v. Integrated pest manag techniques and resource

Cotton growers generally rely on chemical treatments to control serious infestations by a wide range of pests, as immediate visible results can be obtained. There are many risks associated with repeated pesticide treatments, e.g. upsetting the established fauna balance, development of pesticide resistance, possibility of intoxicating farmers, and environmental pollution. For several years, CIRAD entomologists have been conducting studies in cotton fields with the aim of limiting pesticide use through development of an integrated approach to pest management involving various control techniques. Harvest debris in a cotton field. Photo CIRAD-UREA

otton crops are threatened by Chemical pest control is still essential a very wide range of pests, in many agrosystems. Nevertheless, to reduce the dependence on pesti- C with a list of more than 70 cides for crop protection, adapted pest species — mainly cropping techniques, plant varieties homopterans (jassids, aphids and with insect-tolerant traits, entomo- whiteflies), heteropterans (bugs and phagous , entomopathogenic minds), lepidopterans (leaf- and boll- agents and chemical mediators eating worms) and coleopterans, as should be taken into serious conside- well as mites (Tarsonemidae and ration. Tetranychidae), diplopods and

M. VAISSAYRE, J. CAUQUIL, P. SILVIE nematodes (Table 1). In tropical This review mainly focuses on CIRAD-CA BP 5035 , there can be losses of 30% to CIRAD projects under way in tropical 3 4 0 3 2 Montpellier Cedex 1, 100% of the crop yield potential due Africa, as well as Latin America and ______Frcmce t o in f e s t a t i o n s of th e s e pest s. Southeast .

Agriculture et développement ■ SpeCtQÜ/Issitó - November 1997 ement s

A larval Asopinae insect preying on a Spodoptera littoralis worm. Photo CIRAD-UREA

Cultural practices Intercropping Fertilization In some countries, hardy cotton spe- A few studies have highlighted that This involves all crop management cies (often Cossypium arboreum L.) interactions between fertilization and practices: sowing, intercropping, are intercropped with other annual or crop protection techniques can be planting density, weeding, monito- perennial crops in traditional cotton complementary, i.e. crop protection ring plant growth and fertilization. cropping systems. This practice has programmes adapted to the crop continued with the introduction potential have to be set up to enhan- of G. hirsutum L., especially ce the cost-effectiveness of fertilizer in Southeast Asia (CROZAT Plant and pest life cycles inputs (JOLY, 1980; CRETENET & et ai, 1997). Although there have not VAISSAYRE, 1986; EKUKOLE, 1992). Cotton growth and development been many investigations on the pest cycles should be monitored in terms control impact, it seems that inter- of the dynamics of the pest popula- cropping various crop species with tion present. In addition, the flowe- cotton can alter the population dyna- Destruction of harvest ring period, factors prompting the mics of some pests (i.e. favouring debris fall of flowering and fruiting organs, insects, or attracting them away from and the plants' compensation poten- cotton plants), or boost beneficial The traditional practice of destroying tial should be generally understood insect populations (NIBOUCHE, harvest debris can be very efficient when making treatment decisions. 1995; SOGNIGBE, 1989). when there is a well-defined interval between crop seasons. Pests adapt to In the African areas studied, plants the absence of their host plants by sown early generally yielded the Weed control undergoing diapause or migrating to most cotton because of the favou- other hosts or sites. The reduced rable climatic conditions. However, DEGUINE (1995) began an inventory number of host plants during the dry another type of crop is planted at the of refuges of beneficiais for control- season or the cold season reduces the beginning of the crop season, to ling A. gossypii populations in nor- survival potential for species that thern Cameroon. Although weeds avoid cotton pest attacks. cannot easily migrate. can shelter pest populations in crop- In central Côte d'Ivoire, before the fields, they can also serve as a reser- Populations of monophagous or oli- advent of pyrethroids, farmers were voir of beneficial entomophagous gophagous insects that survive by thus advised to use the maize-cotton organisms which could, in some undergoing diapause, especially the crop sequence to control C. leuco- cases, be managed to the benefit of pink bollworm (P. gossypiella), can treta damage (ANGELINI, 1963). the cotton crop (PERRIN, 1 975). be reduced by carefully destroying

Agriculture et développement ■ SpaciQÜ/Lssitó - Novem ber 1 997 Table 1. Inventory of insects referred to in the present article. harvest debris. This is done mechani- cally with a rotary cultivator or by feeding the green plant parts to live- Family and species stock. Diapausing insects burrowed in the top soil layers can be efficient- Coleoptera Anthonomus grandis (Boheman) ly destroyed by ploughing. Any chry- Cheilomcnes sp. salides on the soil surface are gene- Exochomus sp. rally destroyed by the heat or Orthoptera Oecanthus sp. predators.

