Climatic limits of pink bollworm in Arizona and California: effects of climate warming

The distribution and abundance of pink bollworm (Pectinophora gossypiella Saunders (PBW)) in cotton in Arizona and California was examined using a validated weather-driven, physiologically based demographic model of cotton and PBW integrated into a geographic information system (GIS). Survival of diapause larvae during winter as affected by low temperatures is a key factor determining the range of PBW. Winter survival was estimated using data from Gutierrez et al. (Can. Entomol. 109 (1977) 1457) and Venette et al. (Environ. Entomol. 29 (5) (2000) 1018). The model was run continuously over the period 1 January 1995 to 31 December 2003 using observed weather data from 121 locations. Three output variables were mapped as measures of PBW persistence: over-winter survival of diapause PBW larvae, cumulative daily PBW larval densities over the season, and the number of diapause larvae produced during the season. The distribution of pink bollworm is predicted to be restricted to the relatively frost-free cotton growing areas of Arizona and Southern California where it currently reaches pest status. The model predicts that extension of PBW's range into the Central Valley of California is unlikely. The analysis questions the efficacy of an ongoing area-wide effort to prevent the establishment of PBW in the Central Valley of California. Four global warming scenarios were examined to estimate the effects on the potential geographic range of PBW. Average observed daily temperatures were increased 1.0, 1.5, 2.0 or 2.5 °C, respectively, in the four scenarios. Scenarios with average increases of 1.5–2.5 °C predicted that the range of PBW would expand into the Central Valley of California and the severity of the pest would greatly increase in areas of current infestation.     

A new test for measuring diapause in the pink bollworm Pectinophora gossypiella Sunders.

An ELISA test was developed to assay for the presence of a protein, pectinophorin, that is expressed only in diapausing last instar larvae of the pink bollworm, Pectinophora gossypiella Saunders. Use of the test provides a good estimation of the percent of diapause larvae in populations of pink bollworm in cotton fields in California and Arizona. All plow down dates are chosen before the majority of larvae enter diapause so as to eliminate as many overwintering survivors as possible. These dates may now be determined more precisely for any given field by use of the new ELISA procedure.     

Predicting spring moth emergence in the pink bollworm (Lepidoptera: Gelechiidae): implications for managing resistance to transgenic cotton.

Cultural control methods have been central in the southwestern United States for reducing pink bollworm, Pectinophora gossypiella (Saunders), damage to cotton. Nevertheless, it is not clear at present how such methods could be integrated within the novel pest management framework allowed by introduction of cotton producing a toxin from Bacillus thuringiensis (Bt) for pink bollworm control. Using statewide pheromone trapping and climatic data in conjunction with deterministic simulation models, we investigated whether manipulation of cotton planting date and use of other cultural control methods could represent valuable tactics for control of the pink bollworm in Arizona. Accumulation of heat units from one January accurately predicted the rate of pink bollworm emergence from diapause in 15 cotton-producing regions. Significant variation in rate of emergence from diapause was present among regions, with earlier emergence at higher altitudes. Most adults emerge from diapause too early to reproduce successfully on cotton, a phenomenon known as suicidal emergence. A method for prediction of the fraction of suicidal emergence resulting from adoption of a given cotton planting date is presented. Results from simulation models suggest that manipulation of planting date and implementation of other control cultural methods reduce the rate of application of insecticides and delay the evolution of resistance to Bt cotton in the pink bollworm.     

Earliness index deters <Emphasis Type="Italic">Pectinophora gossypiella</Emphasis> incidence on advanced cultivars of <Emphasis Type="Italic">Bt</Emphasis> cotton

