Kris A. G. Wyckhuys

Mirid Bug Outbreaks in Multiple Crops Correlated with Wide-Scale Adoption of Bt Cotton in China

Collateral Damage Cotton crops that have been bioengineered to express the insecticidal toxin derived from Bacillus thuringiensis (Bt) carry their own insect control, particularly against the cotton bollworm, and are less dependent on externally applied pesticides. Lu et al. (p. 1151, published online 13 April) now show that reduction in general pesticide use in cotton-growing regions of northern China has shifted the balance of regional pest populations. Bt-expressing cotton now serves as a source of herbivorous insects of the Miridae family, rather than the sink that nonengineered cotton was when less specific pesticides were used. Because these insects will eat a variety of plants, they are emerging as a threat to other crops, including grape, apple, peach, and pear. The use of more specific pesticides results in the resurgence of nontargeted insect populations. Long-term ecological effects of transgenic Bacillus thuringiensis (Bt) crops on nontarget pests have received limited attention, more so in diverse small holder–based cropping systems of the developing world. Field trials conducted over 10 years in northern China show that mirid bugs (Heteroptera: Miridae) have progressively increased population sizes and acquired pest status in cotton and multiple other crops, in association with a regional increase in Bt cotton adoption. More specifically, our analyses show that Bt cotton has become a source of mirid bugs and that their population increases are related to drops in insecticide use in this crop. Hence, alterations of pest management regimes in Bt cotton could be responsible for the appearance and subsequent spread of nontarget pests at an agro-landscape level.

Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control.

The tomato leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is a devastating pest of tomato originating from South America. After its initial detection in eastern Spain in 2006, it rapidly invaded various other European countries and spread throughout the Mediterranean basin. If no control measures are taken, then the pest can cause up to 80–100% yield losses in tomato crops in recently invaded areas and may pose a threat to both greenhouse and open-field tomato production. The exceptional speed and extent of T. absoluta invasion have called for studies documenting its biology and ecology, while indicating an urgent need for efficient and sustainable management methods. The development of approaches to manage T. absoluta would be facilitated through a detailed revision of information on this pest in its area of origin. This review combines information on the invasion by T. absoluta, its ecology, and potential management strategies, including data that may help the implementation of efficient biological control programs. These programs, together with a variety of other management tactics, may allow efficient integrated pest management of T. absoluta in Europe and Mediterranean Basin countries.

Population responses by Orius insidiosus to vegetational diversity

The abundance of different life stages of Orius insidiosus (Say) (Heteroptera: Anthocoridae) and its prey were recorded in vegetationally diverse (soybean and agronomic weeds) and monoculture (soybean only) fields. Orius insidiosus adults and nymphs were more abundant in diversified plots than in monocultures. A similar number of O. insidiosus eggs were found in the two treatments, but twice as many eggs were laid on non-crop plants than on soybeans within the vegetationally diverse plots. Prey densities were equivalent in the two treatments. In olfactometer assays, naïve O. insidiosus females were unresponsive to odors from three weed species (morning glory, redroot pigweed and velvetleaf). The current results, coupled with previous experimental observations, lead us to believe that higher abundance of O. insidiosus in vegetationally diverse habitats could be related to improved fitness of the predator, which in turn is related to certain plant qualities (e.g., nutrition, plant architecture, etc.). Proximal cues are likely more influential to oviposition decisions by O. insidiosus females than volatile signals.

Flight Performance of the Soybean Aphid, Aphis glycines (Hemiptera: Aphididae) Under Different Temperature and Humidity Regimens

Abstract The soybean aphid, Aphis glycines (Matsumura), is native to eastern Asia and has recently invaded North America, where it is currently the most important insect pest of soybeans. The soybean aphid has spread rapidly within North America, presumably through a combination of active and passive (wind-aided) flight. Here, we studied the active flight potential of A. glycines under a range of environmental conditions using an aphid flight mill. Winged (alate) A. glycines were tested on a specially designed 32-channel, computer-monitored flight mill system. Aphids that were 12–24 h old exhibited the strongest flight behavior, with average flight durations of 3.3–4.1 h, which represented flight distances of 4.6–5.1 km. After the age of 72 h, A. glycines flight performance rapidly declined. The optimum temperature range for flight was 16–28°C, whereas optimum relative humidity was 75%. Our findings show that A. glycines posseses a fairly strong active flight aptitude (ability and inclination) and point to the possibility of flight initiation under a broad range of environmental conditions. These results have the potential to aid forecasting and management protocols for A. glycines at the landscape level.

Relationship of soybean aphid (Hemiptera: Aphididae) to soybean plant nutrients, landscape structure, and natural enemies.

