Effects of climate change and crop planting structure on the abundance of cotton bollworm,Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae)

The interactions between plants and insects play an important role in ecosystems. Climate change and cropping patterns can affect herbivorous pest insect dynamics. Understanding the reasons for population fluctuations can help improve integrated pest management strategies. Here, a 25‐year dataset on climate, cropping planting structure, and the population dynamics of cotton bollworms (Helicoverpa armigera) from Bachu County, south Xinjiang, China, was analyzed to assess the effects of changes in climate and crop planting structure on the population dynamics of H. armigera. The three generations of H. armigera showed increasing trends in population size with climate warming, especially in the third generation. The relative abundances of the first and second generations decreased, but that of the third generation increased. Rising temperature and precipitation produced different impacts on the development of different generations. The population numbers of H. armigera increased with the increase in the non‐Bacillus thuringiensis (Bt) cotton‐planted area. Asynchrony of abrupt changes existed among climate change, crop flowering dates, and the phenology of H. armigera moths. The asynchronous responses in crop flowering dates and phenology of H. armigera to climate warming would expand in the future. The primary factors affecting the first, second, and third generations of moths were T_mean in June, the last appearance date of the second generation of moths, and the duration of the third generation of moths, respectively. To reduce the harm to crops caused by H. armigera, Bt cotton should be widely planted.     

Regulation of the seasonal population patterns of <Emphasis Type="Italic">Helicoverpa armigera</Emphasis> moths by <Emphasis Type="Italic">Bt</Emphasis> cotton planting

Transgenic cotton expressing the Bacillus thuringiensis (Bt) Cry1Ac toxin has been commercially cultivated in China since 1997, and by 2000 Bt cotton had almost completely replaced non-transgenic cotton cultivars. To evaluate the impact of Bt cotton planting on the seasonal population patterns of cotton bollworm, Helicoverpa armigera, the dynamics of H. armigera moths were monitored with light traps from four locations (Xiajin, Linqing and Dingtao of Shandong Province; Guantao of Hebei Province) in high Bt density region and five locations (Anci and Xinji of Hebei Province; Dancheng and Fengqiu of Henan Province; Gaomi of Shandong Province) in low Bt density region from 1996 to 2008. A negative correlation was found between moth densities of H. armigera and the planting years of Bt cotton in both high and low Bt density areas. These data indicate that the moth population density of H. armigera was reduced with the introduction of Bt cotton in northern China. Three generations of moths occurred between early June and late September in the cotton regions. Interestingly, second-generation moths decreased and seemed to vanish in recent years in high Bt density region, but this tendency was not found in low Bt density region. The data suggest that the planting of Bt cotton in high Bt density region was effective in controlling the population density of second-generation moths. Furthermore, the seasonal change of moth patterns associated with Bt cotton planting may regulate the regional occurrence and population development of this migratory insect.     

Cotton bollworm resistance to Bt transgenic cotton: A case analysis

Cotton bollworm (Helicoverpa armigera) is one of the most serious insect pests of cotton. Transgenic cotton expressing Cry toxins derived from a soil bacterium, Bacillus thuringiensis (Bt), has been produced to target this pest. Bt cotton has been widely planted around the world, and this has resulted in efficient control of bollworm populations with reduced use of synthetic insecticides. However, evolution of resistance by this pest threatens the continued success of Bt cotton. To date, no field populations of bollworm have evolved significant levels of resistance; however, several laboratory-selected Cry-resistant strains of H. armigera have been obtained, which suggests that bollworm has the capacity to evolve resistance to Bt. The development of resistance to Bt is of great concern, and there is a vast body of research in this area aimed at ensuring the continued success of Bt cotton. Here, we review studies on the evolution of Bt resistance in H. armigera, focusing on the biochemical and molecular basis of Bt resistance. We also discuss resistance management strategies, and monitoring programs implemented in China, Australia, and India.     

The seesaw effect of winter temperature change on the recruitment of cotton bollworms Helicoverpa armigera through mismatched phenology