Pink bollworm (Pectinophora gossypiella) is recognized as an important pest of cotton and can damage flowers and bolls of both Bt and non-Bt cultivars. Cry-1Ac in Bt cultivars is considered very effective in controlling lepidopterous larvae; therefore, the present study was carried out to investigate the impact of Cry1-Ac and the earliness index on the natural incidence of P. gossypiella at the Cotton Research Institute, Faisalabad. During 2015–2016, ten cultivars were used to determine the incidence of pink bollworm infestation. The experiment was repeated for 2 years. During the next year, Cry1-Ac and earliness traits of selected cultivars were also observed to determine their impact on pink bollworm. Correlation coefficient results regarding days to first flower (r value = 0.66) as well as the earliness index (r value = ? 0.62) exhibited a strong association with pink bollworm, but Cry1-Ac had a weak association (r value = ? 0.058) with pink bollworm. The coefficient of determination (R ²) explained that variability of pink bollworm due to Cry1-Ac, the earliness index, and days to first flower was 18.0, 38.5, and 43.5%, respectively. Principal component analysis results showed that the first two PCs expressed 87% of the total variability. Clusters made on the basis of the studied parameters revealed that clusters 2 and 3 comprised the cotton cultivars possessing earliness traits compared with cluster 1. Therefore, it can be concluded that the earliness index in cotton is an important component for the sustainable management of pink bollworm infestation, the need for which is endless to evade the pink bollworm problem in the era of climate change.     

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.     

Sustained susceptibility of pink bollworm to Bt cotton in the United States

Evolution of resistance by pests can reduce the benefits of transgenic crops that produce toxins from Bacillus thuringiensis (Bt) for insect control. One of the world's most important cotton pests, pink bollworm (Pectinophora gossypiella), has been targeted for control by transgenic cotton producing Bt toxin Cry1Ac in several countries for more than a decade. In China, the frequency of resistance to Cry1Ac has increased, but control failures have not been reported. In western India, pink bollworm resistance to Cry1Ac has caused widespread control failures of Bt cotton. By contrast, in the state of Arizona in the southwestern United States, monitoring data from bioassays and DNA screening demonstrate sustained susceptibility to Cry1Ac for 16 y. From 1996-2005, the main factors that delayed resistance in Arizona appear to be abundant refuges of non-Bt cotton, recessive inheritance of resistance, fitness costs associated with resistance and incomplete resistance. From 2006-2011, refuge abundance was greatly reduced in Arizona, while mass releases of sterile pink bollworm moths were made to delay resistance as part of a multi-tactic eradication program. Sustained susceptibility of pink bollworm to Bt cotton in Arizona has provided a cornerstone for the pink bollworm eradication program and for integrated pest management in cotton. Reduced insecticide use against pink bollworm and other cotton pests has yielded economic benefits for growers, as well as broad environmental and health benefits. We encourage increased efforts to combine Bt crops with other tactics in integrated pest management programs.     

Pink bollworm moth （Lepidoptera： Gelechiidae） catches in the Imperial Valley, California from 1989 to 2003

We examined the patterns of male pink bollworm （PBW）, Pectinophora gossypiella （Saunders）, moth catches in gossyplure-baited traps over a 15-year period from 1989 to 2003 in the Imperial Valley, California, USA. Monitoring was conducted during periods when different pink bollworm areawide control strategies were being used. Numbers of male pink bollworm moths caught in gossyplure-baited traps progressively decreased each year from 1990 to 1994 during short-season cotton production. High numbers of male moths caught in traps from 1995 to 1997 may have been related to moth migrations from the large cotton acreages grown in the Mexicali Valley bordering the Imperial Valley. Transgenic Bollgard （Bt） cotton was planted in 3% of the cotton area in 1996 and thereafter in 80%- 94% of the cotton area from 1997 to 2003. Pink bollworm moth trap catches were significantly lower from 1998 to 2003 than catches in 1995 to 1997, except for 1999. The trapping results suggested that Bt cotton had significant input on reduction of pink bollworm populations, confirming results of other investigators and providing additional documentation on the benefits of the Bt cotton culture.     

