ICAC Workshop Ouagadougou, October 29-31, 2007

Bt Cotton’s Place in Integrated Pest Management in West Africa

Dr. Maurice Vaissayre Entomologist CIRAD [Center for International Cooperation in Agronomy Research for Development], Unité de Recherche Systèmes cotonniers en petit paysannat [Department of Research on Cotton Systems for Small Farmers], TA B10/02, Montpellier (France)

Statement of Problem

Cotton crops in western and central Africa have to contend with a wide variety of parasites, predominantly the bollworms Helicoverpa armigera Hübn., Diparopsis watersi Roth., Earias insulana Boisd. and Pectinophora gossypiella Saund. In coastal countries, E. biplaga and Cryptophlebia leucotreta Meyr are also encountered. These are not the only harmful lepidopterous , since the phyllophage species Anomis flava and Syllepte derogata Fab., along with some species of the Sodoptera, are also found. Lepidopterous insects have long been considered to be the main pests, but in fact share their status as harmful insects with a whole host of biting insects, more diverse in the south than in the north, where Homoptera (the aphid Aphis gossypii Glov.; the Aleyrodidae, especially Bemisia tabaci Genn.; Typhlocibidae, commonly called “jassids”—Jacobi’s Jacobiella fascialis and Bergevin and Zanon’s Austroasca lybica )) and Heteroptera (specifically Miridae at the beginning of the season, and Pentatomidae and Pyrrhocoridae during the boll maturation phase) are found. Alongside these insects are found acarids, Tetranychidae in the dry regions and Tarsonemidae in wet regions.

Harvest losses due to this parasitic activity vary greatly from one region to another and from one year to the next. Statistics are available for the various western and central African countries, and range from 30 to 80% of potential production, depending on the production zone and the crop year. The quality of the fiber and seed can also be affected.

There are few effective natural means of combating this host of parasites. While the inventory of predatory insects and parasitoids appears to be very large (Silvie et al. 1989; 1993), few of them are up to the task of controlling the proliferation of the harmful insects, whether or Homoptera. pathogens have been shown to be the most effective auxiliary agents, especially for controlling aphid and Aleyrodidae populations during the rainy season.

The first element of an integrated pest management system consists of avoiding some of the parasitic insects through the choice of crop zone and planting date. The second is to plant a crop variety that has some degree of resistance to the pests. Such resistance can result from an ability to compensate, or morphological or biochemical barriers. Obviously, no barrier exists that can withstand all of the parasitic insects. In western and central Africa, the varieties distributed have both a strong ability to compensate for losses from parasites (at the cost of a longer growth cycle) and sufficiently glabrous foliage to reduce the incidence of jassids. To control the remaining parasites, farmers have turned to chemical means. This chemical warfare was a factor in the undisputed success seen from the 1960s to the 1980s. Though very moderate compared to practices employed in other cotton-growing countries and for other crops, it was called into question in the mid 1990s when the pests developed resistance, first and foremost the noctuid H. armigera (Martin et al. 2005; Brévault and Achaleké 2005). ICAC Workshop Ouagadougou, October 29-31, 2007

Bt Cotton

A so-called “Bt cotton” plant has been altered by inserting genes from the soil bacterium Bacillus thuringiensis. Because of this, it produces one (Cry1Ac) or several (Cry1Ac+Cry2Ab, Cry1Ac +Vip, Cry1Ac+Cry1F) toxins. The choice of these toxins corresponds to the pests targeted by the creation of the insect-resistant cotton. Originally, the targets were the noctuid moth Heliothis virescens and the pink bollworm P. gossypiella (Perlak et al . 2001). It was discovered that in addition to these lepidopterous insects, Cry1Ac is toxic (though less so) to the entire Heliothis/Helicoverpa complex, as well as some lepidopterous phyllophages. So Bt cotton has met with considerable success in cotton- growing countries where H. armigera had become resistant to insecticides: namely Australia, China and India (James, 2005).