Knowing how climate change affects the population dynamics of insect pests is critical for the future of integrated pest management. Rising winter temperatures from global warming can drive increases in outbreaks of some agricultural pests. In contrast, here we propose an alternative hypothesis that both extremely cold and warm winters can mismatch the timing between the eclosion of overwintering pests and the flowering of key host plants. As host plants normally need higher effective cumulative temperatures for flowering than insects need for eclosion, changes in flowering time will be less dramatic than changes in eclosion time, leading to a mismatch of phenology on either side of the optimal winter temperature. We term this the “seesaw effect.” Using a long‐term dataset of the Old World cotton bollworm Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in northern China, we tested this seesaw hypothesis by running a generalized additive model for the effects of the third generation moth in the preceding year, the winter air temperature, the number of winter days below a critical temperature and cumulative precipitation during winter on the demography of the overwintering moth. Results confirmed the existence of the seesaw effect of winter temperature change on overwintering populations. Pest management should therefore consider the indirect effect of changing crop phenology (whether due to greenhouse cultivation or to climate change) on pest outbreaks. As arthropods from mid‐ and high latitudes are actually living in a cooler thermal environment than their physiological optimum in contrast to species from lower latitudes, the effects of rising winter temperatures on the population dynamics of arthropods in the different latitudinal zones should be considered separately. The seesaw effect makes it more difficult to predict the average long‐term population dynamics of insect pests at high latitudes due to the potential sharp changes in annual growth rates from fluctuating minimum winter temperatures.     

A simple and reliable method for discriminating between Helicoverpa armigera and Helicoverpa assulta (Lepidoptera: Noctuidae)

Abstract The cotton bollworm Helicoverpa armigera and the oriental tobacco budworm H. assulta are sibling species, both being important agricultural pests. Morphologically, the two insects are almost indistinguishable at the egg, larval and pupal stages. One of the big challenges in the study of these insects, in particular in integrated pest management, is a timely and dependable identification of these insects at their early stages of development. Here, we report a H. armigera‐specific nuclear DNA marker, and demonstrate that it can be employed to reliably discriminate between H. armigera and H. assulta by simple polymerase chain reaction amplification experiment.     

基于生命表参数的棉铃虫种群动态模拟研究

依据对棉铃虫自然种群生命表研究所获得的种群统计参数,采用蒙特卡罗方法,模拟了随机环境条件下的棉铃虫种群发生动态。模拟结果显示,同一输入参数(模拟的1代残虫量),经过确定世代或生活史阶段后,棉铃虫的种群密度既可能为轻发生,也可能种群暴发。环境条件有利时,输入变量(模拟的1代残虫量)影响棉铃虫最大可能的发生程度。当棉铃虫为中等或轻发生时,1代残虫量(模型输入参数)和最终的棉铃虫发生程度(模型输出)没有明显的依赖关系。相同的最终棉铃虫发生程度所对应的模型的输入变量可以有多种水平。模拟结果显示,在环境条件比较有利情况下,棉铃虫只需要1个世代或某一个生活史阶段(如蛹期),种群密度即可达暴发水平。本文的研究结果说明,对棉铃虫中长期发生态势的预测,存在一定程度的不确定性。     

Spring phenology of cotton bollworm affects wheat yield

Climate change has changed numerous species phenologies. Understanding the asynchronous responses between pest insects and host plants to climate change is helpful in improving integrated pest management. It is necessary to use long‐term data to analyze the effects of climate change on cotton bollworm and wheat anthesis. Data for cotton bollworm, wheat yield, and wheat anthesis collected since 1990 were analyzed using linear regression and partial least‐squares regression, as well as the Mann–Kendall test. The results showed that warmer temperatures in the spring advanced the phenologies of cotton bollworm and wheat anthesis, but the phenology changes in overwintering cotton bollworm were faster than those in wheat anthesis, and the eclosion period of overwintering was prolonged, resulting in an increase in overwintering adult abundance. This might lead to more first‐generation larvae and subsequent wheat damage. An early or late first‐appearance date significantly affected the eclosion days. The abrupt changes of phenologies in cotton bollworm, wheat anthesis, and climate were asynchronous, but the abrupt phenology changes occurred after or around the climate abrupt change, especially after or around the abrupt changes of temperature in March and April. The expansion of asynchronous responses in the change rate of wheat anthesis and overwintering cotton bollworm would likely decrease wheat yield due to climate warming in the future. Accumulated temperature was the major affecting factor on the first eclosion date (t₁), adult abundance, and eclosion days. Temperatures in March and April and precipitation in the winter mainly affected the prepeak date (t₂), peak date (t₃), and postpeak date (t₄), respectively, and these factors indirectly affected wheat yield. Thus, the change in the spring phenology of the cotton bollworm and wheat anthesis, and hence wheat yield, was affected by climate warming.     

