non-Bt Cotton Research Articles

Effects of temperature on the feeding behavior of Alabama argillacea (Hübner) (Lepidoptera: Noctuidae) on Bt and non-Bt cotton plants.

The host acceptance behavior and environmental factors as temperature affect the feeding behavior of Lepidoptera pests. Thus, they must be considered in studies about the risk potential of resistance evolution. The current study sets the differences in the feeding behavior of neonate Alabama argillacea (Hübner) (Lepidoptera: Noctuidae) larvae exposed to Bt and non-Bt cotton plants, under different temperatures and time gap after hatching. Two cotton cultivars were used: the Bt (DP 404 BG - bollgard) and the non-transformed isoline, DP 4049. We found that the feeding behavior of neonate A. argillacea is significantly different between Bt and non-Bt cotton. Based on the number of larvae with vegetal tissue in their gut found on the plant and in the organza as well as on the amount of vegetal tissue ingested by the larvae. A. argillacea shows feeding preference for non-Bt cotton plants, in comparison to that on the Bt. However, factors such as temperature and exposure time may affect detection capacity and plant abandonment by the larvae and it results in lower ingestion of vegetal tissue. Such results are relevant to handle the resistance of Bt cotton cultivars to A. argillacea and they also enable determining how the cotton seeds mix will be a feasible handling option to hold back resistance evolution in A. argillacea populations on Bt cotton, when it is compared to other refuge strategies. The results can also be useful to determine which refuge distribution of plants is more effective for handling Bt cotton resistance to A. argillacea.

Larval Dispersal of Spodoptera frugiperda Strains on Bt Cotton: A Model for Understanding Resistance Evolution and Consequences for its Management

High dispersal of Lepidoptera larvae between non-Bt and Bt cotton plants can favour the evolution of insect resistance; however, information on host acceptance of neonates in tropical transgenic crops is scarce. Therefore, the purposes of this study were as follows: (i) to investigate the feeding behaviour of susceptible and Cry1F-resistant strains of Spodoptera frugiperda (J.E. Smith) on Bt and non-Bt cotton (Gossypium hirsutum L.) varieties and (ii) to understand the possible effects of cotton field contamination on the dispersal and infestation capacity of S. frugiperda larvae by using an individual-based model. The main results of this paper are as follows: (1) the highest post-feeding larval dispersal of the Cry1F-resistant strain occurred at an exposure time of 18–24 h; (2) via video tracking assays, we found that the least distance moved was by larvae resistant to Cry1F on non-Bt cotton; and (3) the model indicated differences in mobility capacity between Bt and non-Bt cotton. We conclude that resistant neonates exhibit sedentary behaviour. Our report represents the first findings concerning the fitness cost of larval behaviour traits of S. frugiperda associated with Cry1F resistance in Brazilian populations.

Transgenic cotton co-expressing chimeric Vip3AcAa and Cry1Ac confers effective protection against Cry1Ac-resistant cotton bollworm.

Wide planting of transgenic Bt cotton in China since 1997 to control cotton bollworm (Helicoverpa armigera) has increased yields and decreased insecticide use, but the evolution of resistance to Bt cotton by H. armigera remains a challenge. Toward developing a new generation of insect-resistant transgenic crops, a chimeric protein of Vip3Aa1 and Vip3Ac1, named Vip3AcAa, having a broader insecticidal spectrum, was specifically created previously in our laboratory. In this study, we investigated cross resistance and interactions between Vip3AcAa and Cry1Ac with three H. armigera strains, one that is susceptible and two that are Cry1Ac-resistant, to determine if Vip3AcAa is a good candidate for development the pyramid cotton with Cry1Ac toxin. Our results showed that evolution of insect resistance to Cry1Ac toxin did not influence the sensitivity of Cry1Ac-resistant strains to Vip3AcAa. For the strains examined, observed mortality was equivalent to the expected mortality for all the combinations of Vip3AcAa and Cry1Ac tested, reflecting independent activity between these two toxins. When this chimeric vip3AcAa gene and the cry1Ac gene were introduced into cotton, mortality rates of Cry1Ac resistant H. armigera larvae strains that fed on this new cotton increased significantly compared with larvae fed on non-Bt cotton and cotton producing only Cry1Ac. These results suggest that the Vip3AcAa protein is an excellent option for a "pyramid" strategy for pest resistance management in China.