Homoptera Amrasca spp. In Africa, cotton plants are also often Amrasca biguttula (Ishida) cut up and burned. It is essential to destroy all stems and regrowth. Aphis gossypii (Clover) Indeed, some pests (homopterans) Bemisia tabaci (Gennadius) can propagate on regrowth, which Jacobiasca spp. can also shelter infectious agents Alabama argillacea (Hübner) (viruses and phytoplasms). Amsacta meloneyi (Druce) Ratooning, which is sometimes carried out by growers who have a Anagasta kuehniella (Zeller) shortage of seed, can enhance the Anomis (Cosmophila) flava (Fabricius) possibility of pest propagation and Autographa californica (Speyer) infestations. leucotreta (Meyrick) Pests can also be disseminated Cryptophlebia peltastica (Meyrick) through seeds. It is important to strict- watersi (Rothschild) ly control seed being transported (Hampson) from one ecological zone to another insulana (Boisduval) — especially to avoid disseminating pink bollworms. (Walker) armigera (Hübner) Helicoverpa zea (Boddie) Heliothis virescens (Fabricius) Varietal characters Mamestra brassicae L. A plant's resistance to pests can be of Pectinophora gossypiella (Saunders) morphological, biochemical or gene- Spodoptera littoralis (Boisduval) tically engineered (i.e. a variety Spodoptera exigua (Hübner) modified by introducing foreign plant Spodoptera exempta (Walker) genes). Spodoptera frugiperda (Smith) Spodoptera su nia (Guénée) Morphological characters - ' Syllepte derogata (Fabricius) Various morphological plant traits Hymenoptera Aphelinus albidopus (Hayat & Kausari) function as physical barriers to pests Brachymeria olethria (Waterson) or alter their development condi- Chelonus curvimaculatus (Cameron) tions. Encarsia lutea (Masi) Variations in leaf hairiness Eretmocerus mundus (Mundus) Leaf hairiness is the most commonly Gonozius sp. promoted morphological character. Microbracon kirpatricki (Wilkinson) Hairy leaves hamper the develop- Syrphophagus africanus (Gahan) ment of jassids, i.e. African Spodophagus lepidopterae (Delvare & Rasplus) (Jacobiasca spp.) and Asian (.A m r a s c a spp.) species. The efficien- Trichogramma brasiliensis cy of this trait depends on hair Trichogramma lutea (G irau It) implantation patterns, length, shape Fteteroptera Rhinocoris albopilosus (Signoret) and especially density (PARNELL et al., 1949). Leaf hairiness is detrimen- Mites Polyphagotarsonemus latus (Banks) tal to insects' feeding and oviposition Bacteria Bacillus thuringiensis behaviours. This can stall pest infes-

Agriculture et développement ■ SpiClCLÊIssitó - November 1997 coto pest tvmaqmafc

tations, which is a major advantage favour aphid development (DEGUI- during the vegetative stage of the cot- NE, 1995). According to WILSON ton plant. Cotton therefore does not (1986), under field cropping condi- have to be sprayed with pesticides, tions, this glabrous trait helps avoid and beneficial insects (which are cotton fibre contamination by plant highly active during this period) will debris, whereas the entomological consequently not be endangered. advantages are questionable.

Conversely, it has been reported that Lamina glabrous leaves can hinder oviposi- The thickness, hardness and shape of tions of some lepidopterans, espe- the lamina — with "okra-type" laci- cially the Heliothis virescens/ niate leaves — could have a role in Heteroptera armigera complex pest resistance. Some varieties with (BHAT et al., 1986). This character is laciniate leaves are now being crop- Pectinophoro gossypiella also useful for avoiding whitefly out- ped on large cotton plantations, e.g. on a cotton flower. breaks (GERLING, 1990), but can cv Siokra in Australia and cv Sudae K Photo CIRAD-UREA in Sudan. These "okra-type" leaves enable high air circulation, thus drying out pest larvae (e.g. B. t a b a c i ) and enhancing pesticide penetration. DEGUINE (1 995) focused on the im pact of this character on /4. gossypii outbreaks but found that it is not very efficient. Moreover, weed growth is favoured with this type of leaf cover as a considerable amount of light reaches the ground.

Bracts Atrophied or absent bracts, or those that are separated from the cotton boll ("frego" bracts), can hinter ovi- positioning by some lepidopterans and A. grandis infestations (ANGELI- Nl et ai, 1965; JENKINS, 1989).

Nectary glands As often pointed out, an absence of nectary glands can be beneficial, i.e. the cotton plant is not an interesting food source or attractive to certain insects (especially sucking pests). However, this character can be detri- mental since beneficial insects are also affected.

Conclusion In cotton, plant breeders have not promoted many morphological plant characters that are known to hamper pest attacks because they are often negatively correlated with technolo- gical aspects of the fiber (PAULY & VAISSAYRE, 1980).

Biochemical characters Various biochemical pest-resistant characters of cotton plants — pH

Agriculture et développement ■ SpêCtQÜ/Lssiia - November 1997 level of the cell contents, foliar tur- gescence, the plant's sugar, protein and mineral salt composition — modify pest behaviour and develop- ment. Chemical substances (gossy- pol, tannins, flavonoids) have an antibiotic effect on some pests such as H. armigera, jassids and flea beetles. In USA, many plant breeding studies are under way on these bio- chemical traits, but no significant results have been obtained to date (JENKINS, 1994).