Still, the insect resistance conferred upon cotton by insertion of the previously-mentioned genes has its limits. Indeed, Bt cotton controls neither the Coleoptera nor biting and sucking insects. So before introducing Bt cotton in a cotton-growing area, it is important to consider what its impact would be on the entire parasitic complex, given the new equilibria that would form among injurious species.

A second issue has already been widely discussed, namely the question of effects on non- targeted fauna, whether predators/parasitoids, cotton-pollinating insects or the biodiversity of the agricultural system’s entomological fauna as a whole. Most studies done have concluded that aside from the targeted insects, the toxins have no effect on beneficial insects (Romeis et al. 2006).

A third question concerns toxin production by the plant. While this is indisputable during the cotton plant’s first weeks of growth, the quantity of the toxins exuded gradually decreases over the development and maturation phase (Olsen and Daly, 2000; Kranti et al. 2005). Moreover, exudation can be affected by stress conditions, especially high temperatures and water shortages, which rainfed crops frequently experience (Chen et al. 2005; Olsen et al. 2005).

Finally, the issue of the sustainability of resistance conferred by inserting one or several genes in the plant (Bates et al, 2005) has arisen. To limit the nearly constant selection pressure on the targeted insects, two strategies have been proposed. The first, called HD+R, is based on heavy exudation of the toxin by the cotton plant, associated with the planting of blocks of non-Bt cotton in which insect populations develop with no selection pressure at all and can “dilute” the resistance genes present in any survivors from the Bt parcels. This strategy, which was implemented in the United States, is now being abandoned. On the small farms of China and India, farmers are returning to mixed farming systems and the presence of non-cultivated hosts to “dilute” the resistance genes (Green et al. 2003). It is obvious that these strategies are based on models that are by nature complex, since predictions are involved, and in which ignorance or underestimation of a factor can have very large consequences for the final result (Vaissayre et al. 2006; Nibouche et al. 2007).

Since this paper is limited to the plant-health aspects of the consequences of growing Bt cotton on small farms, we will not discuss here the issues related to the socioeconomic consequences of adopting Bt cotton, which are covered in an extensive body of literature.

ICAC Workshop Ouagadougou, October 29-31, 2007

Introduction of Bt Cotton and Integrated Cotton Protection in West Africa

Cultivars that express a Bt toxin gene could be an answer to the demand for integrating non- chemical methods to protect cotton on small farms, all the more so because H. armigera populations have become resistant to pesticides. By controlling some important elements of the parasitic complex, the introduction of Bt cotton plants logically should have two effects: an immediate one, namely a reduction in the number of chemical treatments; and a more uncertain one, namely increased yield thanks to better control of key insects. Such an introduction thus presupposes a redefinition of integrated protection in cotton-based agricultural systems (Hillocks, 2005). In order for the result to be satisfactory for the farmers, a certain number of points still must be considered.

• Incorporate the genes of interest into adapted cultivars

To obtain the desired results, the genes of interest must be incorporated into the genome of cultivars adapted to western and central Africa’s growing conditions, and these altered cultivars must be reworked by the selectors. It is essential to preserve the hairiness necessary for controlling the jassids. Preserving a certain level of compensation could also be an answer to the damage that the Miridae will continue to inflict on the flower buds.

• Modify technical programs to make better use of the innovation

It is quite obvious that the presence of a gene of interest in the plant’s genome makes the seed more valuable. Bt cotton growing cannot be developed unless seed with guaranteed germination quality is available, and if sowing density is optimal as defined by research. It is equally obvious that random factors such as the beginning of the rains are hardly favorable to this constraint.

It is too often forgotten that weed control is the main factor in successfully growing cotton. Success in growing Bt cotton will require early hoeing or the use of herbicides, a major factor that increases the necessary investment.

The second additional cost will be related to increased mineral fertilization, a type of fertilization that has had too many constraints on it in recent years, leading farmers to reduce the amount of fertilizer they use to below the threshold of effectiveness, as witnessed by the many cases of potassium deficiency observed in the cotton-growing zone.