Quantification of diapausing fourth generation and suicidal fifth generation cotton bollworm, Helicoverpa armigera, in cotton and corn in northern China

Cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), is a major pest of cotton and corn crops in northern China. A phenological differentiation between fourth generation cotton bollworms from cotton and those from corn fields was observed in northern China during 1999–2000. The proportion of pupation in late fall was marginally higher in cotton fields compared to that in corn fields; however, the proportions of fall emergence of moths from cotton fields were significantly higher than those from corn fields. The proportion of spring emergence of moths was also significantly higher for larvae collected from cotton (28.0%) than from corn (14.5%). The overwintering duration of females was significantly shorter than that of males in both crops. Moreover, the overwintering duration of bollworm populations from cotton was significantly longer than that from corn. The early spring population of H. armigera came from both cotton and corn fields, but the spring emergence of moths from larvae collected from cotton took about 5 days longer to reach 100% emergence compared to that from corn.     

Diet-delivered RNAi in Helicoverpa armigera – Progresses and challenges

Helicoverpa armigera (the cotton bollworm) is a significant agricultural pest endemic to Afro-Eurasia and Oceania. Gene suppression via RNA interference (RNAi) presents a potential avenue for management of the pest, which is highly resistant to traditional insecticide sprays. This article reviews current understanding on the fate of ingested double-stranded RNA in H. armigera. Existing in vivo studies on diet-delivered RNAi and their effects are summarized and followed by a discussion on the factors and hurdles affecting the efficacy of diet-delivered RNAi in H. armigera.     

Diminishing Returns from Increased Percent Bt Cotton: The Case of Pink Bollworm

Regional suppression of pests by transgenic crops producing insecticidal proteins from Bacillus thuringiensis (Bt) has been reported in several cropping systems, but little is known about the functional relationship between the ultimate pest population density and the pervasiveness of Bt crops. Here we address this issue by analyzing 16 years of field data on pink bollworm (Pectinophora gossypiella) population density and percentage of Bt cotton in the Yangtze River Valley of China. In this region, the percentage of cotton hectares planted with Bt cotton increased from 9% in 2000 to 94% in 2009 and 2010. We find that as the percent Bt cotton increased over the years, the cross-year growth rate of pink bollworm from the last generation of one year to the first generation of the next year decreased. However, as the percent Bt cotton increased, the within-year growth rate of pink bollworm from the first to last generation of the same year increased, with a slope approximately opposite to that of the cross-year rates. As a result, we did not find a statistically significant decline in the annual growth rate of pink bollworm as the percent Bt cotton increased over time. Consistent with the data, our modeling analyses predict that the regional average density of pink bollworm declines as the percent Bt cotton increases, but the higher the percent Bt cotton, the slower the decline in pest density. Specifically, we find that 95% Bt cotton is predicted to cause only 3% more reduction in larval density than 80% Bt cotton. The results here suggest that density dependence can act against the decline in pest density and diminish the net effects of Bt cotton on suppression of pink bollworm in the study region. The findings call for more studies of the interactions between pest density-dependence and Bt crops.     

Developmental control of Helicoverpa armigera by ingestion of bacteria expressing dsRNA targeting an arginine kinase gene

Cotton bollworm (Helicoverpa armigera) is a polyphagous pest that causes agricultural and commercial losses in many parts of the world. These losses are compounded by insecticide abuse, which leads to insecticide resistance as well as environmental and food pollution. RNA interference (RNAi) is a powerful tool used in gene functional research and RNAi-based pest control. In this study, arginine kinase (AK) of cotton bollworm was selected as the target gene, as it plays a critical role in cellular energy metabolism in invertebrates. Two fragments of the H. armigera AK gene (HarmAK) were cloned into the L4440 vector to express double-stranded RNA (dsRNA) in Escherichia coli (HT115). The effects of different factors on dsRNA stability and the effect of silencing HarmAK on cotton bollworm were subsequently investigated. Both AK gene and protein expression levels were significantly inhibited in larvae, and the peak cumulative mortality rate of 44.44% was recorded on day 5, after 2^nd instar larvae were exposed to the artificial diet coated with the engineered bacteria. The two dsRNAs (dsAK1 and dsAK2) also caused drastic reductions in body weight (38.43% and 17.37%, respectively), body length (26.73% and 11.23%, respectively) and pupation rate (48.89% and 42.95%, respectively) compared to the control on day 5. The development and morphology of the larvae, pupae and adults that fed on the dsAK1 and dsAK2 bacteria were significantly impaired, while the control was not. Thus, AK is a potential target gene for RNAi-mediated cotton bollworm control.     