In French-speaking Africa, there has been some success in breeding glandless cotton varieties, with the aim of promoting cottonseed and derivatives. More than 350 000 ha were cropped with glandless cotton in 1994-95. The problem is that the lack of gossypol glands weakens the plant's natural defenses, which Deltapine cultivar with "fregó" bracts. means that pest management staff Photo CIRAD-UREA have to be highly vigilant. Glandless cotton plants can be attacked by many different insect pests at the onset of the growth cycle, especially Glossary coleopterans such as Halticinae spe- cies in Africa and Chrysomelidae Antibiosis: the plant adversely affects the metabolism of the insect pest, sometimes to species in Southeast Asia the extent of killing it. (BRADER, 1967; GENAY, 1994). Antixenosis: morphological or physiological characters of the plant that have a Moreover, non-insect pests, which repellent effect on insect pests. are rare in traditional cotton cropping systems, can be Attract and kill: a concept that involves attracting the insect with a sex pheromone present with glandless varieties: birds and then killing it with a contact pesticide. during planting and rodents and Chem ical mediator: a volatile substance that provides the insect with certain other mammals during the harvest information, thus altering its behaviour with respect to host plant choices, egg-laying period. sites and sexual partners. E n to m o p ath o g en ic organism : a microorganism (virus, bacterium, fungus) that can cause diseases in insect pests. Transgenic cotton Hyperparasite: a parasite that can be parasitic to another parasite. Genes encoding toxins derived from GV: granulosis virus, where a single virion is incorporated in a protein body. the bacterium Bacillus thuringiensis M ating disruption: spraying a specific pheromone upsets male detection of females, can now be inserted in cotton plants thus reducing mating. through genetic engineering tech- NPV: nuclear polyhedrosis virus, where several viruses are incorporated in an protein niques. Genetically modified varie- body. ties are now available on the market (PANNETIER et ai, 1995). P arasitoid: an organism that lives through part of its development cycle within the body of a host insect and subsequently causes its death. Toxins corresponding to the genes Phytoplasm : microorganisms close to bacteria that are pathogenic to plants Cry lA(b) and Cry IA(c) are active (previously called mycoplasmal organisms). against the H. virescens/H.armigera complex and P. gossypiel la Pib: polyhedral inclusion bodies containing active viral elements or virions that are (MclNTOSH etal., 1990). Recent released in the digestive tract of the host insect. tests by CIRAD highlighted that Tolerance: the plant is able to withstand pest infestations, without being seriously Cry IB has a similar spectrum of acti- damaged. vity. Cry IIIA, a coleopteran-specific gene, could provide glandless cotton

Agriculture et développement ■ Sp^ClQÜ/Issitó - November 1 997 varieties with resistance to coleopte- rans in the Chrysomelidae family (SEKAR et ai, 1987).

Problems involved in introducing transgenic plants should not be over- shadowed by the positive aspects of these innovations (e.g. improvement of common varieties). There is a considerable risk that some insects will quickly develop resistance to B. t h u r in g ie n s is toxins (Me GAUGHEY, 1 985; TABASHNIK, 1994). Research programmes are pri- marily focused on insertion of genes coding for protease inhibitors, or other factors (e.g. oxidases), while attempting to minimize any possible development of resistance in the tar- Egg laying of get pest. Secondly, precautionary Trichogramma minutum on measures that should be taken when Helicoverpa armigera egg. cropping transgenic plants are being Photo CIRAD-UREA investigated in terms of mosaic crop- ping patterns, crop alternation, and refuge cropping with a mixture of transgenic and unmodified plants (GOULD, 1995).

Entomologists are also closely inves- tigating how these genetic manipula- tions could upset the balance of the pest spectrum.

Spodophagus lepidopterae preying on a Spodoptera littoralis Entomophagous larva. insects Photo CIRAD-UREA

Entomophagous insect populations evolve throughout the agrosystem, including cropfields, fallows and uncultivated host plants growing near farms.

There have been many studies aimed at identifying and enumerating auxi- liary organisms in cotton cropping systems, while also investigating their roles in reducing pest populations and assessing unwanted side-effects of pesticides on these beneficial spe- cies. Indeed, very little is known about the wide variety of entomo- phagous insects. Apanteles sagax larvae on Syllepte Entomophagous insects have been derogata. inventoried in several African coun- Photo CIRAD-UREA tries (Burkina, Cameroon, Côte

Agriculture et développement ■ SpcciO&iss^- November 1 997 d'Ivoire, Mali, Chad and Togo), and Cotton pest complexes in Paraguay (MICHEL & PRUDENT, 1987). There are reference collec- Cotton pest complexes have been reviewed by several research teams, including: tions at CIRAD (Montpellier, France), SILVIE et al., 1989; BOURNIER, 1991; DECUINE, 1991; LECOEUR & VAISSAYRE, in some countries (e.g. Togo), and at 1991 ; BAGAYOKO et al., 1993; EKUKOLE, 1993; GALVA, 1993; SILVIE et al., 1993; the International Institute of Tropical STREITO, 1994. Agriculture (I IT A) in Benin. Auxiliary organisms observed on H. armigera Data obtained on entomophagous A long list of auxiliary organisms have been identified for H. armigera but, as is the insects in French-speaking Africa are case for most pests, this list is not yet exhaustive. T. lutea, an oophagous pest of summarized in Table 2. the Trichogrammatidae family, was recently identified in Burkina. Parasitoids of S. l it to r a li s Effects of some secondary No oophagous parasites have been reported for 5. littoralis. In 1988, there was a host plants on their major discovery of a new parasite, S. lepidopterae (Pteromalidae), with unusual biological characteristics, which have been the focus of some attention (BOURNIER population dynamics & BENMOUSSA, 1993; RASPLUS & DELVARE, 1994). Possible hosts were identified Secondary host plants for bugs and by CIRAD research teams, i.e. S. t'rugiperda, S. exigua, S. sunia and H. armigera. A. gossypii were identified along the Parasitoids of P. gossypiella and 5. derogata edges of cottonfields (POUTOULI, In continental Africa and Madagascar, only a few parasitoid species have been 1994; DEGUINE, 1 995), but very reported on P. gossypiella: Gonozius sp. (Bethylidae); Apanteles sp. (Braconidae); little is known about their roles with respect to beneficial insects. B. olethria (Chalcididae), M. kirkpatricki (Braconidae), and C. curvimaculatus (Braconidae). A pest complex with a wide range of species was described for As early as 1974, PEYRELONGUE S. derogata in Chad and Togo (SILVIE, 1991 & 1993). & BOURNIER reported four parasi-

