Kongming Wu

Suppression of Cotton Bollworm in Multiple Crops in China in Areas with Bt Toxin-Containing Cotton

Transgenic cotton that has been engineered to produce insecticidal toxins from Bacillus thuringiensis (Bt) and so to resist the pest cotton bollworm (Helicoverpa armigera) has been widely planted in Asia. Analysis of the population dynamics of H. armigera from 1992 to 2007 in China indicated that a marked decrease in regional outbreaks of this pest in multiple crops was associated with the planting of Bt cotton. The study area included six provinces in northern China with an annual total of 3 million hectares of cotton and 22 million hectares of other crops (corn, peanuts, soybeans, and vegetables) grown by more than 10 million resource-poor farmers. Our data suggest that Bt cotton not only controls H. armigera on transgenic cotton designed to resist this pest but also may reduce its presence on other host crops and may decrease the need for insecticide sprays in general.

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.

Diverse genetic basis of field-evolved resistance to Bt cotton in cotton bollworm from China

Evolution of pest resistance reduces the efficacy of insecticidal proteins from Bacillus thuringiensis (Bt) used in sprays or in transgenic crops. Although several pests have evolved resistance to Bt crops in the field, information about the genetic basis of field-evolved resistance to Bt crops has been limited. In particular, laboratory-selected resistance to Bt toxin Cry1Ac based on recessive mutations in a gene encoding a toxin-binding cadherin protein has been identified in three major cotton pests, but previous work has not determined if such mutations are associated with field-selected resistance to Bt cotton. Here we show that the most common resistance alleles in field populations of cotton bollworm, Helicoverpa armigera, selected with Bt cotton in northern China, had recessive cadherin mutations, including the deletion mutation identified via laboratory selection. However, unlike all previously studied cadherin resistance alleles, one field-selected cadherin resistance allele conferred nonrecessive resistance. We also detected nonrecessive resistance that was not genetically linked with the cadherin locus. In field-selected populations, recessive cadherin alleles accounted for 75–84% of resistance alleles detected. However, most resistance alleles occurred in heterozygotes and 59–94% of resistant individuals carried at least one nonrecessive resistance allele. The results suggest that resistance management strategies must account for diverse resistance alleles in field-selected populations, including nonrecessive alleles.

Large-scale test of the natural refuge strategy for delaying insect resistance to transgenic Bt crops

The ‘natural refuge strategy” for delaying insect resistance to transgenic cotton that produces insecticidal proteins from Bacillus thuringiensis (Bt) relies on refuges of host plants other than cotton that do not make Bt toxins. We tested this widely adopted strategy by comparing predictions from modeling with data from a four-year field study of cotton bollworm (Helicoverpa armigera) resistance to transgenic cotton producing Bt toxin Cry1Ac in six provinces of northern China. Bioassay data revealed that the percentage of resistant insects increased from 0.93% in 2010 to 5.5% in 2013. Modeling predicted that the percentage of resistant insects would exceed 98% in 2013 without natural refuges, but would increase to only 1.1% if natural refuges were as effective as non-Bt cotton refuges. Therefore, the results imply that natural refuges delayed resistance, but were not as effective as an equivalent area of non-Bt cotton refuges. The percentage of resistant insects with nonrecessive inheritance of resistance increased from 37% in 2010 to 84% in 2013. Switching to Bt cotton producing two or more toxins and integrating other control tactics could slow further increases in resistance.

Evaluation of the Natural Refuge Function for Helicoverpa armigera (Lepidoptera: Noctuidae) within Bacillus thuringiensis Transgenic Cotton Growing Areas in North China

Abstract The density of Helicoverpa armigera (Hübner) populations on Bacillus thuringiensis Berliner (Bt) transgenic cotton, corn, peanut, and soybean; differences in its development on Bt cotton and common (nontransgenic) cotton; and the potential for mating among populations from Bt cotton fields and other crop fields were investigated in the suburbs of Xinxiang City (Henan Province) and Langfang City (Hebei Province) in the southern and northern parts of north China, respectively. Although development of H. armigera on Bt cotton was much slower than on common cotton, there was a still high probability of mating between populations from Bt cotton and other sources due to the scattered emergence pattern of H. armigera adults, and overlap of the second and third generations. In a cotton and corn growing region, early and late planted corn provided suitable refugia for the third and fourth generations of H. armigera, but not for the second generation. In a cotton and soybean/peanut mix system, noncotton crops provided a natural refugia from the second- to fourth-generation H. armigera, but function of the refuge would closely depend on the proportion of Bt cotton. Consequently, it may be necessary to compensate the original mixed cropping patterns in different areas for delaying resistance development of H. armigera to Bt cotton.

