Aphid and whitefly management in cotton growing: Review and challenges for the future

J.P. Deguine1, M. Vaissayre1 and P. Ferron2 1 Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), Montpellier FRANCE 2 Institut National de la Recherche Agronomique (INRA), FRANCE Correspondence author [email protected] Aphid and whitefly management in cotton growing: Review and challenges for the future

ABSTRACT used only in the last resort. Appropriate agronomic techniques for the phytosanitary situations in cot- In many cotton-growing regions in the world, the ton growing are mentioned. It is proposed that phytosanitary situation of cotton has been marked agronomists and crop protection specialists should in the past two decades by, among other things, a adopt a concerted approach in following these new renewed increase in the populations of certain pathways and report the results obtained in the piercing-sucking insects and especially the aphid medium term. Aphis gossypii Glover and the whitefly Bemisia tabaci (Gennadius). These pests are polyphagous Introduction and display very special biological and ecological In recent decades, the entomological problems features causing damage with extremely serious experienced in agriculture have been marked by two economic consequences. The methods generally major phenomena related to the intensification of pro- used to control these sucking insects were based duction and, more particularly, it increased use of in- mainly on the use of insecticides targeting aphids puts (fertilizers and pesticides). Indeed, it has been or whitefly, in most cases with the same spray pro- observed on the one hand that certain pests have be- cedures as for those used to control other major come resistant to insecticides and on the other that other insects that hitherto had a minor effect on yields and cotton pests such as bollworms. This chemical con- production quality rapidly gained major economic im- trol has finally proved not very effective, it is ex- portance. In most cases, the control of outbreaks was pensive and forms a real danger for the conserva- not satisfactory using common control resources. tion of biological diversity and for the environment as a whole. Alternative control methods that are Cotton growing is no exception to this general better suited to the integrated management of observation. Phenomena of resistance to insecticides have thus been observed, and are widespread today aphid and whitefly populations are proposed within in certain important lepidopteran pests of cotton fruit the framework of more rational and sustainable organs, including the noctuids Helicoverpa armigera farming. They are based on the principle of seek- (Hübner), Heliothis virescens F. and Spodoptera spp. ing a return towards a balance between these pests This also applies to Hemiptera such as the aphid Aphis and the various accompanying indigenous benefi- gossypii Glover and the whitefly Bemisia tabaci cial insects. For this, a break with past practices is (Gennadius), which have recently become major cot- ton pests in various parts of the world. This new first recommended in order to prevent an aggra- phytosanitary situation has alerted both farming com- vation of the phytosanitary situation, followed by munity stakeholders and research scientists. the application of a new strategy based on the integrated pest management concept. The role of The present update is aimed at changing the sta- preventive measures would thus become prepon- tus of these piercing-sucking pests in cotton growing. derant. These are based on a strategy enabling It covers first of all their biological characteristics and the damage that they cause to crops and briefly de- plants to escape attacks by these pests thanks to scribes the evolution of the control techniques used. various procedures such as early sowing, choice The reasons for the outbreaks of these new pests are of varieties with short cycles, limited vegetative described and an inventory drawn up of the main pa- development and vegetation with low appetency rameters to be taken into account to achieve sustain- for the insects. Traditional agronomic techniques able management of pest populations. A phytosanitary such as rotations and cropping patterns, rational approach - both technical and strategic - for solving this crop protection problem is then proposed. Although combinations of crop plants, trap crops, etc., also a great variety of agro-ecological situations are ob- have complementary effects by limiting pest out- served in cotton growing around the world, the infor- breaks and enhancing populations of beneficial mation presented here is drawn in particular from small- organisms. The prospects opened up by geneti- scale cotton growing in Africa and has been used to cally modified varieties are discussed. The make general recommendations that can be applied phytosanitary situations of the field are then moni- most, if not to all of these situations. tored using population count techniques and eco- Pests that have gained major nomic thresholds are set. If it is then found to be economic importance essential to use curative control measures, priority economic importance should be awarded to alternative techniques and Evolution of their status and chemical spraying with active substances causing geographical distribution the least damage to the environment should be