ABSTRACT In the north central United States, populations of the exotic soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), are highly variable across space, complicating effective aphid management. In this study we examined relationships of plant nutrients, landscape structure, and natural enemies with soybean aphid abundance across Iowa, Michigan, Minnesota, and Wisconsin, representing the range of conditions where soybean aphid outbreaks have occurred since its introduction. We sampled soybean aphid and its natural enemies, quantified vegetation land cover and measured soybean nutrients (potassium [K] and nitrogen [N]) in 26 soybean sites in 2005 and 2006. Multiple regression models found that aphid abundance was negatively associated with leaf K content in 2005, whereas it was negatively associated with habitat diversity (Simpsons index) and positively associated with leaf N content in 2006. These variables accounted for 25 and 27% of aphid variability in 2005 and 2006, respectively, suggesting that other sources of variability are also important. In addition, K content of soybean plants decreased with increasing prevalence of corn-soybean cropland in 2005, suggesting that landscapes that have a high intensification of agriculture (as indexed by increasing corn and soybean) are more likely to have higher aphid numbers. Soybean aphid natural enemies, 26 species of predators and parasitoids, was positively related to aphid abundance; however, enemy-to-aphid abundance ratios were inversely related to aphid density, suggesting that soybean aphids are able to escape control by resident natural enemies. Overall, soybean aphid abundance was most associated with soybean leaf chemistry and landscape heterogeneity. Agronomic options that can ameliorate K deficiency and maintaining heterogeneity in the landscape may reduce aphid risk.

Electrophysiological and behavioral responses of Microplitis mediator (Hymenoptera: Braconidae) to caterpillar-induced volatiles from cotton.

ABSTRACT Microplitis mediator Haliday (Hymenoptera: Braconidae) is an important larval endoparasitoid of various lepidopteran pests, including Helicoverpa armigera (Hübner). In China, H. armigera is a key pest of cotton and is currently the focus of several biological control efforts that use M. mediator as principal natural enemy of this pest. To improve the success of biological control efforts, behavioral studies are needed that shed light on the interaction between M. mediator and H. armigera. In this study, we determined M. mediator response to volatile compounds from undamaged, mechanically injured, or H. armigera--damaged plants and identified attractive volatiles. In Y-tube olfactometer assays, we found that mechanically damaged plants and/or plants treated with H. armigera oral secretions did not attract wasps. However, volatiles from H. armigera—damaged plants elicited a strong attraction of both M. mediator sexes. Headspace extracts from H. armigera—damaged cotton were analyzed by coupled gas chromatography—electroantennographic detection (GC-EAD), and a total of seven different compounds were found to elicit electroantennogram (EAG) responses, including an unknown compound. Six different EAD-active volatiles were identified from caterpillar-damaged cotton plants, of which 3, 7-dimethyl-1, 3, 6-octatriene and (Z)-3-hexenyl acetate were the principal compounds. Olfactometer assays indicated that individual synthetic compounds of 3, 7-dimethyl-1, 3, 6-octatriene, (Z)-3-hexenyl acetate, and nonanal were attractive to M. mediator. Field cage studies showed that parasitism of H. armigera larvae by M. mediator was higher on cotton plants to which 3, 7-dimethyl-1, 3, 6-octatriene was applied. Our results show that the combination of terpenoids and green leaf volatiles may not only facilitate host, mate, or food location but may also increase H. armigera parasitism by M. mediator.

Response of the soybean aphid parasitoid Binodoxys communis to olfactory cues from target and non‐target host‐plant complexes

The parasitoid Binodoxys communis (Gahan) (Hymenoptera: Braconidae) is a candidate for release against the Asian soybean aphid, Aphis glycines Matsumura (Homoptera: Aphididae), in North America. Using a series of Y‐tube olfactometer assays, we recorded responses of naïve and experienced B. communis females to odors from both target and non‐target host plant complexes. The non‐target host plant complexes included three aphid species native to North America [Aphis monardae Oestlund, Aphis oestlundi Gillette, and Aphis asclepiadis (Fitch)] and one species presumed to be exotic to North America (Aphis nerii Boyer de Fonscolombe), all on their respective host plants. We also investigated whether the parasitoid distinguishes between volatiles from soybean infested with A. glycines vs. those of uninfested plants. Volatiles from A. glycines‐infested soybean plants and several non‐target host plant complexes elicited a response in B. communis, which seemed to be reinforced through oviposition experience. Wasps with experience on a specific host plant complex increased their response to odors of this complex. Neither naïve nor experienced wasps, however, preferred odors from target vs. non‐target host plant complexes in choice tests. Our data also indicate that B. communis is unable to distinguish between volatiles from infested vs. uninfested soybean plants. This study shows that B. communis females respond to a broad array of olfactory stimuli, exhibit low fidelity for any particular odor, and employ some behavioral plasticity in their response to volatile cues. We discuss implications of these results for establishment of B. communis and potential undesirable non‐target effects associated with the release of this species in North America.