Increased Frequency of Pink Bollworm Resistance to Bt Toxin Cry1Ac in China

Transgenic crops producing insecticidal proteins from Bacillus thuringiensis (Bt) kill some key insect pests, but evolution of resistance by pests can reduce their efficacy. The main approach for delaying pest adaptation to Bt crops uses non-Bt host plants as “refuges” to increase survival of susceptible pests. To delay evolution of pest resistance to transgenic cotton producing Bt toxin Cry1Ac, the United States and some other countries have required refuges of non-Bt cotton, while farmers in China have relied on “natural” refuges of non-Bt host plants other than cotton. The “natural” refuge strategy focuses on cotton bollworm (Helicoverpa armigera), the primary target of Bt cotton in China that attacks many crops, but it does not apply to another major pest, pink bollworm (Pectinophora gossypiella), which feeds almost entirely on cotton in China. Here we report data showing field-evolved resistance to Cry1Ac by pink bollworm in the Yangtze River Valley of China. Laboratory bioassay data from 51 field-derived strains show that the susceptibility to Cry1Ac was significantly lower during 2008 to 2010 than 2005 to 2007. The percentage of field populations yielding one or more survivors at a diagnostic concentration of Cry1Ac increased from 0% in 2005–2007 to 56% in 2008–2010. However, the median survival at the diagnostic concentration was only 1.6% from 2008 to 2010 and failure of Bt cotton to control pink bollworm has not been reported in China. The early detection of resistance reported here may promote proactive countermeasures, such as a switch to transgenic cotton producing toxins distinct from Cry1A toxins, increased planting of non-Bt cotton, and integration of other management tactics together with Bt cotton.

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.

The Endosymbiont Arsenophonus Is Widespread in Soybean Aphid, Aphis glycines, but Does Not Provide Protection from Parasitoids or a Fungal Pathogen

Aphids commonly harbor bacterial facultative symbionts that have a variety of effects upon their aphid hosts, including defense against hymenopteran parasitoids and fungal pathogens. The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is infected with the symbiont Arsenophonus sp., which has an unknown role in its aphid host. Our research goals were to document the infection frequency and diversity of the symbiont in field-collected soybean aphids, and to determine whether Arsenophonus is defending soybean aphid against natural enemies. We performed diagnostic PCR and sequenced four Arsenophonus genes in soybean aphids from their native and introduced range to estimate infection frequency and genetic diversity, and found that Arsenophonus infection is highly prevalent and genetically uniform. To evaluate the defensive role of Arsenophonus, we cured two aphid genotypes of their natural Arsenophonus infection through ampicillin microinjection, resulting in infected and uninfected isolines within the same genetic background. These isolines were subjected to parasitoid assays using a recently introduced biological control agent, Binodoxys communis [Braconidae], a naturally recruited parasitoid, Aphelinus certus [Aphelinidae], and a commercially available biological control agent, Aphidius colemani [Braconidae]. We also assayed the effect of the common aphid fungal pathogen, Pandora neoaphidis (Remaudiere & Hennebert) Humber (Entomophthorales: Entomophthoraceae), on the same aphid isolines. We did not find differences in successful parasitism for any of the parasitoid species, nor did we find differences in P. neoaphidis infection between our treatments. Our conclusion is that Arsenophonus does not defend its soybean aphid host against these major parasitoid and fungal natural enemies.

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.

Comparative study of temperature-dependent life histories of three economically important Adelphocoris spp.

Subsequent to the widespread adoption of Bt transgenic cotton in China and an associated reduction in pesticide use, Adelphocoris spp. (Hemiptera: Miridae) are the key pests of this crop. Three species (Adelphocoris suturalis, Adelphocoris fasciaticollis and Adelphocoris lineolatus) are found in Chinese Bt cotton fields, each with a distinct geographic distribution and phenology. In the present study, the development and fecundity of the three species are compared in the laboratory at various temperatures in the range 10–35 °C. Although nymphal development and adult moulting occurs under all temperature regimes, egg eclosion is not observed at 10 °C. In general, egg and nymphal development periods decrease with increasing temperature up to 30 °C. The lower and upper development thresholds are, respectively, 5.6 and 40.1 °C for A. suturalis eggs; 5.0 and 38.4 °C for nymphs; 6.3 and 39.0 °C for A. fasciaticollis eggs, 3.0 and 41.9 °C for nymphs; 5.6 and 41.3 °C for A. lineolatus eggs; and 6.2 and 38.8 °C for nymphs. Thermal constants are 189.9 degree days (DD) (egg) and 308.8 DD (nymph) for A. suturalis, 188.8 DD (egg) and 366.7 DD (nymph) for A. fasciaticollis, and 231.7 DD (egg) and 291.6 DD (nymph) for A. lineolatus. Temperatures above 30 °C affect egg development of A. fasciaticollis and A. lineolatus adversely, but not that of A. suturalis. At the same time, nymphal survival of A. suturalis is reduced at 10 °C. Longevity of all species declines with increasing temperature, whereas extremes of temperature (i.e. 10 and 35 °C) interfere with oviposition. The estimated optimum range for oviposition is 23–25 °C, irrespective of species. In general, development and fecundity of the three Adelphocoris spp. is consistent with their respective distribution and seasonal dynamics. The present study provides insight into the distribution and phenology of Adelphocoris spp., and contributes to the modelling of their population dynamics.