Effects of seasonal changes in cotton plants on the evolution of resistance to pyramided cotton producing the Bt toxins Cry1Ac and Cry1F in Helicoverpa zea.

In pests with inherently low susceptibility to Bacillus thuringiensis (Bt) toxins, seasonal declines in the concentration of Bt toxins in transgenic crops could accelerate evolution of resistance by increasing the dominance of resistance. Here, we evaluated Helicoverpa zea survival on young and old cotton plants that produced the Bt toxins Cry1Ac and Cry1F or did not produce Bt toxins. Using a strain selected for resistance to Cry1Ac in the laboratory, its parent strain that was not selected in the laboratory, and their F1 progeny, we showed that resistance to Cry1Ac + Cry1F cotton was partially dominant on young and old plants. On Cry1Ac + Cry1F cotton, redundant killing was incomplete on young plants but nearly complete on old plants. No significant fitness costs on non-Bt cotton occurred on young plants, but large recessive costs affected survival on old plants. Simulation models incorporating the empirical data showed that the seasonal changes in fitness could delay resistance to Cry1Ac + Cry1F cotton by inducing low equilibrium frequencies of resistance alleles when refuges are sufficiently large. Our results suggest that including effects of seasonal changes in fitness of pests on Bt crops and refuge plants can enhance resistance risk assessment and resistance management. © 2017 Society of Chemical Industry.

Population Dynamics of Thrips tabaci (Lindeman) in Relation to Abiotic Climate Factors on Bt and Non-Bt Cotton Cultivars

Population Dynamics of Thrips tabaci (Lindeman) in Relation to Abiotic Climate Factors on Bt and Non-Bt Cotton Cultivars

Phenology, plant height and dry matter production plant-1of Bt and non-Bt cotton (Gossypium hirsutum L.) cultivars at different stages as influenced by different plant densities and nitrogen levels

Phenology, plant height and dry matter production plant-1of Bt and non-Bt cotton (Gossypium hirsutum L.) cultivars at different stages as influenced by different plant densities and nitrogen levels

Efficacy ofBacillus thuringiensisSprays and Cotton Cultivars Expressing Cry Proteins in the Control ofEarias biplaga(Walker) (Lepidoptera: Noctuidae)

Earias biplaga (Walker) (Lepidoptera: Noctuidae) forms part of the bollworm pest complex of cotton in South Africa. Genetically modified Bt cotton that expresses Cry insecticidal proteins successfully controls the bollworm complex in South Africa. Although many insecticides are registered for use against Lepidoptera on this crop, Bt sprays are not registered for control of E. biplaga. The aim of this study was to determine the efficacy of Bacillus thuringiensis spray applications for the control of E. biplaga on non-Bt cotton and to compare the efficacy of sprays to that provided by Bt cotton. Bioassays were conducted in which cotton bolls of a non-Bt cotton cultivar (Delta Opal) were sprayed with different dosage rates of Dipel DF®, which contains the following insecticidal proteins: Cry1Aa, Cry1Ab, Cry1Ac, Cry2Aa and Cry2Ab. Bollgard® and Bollgard II® cotton which expresses Cry1Ac and both Cry 1Ac and Cry2Ab were used in the study. Neonate larvae were inoculated onto cotton bolls and survival observed 4, 7 and 10 days later. The Bt spray dosage rate recommended for control of Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) on groundnut and sunflower in South Africa was used in this study and provided between 77 and 88%control of E. biplaga after 10 days. Bt cotton provided 100%control after 10 days. This study provides baseline data on the susceptibility of E. biplaga against Bt cotton which can also be used for future monitoring of resistance evolution.

Transgenic cotton coexpressing Vip3A and Cry1Ac has a broad insecticidal spectrum against lepidopteran pests.