Parasitoids of A. gossypii toids of larvae and one of E. i n s u l a n a nymphs on a malvaceous plant Many different insects feed on A. gossypii. Concerning predators, DUVERGER (pers. {A. asiaticum L.) in Madagascar. comm.) drew up a map of Exochomus spp. distributions in Africa. DEGUINE (1995) In Burkina, parasitoids from pointed out the high relative numbers of ladybirds (adults and larvae) and especially H. armigera on tomato are mainly Cheilomenes spp. present in Cameroon. A. albipodus accounts for 56% of the overall Tachninidae species, whereas hyme- parasitoid population in the same country, with S. africanus (Encyrtidae) nopterans are generally noted on cot- and Encarsia sp. (Aphelinidae) representing 29% and 13%, respectively, ton. Low parasitism levels occur on of this population. tomato and cotton, i.e. less than 5% Auxiliary organisms preying on B. tabaci (NIBOUCHE, 1 994). In Togo, Apanteles spp. were observed on Exochomus sp. was observed feeding on B. t a b a c i whitefly larvae in Mali Urena lobata (Malvacae) leaves rol- (BAGAYOKO, 1989). led by S. derogata caterpillars prior Green lacewing larvae prey on some whitefly larvae, but very few entomological field to planting the cotton crop. In observations have been reported. A few parasitoids have now been identified, all Cameroon, parasitoids of A. gossypii, belonging to the Aphelinidae family: Encarsia sp.; E. l u t e a (Mali, Cameroon); usually found on cotton plants, were E. t r a n s v e n a (Benin, Burkina, Mali); E. m u n d u s (Burkina, Cameroon, Mali). detected with various bug species on cultivated plants (okra, sorghum) and

Table 2. Beneficial entomophagous insects identified in tropical Africa.

Country Number of genera or species identified Number of species identified predators parasitoids hyperparasites parasites oophagous parasites of predators

Burkina 56 69 10 8 16

Cameroon 41 27 3 - -

Mali 16 12 - --

Chad 34 63 14 15

Togo 28 45 10 1 12

Agriculture et développement ■ SpeciCtftIssue- - November 1 997 wild plants (Calotropis procera 4 7% on worms and 21-23% on Ait.R.Br.). pupa, with high hyperparasitism (70%). In the dry season, substantial infesta- tions of parasites such as A. albipo- Studies were undertaken in the dus have also been noted on other Central African Republic, Cameroon host plants. It is therefore essential to and Chad on entomophagous insects take bug species other than those that that prey on /4. gossypii (VAISSAYRE, damage cotton crops into considera- 1970; DEGUINE, 1995). On untrea- tion when assessing the population ted fields, the predator complex is dynamics of beneficial species. dominated by ladybirds (45-85% of Prey that attract predatory bugs are the sampled population), followed by also found on wild plants growing syrphids (14-37%) and green lace- near cotton plants (SILVIE et a!., wings (up to 25%). Surveys in 1993; POUTOULI, 1994). Togo and Benin revealed high local concentrations of some families such as Hemerobiidae and Role of auxiliary Chamaemyidae. These data are com- parable to those obtained by MICHEL organisms under natural (1992 a & b, 1993) in Paraguay.

conditions The dynamics of auxiliary organisms Auxiliary organisms were investiga- on /\. gossypii in western and central ted in untreated fields. Africa are well documented. Predators are active at the beginning Impact on some pest insect of the crop cycle, then a fungal disea- populations se caused by Neozygites fresenii (Entomophthorales) appears from POUTOULI (1994) reported highly August on. Parasitoids occur at the original data on oophagous parasi- end of the crop season (September, toids of bugs in Togo, where parasi- October), but their levels seem to be tism by various species ranged from too low to have a serious impact on 13% to 76%. In Burkina, samples of pest populations at this phase of the H. armigera populations were found crop cycle. to have a low rate of parasitism (1.4%), whereas pathogens induced Larval ladybird (Cheilomenes vicinia) high mortality (48.3%). In Chad and preying on aphids. The percentages of parasitism noted Togo, parasitism rates on 5. derogata PhotoJ.-P. Degu ine in Mali on B. t a b a c i showed that for various years ranged from 1 8% to auxiliary organisms actually have a

Aphis gossypii first and second instars. PhotoJ.-P. Deguine.