The halo effect: suppression of pink bollworm on non-bt cotton by bt cotton in china

In some previously reported cases, transgenic crops producing insecticidal proteins from Bacillus thuringiensis (Bt) have suppressed insect pests not only in fields planted with such crops, but also regionally on host plants that do not produce Bt toxins. Here we used 16 years of field data to determine if Bt cotton caused this "halo effect" against pink bollworm (Pectinophora gossypiella) in six provinces of 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 found that Bt cotton significantly decreased the population density of pink bollworm on non-Bt cotton, with net decreases of 91% for eggs and 95% for larvae on non-Bt cotton after 11 years of Bt cotton use. Insecticide sprays targeting pink bollworm and cotton bollworm (Helicoverpa armigera) decreased by 69%. Previously reported evidence of the early stages of evolution of pink bollworm resistance to Bt cotton in China has raised concerns that if unchecked, such resistance could eventually diminish or eliminate the benefits of Bt cotton. The results reported here suggest that it might be possible to find a percentage of Bt cotton lower than the current level that causes sufficient regional pest suppression and reduces the risk of resistance.     

Engineered Repressible Lethality for Controlling the Pink Bollworm, a Lepidopteran Pest of Cotton

The sterile insect technique (SIT) is an environmentally friendly method of pest control in which insects are mass-produced, irradiated and released to mate with wild counterparts. SIT has been used to control major pest insects including the pink bollworm (Pectinophora gossypiella Saunders), a global pest of cotton. Transgenic technology has the potential to overcome disadvantages associated with the SIT, such as the damaging effects of radiation on released insects. A method called RIDL (Release of Insects carrying a Dominant Lethal) is designed to circumvent the need to irradiate insects before release. Premature death of insects’ progeny can be engineered to provide an equivalent to sterilisation. Moreover, this trait can be suppressed by the provision of a dietary antidote. In the pink bollworm, we generated transformed strains using different DNA constructs, which showed moderate-to-100% engineered mortality. In permissive conditions, this effect was largely suppressed. Survival data on cotton in field cages indicated that field conditions increase the lethal effect. One strain, called OX3402C, showed highly penetrant and highly repressible lethality, and was tested on host plants where its larvae caused minimal damage before death. These results highlight a potentially valuable insecticide-free tool against pink bollworm, and indicate its potential for development in other lepidopteran pests.     

Adult emergence pattern of parasitoidApanteles angaleti and its known hosts during off-season in Punjab

Observations on emergence pattern of parasitoidApanteles angaleti Muesebeck and its 2 hosts, cotton pink bollwormPectinophora gossypiella (Saunders) and saprophyteSathrobrota simplex Wlsm. were made during 1980–81 to 1983–84. The adult emergence of parasitoidA. angaleti and non-pestS. simplex was similar and completed by end April. ParasitoidA. angaleti overwintered mostly in the larvae of non-pestS. simplex and not in pink bollworm larvaeP. gossypiella. The early breeding activity ofS. simplex in the rotten bolls in the cotton stacks helped in the carryover and initial build-up ofA. angaleti to the main crop season. The initiation and peak moth emergence in pink bollworm varied with different sources of its carryover but all adults emerged until end August.     

Control of Resistant Pink Bollworm (Pectinophora gossypiella) by Transgenic Cotton That Produces Bacillus thuringiensis Toxin Cry2Ab

Crops genetically engineered to produce Bacillus thuringiensis toxins for insect control can reduce use of conventional insecticides, but insect resistance could limit the success of this technology. The first generation of transgenic cotton with B. thuringiensis produces a single toxin, Cry1Ac, that is highly effective against susceptible larvae of pink bollworm (Pectinophora gossypiella), a major cotton pest. To counter potential problems with resistance, second-generation transgenic cotton that produces B. thuringiensis toxin Cry2Ab alone or in combination with Cry1Ac has been developed. In greenhouse bioassays, a pink bollworm strain selected in the laboratory for resistance to Cry1Ac survived equally well on transgenic cotton with Cry1Ac and on cotton without Cry1Ac. In contrast, Cry1Ac-resistant pink bollworm had little or no survival on second-generation transgenic cotton with Cry2Ab alone or with Cry1Ac plus Cry2Ab. Artificial diet bioassays showed that resistance to Cry1Ac did not confer strong cross-resistance to Cry2Aa. Strains with >90% larval survival on diet with 10 μg of Cry1Ac per ml showed 0% survival on diet with 3.2 or 10 μg of Cry2Aa per ml. However, the average survival of larvae fed a diet with 1 μg of Cry2Aa per ml was higher for Cry1Ac-resistant strains (2 to 10%) than for susceptible strains (0%). If plants with Cry1Ac plus Cry2Ab are deployed while genes that confer resistance to each of these toxins are rare, and if the inheritance of resistance to both toxins is recessive, the efficacy of transgenic cotton might be greatly extended.     