Although farmers in China have grown transgenic Bt-Cry1Ac cotton to resist the major pest Helicoverpa armigera since 1997 with great success, many secondary lepidopteran pests that are tolerant to Cry1Ac are now reported to cause considerable economic damage. Vip3AcAa, a chimeric protein with the N-terminal part of Vip3Ac and the C-terminal part of Vip3Aa, has a broad insecticidal spectrum against lepidopteran pests and has no cross resistance to Cry1Ac. In the present study, we tested insecticidal activities of Vip3AcAa against Spodoptera litura, Spodoptera exigua, and Agrotis ipsilon, which are relatively tolerant to Cry1Ac proteins. The bioassay results showed that insecticidal activities of Vip3AcAa against these three pests are superior to Cry1Ac, and after an activation pretreatment, Vip3AcAa retained insecticidal activity against S. litura, S. exigua and A. ipsilon that was similar to the unprocessed protein. The putative receptor for this chimeric protein in the brush border membrane vesicle (BBMV) in the three pests was also identified using biotinylated Vip3AcAa toxin. To broaden Bt cotton activity against a wider spectrum of pests, we introduced the vip3AcAa and cry1Ac genes into cotton. Larval mortality rates for S. litura, A. ipsilon and S. exigua that had fed on this new cotton increased significantly compared with larvae fed on non-Bt cotton and Bt-Cry1Ac cotton in a laboratory experiment. These results suggested that the Vip3AcAa protein is an excellent option for a "pyramid" strategy for integrated pest management in China.

Herbicide and insect resistant Bt cotton pollen assessment finds no detrimental effects on adult honey bees

One important concern regarding the use of transgenic cotton expressing insecticidal toxins from the bacterium Bacillus thuringiensis (Bt) is its potential detrimental effect on non-target organisms. The honey bee (Apis mellifera) is the most important pollinator species worldwide and it is directly exposed to transgenic crops by the consumption of genetically modified (GM) pollen. However, the potential effects of Bt cotton on A. mellifera remain unclear. In the present study, we assessed the effects of two Bt cotton varieties; ZMSJ expressing the Cry1Ac and Cry2Ab insecticidal proteins, and ZMKCKC producing Cry1Ac and EPSPS, on A. mellifera. Feeding on pollen from two Bt cotton varieties led to detection of low levels of Cry toxins (<10 ng/g fresh weight) in the midgut of A. mellifera adults, yet expression of detoxification genes did not change significantly compared to feeding on non-Bt cotton. Binding assays showed no Cry1Ac or Cry2Ab binding to midgut brush border membrane proteins from A. mellifera adults. Taken together, these results support minimal risk for potential negative effects on A. mellifera by exposure to Bt cotton.

Effects of soil salinity on rhizosphere soil microbes in transgenic Bt cotton fields

With increased cultivation of transgenic Bacillus thuringiensis (Bt) cotton in the saline alkaline soil of China, assessments of transgenic crop biosafety have focused on the effects of soil salinity on rhizosphere microbes and Bt protein residues. In 2013 and 2014, investigations were conducted on the rhizosphere microbial biomass, soil enzyme activities and Bt protein contents of the soil under transgenic Bt cotton (variety GK19) and its parental non-transgenic cotton (Simian 3) cultivated at various salinity levels (1.15, 6.00 and 11.46 dS m−1). Under soil salinity stress, trace amounts of Bt proteins were observed in the Bt cotton GK19 rhizosphere soil, although the protein content increased with cotton growth and increased soil salinity levels. The populations of slight halophilic bacteria, phosphate solubilizing bacteria, ammonifying bacteria, nitrifying bacteria and denitrifying bacteria decreased with increased soil salinity in the Bt and non-Bt cotton rhizosphere soil, and the microbial biomass carbon, microbial respiration and soil catalase, urease and alkaline phosphatase activity also decreased. Correlation analyses showed that the increased Bt protein content in the Bt cotton rhizosphere soil may have been caused by the slower decomposition of soil microorganisms, which suggests that salinity was the main factor influencing the relevant activities of the soil microorganisms and indicates that Bt proteins had no clear adverse effects on the soil microorganisms. The results of this study may provide a theoretical basis for risk assessments of genetically modified cotton in saline alkaline soil.

