bollworm resistance to bt cotton in india

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1476 VOLUME 23 NUMBER 12 DECEMBER 2005 NATURE BIOTECHNOLOGY Relationships between characters of the traits and landscape-scale impacts need to be informed by appropriate large-scale monitoring, experimentation and modeling, whereas impacts need to be interpreted on the basis of a clear understanding of what people want from the agricultural landscape. The use of environmental risk assessment (ERAs) which involve the development of conceptual models outlining assessment and measurement endpoints could offer a powerful framework 3 for us to move forward and allow larger scale studies to start receiving the attention they deserve. Les Firbank 1 , Mark Lonsdale 2 & Guy Poppy 3 1 Center for Ecology and Hydrology, Lancaster LA1 4AP, UK. 2 CSIRO, Australian Commonwealth Scientific and Industrial Research Organization, Entomology, GPO Box 1700, Canberra 2601, Australia. 3 School of Biological Sciences, University of Southampton, Southampton SO16 7PX, UK. e-mail: [email protected] 1. Poppy, G. Trends Plant Sci. 5, 4–6 (2000). 2. Snow, A.A. et al. Ecol. Appl. 15, 377–404 (2005). 3. Poppy, G.M. & Wilkinson, M.J. (eds.) Gene Flow from GM plants (Blackwell Scientific, Oxford, UK, 2005). 4. Crawley, M.J., Brown, S.L., Hails, R.S., Kohn, D.D. & Rees, M. Nature 409, 682–683 (2001). 5. Jorgensen, R.B. & Wilkinson, M.J. in Gene Flow from GM plants (eds. Poppy, G.M. & Wilkinson, M.J.) 113– 142 (Blackwell Scientific, Oxford, UK, 2005). 6. Smith, C.S., Lonsdale, W.M. & Fortune, J. Biological Invasions 1, 89–96 (1999). 7. Lovei, G.L. & Arpaia, S. Entomol. Exp. Appl. 114, 1–14 (2005). 8. Firbank, L.G. et al. The Implications of Spring-sown Genetically Modified Herbicide-tolerant Crops for Farmland Biodiversity: A Commentary on the Farm Scale Evaluations of Spring Sown Crops (Defra, London, 2003). 9. Firbank, L.G. & Forcella, F. Science 289, 1481–1482 (2000). 10. FAO Expert consultation. Genetically Modified Organisms in Crop Production and Their Effects on the Environment: Methodologies for Monitoring and the Way Ahead (FAO, Rome, Italy, 2005). Bollworm resistance to Bt cotton in India To the editor: I am writing in response to a letter of correspondence from Govind Gujar in the August issue (Nat. Biotechnol. 23, 927–928, 2005) and a news story by K. Jayaraman, Jeffrey Fox, Hepeng Jia and Claudia Orellana in the February issue of Nature Biotechnology (23, 158, 2005) that refer to research in my group describing a stochastic model to predict the emergence of resistance in the cotton bollworm Helicoverpa armigera to cotton varieties containing the cry1Ac gene encoding Bacillus thuringiensis (Bt) toxin 1 . The former article contains serious factual errors and the latter misrepresents the implications of our work. In his letter, Gujar points out that we predicted that Bt cotton will fail in India within the next 3 to 4 years. We never said anything of the sort, either in our paper or elsewhere. First of all, he presumes (incorrectly) that 70–80% of Gujarat was under Bt cotton cultivation for the past 3 years. On this basis he goes on to ask: “Given that the Bt crop in Gujarat covers the requisite area and is already in its fourth year of cultivation, why have we not witnessed the failure of Bt cotton due to resistance development in the cotton bollworm, Helicoverpa armigera?” The reason is that Gujar’s calculations and assumptions of the requisite area of Gujarat under Bt cotton cultivation are simply wrong. In fact, the 100- to 200- km radius area of Bt cotton cultivation modeled in our paper represents 7.8–31.4 million acres—about 100–200 times greater than the acreage he calculates. He compounds his error by assuming that 70–80% of this area (77,628–155,256 acres by his reckoning) was used to grow Bt cotton. This is subsequently used as a basis to argue that because resistance has not yet been detected in Gujarat (despite 70–80% of the area being under Bt cotton cultivation), “the effectiveness of insect resistance management strategy is likely just one of several factors that will determine the effectiveness of Bt cotton in suppressing bollworm populations.” Because his presumptions are wrong his subsequent assumptions are invalid. Realistic estimates of the area in Gujarat cultivating authorized Bt cotton hybrid are 22,500 acres in 2002, 130,000 acres in 2003 and 330,000 acres in 2004. Even if the area under unapproved illegal Bt cotton were five times (it could actually be only 2–3 times) that of the area cultivating authorized Bt cotton, it would still have been only 4% of 3.75 million acres in 2002, 16% of 4.12 million acres in 2003 and 33% of 4.98 million acres in 2004. Farmers in Gujarat have been cultivating Gossypium herbaceum diploid cotton ‘Wagad’ varieties on saline soils, which are unsuitable for hybrid cotton, in about 50% of the area under cotton cultivation over the past several years. Thus, in all likelihood the area used to grow Bt cotton would not exceed 50% of the total cotton area in the province. Our surveys in 2004 showed that the area under Bt cotton cultivation in Gujarat was 60– 70% of the area under hybrid cotton, which would constitute about 30–35% of the total cotton area. With a scenario such as this, our model predicts insect resistance will evolve under field conditions not for at least another 10 years. And if resistance management strategies are implemented, it will take much longer. On the basis of the model output, our paper suggested strategies appropriate for Indian conditions that have the potential to delay resistance up to 45 years, even with the complete hybrid cotton area converted to Bt cotton. Our statement in the paper (which was misquoted by Gujar) says “it is likely that some regions may develop into ‘hot spots’ of resistance within 3–4 years of introduction of the technology, if the area under Bt cotton hybrids increases beyond 70–80% of the total acreage under cotton.” Development of hot spots contributes to the spread of resistant alleles in the region through migrant moths and does not necessarily cause control failures at the spot itself. The views of Tabashnik 2 support our model predictions and highlight the importance of refuges as a key factor in contributing to the delay in insect resistance development, despite the cultivation of Bt cotton and Bt corn in more than 90 million hectares worldwide since 1996. Though Jayaraman and his associates interpreted our results to state that “Indian Bt gene monoculture” was like a “potential time bomb,” our aim was never to create panic by predicting resistance through stochastic modeling. We strongly believe that the Bt technology is the best eco-friendly tool available for cotton pest management in India. We wanted to integrate all factors that influence development of insect resistance to the toxin, through stochastic modeling, so that appropriate strategies can be devised to CORRESPONDENCE © 2005 Nature Publishing Group http://www.nature.com/naturebiotechnology