Incorporation of these factors is the primary condition for the innovation’s success. The innovation leads to higher productivity, which alone can absorb the additional cost that cannot fail to accompany the introduction of Bt seed.

• Beware pests not controlled by Bt toxins

Bt cotton is not resistant to all insects. According to a well-known principle, the scarcity of some harmful species opens up new opportunities for species that until that point had been considered “secondary.” This phenomenon will be accentuated in western and central Africa because currently, many interventions are done with broad-spectrum insecticides or associations of active substances. So it is predictable that species will emerge from among the ranks of the pests that have the most effect on high yield. From ICAC Workshop Ouagadougou, October 29-31, 2007

experience in other countries (Green et al. 2001; Wu et al. 2002; Hofs et al. 2005), one can predict without going too far out on a limb that biting insects in general, Homoptera of course but also especially Heteroptera, will be likely to achieve the threshold of harm. We are poorly prepared for this eventuality because of a lack of research in this area. Looking back to the past, there was a similar situation when pyrethrinoids were introduced in French-speaking Africa in the mid-1970s. Although the cotton plant was remarkably well protected from bollworms by these new molecules, the full potential of cotton production was not revealed until the institution of supplementary use of organophosphates. In Chad and Cote d'Ivoire, the increase in yield—at the time attributed to the control of biting insects—was 300 kg of cottonseed per hectare, or between 10 and 20% of the potential production. The savings achieved by reduced pesticide consumption after the introduction of Bt cottons may not be as great as hoped (Pemsl et al. 2005; Hofs et al. 2006).

• Monitor bollworm activity

While bollworms are the target of Bt cottons, failure to produce these toxins, whether because the plant ages or because there are pockets of drought during the growing season leads to the risk of local infestations by these insects. Today, farmers have the tools to handle situations such as this, in the form of decision trees developed by research. Still, they require resources for the intervention (access to agricultural production factors and credit).

• Measure the impact on biodiversity and the environment

A significant reduction in the number of pesticide applications could favor activity by a secondary insect fauna (Marvier et al. 2007). The pressure exerted by the parasitic complex, as a whole or for certain components, could be reduced because of this.

A reduction in the number of chemical interventions could also reduce health problems among the farmers and contamination of the environment (Lu et al. 2002; Knox et al. 2006)

• Expect resistance to the transgenes to develop

At this time, there is no well-thought-out mechanism for sustainably managing Bt- resistant populations on small farms. We can suggest strategies only by working with models, in which some factors are still poorly understood.

In particular, we are trying to learn the frequency of resistance genes among “virgin” populations that have not yet been exposed to selection pressure, and to evaluate the contribution of spontaneous refuge crops or plants to the annual genetic mixing in H. armigera populations. This work is essential if the results of modeling are to be reliable.

So it would seem that to be on the safe side, Bt cotton should be introduced in only a fraction of the cotton-growing acreage and a fraction of the regions where it is grown, so as to be able to track the development of resistance among the targeted populations (Nibouche et al. 2007). Such an approach would also allow for the coexistence of Bt cotton and other production modes (biological or conventional pest control).

ICAC Workshop Ouagadougou, October 29-31, 2007

Conclusion

Bt cotton plants are already a part of the agricultural landscape, especially on small farms in China and India. So it is quite logical that they are attracting the attention of cotton growers in Africa. Putting this type of cotton into production can be a factor for progress (resistance to bollworms). It presupposes an intensification of cultivation that not everyone may be ready to accept. Vigilance is needed so that small farmers can benefit from the innovation, but so that it also remains sustainable.

Alongside the socioeconomic issues, three technical questions will affect the technical success of introducing Bt cotton in western and central Africa: What level of intensification will need to accompany dissemination of the innovation in order to realize its potential? What will the impact be on reducing chemical controls? And what method for managing cotton growing will ensure that the innovation is sustainable?