Fifteen Years of Bt Cotton in China: Results from Household Surveys

Summary The short-run benefit of insect-resistant Bacillus thuringiensis (Bt) crops has been well documented, but its sustainability in the long run has not been well studied. On the other hand, pest resistance build-up and secondary pest outbreaks have caused concern regarding the sustainability of this benefit. Using seven unique waves of panel data collected during 1999–2012, we show that pesticide use against bollworms has not increased significantly over time, indicating that the buildup of pest resistance is still not a concern because of the existence of a large number of nature refuge areas. In addition, we show that Bt cotton adoption has not led to outbreaks of secondary pests. Finally, we show that the benefit has been shared by both Bt and non-Bt cotton adopters as the widespread adoption of Bt cotton has successfully suppressed the density of the pest population regionally. We conclude that the benefit of Bt cotton adoption continues 15 years after its introduction, albeit with evidence of a decline in the comparative advantage over non-Bt cotton in late adoption period. We believe that this contribution is theoretically and practically relevant because of the long length of our dataset and because we categorize pesticide use into that for controlling bollworms and that for controlling secondary pests.

A comparative assessment of crop phenology, agrometeorological indices and yield of Bt and non-Bt cotton in Akola, Maharashtra

A comparative assessment of crop phenology, agrometeorological indices and yield of Bt and non-Bt cotton in Akola, Maharashtra

Comparison of rhizosphere properties as affected by different Bt- and non-Bt-cotton (Gossypium hirsutum L.) genotypes and fertilization.

Incorporation of genetically modified crops in the cropping system raises the need for studying the effect of these crops on the soil ecosystem. The current study aimed to compare the effect of Bacillus thuringiensis (Bt)- and non-Bt-cotton (Gossypium hirsutum L.) genotypes on rhizosphere properties under fertilized and unfertilized soil conditions. One non-Bt-cotton (IUB 75) and four Bt-cotton varieties (IUB-222, MM-58, IUB-13, FH-142) were sown in a Randomized Complete Block Design (RCBD) in a factorial fashion with three replications under unfertilized (T1) and fertilized (T2 at NPK 310-170-110kgha-1) soil conditions. The culturable soil bacterial population was recorded at flowering, boll opening, and harvesting stages, while other rhizosphere biological and chemical properties were recorded at harvesting. Results revealed that Bt-cotton genotypes IUB-222 and FH-142 showed significantly higher rhizosphere total nitrogen, NH4+-N, available phosphorus, and available potassium. Total organic carbon and microbial biomass carbon was also maximum in the rhizosphere of IUB-222 under fertilized conditions. Similarly, bacterial population (CFU g-1) at flowering stage and at harvesting was significantly higher in the rhizosphere of IUB-222 as compared to non-Bt- (IUB-75) and other Bt-cotton genotypes under same growth conditions. It showed that Bt genotypes can help in maintaining soil macronutrients (total nitrogen, available phosphorus, and available potassium) under proper nutrient management. Moreover, Bt-cotton genotypes seem to strengthen certain biological properties of the soil, thus increasing the growth and yield capability, maintaining available nutrients in the soil as compared to non-Bt cotton, while no harmful effects of Bt cotton on soil properties was detected.

Hybridizing transgenic Bt cotton with non-Bt cotton counters resistance in pink bollworm

Extensive cultivation of crops genetically engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) has suppressed some major pests, reduced insecticide sprays, enhanced pest control by natural enemies, and increased grower profits. However, these benefits are being eroded by evolution of resistance in pests. We report a strategy for combating resistance by crossing transgenic Bt plants with conventional non-Bt plants and then crossing the resulting first-generation (F1) hybrid progeny and sowing the second-generation (F2) seeds. This strategy yields a random mixture within fields of three-quarters of plants that produce Bt toxin and one-quarter that does not. We hypothesized that the non-Bt plants in this mixture promote survival of susceptible insects, thereby delaying evolution of resistance. To test this hypothesis, we compared predictions from computer modeling with data monitoring pink bollworm (Pectinophora gossypiella) resistance to Bt toxin Cry1Ac produced by transgenic cotton in an 11-y study at 17 field sites in six provinces of China. The frequency of resistant individuals in the field increased before this strategy was widely deployed and then declined after its widespread adoption boosted the percentage of non-Bt cotton plants in the region. The correspondence between the predicted and observed outcomes implies that this strategy countered evolution of resistance. Despite the increased percentage of non-Bt cotton, suppression of pink bollworm was sustained. Unlike other resistance management tactics that require regulatory intervention, growers adopted this strategy voluntarily, apparently because of advantages that may include better performance as well as lower costs for seeds and insecticides.

What are farmers really planting? Measuring the presence and effectiveness of Bt cotton in Pakistan.