Agriculture et développement ■ Special Issue - November 1 997 considerable effect on crop pest high primary parasitoid populations populations: 9-23% for E. l u t e a and (e.g. S. derogata). 6-25% for E. mundus. All research conducted on the effects The effects of predators have not yet of auxiliary organisms and their prac- been seriously quantified, as their tical interest should take these inter- activities are difficult to monitor actions into account. under natural conditions. The effects of this type of auxiliary organism are Release of auxiliary also limited by parasitoids. Egg parasitism is hindered by specific organisms behavioural activities, e.g. the male In Madagascar, tests began as early predatorial bug R. a l b o p i l o s u s as 1971 on introducing auxiliary (Reduviidae) guards its eggs until organisms and rearing them for mass they hatch in order to ward off threa- propagation and subsequent release tening parasitoids. in cotton cropfields (as part of a bio- In addition, "opportunistic" predators logical control programme). The aim (assassin bugs, spiders) sometimes was to delay the time of the initial attack other predators. pesticide treatment, as some cases of pesticide resistance had been repor- Entomophagous insects generally ted (BOURNIER & PEYRELONGUE, seem to have a moderate effect, 1973). The introduced parasite was a except in terms of egg parasitism (a T. brasiliensis strain from El Salvador mechanism that has not yet been ful- and H. armigera was the target pest. Spodoptera littoralis on a cotton flower. ly clarified). Hyperparasitic insects The imported strain was propagated Photo CIRAD-UREA become active in the presence of on a substitute host (the pyralid A. kuehniella) b e f o r e r e l e a s e . T h e results were not very encouraging as Table 3. Effects of various pesticide active ingredients on auxiliary organisms. it was difficult to apply the technique (Source: SIGRIST eta!., 1994) in farmers' fields. Similar experi- ments were carried out more recently Active ingredient Dose Effects on Effects on Effects on in Senegal (1979-1980), Togo and tested (g/ha) ladybirds syrphids spiders Cameroon (1982-1983) (SOGNIGBE, 1 989; BOURNIER, 1991) using alphacypermethrin 18 highly toxic highly toxic non toxic insects from CIRAD's Montpellier bifenthrin 30 highly toxic highly toxic highly toxic (France) laboratories. cypermethrin 36 highly toxic highly toxic highly toxic Although considerable skills have esfenvalerate 22 non toxic non toxic non toxic been developed for studying auxi- fenvalerate 60 moderately toxic non toxic highly toxic liary organisms, it is still difficult to endosulfan 750 slightly toxic highly toxic highly toxic apply the results on a large scale chlorpyriphos-E 450 non toxic highly toxic highly toxic under tropical African cotton crop- ping conditions. chlorpyriphos-M 500 non toxic highly toxic highly toxic

dimethoate 400 slightly toxic highly toxic non toxic

isoxathion 350 slightly toxic highly toxic moderately toxic Impact of active isazophos 200 highly toxic highly toxic non toxic

omethoate 300 slightly toxic highly toxic moderately toxic ingredients on auxiliary

methamidophos 300 slightly toxic slightly toxic non toxic organisms

monocrolophos 250 highly toxic highly toxic highly toxic Since 1990, the effects of pesticide profenofos 150 highly toxic moderately toxic highly toxic active ingredients have mainly been triazophos 125 slightly toxic highly toxic non toxic investigated in Chad, Cameroon and benfuracarb 250 slightly toxic slightly toxic moderately toxic Côte d'Ivoire. Despite the methodo-

carbosulfan 300 highly toxic highly toxic slightly toxic logical problems involved in these studies, an active ingredient classifi- thidicarbe 800 slightly toxic slightly toxic slightly toxic cation has been drawn up on the imidacloprid 50 slightly toxic slightly toxic non toxic basis of their results (Table 3).

Agriculture et développement ■ SpecialIssiaã - November 1997 osÈÈmpssb w m ü ûm M

Amsacta sp. (ANGELINI & VAN- Entomopathogenic DAMME, 1969; CROIZIER et al., 1983; ANGELINI & JACQUEMARD, agents 1984).

Insect populations are controlled by Virus infections were observed in various epizootic diseases involving A. flava in Mali and in S. littoral is in viruses, bacteria, fungi and proto- Chad (ATGER & CHEVALET, 1975; zoans. Research undertaken in Africa ATGER, 1970). However, no virus on this topic was first reviewed by infections have been noted in the ATGER (1970). Bibliographical sum- bollworm P. gossypiella or in the maries have been published on lepi- phyllophagous caterpillar S. d e r o g a t a . do pte r a n viruses and on using There have been several attempts to B. thuringiensis as a biopesticide. propagate locally isolated viruses (in More recent results obtained in Chad and Côte d'Ivoire), and finally Cameroon and Togo have also been experiments were conducted on published (ANGELINI & JACQUE- using viruses isolated from other MARD, 1 984; JACQUEMARD, 1987; insects — at lower cost than would MONTALDO, 1991 ; SILVIE et al., have been possible with locally pro- 1993). duced viruses. The most commonly used pathogens are nuclear Insect viruses polyhedrosis viruses (NPV) from /\. California and M. brassicae When conditions are suitable for (JACQUEMARD & DELATTRE, 1977; their development, epizootic viruses JACQUEMARD, 1978). can have spectacularly destructive Some entomopathogenic viruses effects on some lepidopteran larval have been mass-reared in vivo from populations, e.g. S. exempta out- insect tissue cultures and marketed breaks in grass crops (Africa) and by pesticide manufacturers. CIRAD A. argillacea in cotton crops (Latin studies revealed that these products America). can be used to control some cotton Virus infections have been detected pests (Table 4). in most lepidopterans found on cot- Research scientists have tried to utili- ton crops in Africa, i.e. in major pests ze possible synergetic interactions such as H. armigera, D. watersi, between entomopathogenic agents E. insulana and C. leucotreta, and in and chemical pesticides — often secondary species such as S. e x i g u a , pyrethroids at low doses (FERRON et al., 1 983). Studies on this feature were conducted in Cameroon, Côte d'Ivoire, Chad and Togo (JACQUE- Table 4. Potential use of commercialized insect virus diseases (RIBA & SILVY, 1993). MARD, 1982; RENOU, 1987; MO N- TALDO, 1991; VAISSAYRE, 1994). Pathogen Brand name Origin Potential target (species) Treatment of cotton plants Heliothis NPV Elcar Switzerland H. armigera Viron H USA H. armigera Biopesticide treatments of cotton Biotrol VZH USA H. armigera plants with these insect viruses are efficient when the control operator Spodoptera NPV Spodopterin France S. l i t t o r a l is complies with a treatment schedule Viron P USA S. l i t t o r a l is and a dose of 1013 Pib (polyhedral Biotrol VPO USA S. l i t t o r a l is inclusion bodies) per hectare for most of the baculoviruses tested Mamestra NPV Mamestrin France H. armigera (CAUQUIL, 1985).

