Liu et al., 2003). Dishes were kept under the environmental conditions described above, and larval development time (time from oviposition to mummy formation), pupal development time (time from mummy formation to eclosion of the adult parasitoid), mummification rate were evaluated daily Data analysis Frequency data were analyzed using Chi-Square tests, and flight distance, flight duration and flight speed were compared between parasitized and un-parasitized aphids using Student s t-tests. Flight parameters were tested for interaction between treatment (parasitism) and aphid age using Two-way Analysis of Variance (ANOVA). In addition we compared flight parameters between parasitized and unparasitized aphids for each aphid age with Student s t-tests. The development parameters of B. communis after different flight durations were analyzed using One-way Analysis of Variance (ANOVA). Prior to analysis, we ensured that all data met assumptions of normality and heteroscedasticity. All statistical analyses were executed using SAS (SAS Institute, 1988). 3. Results 3.1. Influence of parasitism on A. glycines wing development Among aphids that were parasitized as L3 alatoid nymphs, 65% developed into apterous mummies, 10% developed into mummies with deformed or partly formed wings, and 25% developed into alate mummies, a significantly lower rate than for unparasitized L3 alatoid nymphs in which alate formation rate were 100% (v 2 = 5.625; p < 0.05). Among aphids parasitized as L4 alatoid nymphs, 100% turned into alate mummies, as did all unparasitized aphids. Aphids parasitized as L3 alatoids were significantly less likely to fully develop wings than those parasitized as L4 alatoids (v 2 = 24.3; p < 0.05) Effect of parasitism on A. glycines flight The two-way ANOVA indicated a significant effect of parasitism on flight distance and flight duration (Tables 1 and 2). Parasitism time also significantly affected both distance and duration as did the interaction between parasitism and parasitism time. However, we found no significant effect of parasitism on flight speed (F = , p = ). No significant differences were found for flight distance, flight duration or flight speed between unparasitized individuals and those parasitized for 24 h (Student s t-tests, Distance: t = , p = ; Duration: t = , p = ; Speed: t = , p = ) or 48 h (Distance: t = , p = ; Duration: t = , p = ; Speed: t = , p = ). However, at 72 h following parasitism, flight distance (t = , p = ) of parasitized alates was significantly lower than for unparasitized alates, although no differences were found for flight duration (t = , p = ) or the flight speed (t = , p = ). At 96 h post-parasitism, flight distance (t = , p = ), flight duration (t = , p = ), flight speed (t = ; p = ) and flight incidence (v 2 = ; p = ) of parasitized alates were all significantly lower than for unparasitized individuals (Table 2) Effect of A. glycines flight on parasitoid development There was no significant effect of alate flight duration on the larval (F 3, 43 = ; p = ) or pupal (F 3, 43 = ; p = Table 1 Analysis of effects of parasitism and parasitism time on the flight performance (including flight distance, flight duration and flight speed) of soybean aphids. Flight performance Effects DF MS F p Distance Parasitism Parasitism time Parasitism parasitism time Error Duration Parasitism Parasitism time Parasitism parasitism time Error

4 Y. Zhang et al. / Biological 62 (2012) Table 2 Flight performance of parasitized and un-parasitized soybean aphids at different times following parasitism. L4 alatoid nymphs were subjected to parasitism and flight performance was subsequently determined for resulting alates at 24, 48, 72 and 96 h following parasitism. Flight performance was expressed as flight distance, flight duration, flight speed and flight incidence. See text for statistical comparison between same-aged parasitized and unparasitized alate aphids. Time after parasitism (h) n Flight distance (km) Flight duration (h) Flight speed (km/h) % Fliers Parasitized Parasitized Mean ± SE Parasitized Parasitized Parasitized ± 0.50a 1.75 ± 0.31a 1.83 ± 0.43a 1.63 ± 0.31a 1.19 ± 0.10a 1.18 ± 0.13a ± 0.33a 2.40 ± 0.36a 1.47 ± 0.25a 2.12 ± 0.32a 1.45 ± 0.37a 1.19 ± 0.06a ± 0.35a 3.83 ± 0.77b 1.93 ± 0.25a 2.58 ± 0.40a 1.29 ± 0.13a 1.36 ± 0.13a ± 0.24a 2.08 ± 0.44b 0.58 ± 0.20a 1.85 ± 0.33b 0.64 ± 0.14a 1.03 ± 0.08b Means of flight distance, flight duration and flight speed followed by different letters are significantly different between parasitized aphid and control (Student s t-tests, P < 0.05). Table 3 Development of Binodoxys communis within parasitized Aphis glycines alates of varying flight experience. Flight duration (h) n Mummy formation rate Larval development time (d) Female pupal development time (d) Male pupae development time (d) Mummy weight (mg) Sex ratio (prop. male) ± 0.15a 4.56 ± 0.18a 4.57 ± 0.30a 0.16 ± 0.001a ± 0.30a 4.50 ± 0.50a 5.50 ± 0.29a 0.15 ± 0.003a ± 0.33a 4.33 ± 0.23a 5.33 ± 0.67a 0.15 ± 0.015a ± 1.43a 4.80 ± 0.58a 4.00 ± 0.32a 0.15 ± 0.017a Means in the same column followed by different letters are significantly different (Duncan s multiple range test, P < 0.05). Adult emergence rate ) development time of B. communis, or on the mummification rate (v 2 = ; p = ), mummy weight (F 3, 67 = ; p = ), sex ratio (proportion males) (v 2 = ; p = ), or adult emergence rate (v 2 = ; p = ) (Table 3). 