Genetically modified, insect-resistant Bacillus thuringiensis (Bt) cotton is cultivated extensively in Pakistan. Past studies, however, have raised concerns about the prevalence of Bt cotton varieties possessing weak or nonperforming insect-resistance traits conferred by the cry gene. We examine this issue using data drawn from a representative sample of cotton-growing households that were surveyed in six agroclimatic zones spanning 28 districts in Pakistan in 2013, as well as measurements of Cry protein levels in cotton tissue samples collected from the sampled households’ main fields. The resultant dataset combines information from 593 sampled households with corresponding plant tissue diagnostics from 70 days after sowing, as well as information from 589 sampled households with corresponding diagnostics from 120 days after sowing. Our analysis indicates that 11 percent of farmers believed they were cultivating Bt cotton when, in fact, the Cry toxin was not present in the tested tissue at 70 days after sowing (i.e., a Type I error). The analysis further indicates that 5 percent of farmers believed they were cultivating non-Bt cotton when, in fact, the Cry toxin was present in the tested tissue (i.e., a Type II error). In addition, 17 percent of all sampled farmers were uncertain whether or not they were cultivating Bt cotton. Overall, 33 percent of farmers either did not know or were mistaken in their beliefs about the presence of the cry gene in the cotton they cultivated. Results also indicate that toxic protein levels in the plant tissue samples occurred below threshold levels for lethality in a significant percentage of cases, although these measurements may also be affected by factors related to tissue sample collection, handling, storage, and testing procedures. Nonetheless, results strongly suggest wide variability both in farmers’ beliefs and in gene expression. Such variability has implications for policy and regulation in Pakistan’s transgenic cotton seed market.

Fitness of Bt-resistant cabbage loopers on Bt cotton plants.

SummaryDevelopment of resistance to the insecticidal toxins from Bacillus thuringiensis (Bt) in insects is the major threat to the continued success of transgenic Bt crops in agriculture. The fitness of Bt‐resistant insects on Bt and non‐Bt plants is a key parameter that determines the development of Bt resistance in insect populations. In this study, a comprehensive analysis of the fitness of Bt‐resistant Trichoplusia ni strains on Bt cotton leaves was conducted. The Bt‐resistant T. ni strains carried two genetically independent mechanisms of resistance to Bt toxins Cry1Ac and Cry2Ab. The effects of the two resistance mechanisms, individually and in combination, on the fitness of the T. ni strains on conventional non‐Bt cotton and on transgenic Bt cotton leaves expressing a single‐toxin Cry1Ac (Bollgard I) or two Bt toxins Cry1Ac and Cry2Ab (Bollgard II) were examined. The presence of Bt toxins in plants reduced the fitness of resistant insects, indicated by decreased net reproductive rate (R 0) and intrinsic rate of increase (r). The reduction in fitness in resistant T. ni on Bollgard II leaves was greater than that on Bollgard I leaves. A 12.4‐day asynchrony of adult emergence between the susceptible T. ni grown on non‐Bt cotton leaves and the dual‐toxin‐resistant T. ni on Bollgard II leaves was observed. Therefore, multitoxin Bt plants not only reduce the probability for T. ni to develop resistance but also strongly reduce the fitness of resistant insects feeding on the plants.

Effectiveness of Microbial and Chemical Insecticides for Supplemental Control of Bollworm on Bt and Non-Bt Cottons.

Laboratory and field experiments were conducted to determine the effectiveness of microbial and chemical insecticides for supplemental control of bollworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae), on non-Bt (DP1441RF) and Bt (DP1321B2RF) cottons. Neonate and 3rd instar larvae survival was evaluated on leaf tissue treated with microbial and chemical insecticides including a commercial formulation of Bacillus thuringiensis (Dipel), a Heliothis (Helicoverpa) nuclear polyhedrosis virus (NPV; Gemstar), λ-cyhalothrin (Karate Z), and chlorantraniliprole (Prevathon). Residual activity of insecticides was measured in a small plot field experiment. The performance of microbial insecticides, with the exception of a mid-rate of Dipel with neonate larvae, was comparable with that of chemical treatments on non-Bt cotton leaves with regard to 1st and 3rd instar bollworm mortality at 10 d and pupal eclosion at 20-d post treatment. Production-level field evaluations of supplemental bollworm control in non-Bt and Bt cottons with NPV, λ-cyhalothrin, and chlorantraniliprole were also conducted. During both years of the field study, all chemical and microbial treatments were successful in suppressing bollworm larval densities in non-Bt cotton below economic threshold levels. Overall, net returns above bollworm control, regardless of treatment, were negatively correlated with larval abundance and plant damage. In addition, there was no economic benefit for supplemental control of bollworms in Bt cotton at the larval densities observed during this study. These data provide benchmark comparisons for insect resistance management with microbial and chemical insecticides in Bt and non-Bt cottons and strategic optimization of the need to spray non-Bt and Bt cotton in IRM programs.