Limits to the potential distribution of light brown apple moth in Arizona–California based on climate suitability and host plant availability

The highly polyphagous light brown apple moth (LBAM) (Epiphyas postvittana (Walk.): Tortricidae) is indigenous to Australia and was first found in California in 2006. It is currently found in 15 coastal counties in California, but nowhere has it reached outbreak status. The USDA projects the geographic range of LBAM will include much of Arizona and California and the southern half of the US, which together with economic estimates of potential crop losses have been used as the rationale for an eradication program in California. We report a temperature-driven demographic model to predict the likely distribution and relative abundance of LBAM using the detailed biology reported by Danthanarayana and colleagues, and climate data from 151 locations in California and Arizona for the period 1995–2006. The predictions of our model suggest that the near coastal regions of California are most favorable for LBAM, the northern Central Valley of California being less favorable, and the desert regions of Arizona and California being unfavorable. The model also predicts that LBAM populations can develop at two of the hottest locations in SE Australia where it is has long been known to occur. This reassessment of the potential distribution of LBAM in California and Arizona suggests that its likely ecological and economic impacts would be less than previously assessed by USDA and that its current pest status warrants re-evaluation.     

DNA screening reveals pink bollworm resistance to Bt cotton remains rare after a decade of exposure

Transgenic crops producing toxins from the bacterium Bacillus thuringiensis (Bt) kill insect pests and can reduce reliance on insecticide sprays. Although Bt cotton (Gossypium hirsutum L.) and Bt corn (Zea mays L.) covered 26 million ha worldwide in 2005, their success could be cut short by evolution of pest resistance. Monitoring the early phases of pest resistance to Bt crops is crucial, but it has been extremely difficult because bioassays usually cannot detect heterozygotes harboring one allele for resistance. We report here monitoring of resistance to Bt cotton with DNA-based screening, which detects single resistance alleles in heterozygotes. We used polymerase chain reaction primers that specifically amplify three mutant alleles of a cadherin gene linked with resistance to Bt cotton in pink bollworm, Pectinophora gossypiella (Saunders), a major pest. We screened DNA of 5,571 insects derived from 59 cotton fields in Arizona, California, and Texas during 2001-2005. No resistance alleles were detected despite a decade of exposure to Bt cotton. In conjunction with data from bioassays and field efficacy tests, the results reported here contradict predictions of rapid pest resistance to Bt crops.     

An appetite for pests: Synanthropic insectivorous bats exploit cotton pest irruptions and consume various deleterious arthropods

Conservation biological control (CBC) seeks to minimize the deleterious effects of agricultural pests by enhancing the efficiency of natural enemies. Despite the documented potential of insectivorous bats to consume pests, many synanthropic bat species are still underappreciated as beneficial species. We investigated the diet of Kuhl's pipistrelle (Pipistrellus kuhlii), a common synanthropic insectivorous bat that forages in urban and agricultural areas, to determine whether it may function as a natural enemy in CBC. Faecal samples of P. kuhlii were collected throughout the cotton‐growing season from five roost sites near cotton fields located in a Mediterranean agroecosystem, Israel, and analyzed using DNA metabarcoding. Additionally, data on estimated abundance of major cotton pests were collected. We found that the diet of P. kuhlii significantly varied according to sites and dates and comprised 27 species of agricultural pests that were found in 77.2% of the samples, including pests of key economic concern. The dominant prey was the widespread cotton pest, the pink bollworm, Pectinophora gossypiella, found in 31% of the samples and in all the roosts. Pink bollworm abundance was positively correlated with its occurrence in the bat diet. Furthermore, the bats’ dietary breadth narrowed, while temporal dietary overlap increased, in relation to increasing frequencies of pink bollworms in the diet. This suggests that P. kuhlii exploits pink bollworm irruptions by opportunistic feeding. We suggest that synanthropic bats provide important pest suppression services, may function as CBC agents of cotton pests and potentially contribute to suppress additional deleterious arthropods found in their diet in high frequencies.     