4. Discussion Our study demonstrated the potential for alate-assisted transport of B. communis within A. glycines summer migrants. Parasitized aphids engaged in long-distance flights in our flight-mill assays when parasitism occurred during the 4th nymphal instar. Although not tested, we presume that aphids stung by B. communis as alates would also engage in flight, as found previously for the parasitoid Aphelinus varipes (Zhang et al., 2009b). However, parasitism of 3rd-instar alatoid nymphs strongly interferes with aphid flight by disrupting A. glycines wing development. Thus, timing of parasitism is critical for alate-mediated movement of immature B. communis. We also found that A. glycines flight activity did not have any measurable impact on B. communis fitness in terms of survival to adult, developmental time, mummy weight, or adult sex ratio. Parasitoid-induced interference in wing development has been reported from other parasitoid-aphid systems, and these developmental effects appear to be associated with early, rather than later, stages of parasitism (Johnson, 1959; Christiansen-Weniger and Hardie, 1998, 2000; Demmon et al., 2004). Disruption of wing formation could be mediated by a component of the calyx fluid or by teratocytes (Falabella et al., 2000, 2009; Le Ralec et al., 2011). Parasitism of A. glycines by B. communis did not appear to disrupt A. glycines wing development when aphids were parasitized as L4 nymphs, and this was also found in Aphelinus varipes attacking L4 alatoid A. glycines (Zhang et al., 2009b). B. communis-parasitized summer alates engaged in long-distance flights of similar duration to unparasitized individuals during the first 48 h post-parasitism, which is consistent with previous observations of a gradual decline in flight performance of A. glycines alates h after parasitism by A. varipes (Zhang et al., 2009b). This suggests that the decline may be related to egg hatching, which likely occurs between 48 and 72 h after parasitism (Christiansen-Weniger, 1994). Parasitoid larvae can impede host movement through depletion of host energy reserves or damage to host tissue (Sequeira and Mackauer, 1992). Our results are similar to those of Rauwald and Ives (2001), who reported impeded flight of Acyrthosiphon pisum alates in the presence of older Aphidius ervi larvae. Development time, mummy emergence and sex ratio of B. communis did not change with flight duration, indicating that alate A. glycines provide sufficient nutrient for B. communis development after flight. Aphids typically use most of their glycogen during the first 1 2 h of tethered flight, after which time they switch to utilizing lipid reserves (Cockbain, 1961). In our study, lipid reserves may not have declined in A. glycines alates during flight to such a degree to where significant reduction in oocyte or embryo provisioning occurred, both of these being important nutrient sources for parasitoid development (Falabella et al., 2000; Walker and Hoy, 2003; Colinet et al., 2005). B. communis-infested summer migrants engaged in long-distance, active flight in flight mill tests. Parasitized alates can presumably also engage in wind-aided, passive dispersal or migration, which could carry parasitoid larvae for hundreds of kilometers (Taylor et al., 1979; Robert, 1987; Irwin and Thresh, 1988; Isard and Gage, 2001; Venette and Ragsdale, 2004; Zhu et al., 2006). Given the substantial movement potential of A. glycines alates, coupled with the narrow host range of B. communis (Desneux et al., 2009a), alate-assisted movement could increase parasitoid fitness by permitting more reliable tracking of its host. In North America, however, long distance alate migration may serve to dilute introduced B. communis populations by spreading parasitoids well beyond release areas (Heimpel and Asplen, 2011). This could lead to a decreased probability of mate location at the edges of the introduced range, a well-known driver of Allee effects (Hopper and Roush, 1993; Stephens et al., 1999; Fauvergue and Hopper, 2009; Gascoigne et al., 2009). Thus, the relative fitness effects of alate-mediated movement for B. communis (and other soybean aphid parasitoids) likely depend on whether it occurs in the native range (where conspecifics are more uniformly