1178 World Cotton Research Conference-3 2003 Cape Town - South Africa

A. gossypii and B. tabaci have long been on the Several hundred A. gossypii host plants have been list of cotton pests (Hargreaves, 1948). But whereas counted in the world (Essig, 1947; Leonard et al., 1971; they were still considered to be of minor importance Roy and Behura, 1983; Inaizumi, 1980; Millar, 1994; until recently, they gained major importance at the end Deguine et al., 1999). In addition to cotton, the culti- of the twentieth century in many parts of the world (But- vated plants of economic importance that suffer from ler and Henneberry, 1994; Leclant and Deguine, 1994). infestation are both vegetable crops (aubergine (egg- plant), cucurbits, gumbo, melon, peppers, etc.) and A. gossypii can be considered as the most im- ornamental species (Bougainvillea, Hibiscus, Lantana, portant and most harmful aphid species in the world, etc.) and a few perennials (Theobroma, Citrus, Coffea) especially on cotton and cucurbit crops in North are also attacked. B. tabaci is also well known for its America, Africa and Asia. A ubiquitous species, it flour- polyphagia and Greathead (1986) mentions 506 host ishes in the tropics and subtropics but can also flourish plants belonging to 74 different families: Asteraceae in continental climates as in the Xin Jiang in China (56 species), Convolvulaceae (20 species), (Zhang et al., 2000). It is the commonest and most Cucurbitaceae (17 species), Euphorbiaceae (32 spe- polyphagous aphid in sub-Saharan Africa. It is found cies), Fabaceae (96 species), Malvaceae (35 species) on all species of the genus Gossypium, and especially and Solanaceae (33 species). on G. hirsutum and G. barbadense (Mursal, 1993). Outbreaks have been particularly severe in the past The two insects also display strong reproductive two decades: in China since 1983 (Luo and Gan, 1986), capacities varying according to the climatic conditions. in the Middle East since 1984 (Broza, 1986) and in the Parthenogenesis in A. gossypii in the tropics should be United States since 1986 (Akey and Butler, 1989; noted. This property enables residual populations to Grafton-Cardwell, 1991; Steinkraus et al., 1991). In develop very rapidly, sometimes with an exponential West Africa, Onu (1989), Silvie (1989). Renou and pattern (Deguine and Leclant, 1997). Deguine (1992) drew attention to the growth of the populations of this aphid in West Africa, in particular in Both insects are also remarkable in their capac- Cameroon and Chad, where Couilloud (1965) had ity for adaptation to the environment and their opti- described them 25 years earlier as being of little im- mum exploitation of it. This feature goes a long way portance or even practically non-existent. A gossypii towards accounting for their harmfulness as it enables thus suddenly became a key pest in cotton growing in rapid exploitation of plants; no less rapid colonisation many countries at the end of the twentieth century. of new host-plants, adaptation to climatic conditions through modification of the biological and reproduc- B. tabaci was described as a cotton pest in India tion cycles and the ability of both aphids and whitefly in the early twentieth century (Husain and Trehan, 1933). to engender biotypes. The intraspecific morphological Outbreaks were reported between 1970 and 1980 in variability of A. gossypii is now clearly recognized (Wool the Sudan, Turkey and Israel (Gerling and Henneberry., and Hales, 1997; Komazaki and Osakabe, 1998; 1998). It has been considered as a pest of economic Vanlerberghe-Masutti and Chavigny, 1998; Zou et al., importance in the United States, and particularly in 2001). The phytosanitary importance of this property California and Arizona, since 1981 (Toscano et al., is known for B. tabaci, with the appearance of the B- 1998). The losses caused are estimated at nearly two biotype in the United States in 1986. This biotype can hundred million dollars in certain years (Henneberry spread more diseases and more easily acquire resis- and Faust, 1999). It is a cosmopolitan whitefly and tance to insecticides and is now widely distributed found in the zone lying between the 40th parallels, and around the world (Peterschmitt et al., 2001). The B. even further north in Europe. B. tabaci is reported to- tabaci species complex was the subject of a synthesis day in most countries in western, central and southern and revision by Perring (2001). However, it should be Africa and in the Indian Ocean islands (Cock, 1986). remembered that certain characteristics of the B. tabaci species, such as polyphagia and strong reproductive The main biological characteristics capacity, are not found in certain biotypes (Peterschmitt, of the ‘new’ pests personal communication). Numerous studies on whitefly and aphids have It is difficult to draw up the general characteris- been published, including those on cotton. Recent bib- tics of the population dynamics of aphid and whitefly liographical syntheses have been published concern- populations in cotton because of the diversity of the ing the latter plant, and we refer in particular to those agro-climatic conditions observed. However, in many of Leclant and Deguine (1994) on A. gossypii and of cases, the outbreaks at the beginning of the vegetative Butler and Henneberry (1994), Cock (1986) and cycle before flowering, like those observed at the end Oliveira et al. (2001) on B. tabaci. In addition to their of the cycle after cut-out and during boll dehiscence very broad distribution on a global scale, aphids and when there is shortage of rainfall or moisture, are par- whitefly display remarkable intrinsic biological charac- ticularly harmful to crop yields and production quality teristics and in particular polyphagia and the capcity (Deguine et al., 1994 and 2000; Nibouche et al., for multiplication and adaptation to a range of envi- 1998). ronmental conditions.

1179 Aphid and whitefly management in cotton growing: Review and challenges for the future

Damage and economic more recently in Pakistan (Ahmad and Ali, 1998) and consequences in India (Singh et al., 1998) in G. hirsutum. Another type of virus disease is spread by B. tabaci causes mo- For these various reasons, aphids and whitefly saic diseases involving different pathogens, both in now have major economic effects in most cotton re- Africa (African Mosaic) and America (mosaico and gions. Sucking-piercing insects are held to be respon- rugosidad) (Cauquil and Follin, 1983). B. tabaci is also sible for both loss of seed cotton production and de- held responsible for other syndromes such as red cot- preciation of cotton fiber quality. Three types of dam- ton disease that appeared recently in Africa (Nibouche age are caused: trophic damage by the withdrawal of et al., 1998). sap from the plants, plant pathology effects by the spread of virus diseases and technological damage resulting from honeydew production that hinders cot- Evolution of the control of sucking- ton processing. piercing insects