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Page 1: Bollworm resistance to Bt cotton in India

1476 VOLUME 23 NUMBER 12 DECEMBER 2005 NATURE BIOTECHNOLOGY

Relationships between characters of the traits and landscape-scale impacts need to be informed by appropriate large-scale monitoring, experimentation and modeling, whereas impacts need to be interpreted on the basis of a clear understanding of what people want from the agricultural landscape. The use of environmental risk assessment (ERAs) which involve the development of conceptual models outlining assessment and measurement endpoints could offer a powerful framework3 for us to move forward and allow larger scale studies to start receiving the attention they deserve.

Les Firbank1, Mark Lonsdale2 & Guy Poppy3

1Center for Ecology and Hydrology, Lancaster LA1 4AP, UK. 2CSIRO, Australian Commonwealth Scientific and Industrial Research Organization, Entomology, GPO Box 1700, Canberra 2601, Australia. 3School of

Biological Sciences, University of Southampton, Southampton SO16 7PX, UK. e-mail: [email protected]

1. Poppy, G. Trends Plant Sci. 5, 4–6 (2000).2. Snow, A.A. et al. Ecol. Appl. 15, 377–404 (2005).3. Poppy, G.M. & Wilkinson, M.J. (eds.) Gene Flow from

GM plants (Blackwell Scientific, Oxford, UK, 2005).4. Crawley, M.J., Brown, S.L., Hails, R.S., Kohn, D.D. &

Rees, M. Nature 409, 682–683 (2001).5. Jorgensen, R.B. & Wilkinson, M.J. in Gene Flow from

GM plants (eds. Poppy, G.M. & Wilkinson, M.J.) 113–142 (Blackwell Scientific, Oxford, UK, 2005).

6. Smith, C.S., Lonsdale, W.M. & Fortune, J. Biological Invasions 1, 89–96 (1999).

7. Lovei, G.L. & Arpaia, S. Entomol. Exp. Appl. 114, 1–14 (2005).

8. Firbank, L.G. et al. The Implications of Spring-sown Genetically Modified Herbicide-tolerant Crops for Farmland Biodiversity: A Commentary on the Farm Scale Evaluations of Spring Sown Crops (Defra, London, 2003).

9. Firbank, L.G. & Forcella, F. Science 289, 1481–1482 (2000).

10. FAO Expert consultation. Genetically Modified Organisms in Crop Production and Their Effects on the Environment: Methodologies for Monitoring and the Way Ahead (FAO, Rome, Italy, 2005).

Bollworm resistance to Bt cottonin IndiaTo the editor:I am writing in response to a letter of correspondence from Govind Gujar in the August issue (Nat. Biotechnol. 23, 927–928, 2005) and a news story by K. Jayaraman, Jeffrey Fox, Hepeng Jia and Claudia Orellana in the February issue of Nature Biotechnology (23, 158, 2005) that refer to research in my group describing a stochastic model to predict the emergence of resistance in the cotton bollworm Helicoverpa armigera to cotton varieties containing the cry1Ac gene encoding Bacillus thuringiensis (Bt) toxin1. The former article contains serious factual errors and the latter misrepresents the implications of our work.

In his letter, Gujar points out that we predicted that Bt cotton will fail in India within the next 3 to 4 years. We never said anything of the sort, either in our paper or elsewhere.