5 14 Y. Zhang et al. / Biological 62 (2012) distributed through the landscape) or the introduced range (where conspecific densities are likely much lower at the edges), at least the parasitoid has established in a broader geographic area of North America. It is expected that B. communis, upon successful establishment, will gradually expand its geographic distribution in its novel environment. Parallel to this, outcomes for the parasitoid in North America could become more similar to those in its native range. The most important factor in determining the potential ecological impacts of alate-assisted movement of B. communis, however, is predicting the likelihood of its occurrence under field conditions. Two major variables play into this: (1) the relative oviposition rate into alatoid or alate aphids by B. communis, and (2) for alatoid nymphs, the frequency at which parasitized nymphs develop into flight-capable adults. With regard to the former, the available evidence for the B. communis A. glycines system suggests that L4 alatoid and alate aphids may be relatively poor hosts for B. communis. For summer stages, Wyckhuys et al., (2008) showed that, while both alates and L4 alatoid nymphs were physiologically suitable hosts, these stages were attacked at lower rates relative to apterae. The lower attack rate of alate and alatoid stages was likely due to more effective defense behaviors (Wyckhuys et al., 2008; Desneux et al., 2009a,b). Asplen et al. (2011) found a similar result for the fall-stage female alate morphs (gynoparae) and L4 alatoid nymphs, and preliminary tests suggested that alate male aphids were physiologically unsuitable hosts in no-choice tests (Heimpel et al., 2010; Asplen et al., 2011). Gynoparous L3 alatoid nymphs, however, were attacked at a rate more comparable to summer apterae during the course of these experiments. If younger alatoid A. glycines nymphs are more suitable hosts than L4 or alate adult conspecifics, then a critical factor in determining levels of alate-mediated dispersal is the probability of nymphs reaching the alate stage prior to host death. In our trials, only 25% of L3 summer alatoid nymphs formed mummies with normal wings, with the other 75% forming either apterous mummies (65%), or mummies with apparent wing deformities (10%). Similar to these results, Asplen et al. (2011) showed that L3 alatoid gynoparae could reach the adult winged stage prior to mummification, but that this only occurred in a small fraction (ca. 7%) of stung nymphs (the remaining nymphs mummified before reaching the winged stage). These data suggest that the more suitable younger alatoid stages are significantly less likely to yield parasitized, flight-capable aphids. Taken together, these lines of evidence suggest that the likelihood of alate-assisted transport of B. communis should be low when aphid populations are polyphenic. However, natural A. glycines populations contain high proportions of alatoids and alates during certain parts of the year. For example, major A. glycines migrations occur during the summer (soybean to soybean), fall (soybean to buckthorn), and spring (buckthorn to soybean) in North America (Ragsdale et al., 2004; Hodgson et al., 2005; Bahlai et al., 2010; Mueller et al., 2010). During these peak flight periods, the relatively higher alatoid proportions may result in far greater levels of alate parasitism and movement, especially if B. communis presence actually triggers alate production in A. glycines, as demonstrated in other aphid-parasitoid systems (e.g., Sloggett and Weisser, 2002). In summary, our results show that soybean aphids parasitized by the parasitoid B. communis as 4th-instar nymphs develop into alate adults and can fly normal distances while parasitized. This could lead to long-distance transport of the parasitoids possibly farther than they are able to travel on their own. The extent to which this occurs in the field is likely limited by a preference of B. communis for apterous rather than alatoid nymphs of the soybean aphid, but it could still occur at non-trivial levels. Acknowledgments We thank Dr. Dengfa Cheng (Institute of Plant protection, Chinese Academy of Agricultural Sciences, Beijing) for providing the aphid flight-mill. This research was supported by financial assistance from National Natural Science Foundation of China ( ), Chinese Ministry of Science and Technology (2006CB102007), and NCSRPC and USDA RAMP funding. 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