Autographa NPV MGS 400 USA H. armigera However, this efficacy is limited by: - the biopesticide persistence, which Cydia GV SAN 406 Switzerland C. l eucot r et a is often insufficient because of the Carpovirusin France C. l eucot r et a presence of antagonistic factors such Granupom Germany C. l eucot r et a as UV-rays or foliar secretions and Decyde USA C. l eucot r et a their pH levels;

Agriculture et développement ■ SpaciûAlssLia- November 1 997 - the fact that the agent generally has toxins such as the 9-endotoxin, i.e. to be ingested in order to become the most important and only legally- active, which is always difficult with applicable species. It is released after bollworms (but phagostimulants can ingestion by the insect and binds to be added to enhance ingestion); membrane receptors of the midgut, -th e specificity, i.e. requiring propa- which is subsequently destroyed. gation of the strains so as to control the constantly changing nature of the Initial investigations highlighted the parasitism; activity of the Anduze strain against - the problems that arise in obtaining E. i n s u l a n a (LE GALL, 1957; BUR- suitable quantities of the virus, which GERJON & GRISON, 1959). Other is propagated on reared insects or strains of this baccillus were then iso- tissue cultures. lated from D. watersi, E. insulana and A. m oloneyi (JACQUEMARD, The most recent "combined control" 1 965; ATGER & JACQUEMARD, strategy involved associating a poly- 1965). Variations in the virulence of hedral virus (usually NPV from different strains of this bacterium M. brassicae ), a phagostimulant and against Earias sp. were noted in labo- a low dose of chemical pesticide. ratory tests (FRUTOS e tal.t 1987). All The results in controlling certain boll- tested treatments conducted in cot- worms (H. armigera and D. watersi ) ton fields with B. thuringiensis formu- were as good as can be obtained with lations revealed the high efficacy of chemical pesticides (RENOU et a i, this bacterium against some pests, 1 985; SILVIE et al., 1 993). whereas it was found to be a poor Nevertheless, possible incompatible interactions (depending on the pesti- biopesticide against bollworms (JAC- QUEMARD, 1987). Vi rus-infected caterpillar cide used) have to be taken into account. Combinations with pyre- on a cotton leaf. Other bacterial strains have been iso- throids generally give suitable results, Photo CIRAD-UREA lated (Serratia, Pseudomonas, whereas the use of some organo- Aerobacter) from diseased insects phosphorus compounds (monocroto- (Diparopsis, Heliothis, Spodoptera), phos) can lead to a loss of efficacy. but their biopesticide efficacy has not In addition, the high cost of treat- yet been tested. Hence, B. t h u r i n - ments, such as those recently tested giensis is the only bacterium that has in Cameroon and Togo, is a conside- been used as a biopesticide to rable constraint for the extension control leaf-eating caterpillars, espe- of microbiological techniques to cially S. d e r o g a t a and A. flava. control bollworms. Prospects Around 10 toxins from B. t h u r i n g i e n - Entomopathogenic sis strains have currently been characterized. Genes that enable bacteria their synthesis have been identified, In the entomopathogenic bacteria with their specificities determined in group, there are many opportunistic lepidopterans and coleopterans. agents that can multiply to the extent A collection of toxins with high effi- of killing the host. Injuries generally cacy against cotton pest insects is provide a port of entry for these bac- available, and includes: Cry IA(b), teria. However, only sporulating Cry IA(c), Cry IB and Cry IIA genes bacilli can infect healthy insects. for bollworms, Cry 1C for Spodoptera sp. and Cry III for Chrysomelidae, Infection mechanisms pests of glandless cotton.

of identified bacteria A cotton improvement programme Most studies undertaken to date on has been set up to develop transgenic entomopathogenic bacteria have cotton plants expressing B. t h u r i n - focused on B. thuringiensis (ARON- giensis toxins. This marks an impor- SON et a i, 1986; NBIAP, 1995). This tant turning point in the quest to gram+ bacterium forms crystals control cotton bollworms that are during sporulation, which contain relatively unsusceptible to standard