Association between resistance to Bt cotton and cadherin genotype in pink bollworm

Two strains of pink bollworm, Pectinophora gossypiella (Saunders), each derived in 1997 from a different field population, were selected for resistance to Bacillus thuringiensis (Bt) toxin Cry1Ac in the laboratory. One strain (MOV97-R) originated from Mohave Valley in western Arizona; the other strain (SAF97-R) was from Safford in eastern Arizona. Relative to a susceptible laboratory strain, Cry1Ac resistance ratios were 1700 for MOV97-R and 520 for SAF97-R. For the two resistant strains, larval survival did not differ between non-Bt cotton and transgenic cotton producing CrylAc. In contrast, larval survival on Bt cotton was 0% for the two unselected parent strains from which the resistant strains were derived. Previously identified resistance (r) alleles of a cadherin gene (BtR) occurred in both resistant strains: r1 and r3 in MOV97-R, and r1 and r2 in SAF97-R. The frequency of individuals carrying two r alleles (rr) was 1.0 in the two resistant strains and 0.02 in each of the two unselected parent strains. Furthermore, in two hybrid strains with a mixture of susceptible (s) and r alleles at the BtR locus, all survivors on Bt cotton had two r alleles. The results show that resistance to Cry1Ac-producing Bt cotton is associated with recessive r alleles at the BtR locus in the strains of pink bollworm tested here. In conjunction with previous results from two other Bt-resistant strains of pink bollworm (APHIS-98R and AZP-R), results reported here identify the cadherin locus as the leading candidate for molecular monitoring of pink bollworm resistance to Bt cotton.     

Effects of transgenic Bt cotton on overwintering characteristics and survival of Helicoverpa armigera

The effects of transgenic Bt cotton on the overwintering generation of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), are unknown. We hypothesized that a Bt cotton diet may adversely affect fitness of this generation and examined fresh weight, lipids, glycogens, low-molecular-weight sugars and SCPs (supercooling points) of pupae, as well as survival of larvae, diapausing pupae and adult emergence in comparison with controls. Field and laboratory experiments showed that larvae fed on Bt cotton had a decreased pupation rate, and fewer entered diapause and emerged as adults compared with larvae fed non-Bt cotton. Furthermore, larvae fed Bt cotton had reduced pupal weight, glycogen content and trehalose levels both in diapausing and in non-diapausing pupae, and only diapausing pupae had an increased SCP compared to controls. The SCPs of diapausing pupae reared on Bt cotton were significantly higher than those reared on non-Bt cotton. The trehalose levels of diapausing pupae reared on Bt cotton were significantly lower than those of larvae reared on non-Bt cotton. Thus, these results suggest that a Bt cotton diet weakens the preparedness of cotton bollworm for overwintering and reduces survival of the overwintering generation, which will in turn reduce the density of the first generation in the following year. Effects of transgenic Bt cotton on the overwintering generation of cotton bollworm appear to have significantly contributed to the suppression of cotton bollworm observed throughout northern China in the past decade.     

Early detection of field-evolved resistance to Bt cotton in China: cotton bollworm and pink bollworm

Transgenic crops producing Bacillus thuringiensis (Bt) toxins kill some major insect pests, but pests can evolve resistance and thereby reduce the effectiveness of such Bt crops. The main approach for slowing 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 cotton producing Bt toxin Cry1Ac, several 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. This strategy is designed for cotton bollworm (Helicoverpa armigera), which attacks many crops and is the primary target of Bt cotton in China, but it does not apply to pink bollworm (Pectinophora gossypiella), which feeds almost entirely on cotton in China. Here we review evidence of field-evolved resistance to Cry1Ac by cotton bollworm in northern China and by pink bollworm in the Yangtze River Valley of China. For both pests, results of laboratory diet bioassays reveal significantly decreased susceptibility of field populations to Cry1Ac, yet field control failures of Bt cotton have not been reported. The early detection of resistance summarized here may spur countermeasures such as planting Bt cotton that produces two or more distinct toxins, increased planting of non-Bt cotton, and integration of other management tactics together with 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.