Climate drivers of bark beetle outbreak dynamics in Norway spruce forests

Bark beetles are among the most devastating biotic agents affecting forests globally and several species are expected to be favored by climate change. Given the potential interactions of insect outbreaks with other biotic and abiotic disturbances, and the potentially strong impact of changing disturbance regimes on forest resources, investigating climatic drivers of destructive bark beetle outbreaks is of paramount importance. We analyzed 17 time‐series of the amount of wood damaged by Ips typographus, the most destructive pest of Norway spruce forests, collected across 8 European countries in the last three decades. We aimed to quantify the relative importance of key climate drivers in explaining timber loss dynamics, also testing for possible synergistic effects. Local outbreaks shared the same drivers, including increasing summer rainfall deficit and warm temperatures. Large availability of storm‐felled trees in the previous year was also strongly related to an increase in timber loss, likely by providing an alternative source of breeding material. We did not find any positive synergy among outbreak drivers. On the contrary, the occurrence of large storms reduced the positive effect of warming temperatures and rainfall deficit. The large surplus of breeding material likely boosted I. typographus population size above the density threshold required to colonize and kill healthy trees irrespective of other climate triggers. Importantly, we found strong negative density dependence in I. typographus that may provide a mechanism for population decline after population eruptions. Generality in the effects of complex climatic events across different geographical areas suggests that the large‐scale drivers can be used as early warning indicators of increasing local outbreak probability.     

盐碱旱地转Bt基因抗虫棉田主要害虫及其天敌种群消长动态

【目的】近年来,我国长江流域和黄河流域棉花面积锐减,种植区域向滨海盐碱地或干旱地转移。研究盐碱旱地转基因棉田与非转基因棉田昆虫群落差异,可为盐碱旱地对转基因棉田生物影响和盐碱旱地转基因棉田害虫防治提供理论指导。【方法】在山东东营和河北枣强盐碱干旱地转Bt基因棉田分别设置常规施药田和非施药田,进行了系统的田间昆虫种群消长动态的调查和统计分析。【结果】中轻度盐碱旱地种植转基因棉花对靶标害虫棉铃虫具有较好的控制作用;与非转基因棉花相比,对其他非靶标害虫棉蚜、烟粉虱和盲蝽及自然天敌龟纹瓢虫、草间小黑蛛种群数量无显著影响,草蛉种群数量在转基因棉田低于非转基因棉田;喷施化学农药对棉铃虫幼虫和棉蚜的防治作用较好,对烟粉虱和盲蝽的防治效果年度间和试验点间有差异,对龟纹瓢虫的杀伤力较大,对草间小黑蛛和草蛉未见明显影响。【结论】盐碱旱地对棉田不同的害虫和天敌影响不同,且转基因棉田与非转基因棉田昆虫群落结构与对照棉田无显著差异。     

Influence of the surrounding landscape on crop colonization by a polyphagous insect pest

Landscape composition plays an important, but poorly understood, role in the population dynamics of agricultural pest species with broad host ranges including both crops and weeds. One such pest, the generalist plant bug Lygus hesperus Knight (Hemiptera: Miridae), is a key cotton pest that feeds on various hosts differing in quality in California's San Joaquin Valley (USA). We investigated the effects of 15 common crops and uncultivated agricultural land on L. hesperus populations, by correlating the densities of L. hesperus in focal cotton fields with the areas of the 16 crops in surrounding rings. Insect counts were provided by private pest‐control advisors, and spatial data were obtained from Kern County records. We first calculated Spearman's partial correlation coefficients on an annual basis for each crop separately, and then performed a meta‐analysis of these correlations across years to describe the overall effect of a particular crop on L. hesperus after the effects of the 15 other crops are removed. Consistent with studies conducted in other areas, L. hesperus density was positively correlated with safflower, and negatively with cotton. Lygus hesperus density was also correlated with several other crops that are often not considered in pest management, including grape, oat, and onion (positive correlations), and almond, pistachio, and potato (negative correlations). Lygus hesperus density was also found to be negatively correlated with alfalfa and positively correlated with uncultivated habitats, a relationship that receives mixed support in the literature. Several other crops tested were not significantly correlated with L. hesperus densities in focal cotton fields, suggesting a neutral role for them in L. hesperus dynamics. The improved understanding of the effects of a greater variety of crops on L. hesperus population dynamics will be useful in the design of agricultural landscapes for enhanced management of this important polyphagous pest.     