References

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Brévault T., Achaleke J. (2005). Status of pyrethroïd resistance in the cotton bollworm, Helicoverpa armigera , in Cameroon. Resist. Pest Manage. Newsl. 15 (1), p. 4–7.

Chen D., Ye G., Yang C., Chen Y., Wu Y. (2005). The effect of high temperature on the insecticidal properties of Bt cotton. Environ. Exp. Bot. 53 (3), p. 333–342.

Green JK., Turnipseed SG., Sullivan MJ., May OL. (2001). Treatment thresholds for stink bugs ( Hemiptera: Pentatomidae ) in cotton. J. Econ. Entomol. 94 , p. 403–409.

Green WM., De Billot MC., Joffe T., Van Staden L., Bennett-Nel A., Du Toit CLN., Van der Westhuizen L. (2003). Indigenous plants and weeds on the Makhathini Flats as refuge hosts to maintain bollworm population susceptibility to transgenic cotton. Afric. Entomol. 11 , p. 21–30.

Hillocks R.J.(2005). Is there a role for Bt cotton in IPM for smallholders in Africa? Int. J. Pest Manage. 51 (2), p. 131–141.

Hofs J.L., Schoeman A., Mellet M., Vaissayre M. (2005) Impact des cotonniers génétiquement modifiés sur la biodiversité de la faune entomologique: le cas du coton Bt en Afrique du Sud Int. J. Trop Insect Sci. 25 : 63-72

Hofs J.L., Fok M., Vaissayre M. (2006) Impact of Bt cotton adoption on pesticide use by smallholders: a 2-year survey in Makhatini Flats (South Africa) Crop Prot. 25 : 984- 988

James C. (2005). Executive summary of global status of commercialized Biotech/GM crops: 2005. ISAAA Briefs 34. New York: Intern. Serv. for the Acquis. Agri-Biotech Applic. 12 p. ICAC Workshop Ouagadougou, October 29-31, 2007

Knox O., Constable G., Pyke B., Gupta V.S. (2006) Environmental impact of conventional and Bt insecticidal cotton expressing one and two Cry genes in Australia. Austral. J. Agric. Res. 57 : 501–509

Kranthi KR., Naidu S., Dhawad CS., Tatwawadi A., Mate K., Patil E., Bharose AA., Behere GT., Wadaskar RM., Kranthi S. (2005). Temporal and intra-plant variability of Cry1Ac expression in Bt-cotton and its influence on the survival of the cotton bollworm, Helicoverpa armigera (Hubner). Curr. Sci. 89 (2), p. 291–298.

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Martin T., Ochou G.O., Djihinto A.C., Traore D., Togola M., Vassal J.M., Vaissayre M., Fournier D. (2005) Controlling and insecticide-resistant bollworm in West Africa. Agric.,Ecosyst. and Environ. 107 : 409-411

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Nibouche S., Guérard N., Martin P., Vaissayre M. (2007) Modelling the role of refuges for sustainable management of dual-gene Bt Cotton in West African smallholder farming systems. Crop Prot. 26 : 828-836

Olsen, K. M., and J. C. Daly (2000) Plant-toxin interactions in transgenic Bt cotton and their effects on mortality of Helicoverpa armigera . Entomol. Soc. Am. 93 , 1293—1299.

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Center for International Cooperation in Agronomic Research for Development

Cotton Systems Research Unit

The Role of Bt Cotton in Pest Management in West Africa

Dr. Maurice Vaissayre

ICAC Workshop Ouagadougou, October 2007 Contents

1. The parasitic complex and limits of chemical prevention 2. Bt cotton plants 3. Integration of GMC in the technical process for sustainable management of parasite problems 1. Formulation of the Problem

• A diversified parasitic complex • Of piercing insects – Which are established from year to year – But whose size remains underestimated • Leaf-feeding caterpillars • Caterpillars on the capsule • Little integration of means of prevention A diversified parasitic complex