Production losses result from sap sucked by the The first steps in directed control insects (larvae and adults) during plant growth and the Until the last decade of the twentieth century, simultaneous injection of phytotoxic saliva. These at- cotton crop protection in most regions generally con- tacks cause lateness in plant growth and the vegetative sisted of chemical control applied according to a pre- cycle, especially if they occur at the beginning of the set calendar and subsequently according to the pest season. In some cultivation situations today, the eco- population levels and the risks. The control techniques nomic effects of such trophic damage can exceed those used were aimed essentially at pests of fruit organs (es- of bollworms (Deguine et al., 1994; Nibouche et al., pecially Noctuid lepidopterans) rightly considered at the 1998). A decrease in fiber quality results from the pro- time as the most dangerous pests for seed cotton pro- duction and excretion of honeydew on seed cotton in duction and hence as the most harmful for growers. open bolls ready for picking at the end of the season. In most countries, the sticky cotton phenomenon that As a result of the recent outbreaks of sucking- may be observed in spinning is ascribed to the honey- piercing insects, mainly at the end of the cycle, cotton dew deposits that accompany late outbreaks of A. crop protection in the past two decades has also incor- gossypii and B. tabaci (Hector and Hodkinson, 1989). porated features to control A. gossypii and B. tabaci. Although there are some differences between aphid However, although spraying for control bollworms is and whitefly honeydew with regard to the composition justified and has proved effective, chemical control of (Héquet and Wyatt, 1999) and the size and shape of aphids and whitefly is not as satisfactory and has even the drops (Couilloud, 1986), the difficulties encoun- be considered to be ineffective. tered in cotton processing are similar. Honeydew also forms a culture medium for various saprophytic fungi The first measures taken to control aphids and that cause sooty mould, hindering plant respiration and whitefly in the 1980s consisted of incorporating chlorophyll uptake when they affect leaves. aphicides and whitefly control products, whose active substances were mainly organophosphorus compounds A. gossypii and B. tabaci are also well known for and carbamates, into bollworm control programs based their ability to spread numerous plant diseases, and essentially on pyrethroids. The spraying program and especially virus diseases. The aphid spreads blue dis- the application techniques were not usually greatly ease of cotton in West Africa (Cauquil and Vaissayre, modified. 1971), a disease that is doubtless very close to Cotton Leaf Curl Virus in South-East Asia and mosaico da The first setbacks and the nevuras in Brazil. It is also held to be responsible for evolution of chemical control in the the spread of another disease, anthocyanosis, in the South American continent (vermelhao) (Costa, 1956), 1990s and in India (Mali, 1978). Without control of the vec- The failure to control sucking-piercing insects by tor, damage to certain varieties can be considerable, leaf spraying (aerial or ground treatment using manual as is shown by observations performed in Paraguay techniques) and a correlated increase in economic and Vietnam; this is why the thresholds for insecticide losses, led cotton sector stakeholders, and especially spraying are sometimes very low, as in the Mato Grosso scientists, to revise their intervention strategy, taking the in Brazil. B. tabaci is the vector of more than 70 virus biological and ecological characteristics of the insects diseases that affect numerous plants (Hunter and into account, but still using a chemical approach: in- Polston, 2001). Although it has been confirmed that it creasing the volume of mixture applied to better con- can be the vector of at least seven virus groups (Duffus, tact the pests beneath the leaves, the development of 1987), the spread of geminiviruses is the most frequent. insecticide treatments of seed, treatments triggered In cotton, these diseases are known as Cotton Leaf according to specific thresholds, etc. Crumple Virus, described in the United States in G. hirsutum (Brown and Nelson, 1984) and CLCuV, men- However, in spite of the switch from directed con- tioned in the Sudan in G. barbadense and described trol to supervised control, a glimpse of the limits of

1180 World Cotton Research Conference-3 2003 Cape Town - South Africa chemical control was preceded in the setbacks observed In addition to the limits of its efficacy, chemical in the control of aphids and whitefly (Kuklinski and protection against aphids and whitefly has other major Borgmeiser, 2002), the appearance of phenomena of disadvantages. Like many substances used in resistance to insecticides in both A. gossypii (Gubran et phytopharmacy, the active substances for controlling al., 1992; Sun et al., 1994; Deguine, 1996; Moores et aphids and whitefly have toxic effects on non-target al., 1996; Herron et al., 2001) and B. tabaci (Moores insects and especially beneficial parasitic or predatory et al., 1988; Dittrich et al., 1990; Ahmad et al. 2000), insects. The role of indigenous beneficials is now well the appearance of new diseases and the maintaining recognized. Even if it does not seem sufficient to con- or even increase in population levels and damage. trol outbreaks of Homoptera pests it should be con- Meanwhile, the first integrated protection measures served as much as possible. The same active sub- based on cultural, varietal and biological techniques stances, which was often used for homopteran control were proposed and sometimes applied but without it (such as monocrotophos, omethoate, dimethoate or being always possible to evaluate their efficacy (Butler metamidophos) generally display high toxicity for man and Henneberry, 1994; Leclant and Deguine, 1994). and the environment (ground water, wild fauna) and are increasingly subjected to restrictions, or even the The calling into question of withdrawal of registration, in many countries. chemical control It is now clear that chemical control applied un- The initial recommendations for the chemical der the conditions described above is, if not totally un- control of aphids and whitefly were often taken under suitable for these new pests, at least far from attaining emergency conditions. Use was made of the experi- the level of efficacy expected or acceptable. This situa- ence of protection against well-known cotton pests and tion has considerably disturbed cotton sector stakehold- especially bollworms, whose bio-ecological character- ers, by calling into question well established habits and istics are nevertheless very different. The inappropri- confidence in “all chemical” solutions. ateness of these chemical control techniques for the management of these sucking-piercing insects lies above all in their bio-ecological properties that are The present phytosanitary clearly different from those of cotton bollworms. situation: analysis, consequences and prospects A. gossypii and B. tabaci are insects that live and feed on the undersides of leaves. They are thus physi- The reasons for the change in the cally protected from applications of insecticides whose status of these new pests the micro-droplets fall on the upper faces of the leaves Populations of sucking-piercing insects in cotton by gravity. The phenomenon is aggravated by the fact depend directly on abiotic factors, such as climate, and that spraying is often performed with small volumes of they interact with the plant environment and ecosys- mixture per hectare, whether by ground or aerial tech- tems in the vicinity (Figure 1). Recent outbreaks of these niques (ultra low volume and very low volume spray- insects result from the upsetting of the previous bal- ing). Furthermore, the systemic properties of some of ance between them, their environment and their set of the insecticides used are increasingly weakly expressed natural antagonists. The reasons for this imbalance from the beginning of flowering and then reduce rap- are described below, although it is not easy to rank idly. The targets are then not contacted. In addition them or to be sure that they are exhaustive. the strong multiplication capacity of these piercing-suck- ing insects can very rapidly compensate for the pos- A reminder of the bio-ecological characteristics sible reduction of their numbers as a result of the ac- of these insects should first be made. The strong in- tion of insecticides. For example, it has been shown in traspecific variability of both species is important (aphid central Africa that the progeny of a single aphid can clones and whitefly biotypes) as a favorable factor for attain several thousand individuals in only two weeks their adaptation to changed or different environmental (Deguine and Leclant, 1997). Similar comments can conditions. The destruction of populations of their natu- be made concerning the speed of infestation of a field ral antagonists by pesticides also favors outbreaks. from host-plants or neighbouring crops. For example, Abiotic environmental factors are important and in even if it is supposed that a spray can totally annihilate particular the shortage of rainfall observed in many the whitefly population of a field of cotton, only a few tropical regions since the 1970s. It has been estab- hours are required for massive infestation to high lev- lished that this climatic factor, combined with high tem- els from populations along the edges or in neighbor- peratures, is favorable for the development of sucking- ing fields, especially when a low persistence whitefly piercing insects. pesticide is used (Deguine et al., 1998). Finally, it is essential to remember that both of these insect species The evolution of agricultural practices should also have the capacity to develop insect-resistant popula- be taken into account. The increase in the areas under tions, whether these consist of aphid clones or a white- cotton and the development of other crops such as veg- fly biotype. etables, have considerably increased the food resources available to aphids and whitefly. This evolution has