First of all, he presumes (incorrectly) that 70–80% of Gujarat was under Bt cotton cultivation for the past 3 years. On this basis he goes on to ask: “Given that the Bt crop in Gujarat covers the requisite area and is

already in its fourth year of cultivation, why have we not witnessed the failure of Bt cotton due to resistance development in the cotton bollworm, Helicoverpa armigera?” The reason is that Gujar’s calculations and assumptions of the requisite area of Gujarat

under Bt cotton cultivation are simply wrong.

In fact, the 100- to 200-km radius area of Bt cotton cultivation modeled in our paper represents 7.8–31.4 million acres—about 100–200 times greater than the acreage he calculates. He compounds his error by assuming that 70–80% of this area (77,628–155,256 acres by his reckoning) was used to grow Bt cotton. This is subsequently used as a

basis to argue that because resistance has not yet been detected in Gujarat (despite 70–80% of the area being under Bt cotton cultivation), “the effectiveness of insect resistance management strategy is likely just one of several factors that will determine the effectiveness of Bt cotton in suppressing bollworm populations.”

Because his presumptions are wrong his subsequent assumptions are invalid. Realistic estimates of the area in Gujarat cultivating

authorized Bt cotton hybrid are 22,500 acres in 2002, 130,000 acres in 2003 and 330,000 acres in 2004. Even if the area under unapproved illegal Bt cotton were five times (it could actually be only 2–3 times) that of the area cultivating authorized Bt cotton, it would still have been only 4% of 3.75 million acres in 2002, 16% of 4.12 million acres in 2003 and 33% of 4.98 million acres in 2004. Farmers in Gujarat have been cultivating Gossypium herbaceum diploid cotton ‘Wagad’ varieties on saline soils, which are unsuitable for hybrid cotton, in about 50% of the area under cotton cultivation over the past several years. Thus, in all likelihood the area used to grow Bt cotton would not exceed 50% of the total cotton area in the province.

Our surveys in 2004 showed that the area under Bt cotton cultivation in Gujarat was 60–70% of the area under hybrid cotton, which would constitute about 30–35% of the total cotton area. With a scenario such as this, our model predicts insect resistance will evolve under field conditions not for at least another 10 years. And if resistance management strategies are implemented, it will take much longer. On the basis of the model output, our paper suggested strategies appropriate for Indian conditions that have the potential to delay resistance up to 45 years, even with the complete hybrid cotton area converted to Bt cotton. Our statement in the paper (which was misquoted by Gujar) says “it is likely that some regions may develop into ‘hot spots’ of resistance within 3–4 years of introduction of the technology, if the area under Bt cotton hybrids increases beyond 70–80% of the total acreage under cotton.” Development of hot spots contributes to the spread of resistant alleles in the region through migrant moths and does not necessarily cause control failures at the spot itself.

The views of Tabashnik2 support our model predictions and highlight the importance of refuges as a key factor in contributing to the delay in insect resistance development, despite the cultivation of Bt cotton and Bt corn in more than 90 million hectares worldwide since 1996.

Though Jayaraman and his associates interpreted our results to state that “Indian Bt gene monoculture” was like a “potential time bomb,” our aim was never to create panic by predicting resistance through stochastic modeling. We strongly believe that the Bt technology is the best eco-friendly tool available for cotton pest management in India. We wanted to integrate all factors that influence development of insect resistance to the toxin, through stochastic modeling, so that appropriate strategies can be devised to

CORRESPONDENCE©

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Page 2: Bollworm resistance to Bt cotton in India

NATURE BIOTECHNOLOGY VOLUME 23 NUMBER 12 DECEMBER 2005 1477

ensure the sustainability of Bt cotton under Indian farming conditions. We had clearly stated in our paper that “model outputs cannot be treated as predictive. They assist in the identification of parameters that have the largest effects on resistance development. Once the critical factors and conditions responsible for rapid development of resistance are properly identified through simulation, it would then enable the development of proactive resistance management strategies.” Thus, our model integrates ecological, genetic and biological factors to understand which factors contribute most toward the development of resistance.

Our results1 clearly show that insect resistance management strategies indeed hold the key to sustainable use of a technology such as Bt cotton. Indian farmers have always

overused good technologies to the point that they are rendered useless, as was the case with good varieties and insecticides such as pyrethroids. What India needs is a set of resistance management strategies that are scientifically sound, compatible with Indian farming conditions and are acceptable to the Indian farmer. Our attempt was precisely to do that and we hope to succeed.

Keshav R. Kranthi

Crop Protection Division, Central Institute for Cotton Research, Nagpur 440 010, India.e-mail: [email protected]

1. Kranthi, K.R. & Kranthi, N.R. Curr. Sci. 87, 1096–1107 (2004).

2. Tabashnik, B. Nat. Biotechnol, 23, 414 (2005).

What India needs is a set of resistance management strategies that are scientifically sound, compatible withIndian farming conditionsand are acceptable to the Indian farmer.

CORRESPONDENCE©

2005

Nat

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