Potential exposure of a classical biological control agent of the soybean aphid, Aphis glycines, on non-target aphids in North America

In summer 2007, the Asian parasitoid Binodoxys communis (Hymenoptera: Braconidae) was released in North America for control of the exotic soybean aphid, Aphis glycines (Hemiptera: Aphididae). Despite its comparatively narrow host range, releases of B. communis may still constitute a risk to native aphid species. To estimate the risk of exposure of non-target aphids to B. communis, we merged assessments of temporal co-occurrence with projections of spatial overlap between B. communis and three native aphid species, and in-field measurements of the incidence of ecological filters that may protect these aphids from parasitism. Temporal co-occurrence was assessed between A. glycines and native aphids (Aphis asclepiadis, Aphis oestlundi, and Aphis monardae) at four different locations in Minnesota, USA. The degree of temporal overlap depended greatly on location and aphid species, ranging between 0 and 100%. All of the native aphids were tended by multiple species of ants, with overall ant-attendance ranging from 26.1 to 89.6%. During temporal overlap with A. glycines, 53 ± 11% of A. monardae colonies were partly found in flower heads of their host plant, with flowers acting as a physical refuge for this aphid. The extent of geographic overlap between B. communis and native aphids based upon Climex modeling was 17–28% for A. monardae, 13–22% for A. oestlundi, 46–55% for A. asclepiadis and 12–24% for the A. asclepiadis species complex. The estimated overall probability of potential exposure of B. communis on native aphids was relatively low (P = 0.115) for A. oestlundi and high (P = 0.550) for A. asclepiades. Physical and ant-mediated refuges considerably lowered probability of population-level impact on A. monardae, and could lead to substantial reduction of exposure for the other native aphids. These findings are used to make broader statements regarding the ecological safety of current B. communis releases and their potential impact on native aphid species in North America.

Comparative flight performance of three important pest Adelphocoris species of Bt cotton in China

The massive adoption of Bt cotton throughout China has been accompanied by outbreaks of secondary pests such as Adelphocoris spp. (Heteroptera: Miridae). The Adelphocoris group primarily consists of three species: A. suturalis, A. fasciaticollis and A. lineolatus, which greatly differ in geographical distribution and seasonal dynamics. However, the underlying drivers of these differences remain to be understood. The study of flight behaviour of these three species can yield important insight into their spatial and temporal dynamics and help explain their distribution. We examined flight propensity of the three Adelphocoris spp. under a range of biological and environmental conditions using a computer-monitored flight-mill. Gender and mating status only had minor effects on flight performance in these species, while age exerted great effects on it. Flight capacity was low for one-day-old adults and increased with age until day 10-13, then gradually decreased afterwards. Temperature and relative humidity affected flight propensity, with 20-23 degrees C and 64-68% RH considered optimal for flight of all three species. Between-species comparisons indicated that A. suturalis and A. fasciaticollis had similar flight distance and duration, which were significantly greater than for A. lineolatus. Our findings provide crucial information for understanding geographical distribution and seasonal occurrence and for developing regional forecasting and pest management protocols for Adelphocoris species.

Trade-Offs Between Flight and Fecundity in the Soybean Aphid (Hemiptera: Aphididae)

ABSTRACT The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is native to eastern Asia and was accidentally introduced into North America in 2000. Within a few years, it was found throughout the U.S. and Canadian soybean-growing regions. The spread of A. glycines in North America is partly ascribed to its great flight capacity. We conducted direct measurements of flight performance of winged A. glycines adults and correlated this to their subsequent longevity and fecundity to determine whether there are trade-offs between flight and fecundity. We also estimated fecundity and development time of the offspring of females that had flown varying distances to examine potential maternal effects linked to flight. The experiment was conducted using a specifically designed aphid flight mill system in which winged aphids were tethered by their abdomens and flight duration, distance and speed were quantified. Fecundity, longevity and reproductive periods of 12-h-old A. glycines alates that had engaged in >0.5 km long flights were significantly lower than those of <0.5-km individuals. The offspring of alates with flight experiences of >1.5 km also had lower fecundity than those produced by individuals that had engaged in flights <1.5 km. Our results are therefore consistent both with direct trade-offs between flight and fecundity and a trade-off between flight and fecundity via maternal effects.