1181 Aphid and whitefly management in cotton growing: Review and challenges for the future

had an effect at all levels - local, regional and conti- There should thus first be a break with the proce- nental. dures and habits used for the past twenty years or so to control the damage caused by piercing-sucking insects The changes in crop management sequences, to prevent an aggravation of the problem. Such a cultural practices and crop protection procedures have change requires a change in the mentalities of all the also contributed to upsetting the previous balance in stakeholders in the cotton sectors, and especially those entomofauna. The increase in inorganic fertilizer doses, of research scientists (who should agree to re-orient especially nitrogen fertilizer, causes substantial foliar their lines of research), extension agents (who should masses of excellent nutritive quality, favoring the es- agree to favor long-term rather than short-term mea- tablishment of large populations of piercing-sucking sures) and growers (who should accept the presence of insects. Low-volume crop spraying techniques (ULV and a certain level of pests in their fields). VLV), whether aerial, ground-based or manual, do not cover the undersides of leaves sufficiently and are there- Adopting a new approach and fore not suited to the pests that live there (aphids and practices that enable a return to a whitefly and also mites, bugs, etc.). Furthermore, some balanced situation of the active substances used, such as pyrethroids, have In the future, the aim of rational (supervised) only limited efficacy on these insects in the tropics. The management of agro-ecosystems should be that of re- choice of varieties grown is doubtless not the most fa- ducing the populations of potential pests to levels that vorable for the conservation of populations of are economically bearable for the crops in question beneficials. The hairiness of varieties, chosen for re- and also take environmental or social considerations sistance to other pests such as jassids, affects the activ- into account (Figure 2). In the light of unfortunate past ity of the natural antagonists of aphids and whitefly, experience, it has become necessary to manage popu- making these varieties more susceptible to the latter lations and no longer hope to eradicate them, discard- (Baloch et al., 1982). Conversely, smooth varieties ing the easy chemical protection reflex and above all enhance the establishment and growth of populations anticipating the appearance of risk by means of a set of the piercing-sucking insects themselves. In addi- of agronomic techniques resulting in a sustainable pro- tion, some varieties have strong vegetative growth, in cedure. Preventive measures thus gain a greater im- particular to enable the formation of quality lint in the portance. This phytosanitary diagnosis is not specific bolls and therefore have a high leaf index, which is to cotton growing, which is just one example among attractive to phyllophagous insects. The massive, some- others. In all cases, consequences of practices that times anarchic, use of insecticides on vegetable crops ignore the biological bases of the functioning of eco- that often adjoin or are intercropped with cotton, where systems can be disastrous for both the economics and the farmers are little supervised, aggravates the gen- sustainability of production and for the protection of eral imbalance observed between piercing-sucking in- human health and the environment as a whole. The sects and their natural antagonist. These practices are attention paid to this particular example, because of also such as to favor the appearance of resistance phe- the outbreaks of pests that are both the vectors of dis- nomena frequently induced by the intensification of in- eases of a major world-wide crop and also have the secticide spraying. Programs for resistance manage- facility for acquiring resistance to insecticides, provides ment are often proposed but they are also something clear arguments for those who recommend a revision of a constraint for users. Palumbo et al. (2001) give of the present phytosanitary strategy (Ferron, 1999). some examples for B. tabaci.

As an example, we know the unfortunate conse- Breaking with past practices or quences of the first green revolution on outbreaks of habits to prevent a worsening of rice brown plant-hopper, Nilaparvata lugens (Stal), re- the situation sulting from the secondary effects on beneficial fauna of the increased use of pesticides required by the culti- The crop health situation, already considered to vation of varieties selected for their high yields. This be critical, may worsen unless appropriate control tech- hopper suddenly became a pest of great economic niques are instigated rapidly. These piercing-sucking importance in Indonesia when cropping intensification insects could become even more dangerous than they had been in progress for only half a dozen years (Oka, are today through both an increase in outbreak levels, 1991; Teng, 1994). Today, a ‘doubly green revolution’ a generalization of resistance to insecticides or by the (Annex 1) is being launched on an ecological basis, selection of new biotypes, which are vectors for dis- which rehabilitates the determinant role of indigenous eases or syndromes that are more damaging than those beneficials. known today. Before the recent outbreaks, aphids and whitefly were in ecological balance with their natural As rice growing is ancestral in the Asian regions enemies in various cropping systems. The changes in concerned, it can reasonably be supposed that a bal- their environment, caused in particular by inappropri- ance gradually became established between popula- ate farming practices, have destroyed this balance. tions specific to this particular agro-system and that the return to supervised agricultural practices has en-