Agriculture et développement ■ Spacl&d/Issitó - November 1 997 osttm p&sb

biopesticide treatments. of these pathogens are still not clear- ly established. The role of entomopathogenic bacte- ria in integrated pest management programmes should therefore be reconsidered. B. thuringiensis formu- Chemical mediators lations could be used as pesticides against phyllophagous caterpillars by For several years, sex attractants have determ ining the most suitable been used to trap lepidopteran spraying techniques, possible asso- insects. CIRAD, in collaboration with ciations with chemical pesticides and the Chemical Mediator Laboratory of the best times, relative to the insects' the French Institut national de la development cycle, to conduct recherche agronomique (INRA), have treatments (e.g. it is best to spray just- developed a number of sex attrac- hatched neonate caterpillars) (DABI, tants such as pheromones from 1988; HUSSEIN et ai, 1990; PLAPP, H. armigera, C. leucotreta, E. insula- 1991). Transgenic varieties will have na and D. watersi (DESCOINS & to be developed to control b o ll- GALLOIS, 1979; ANGELINI et a i, worms (BENEDICT et a i, 1 992, 1976, 1980, 1981). On the basis of 1993; GATEHOUSE et al., 1 992). this work, synthetic sex pheromones were used to investigate the popula- tion dynamics of adult males, e.g. H. armigera, C. leucotreta, S. littora- lis and P. gossypiella (DAIBER, Entomopathogenic fungi 1 978; BOURDOUXHE, 1 982). Epizootic diseases caused by Unfortunately, the results of many tests carried out in seven different Map of receptor sites (located around Entomophthorales can be respon- countries are not yet very useful for intestinal microvilli) of the Cry IAa toxin sible for killing off insect populations agricultural warning purposes or (^) in the midgut of Chilo suppressolis. under natural conditions. This phe- decision-making on pest control Photo L. Fiuza nomenon was noted for aphids in tro- pical Africa (SILVIE & DEGUINE, treatments (JACTEL & VAISSAYRE, 1994). However, spray treatments 1988; MICHEL, 1992a and b). with commercial mixtures, such as In tropical African peasant farming Mycar (Hirsutella thompsonii) or conditions, mating disruption tech- Vertalec (Verticillium lecanii) against niques are difficult to apply because P. latus, aphids and whiteflies, res- of the fragmentation of cotton fields, pectively, have failed. This was likely staggered planting and fruiting dates, due to the fact that the most suitable and technical treatment constraints. ecological conditions for the action

B. thuringiensis spore and protein crystal Trapping and mating Photo CIRAD-IGEPAM disruption Studies conducted by CIRAD on this topic have focused on several diffe- rent species.

H. armigero The population dynamics of H. armi- gera were investigated, but very few or no correlations between captured males and crop damage in the field were noted. Eggs were observed before the adult males were captu- red, suggesting that the cotton fields are actually colonized by gravid females. The usefulness of trapping males to determine when pesticide treatments should be undertaken is therefore questionable.

Agriculture et développement ■ Special Issue - November 1997 industrially for about 15 years. The results of many studies on diffusion of this pheromone have led to a wide variety of solutions (pheromone- soaked microfibres, tape or cord, and spraying water-suspensions of micro- granules), that can be chosen to address different objectives, e.g. investigating population dynamics, mating disruption and, more recent- ly, attract and kill (F1ENNEBERRY et ai, 1981; CRITCHLEY et al., 1983; HOEER & BRAZZEL, 1992). Mating disruption is a popular control method, but the results have been quite variable (USA, Egypt, Pakistan). Interesting test results were obtained at Bouaké (Côte d'Ivoire): damage to fruiting organs was markedly redu- ced by manually spraying cotton leaves with glued microtubes (SAN- DOZ), at 5 000-8 000 microtubes/ha Diparopsis watersi. (VAISSAYRE, 1987) or using impre- Photo J.-P. Degume Moreover, mating disruption would gnated tapes (OCHOU, 1 997). not be applicable for this polypha- Persistence was higher than obtained gous ubiquitous pest. with microgranulated formulations applied with standard spraying Tests on D. watersi equipment. Very few tests have been carried out on D. watersi, apart from monitoring C. leucotreta adult populations. It is possible to There is a problem of specificity attract the first upsurging males of when conducting experiments on this monophagous pest to an early C. leucotreta, as males of other spe- planted or pruned cotton trap-crop. A cies are also captured in the traps, mating disruption or attract and kill especially C. peltastica. There is no trapping strategy could be used, evidence that this lepidopteran could combining a sex pheromone with be controlled by mating disruption. glue or a pesticide. This technique could be combined with that used to control P. gossy- E. i n s u l a n a and E. b i p l a g a piella in areas jointly colonized by No studies have focused on E. insula- these two endocarpal bollworms. na and E. biplaga, despite the fact that these two species (which are S. littoral is and S. derogata often found on the same sites) cause For 5. littoralis, sex pheromones of 20-30% of all caterpillar damage to various origins can be used to moni- cotton fruiting organs. For these oli- tor adult population dynamics. gophagous species, the mating dis- CIRAD has not been too involved in ruption strategy would certainly be such studies because of the low eco- valid and readily possible. Only the nomic impact of this pest in tropical E. insulana sex pheromone is com- Africa — more research is under way mercially available. Moreover, this on this topic in Egypt. pest species can be quite easily rea- A sex attractant was synthesized for red on artificial medium, which S. d e r o g a t a , but it is not yet being means that more advanced studies marketed (HIMENO & HONDA, are would be possible. 1992). It is still quite difficult to rear this lepidopteran pest in an artificial P. gossypiella sex pheromone environment, as it seems to The sex pheromone of P. gossypiella require a natural environment for (gossyplure) has been produced ovipositioning.