Jassides, Plant Louses and White Flies

Mirids and Leaf- hoppers A diversified parasitic complex

Leaf-Feeding Insects: Anomis, Syllepte and Spodoptera

Frugivores: Diparopsis, Earias, Helicoverpa + endocarpic insects Little Integration of Means of Prevention

• Varietal resistance (hairiness =jassides, compensation = all pests) • Cultural Techniques: Early sewing (collage and pink bollworm, but also able to compensate) Due to the low activity level of natural enemies (some parasitoids and predators, pathogens of aphids and white flies) High Dependence on Chemical Prevention

With risks to health and the environment High Dependence on Chemical Prevention

But especially the development of resistances 2. Bt Cotton Plants

• Interest in introducing insect-resistant genes • Conversion of the cotton plant • Limits of the Innovation: – What Bt cotton plants are not – Risks associated with Bt cotton Interest of Bt Cotton Plants

• Varietal resistance is the most satisfactory way of managing stress, for pests and for diseases. • The ideal plant would be one that establishes one (or more) entomopathogenic toxins • Without disturbing the activity of the entomophagous complex • Without justifying chemical intervention What is Bt Cotton?

• A plant in the genome of which one (or two) gene(s) of the Bacillus thuringiensis bacteria was inserted • The plant makes one (or more) entomopathogenic toxins: Cry1Ac (+ Cry2Ab, Cry1F) • It is thereby protected against a certain number of caterpillars (in particular the noctuid moth H. armigera and the pink bollworm P. gossypiella) …and crystals …and and its toxins its and , …

B. thuringiensis thuringiensis B. A bacterium A spores How the Bt toxin acts www.inchem.org/documents/ehc/ehc/v217eh02.gif What can be expected from adopting Bt cotton?

1. For farmers: - better control of pests - less handling of pesticides = positive outcome in terms of production and health

2. For the environment: - improved biodiversity - increased activity of auxiliary fauna by reducing pesticide residues What Bt cotton plants are not

• Bt toxins are specific to a certain number of : Cry1Ac is effective on H. armigera, Earias, and probably Anomis; Cry1F controls the Spodoptera genus.

• The toxins introduced to date do not control the full spectrum of parasites! Integration of GMCs in the Technical Process • Integrate genes of interest into adapted cultivars • Modify technical routes to better develop innovation • Watch for pests not controlled by Bt toxins • Monitor the dynamics of caterpillars on the capsule • Anticipate the appearance of resistance to transgenic plants • Promote the technology financially Why questions about Bt cotton?

1. For farmers, - Is the gene selected adapted to the local parasitic constraints? - Will the toxin be expressed under local abiotic constraints (stress)? - Will chemical treatments still be necessary? - What will be the product generated/cost of the technology balance? Why questions about Bt cotton?

2. For the ecosystem, -Is the gene selected associated with risks (transfers to microorganisms in the soil)? -Can transgenic plants propagate in wild species? -Can the toxin affect useful species (pollinators, auxiliary fauna, fauna from the soil)? -Will the continuous expression of a toxin not create resistances in the targeted insects? Assessment of the Short-term Risk

Research can respond to: - The impact of useful entomofauna (pollinating insects, auxiliary fauna) - The impact of the innovation on new fauna balances in the agrosystem

But in the end, what will be the innovation’s impact on the number and type of chemical interventions still necessary? Management of the Long-term Risk

The CIRAD is now working on prediction models for resistance to the toxin, adapted to the small rural population to the South, based on information acquired on: The initial frequency at which resistant insects in the ecosystem meet - Heritability of the resistance (dominant or recessive) - The role of host plants present in the agrosystem and the importance of genetic cross fertilization in the target populations In Conclusion

• Bt cotton plants are now part of the agricultural landscape, in particular in small rural populations (China, India); •Cultivation of this type of cotton could be a factor of progress (resistance to caterpillars on the capsule, reduced dependence on chemicals); •Oversight is necessary so that small farmers benefit from it, but also so that the innovation remains sustainable. Thank you for your attention!