1182 World Cotton Research Conference-3 2003 Cape Town - South Africa abled a return to the initial state (Settle et al., 1996). true specification, aiming at ensuring the profitability Comparable results have nevertheless been obtained and hence the sustainability of the farm, conservation in agro-systems that are a priori less favorable (orchard of the agronomic potential of the land and the main- fruit crops and protected crops) (Blommers, 1994). The taining of indigenous biological systems in accordance United Nations conference in Rio de Janeiro (1992) with the sustainable development concept. crystalized for the first time an awareness of the im- perative that the biosphere be reserved for the future Account will be taken of the most varied experi- development of human activities. The impact of agri- ences, taking account of their reliability, in the design culture on the conservation of biological diversity, rightly of the approach in a real situation. Although not a considered to be the driving force of ecosystems, was reference or an objective, given the profitability con- stressed in particular and illustrated by the new sus- straints that it induces, organic farming in cotton grow- tainable development concept. ing displays in most cases a marked decrease in the severity of the problems raised by piercing-sucking in- An evolution in crop protection is therefore es- sects and the damage that they cause (Myers and sential and is the subject of forward-looking reflections Stolton, 1999; Boguslawski and Basedow, 2001). that give a proper place to pesticides in an overall inte- grated production strategy (Ferron, 2003). Preventive measures As the object is the avoiding of phytosanitary risks, The bases of sustainable control measures therefore aim at preventing popula- management of the populations of tions of organisms that are potentially harmful for crops piercing-sucking insects from causing economically significant damage. They are based on proved agronomic techniques that have The procedure and the stages generally been abandoned in favor of the systematic use of inputs. Crop rotation, cropping plans, choice of These observations, experience and reflections resistant varieties, tillage operations, prophylaxis, ra- are used to propose the basis for the sustainable man- tional fertilization, trap crops and intercrops, etc. are agement of these piercing-sucking insects. It is based all techniques aimed at the simultaneous creation of on the integrated pest management concept in a con- unfavorable conditions for crop pests and favorable text of sustainable agriculture with an attempt at recon- conditions for their antagonists. They have recently been ciling the advantages of two different strategies. One rehabilitated both by the International Organization for of these is considered as a priority and favors an eco- Biological Control (Boller et al., 1998) and by the Glo- logical approach to population regulation and thus bal Crop Protection Federation (GCPF, 1997). Recent considers the agro-system as the level for organization knowledge of the dynamics and genetics of fragmented and preventive intervention. The other is based on the populations (very common in farming systems) and the curative use at field level of varied techniques includ- recent momentum given to research on biological di- ing the application of easy-to-use, relatively inexpen- versity, strengthen these aims by awarding them scope sive, synthetic pesticides that are very effective but have for application broader than the boundaries of the cul- low selectivity and should only be used as a last resort. tivated field, with consideration of the farm as a whole, surroundings included, or even different farms with the The success of such an approach can clearly only same cropping systems within a given territory (Dron be assured by the strict respect of a single, truly inte- and Ferron, 2002). grated approach, every stage of which must be com- pleted before starting the next, making it very difficult In the particular case of aphids and whitefly on and restricting for farmers applying it. This, therefore cotton crops, preventive strategies can be envisaged at require basic training, technical assistance and deci- field and cropping system level and for the farm as a sion aids that are of high quality. whole.

The initial stage of this integrated strategy is First, we will consider a strategy enabling the plant aimed at reducing phytosanitary risks as much as pos- to escape attacks by its piercing-sucking pests at the sible by means of a set of preventative agro-technical scale of the field and the annual cycle, in particular by measures updated using the most recent knowledge of limiting their incidence at both the beginning and the the dynamics and management of populations. The end of the season by means of the following techniques: second stage is aimed at a diagnosis of the sanitary • Installing the crop as rapidly as possible by early state of the field and its environment, and possibly of sowing in order to limit in time the coinciding of the the whole farm or farms using the same cropping sys- physiological stages of the plant that are the most tem and therefore requires knowledge of the attractive and the most susceptible on the one hand phytosanitary risk in a given socio-economic context. and of these insect populations of the other (Slosser The third and last stage is curative and aimed at per- et al., 1992; Parajulee et al., 2002). The techniques forming the intervention measures that are the least enhancing the rapid installation of the crop are di- harmful for the environment (for human health and rect drilling on plant cover (DMC) (Séguy et al., biological diversity). It therefore forms as a whole, a