Agriculture et développement ■ Special - November 1 997 Bene/LCUJiSs

Coccinellidae eggs in an aphid colony. Photo CIRAD-UREA

Phonoctonus, predator of Dysdercus. Photo CIRAD-UREA

Coccinellidae larva feeding on an aphid colony. Photo CIRAD-UREA

Spodoptera larva killed by Bacillus thuringiensis. Photo CIRAD-UREA

Lacewing larvae feeding on whitefly pupea. Photo CIRAD-UREA

Pentatonid bug infected by the Beouveria fungus. Photo CIRAD-UREA

Agriculture et développement ■ SpecialIssitó - November 1 997 Future research on associations (village communities). also involves preventive measures, Simple inexpensive techniques adapted cropping practices, rational chemical mediators requiring little labour input should be choices of associated crops, and an developed, especially for applying overall understanding of the entomo- Pheromones: availability and pheromones to induce mating dis- phagous insect complex (Table 5). applications ruption. The low number of emission Integrated pest management pro- Sex pheromones are not yet avai- sources and the persistence of the grammes for cotton cropping systems lable for three species (D. watersi, formulation should be future reseach should also include destruction of E. biplaga and S. d e r o g a t a ), and the- focuses. harvest debris, tillage, intercropping, re are no clear correlations between and well chosen planting dates and Regardless of the results of previous trapped insects and field infestations, positions of the crop in the cropping operations, the success of such pro- especially with respect to H. armige- plan. jects will depend on how easily phe- ra. romones can be applied in traditional It is essential to choose the most sui- Mating disruption is only possible for farming systems. table cultivar to be cropped, i.e. phy- oligophagous or monophagous siological characteristics (length of its insects (P. gossypiella). Pests often growth cycle, hardiness, compensa- colonize the same fields, i.e. both tion potential) and some morpholo- exocarpal species (e.g. H. armigera, Conclusion Earias spp.) and endocarpal species gical traits (especially leaf hairiness). (e.g. P. gossypiella, C. leucotreta ). The intensity and complexity of most Integrated pest management pro- pest infestations certainly warrants grammes imply respect for the bene- Field applications the use of chem ical pesticides. ficial fauna. However, the results of It would be very difficult to set up a Treatments should, nevertheless, be mass releases of entomophagous network of traps around cropfields, conducted as part of an integrated auxiliary insects (e.g. trichogrammids even if organized by community pest management programme that for biological control) have generally

Table 5. Combined methods to control the main cotton pests as part of an integrated pest management strategy.

Pest Cultural Varietal Biological Pheromones Chemical control choices control (1) control *** H. armigera * planting date * transgenic ** NPV: * trapping varieties (B. thuringiensis) *** C. leucotreta * planting date * transgenic ** NPV: * trapping varieties

P. gossypiella *** destruction * atrophied or *** mating of harvest debris frego bracts disruption *** Leaf-eating insects ** B. thuringiensis

Jassids *** hairy leaves ** Aphids * destruction of ** natural effect plants after harvest, of beneficiais and seed topping, defoliant entomopathogens treatments ** Whiteflies * destruction * of plants after "okra"leaves harvest, topping defoliant

Mirids * nectari less variet ies *** Bugs *** Mites

*: established method; **: technique used on a reduced scale or with limited efficacy; ***: widely used technique of acknowled- ged efficacy.

(1): entomophagous insects and entomopathogens are included in the biological control category.

Agriculture et développement ■ SpecldAlssitó - November 1997 not been very encouraging. It is will definitively solve all pest and important to have an overall unders- disease problems with respect to this tanding of the population dynamics crop. Nevertheless, with the intro- of the main entomophagous insects duction of such new varieties, insect present in a region, so that they can populations within cropping systems be taken into consideration when could be managed differently, unless making decisions on active ingre- they develop resistance to the toxins dients to be used in pest control treat- involved. ment programmes. Some entomo- In conclusion, the results of these pathogenic organisms efficiently alternatives to chemical pest control reduce pest populations and treat- are still not conclusive enough to be ments are therefore unnecessary (e.g. exploited. There are solutions for Entomophthorales against aphids). In controlling some types of pests, for some cases, microbiological prepara- instance: leaf hairiness against jas- tions can be applied (e.g. viruses, si d s ; entomophagous insects and B. thuringiensis) to control lepido- entomopathogenic agents can redu- pteran pests. Treatments against ce homopteran and lepidopteran bollworms are more likely to be pests; and some transgenic cotton successful when conducted at care- varieties are efficient in controlling fully chosen times. Combining a bollworms. However, substantial pathogen with a low pesticide dose, Sex pheromone-soaked cord attached to crop damage will still occur unless i.e. a "combined control" strategy, a cotton plant. chemical pesticide treatments are Photo P. Silvie will often enhance the efficacy of used. To be economically sustai- the pathogen. nable in the short term, cotton crop Apart from gossyplure (used to dis- management should be based on rupt P. gossypiella mating) and the alternative cultural, varietal and bio- aggregation pheromone of A. gran- logical methods, always combined dis, sex pheromones are not directly with supervised chemical control. useful for pest control — however, This is the current strategy adopted they do provide informative results by CIRAD, through the development that could help in making treatment of new cotton pest management pro- decisions. It should not be assumed grammes in collaboration with its that future transgenic cotton varieties partners. expressing B. thuringiensis toxins

Damage to a young flower bud caused by Earias biplaga. PhotoJ.-P. Bournier

Agriculture et développement ■ SpeclQÃIssitó - November 1 997