Large-Scale Evaluation of Association Between Pheromone Trap Captures and Cotton Boll Infestation for Pink Bollworm (Lepidoptera: Gelechiidae)

Although transgenic cotton producing insecticidal proteins from Bacillus thuringiensis (Bt) is a cornerstone for pink bollworm control in some countries, integrated pest management remains important for bolstering sustainability of Bt cotton and is critical for controlling pink bollworm where Bt cotton is not available or where this pest has evolved resistance to Bt cotton. Here, we used data on moth captures in gossyplure-baited pheromone traps and boll infestations for 163 Bt and 152 non-Bt cotton fields from Arizona to evaluate accuracy of chemical control decisions relying on moth trapping data and capacity of Bt cotton to suppress survival of offspring produced by moths. Assuming an economic injury level of 12% boll infestation, the accuracy of decisions based on moth captures corresponding to economic thresholds of 6%, 8%, and 10% boll infestation increased from 44.7% to 67.1%. The association between moth captures and boll infestation was positive and significant for non-Bt cotton fields but was not significant for Bt cotton fields. Although chemical control decisions based on trapping data were only moderately accurate, pheromone traps could still be valuable for determining when moth populations are high enough to trigger boll sampling to more rigorously evaluate the need for insecticide sprays.

Supplemental Control with Diamides for Heliothines in Bt Cotton

Abstract. Supplemental control with diamides for bollworm, Helicoverpa zea (Boddie), in Bt cotton is becoming more frequent, but there is little information on net returns to growers. The value of spraying Bt cotton with commercially available diamides was evaluated at seven locations in the Mississippi Delta cropping region in 2014 and 2015. Plots of Bollgard II®, Widestrike 3®, and non-Bt cotton varieties planted at each location were divided into five subplots. Treatments randomly assigned to subplots of each cotton cultivar were: 1) lowest labeled rate of chlorantraniliprole applied at threshold, 2) lowest labeled rate of flubendiamide applied at threshold, 3) lowest labeled rate of λ-cyhalothrin + chlorantraniliprole applied at threshold, 4) sprayed check, which was the maximum labeled rate of chlorantraniliprole applied on a 3-week schedule and initiated before first bloom to minimize damage from heliothines, and 5) nontreated check. Each plot was monitored weekly for larval abundance and plant dama...

Interaction of transgenic and natural insect resistance mechanisms against Spodoptera littoralis in cotton.

Insect-resistant transgenic plants that express insecticidal Cry proteins from Bacillus thuringiensis (Bt) are grown on millions of hectares worldwide. While these proteins are efficient in controlling key lepidopteran pests, not all pests are affected and the development of resistance in target pests is always a concern. These shortcomings could be addressed by exploiting the natural insect resistance of cotton, especially inducible terpenoids such as gossypol. To assess the potential of gossypol in supplementing Cry proteins as a resistance trait, we conducted a range of feeding assays with Spodoptera littoralis using artificial diet with defined amounts of Cry proteins and gossypol. This was supplemented by assays with leaf discs of induced and uninduced non-Bt and Bt cotton (expressing Cry1Ac and Cry2Ab). Additionally, we quantified Cry proteins and cotton terpenoids to describe the interactions in planta. We found that gossypol can increase the efficacy of Cry proteins in artificial diet in an additive way. Induced production of gossypol and other cotton terpenoids, however, did not increase the efficacy of Bt cotton owing to the strong impact of the Bt trait. Cotton terpenoids may offer the chance to supplement the insect resistance of Bt cotton in cases were the pest is not strongly affected by the Cry proteins. © 2016 Society of Chemical Industry.