1183 Aphid and whitefly management in cotton growing: Review and challenges for the future

1998) or after limited tillage. This reduces the time less that this pathway has already been explored in required for preparation and installation of the crop Mali to reduce the damage caused to sorghum by head (Torrey et al., 2000). These procedures are increas- bugs (Ratnadass et al., 2002). However, cotton grow- ingly successful around the world, especially in cot- ing is perhaps suitable study material for such investi- ton growing (Séguy et al., 2003). gations, given the diversity of the insect fauna associ- • Shortening the sowing to fruiting period in the ated with it and its different forms in smallholding agri- same way using techniques such as the choice of culture on the one hand and industrial farming on the varieties with shorter cycles; limited vegetative other (Mensah, 1999; Parajulee and Slosser, 1999). In growth; synchronous fruiting lasting for a short time; the latter case, the juxtaposition of vegetable crops and judicious choice of sowing density; coating seed with cotton is certainly an example that is particularly diffi- systemic insecticides;, use of growth regulators, etc. cult to manage but that holds rich lessons. Such solutions have already been adopted in var- ied agro-ecological situations. In addition to the Finally, such preventive measures for aphids and DMC cropping systems in the Mato Grosso in Bra- whitefly only make sense if they are applied for a long zil mentioned above, those of the Ultra Narrow Row period of time in a given situation. Cotton (ULNR) type in the United States (Heitholt et al., 1993) optimize interaction between high sow- The use of cotton plants genetically engineered ing density and plant architecture and size by fa- to express genes for resistance to pests forms a logical voring fast mechanical harvesting. In sub-Saharan part of this preventive approach. Indeed, with the res- Africa (Deguine et al., 2000; Lançon et al., 2003), ervation that the preliminary results obtained in the the rapid installation of the crop under rainfall con- United States with varieties expressing the ditions that are nonetheless limiting is inspired by entomopathogen toxin of Bacillus thuringiensis be con- the same principles. firmed (Carriere et al., 2001; Shelton et al. 2002), the • Shortening the period during which dehiscent use of cotton varieties genetically modified for resis- bolls are exposed to honeydew excreted by aphids tance to certain pests (‘Bt’ against Lepidoptera for ex- and whitefly, if necessary by means of the curative ample) could bring a substantial decrease in insecti- techniques described below but also by early or frag- cide sprays. Questions about possible outbreaks of mented harvesting or by the choice of varieties; or mirids and pentatomids induced by the removal of in- rapid defoliation facilitating and speeding up secticidal application might thus be answered (Greene manual picking (large bolls making picking easier) and Turnipseed, 1998). Under these conditions, we or by mechanical harvesting (plant architecture and might expect a decrease in the selection pressure ex- grouped fruiting required). erted on beneficials that control piercing-sucking in- • Limiting the food resources available to pests at sects. However, appropriate research programs would all times during the cotton season by the selec- be necessary to reveal this property and it would be tion of varieties whose foliage is less palatable and necessary to demonstrate that the overall biological less nutritive both in terms of quality (e.g. leaf color diversity of the agro-ecosystem considered is not af- or texture and high amino acid and sugar contents) fected by this new agronomic practice. Certain recent and quality (leaf area index, leaf shape and size) observations should nevertheless be taken into account; and by appropriate management of organic fertili- these show that piercing-sucking pest populations can zation (Balasubramanian and Mulibaskaran, 2000) increase substantially and become dominant in and inorganic fertilizer, especially nitrogen (Bi et al., transgenic (Bt gene) cotton growing; this concerns both 2001; Nevo and Coll, 2001; Cisneros and Godfrey, B. tabaci (Wilson et al., 1992) and A. gossypii (Cui and 2001; Crafts Brandner, 2002) and of water supply. Xia, 1999 and 2000). Good management of crop residues that may har- bor piercing-sucking insects for several days is also With regard to work on transgenic plants express- recommended. ing a gene of interest for resistance to aphids or white- fly, it is probable that some of the research undertaken Preventive strategies can also be recommended is still confidential, not known, not yet published and at the different scale of cropping system, or even farm. insufficiently confirmed in situ. Much research has been These are aimed at limiting pest outbreaks while favor- performed in Bt strains effective on bollworms but none ing the populations of beneficials through choice of was found to have great direct efficacy on piercing- rotations and cropping plans; rational combinations sucking insects. Today, research on the transfer of genes of crops (Gabr and Sourial, 2001); the introduction of of interest in aphid control mainly concerns lectins trap crops for pests and refuge plants for beneficials; (Rabhé et al., 1995), especially GNA (Glanthus nivalis ‘push-pull systems’ (Nielsen, 2001) and the manage- agglutinin), that causes a certain delay in growth and a ment of reservoir plants between seasons, are all path- decrease in the fertility of several aphid species (Hilder ways to be explored. It is doubtless still premature to et al., 1994; Stoger et al., 1999). There is also Vat encourage farmers to reconsider the shape and area gene in melon (Pitrat et al., 1982), but this has yet to of their fields to enable the optimum regulation of pest be transferred to other plant species or to cotton. Other populations by their indigenous beneficials in a natu- lines of research include work on the OC-I gene (pro- ral biological control approach. It is noted neverthe- tease inhibitor) conducted on A. gossypii and other

1184 World Cotton Research Conference-3 2003 Cape Town - South Africa aphids (Rabhé et al., in press), and the Mi gene envis- Diagnosis and decision aid aged in the control of Macrosiphum euphorbiae (Rossi Population monitoring has a special position in et al., 1998). In all cases, a rational strategy for the such a context, as it makes it possible to determine the use of aphid-resistant transgenic cotton plants should risk of crop damage and, if this is such as to compro- be set out and adopted before its application in the mise the revenue expected from the harvest, the need production environment (Gatehouse et al., 2000). Little for curative interventions. In countries with intensive information on whitefly is available. Few trials on agriculture, warning systems alert stakeholders when transgenic plants such as tobacco are of relevance to such risks are forecastable on the basis of data sup- B. tabaci. There is work on the use of protease inhibi- plied by a local observation network. It is then up to tors for Manduca sexta (Thomas et al., 1995a and the farmers themselves to monitor the sanitary state of 1995b). each of their fields to validate the warning or not. This individual approach requires the provision of simple Among the other research pathways using bio- diagnosis criteria for both the identification of insect technologies, selection assisted by molecular markers pests and for the evaluation of their numbers. These from a resistance donor deserves mention, even though observations should therefore be related to the eco- few results on cotton whitefly and aphids have been nomic thresholds established in principle for each re- published. Certain work has been undertaken indi- gion according to market conditions and biological and rectly with a view to preventing virus diseases, for ex- technical parameters and beyond which direct control ample blue disease spread by A. gossypii or leaf curl or curative measures must be triggered. This is consid- virus and geminiviruses spread by B. tabaci (Lacape, ered to be a fundamental approach by both users of personal communication; Liu et al., 1998; Lapidot and supervised protection and those of integrated pest Friedmann, 2002). Genes of resistance to the viruses management (Audemard, 2003). It implies the train- are identified and marked in both cases and ing and supervision of farmers. A recent study in Thai- introgressed by marker-assisted selection. The chal- land on the obstacles to be overcome to promote an lenge for the future in this domain is the screening of IPM strategy for cotton is a good example of this variability in the genus Gossypium, in wild species and (Castella et al., 1999). tetraploid types, many of which are reported to be ‘re- sistant’ to different insects. Molecular markers will in The design and development of techniques for any case enable easier interspecific genetic transfers. estimating aphid and whitefly populations has been the subject of much research work. The solutions proposed The same approach can be envisaged for other concern the winged forms of whitefly (Munir and resistance characters that can be introgressed from Muhammad, 2002) and aphids (Moericke, 1957; Byrne cotton species other than Gossypium hirsutum, such as et al., 1986; Deguine and Leclant, 1996; Chu and G. barbadense or G. arboreum (Reed et al., 1999; Henneberry, 1998), the mobile or fixed apterous forms Deguine and Hau, 2001). Cultivars harboring smaller and larvae of aphids (Slosser et al., 2002) and whitefly aphid populations have thus been identified; this can larvae and nymphs. The implementation of these tech- be related to a lower amino acid and sugar content in niques has improved our knowledge of the monitoring plant tissue. in space and time of the populations studied. Under- standing their dynamics according to relevant biotic and In conclusion, the importance to be awarded to abiotic factors has been made easier in both space the space-time dimension of the biological factors stud- and time, thus enhancing the development of integrated ied for rational (supervised) management of popula- pest management for these insects. In particular, the tions should be stressed. It is obvious that the prepon- demonstration of the mechanisms of their movements derant, determinant role thus awarded to preventive at different scales—from crop field to continent—has measures in this new crop protection strategy implies been important for the management of their popula- the integration of approaches by pesticide specialists tions. and agronomists. This has doubtless not been sought sufficiently to date (Papy, 2001; Ferron, 2003). These The design and development of a technique for considerations conform perfectly with the recommen- trapping winged forms of A. gossypii in sub-Saharan dations of Hilje et al. (2001), who award a major po- Africa provided two levels of decision aid. Firstly, the sition to agronomic methods in the prospects for suc- dynamics of the first captures in the immediate proxim- cessful management of B. tabaci populations on sev- ity of a crop field makes it possible to predict an out- eral crops. break at the beginning of the vegetative cycle two or three weeks ahead (a good length of time for the choice The revised management of weeds which may of a management method appropriate to the local situ- be considered positively as habitats for beneficials, ation). Secondly, trapping on a countrywide scale in would doubtless be a complementary future approach Cameroon revealed that the populations in a crop fields (Norris and Kogan, 2000). are partly indigenous and descend from local clones and partly of southern origins several hundred kilome- ters away (Deguine and Leclant, 1996). This informa-