Insectivorous bats selectively source moths and eat mostly pest insects on dryland and irrigated cotton farms

Insectivorous bats are efficient predators of pest arthropods in agroecosystems. This pest control service has been estimated to be worth billions of dollars to agriculture globally. However, few studies have explicitly investigated the composition and abundance of dietary prey items consumed or assessed the ratio of pest and beneficial arthropods, making it difficult to evaluate the quality of the pest control service provided. In this study, we used metabarcoding to identify the prey items eaten by insectivorous bats over the cotton‐growing season in an intensive cropping region in northern New South Wales, Australia. We found that seven species of insectivorous bat (n = 58) consumed 728 prey species, 13 of which represented around 50% of total prey abundance consumed. Importantly, the identified prey items included major arthropod pests, comprising 65% of prey relative abundance and 13% of prey species recorded. Significant cotton pests such as Helicoverpa punctigera (Australian bollworm) and Achyra affinitalis (cotton webspinner) were detected in at least 76% of bat fecal samples, with Teleogryllus oceanicus (field crickets), Helicoverpa armigera (cotton bollworm), and Crocidosema plebejana (cotton tipworm) detected in 55% of bat fecal samples. Our results indicate that insectivorous bats are selective predators that exploit a narrow selection of preferred pest taxa and potentially play an important role in controlling lepidopteran pests on cotton farms. Our study provides crucial information for farmers to determine the service or disservice provided by insectivorous bats in relation to crops, for on‐farm decision making.     

Analysis of the spatial-temporal patterns of cotton bollworm population densities and their ecological determinants

Transgenic Bt cotton has been planted in Hubei province of China since 2000. One of the main targets of Bt cotton in the region is cotton bollworm (CBW), Helicoverpa armigera, a polyphagous insect species that feeds not only on cotton but also a number of other host crops. After many years with Bt cotton planting, it is important to know how the population density of CBW has changed at the provincial level. To address the issue, we conduted a monitoring study involving 14 sample sites over 9 years from 2008 to 2016. By data analysis we found that the population density of CBW eggs on cotton plants had significant spatial and temporal differences. Temporally, the population density was significantly lower in 2015–2016 than in 2008–2014. Spatially, the population density was significantly lower in the central plain region than in the northern and southeastern mountain region. Among the six types of non-cotton host crops (i.e. wheat, maize, cole, peanuts, soybean and vegetables), wheat, maize, cole and peanuts had a positive, soybean a negative, and others no significant impact on the population density. Among the two climate factors of temperature and relative humidity, only temperature had a significant impact on the population density, where the impact was negative. The results here help understand the spatial and temporal patterns of CBW population density and their ecological determinants in the study area.     

Oviposition and feeding avoidance in Helicoverpa armigera (Hübner) against transgenic Bt cotton

Helicoverpa armigera (Hübner), the major target pest of transgenic Bacillus thuringiensis (Bt) cotton, remains susceptible to Bt cotton in China at present. Behavioural avoidance by ovipositing females might lead to reduced exposure to Bt cotton and minimize selection for physiological resistance. We examined the behavioural responses of H. armigera to Bt and non‐Bt cottons to determine whether behavioural avoidance to Bt cotton may be present. In oviposition choice tests, the number of eggs on non‐Bt cotton plants was significantly higher than on Bt cotton plants. Similarly, in no‐choice tests, Bt cotton plants attracted significantly fewer eggs compared with non‐Bt cotton plants. H. armigera neonates showed higher dispersal and lower establishment on Bt cotton than on non‐Bt cotton. First instars were found to feed consistently on non‐Bt cotton leaves, creating large feeding holes, but only produced tiny feeding holes on Bt cotton leaves. The H. armigera population used in this study showed avoidance of oviposition and feeding on Bt cotton. Our results provide important insights into one possible mechanism underlying the durability of Bt cotton resistance and may be useful for improving strategies to sustain the effectiveness of Bt crops.     

Lethal and sublethal effects of thiacloprid on survival,growth and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae)

The cotton bollworm Helicoverpa armigera (Hübner) is the most destructive pest of cotton, tomato and chickpea in Iran. In this study, the lethal and sublethal effects of thiacloprid were evaluated against cotton bollworm under laboratory condition at 26?±?1?°C, 70?±?5% RH and a photoperiod of 16:8 (L:D). Bioassay experiments were conducted on first larval instars by mixing the insecticide dilutions with artificial diet. The LC₅₀ value of thiacloprid was 329?mg a.i./l. Sublethal effects of LC₃₀ concentration of thiacloprid was studied on biological parameters. In the study of sublethal effects, thiacloprid at LC₃₀ concentration significantly increased larval and pupal developmental times and reduced adults longevity compared with control but showed no significant effects on fecundity of cotton bollworm. Sublethal effects of thiacloprid also significantly reduced pupal weight compared with control. In general, sublethal effects studies showed that thiacloprid had adverse effects on biological parameters of the pest. Thus, our data suggest that thiacloprid had moderate potential against cotton bollworm.