1185 Aphid and whitefly management in cotton growing: Review and challenges for the future

tion can then be usefully incorporated in strategies to gible if aerial chemical treatments are applied in a non- prevent the development of possible resistance to in- supervised approach (Naranjo, 2001; Kuklinski and secticides. Borgmeister, 2002).

The development of cotton tolerance thresholds The priority awarded to preventive measures is makes it possible to make an objective diagnosis of therefore all the more justified and it is recommended the phytosanitary state of the crop and therefore to that maximum efforts should be made in this field. Pro- decide whether or not supervised curative interventions vided that population levels are forecast objectively by are necessary, for both B. tabaci (Chu et al., 1994) trapping alates or counting individuals, the basis of and A. gossypii (Gozé and Deguine, 1998). In situ supervised curative interventions can be predicted from counts of populations and also of the relative propor- the beginning of the season. Such interventions in- tions of plants or vegetative organs infested are used clude the use of suitable pesticides for a significant re- for this. However, this diagnosis is little used in prac- duction in the populations of aphids and whitefly and tice because of the small impact of supervised chemi- of the damage that they cause; treatments based on cal control of the populations of these piercing-sucking natural or synthetic oils or detergents to reduce the risk insect pests of cotton. Certain decision-aid models of viral infection or the use of formulations based on nevertheless attempt to take these pests into account in plant extracts (such as neem (Azadirachta indica) for an overall approach to the handling of crop manage- example) (Kaadeh et al., 2001; Mann et al., 2001). If ment sequences, but their use is still limited. the preventive measures recommended are found to have been insufficiently effective at the end of the sea- Curative measures son, the following techniques can be planned accord- Although it is indeed necessary to use curative ing to thresholds and the risk of sticky cotton: early techniques, the upholders of supervised protection rec- harvesting or staggered harvesting; manual or me- ommend the choice of methods from the range of non- chanical defoliation or topping of the plants; the chemical procedures available and then, if necessary, application of large quantities of water (Arnold et al., choice among the range of active substances autho- 2002) [washing with water is sometimes envisaged to rized for spraying. In the latter case, it is strongly rec- control A. gossypii on ornamental plants (Stoyenhoff, ommended to choose an active substance reputed to 2001)] or, as a last resort, supervised chemical defo- be the least harmful for the environment. It is known, liation. Chemical control is unsuitable at in the end of unfortunately, that farmers in most countries do not re- the season as farmers are little inclined to make the ally have the choice, even in the so-called developed outlay when the harvest is assured. It is also often inef- countries, and this reduces the scope of this strategy. fective. During this period, the easing up of chemical Supporters of IPM should give priority to the alternative control is also very favorable for enhancing the regu- control measures available to them. Some award an lating role of indigenous beneficials whose numbers increasingly large role to physical control measures: increase. Orozco-Santos et al. (2002) for A. gossypii and B. tabaci, and Vincent et al. (2003) in a more general Several initiatives for the integrated management manner for insects. These practitioners aim at the of piercing-sucking insect populations on cotton have maximum conservation of indigenous beneficial fauna been made in recent years on the basis of the observa- and the use of chemicals is only tolerated as a last tions mentioned above (Hardee et al., 1994; Kogan, resort! There are few alternative measures (biological 1995; Butter and Kular, 1999; Ellsworth and Martinez- control, biotechnological and ethological methods, Carillo, 2001; Sharma et al., 2001; Deguine et al., in autocidal control) suited to particular biological and preparation). agronomic conditions and these are too seldom avail- able (Blum, 2002). All the stages in the approach and the measures proposed are summarised in Table 1. One of the ma- Cotton is no exception. Most of the techniques jor difficulties of the integrated management strategy for protection against aphids and whitefly are chemi- is that of taking ensuring the compatibility of the differ- cal. The use of entomopathogenic fungi, predators ent control techniques used for each of the major pests, and parasitoids found suitable for greenhouse crops bearing in mind the obligation to conserve biological or special production systems are rarely successful in diversity and the environment as a whole. This inte- field cotton crops. This is clearly illustrated by recent grated approach concerns all the sectors of crop pro- syntheses of examples of the control of B. tabaci by tection from entomology to plant pathology and weed fungi (Raria and Wraight, 2001), predators and para- science. It is thus necessary to be informed not only of sitoids (Gerling et al., 2001) and of A. gossypii in Aus- the nature of the secondary effects of commercial ac- tralia (Waterhouse and Sands, 2001). Aphids and tive substances but also to possess accurate knowledge whitefly have a great number of natural antagonists, of the precise functioning of the ecosystems in question whether entomopathogenic fungi, predators and para- to achieve truly rational supervised management. sitoids (Deguine and Leclant, 1997; Butler and Mastery of the situation in the case of crops like cotton, Henneberry, 1994), but their impact becomes negli- that are subjected to particularly strong and varied pest pressure, is very difficult and requires not only farmer

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• Sun, Y.Q., Feng, G.L., Yuan, J.G. and Gong, K.Y. • Zou, C., Yang. X., Chen, X. and Li, Y. (2001). Study (1994). Insecticide resistance of cotton aphid in on geographic population differentiation of cotton North China. Entomologia Sinica, 11: 242-250. aphid, Aphis gossypii, using repeat sequence prim- • Teng, P.S. (1994). Integrated pest management in ers PCR. Entomological Knowledge, 3838: 348-351. rice. Experimental Agriculture, 3030: 115-137. • Thomas, J.C., Adams, D.G., Keppenne, V.D., Annex 1. Wasmann, C.C., Brown, J.K., Kanost, M.R. and Bohnert, H.J. (1995a). Protease inhibitors of Several definitions and details of Manduca sexta expressed in transgenic cotton. Plant Cell Reports, 1414: 758-762. concepts • Thomas, J.C., Adams, D.G., Nessler, C.L., Brown, J.K. and Bohnert, H.J. (1995b). Tryptophan Decar- Integrated controlcontrol: Pest management system that boxylase, Tryptamine, and Reproduction of the in the context of the associated environment and the Whitefly. Plant Physiology, 109109: 717-720. population dynamics of the pest species, utilizes all suit- • Torrey, K., Fife, H., Leonard, B.R. and Hutchinson, able techniques and methods in as compatible man- R.L. (2000). Effect of conservation tillage systems ner as possible and marinating the pest populations at on cotton aphid populations Proceedings of the Sec- levels below those causing economic injury. (FAO, ond World Cotton Research Conference. Athens 1967). (Greece), September 6-12, 1208-1209. • Toscano, N.C., Castle, S.J., Henneberry, T.J. and Integrated Production (Integrated Farming)arming): Prabhaker, N. (1998). Invasions by Bemisia and its Farming system which integrates natural resources and exploitation of agricultural systems. In Mayer R.T. & regulation mechanisms into farming activities to achieve Maxwell D.P. (eds.). 2nd International Workshop on maximum replacement of off-farm inputs, secures sus- Bemisia and geminiviral diseases. June 7-12, San tainable production of high quality food and other prod- Juan, Puerto Rico. L-6. ucts through ecologically preferred technologies, sus- • Vanlerberghe-Masutti, F. and Chavigny, P. (1998). tains farm income, eliminates or reduces sources of Host-based genetic differentiation in the aphid Aphis present environmental pollution generated by agricul- gossypii Glover from RAPD fingerprints. Molecular ture and sustains the multiple functions of agriculture. Ecology, 77: 905-914. (OILB/SROP, 1993). • Vincent, C., Hallman, G., Panneton, B. and Fleurat- Lessard, F. (2003). Management of agricultural in- Green RevolutionRevolution: The Green Revolution has sects with physical control methods. Annual Review tried to fight against poverty and food shortages by of Entomology, 4848: 261-282. selecting varieties and improved production systems, • Waterhouse, D.F. and Sands, D.P. (2001). Classical by the massive use of fertilizers and pesticides. Its im- biological control of arthropods in Australia. ACIAR pact was very important but only in countries with high Monograph, 7777: 560 p. production capacity, water surpluses and high popula- • Wilson, F.D., Flint, H.M., Deaton, W.R., Fishhoff, tion density. Griffon (1995). D.A., Perlak, F.J., Armstrong, T.A., Fuchs, R.L., Berberich, S.A., Parks, N.J. and Stapp, B.R. (1992). Doubly-Green RevolutionRevolution: The aim of the Dou- Resistance of cotton lines containing a Bacillus bly-Green Revolution consists of changing the agricul- thuringiensis toxin to pink bollworm (Lepidoptera: tural development rationale based on the control of Gelechiidae) and other insects. Journal of Economic the environment to another based on the harmony with Entomology, 8585: 1516-1521. the ecosystems: working with and not against the vari- • Wool, D. and Hales, D.F. (1997). Phenotypic plas- ability of systems and making agriculture profit from ticity in Australian cotton aphid (Homoptera: the knowledge acquired by the ecological sciences. It Aphididae): host plant effects on morphological aims to increase production without depleting the envi- variation. Annals of the Entomological Society of ronment or affecting the bio-diversity for future gen- America, 9090: 316-328. erations. It also seeks to alleviate poverty and decrease • Zhang, R., Ren, L.Z.G. (2000). On the manage- food insecurity guaranteeing economic viability and ment strategy of cotton aphid in Xinjiang cotton social equity. Thus, the Doubly-Green Revolution re- fields. Chinese Journal of Biological Control, 1616: quires an interdisciplinary, intersectorial and spatial 183-185. approach Griffon (1995).

1192 World Cotton Research Conference-3 2003 Cape Town - South Africa

Table 1. Integrated management of populations of piercing-sucking insects (aphids and whitefly) in cotton growing.

1193 Aphid and whitefly management in cotton growing: Review and challenges for the future

Table 1. Contd.

Figure 1. Spatio-temporal relations between piercing-sucking insects (aphids and whitefly) and their environment (modified, after Audemard, 2003).

Figure 2. Schematic representation of the evolution of situations of balance or imbalance between populations of piercing-sucking pests in cotton growing and their environ- ment and the evolution of tolerance thresholds for the farmer.

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