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Chapter 11 Pests

Anthony C. Bellotti Pest and Disease Management Project, Centro Internacional de Agricultura Tropical (CIAT), A.A. 6713, Cali, Colombia

Introduction especially if there is a dry season of 3 months or more. When the crop is grown under conditions The dynamics of production, utilization of irregular, limited rainfall as in the lowland sub- and marketing vary considerably from one humid and semiarid tropics, however, arthropod continent and country to another. In recent pest populations increase, causing considerable years there has been a shift in demand for partic- yield reduction (Bellotti et al., 1999). Arthropod ular cassava products in Latin America with a pests can cause low-to-moderate levels of crop noticeable trend towards the production of chips damage in the subtropical regions of Latin and pellets for feed, as well as high- America and Africa and in the highland regions quality flours for human consumption (Henry of Africa (Henry and Gottret, 1995). and Gottret, 1995). This could induce a trend Most cassava is grown by small-scale towards plantation-size production units. farmers, often on marginal or fragile soils under World cassava production, which is con- rainfed conditions, using few purchased inputs centrated in Latin America, Asia and Africa, such as fertilizers or pesticides. In these tradi- can be divided into five principal agroecosystems tional farming systems where cassava is usually (Henry and Gottret, 1995): one of many crops being grown, pest control • is often a low priority and so cassava receives the lowland humid tropics; minimal pesticide applications. Under such • the lowland subhumid tropics; • conditions, yields are often low, with a large gap the lowland semiarid tropics; between potential yield (21.3 t ha−1) and that • the highland tropics; and −1 • achieved by producers: a mean of 11.2 t ha in the subtropics. Latin America and 9.0 in Africa (Henry, 1995). Approximately 65% of the area under Arthropod pests and diseases are major factors in cassava production occurs in the lowland humid causing this yield reduction (Bellotti et al., 1999); and subhumid agroecosystems (Henry and moreover, the vegetative nature of cassava prop- Gottret, 1995). Arthropod pests do not appear to agation contributes to pest build-up and dissemi- cause significant damage in the lowland humid nation across regions and among countries and or the highland tropical agroecosystems, where continents. there is considerable and consistent rainfall In Latin America there are indications of a (Montagnini and Jordan, 1983; Bellotti et al., shift towards large-scale production units, where 1999). Moderate levels of crop damage can occur cassava is grown as a plantation crop. This may in the mid-altitude (1000–1400 m) tropics, result in new or worse pest problems than those

©CAB International 2002. Cassava: Biology, Production and Utilization (eds R.J. Hillocks, J.M. Thresh and A.C. Bellotti) 209

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210 A.C. Bellotti

found in small-scale production. Such a scenario established and native arthropod pests that have is especially feasible in the Neotropics, where a adapted to cassava have not been reported as large complex of arthropod pests has co-evolved causing serious yield losses (Maddison, 1979). with the crop. For example, increased frequency Recent explorations in cassava-growing and severity of cassava hornworm ( ello regions of the Neotropics indicate that the L.) attacks have been recorded, resulting in arthropod pest complex is not geographically increased pesticide applications (LaBerry, 1997). uniform. The evidence suggests that the mealy- In Asia, where there are extensive areas planted bug Phenacoccus herreni, which has caused with cassava, major pest problems have been considerable damage in northeast Brazil, was avoided as the most damaging pest from probably introduced from northern South Amer- the Neotropics have not been introduced. ica (Venezuela or Colombia), where populations are controlled by natural enemies not found in Brazil (Bellotti et al., 1994; Smith The Cassava Arthropod Complex and Bellotti, 1996). P. manihoti, which has caused severe crop damage in Africa, occurs only Cassava (: Manihot esculenta in Paraguay, the Mato Grosso area of Brazil and Crantz) is a perennial shrub grown commer- the Santa Cruz area of Bolivia (Lohr and Varela, cially as an annual or biennial, throughout 1990). tropical and subtropical regions of the world. Studies on the CGM demonstrate a higher This vegetatively propagated crop has a long degree of morphological polymorphism and a growth cycle and is drought-tolerant. As it greater Mononychellus species complex in is often intercropped and planting dates are northern South America than elsewhere in the staggered, cassava is almost always present in Neotropics (Bellotti et al., 1994). This diversity is farmers’ fields. These agronomic characteristics associated with greater species richness within undoubtedly contribute to the considerable the phytoseiid complex that preys upon Mono- diversity of arthropod pests that feed on the crop. nychellus spp. in cassava (Bellotti et al., 1987, Cassava originated in the Neotropics, 1999). The cassava pest complex can be divided although its exact centre of origin is equivocal into two groups: (Renvoize, 1973; Allem, 1994; see Chapter 4); • those that appear to have co-evolved with consequently, the greatest diversity of arthro- cassava, which is their primary or only pods reported attacking the crop (Table 11.1) host; and is from the region (Bellotti et al., 1994). An • generalist feeders that may attack the cas- estimated 200 species have been reported sava crop opportunistically, especially dur- (Bellotti and Van Schoonhoven, 1978a,b), many ing seasonally dry periods when cassava is of which are specific to cassava and have adapted one of the limited food sources available. in varying degrees to an array of natural biochemical defences in the host that include The former group includes the Monony- laticifers and cyanogenic compounds (Bellotti chellus mite complex, (P. herreni and and Riis, 1994). The pest complex varies greatly P. manihoti), the hornworm (E. ello), lacebugs between the main cassava-growing areas, ( illudens, Vatiga manihotae, Amblystira indicating that careful quarantine measures machalana), (Aleurotrachelus socialis could prevent pest introduction into uninfested and Aleurothrixus aepim), the stemborer (Chilo- areas (Frison and Feliu, 1991). The accidental mima clarkei and those of the Coelosternus), introduction of the cassava green mite (CGM; fruitflies (Anastrepha pickeli and Anastrepha Mononychellus tanajoa Bonder) and the cassava manihoti), the shootfly (Neosilba perezi), the white mealybug (Phenacoccus manihoti Mat. Ferr.) from scale (Aonidomytilus albus), thrips (Frankliniella the Americas into Africa has caused considerable williamsi) and the gallmidge (Jatrophobia brasil- crop loss throughout the cassava belt and has iensis; Bellotti et al., 1999). been the object of massive biological control The generalist feeders primarily consist efforts (Herren and Neuenschwander, 1991; of whitegrubs (Phyllophaga spp. and several Neuenschwander, 1994a). In Asia none of the others), termites, cutworms, grasshoppers, leaf- major neotropical cassava pests has become cutting ants, burrower bugs (Cyrtomenus bergi),

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crickets, Tetranychus mite species and stemborers become a major pest if introduced into areas (Lagochirus spp.) (Bellotti and van Schoonhoven, where native natural enemies and/or adapted or 1978a; Bellotti et al., 1999). resistant germplasm are unavailable. P. manihoti Several pests found in the Neotropics could has not yet reached other regions, although potentially cause severe crop losses if introduced there are no evident natural barriers to prevent inadvertently into Asian or African cassava- its movement, especially in Brazil, where cassava growing areas. They include the cassava horn- is grown extensively throughout most of the worm, several mite species, lacebugs, whiteflies country. The Andean mountain range in west- and stemborers. Moreover, a species which is ern South America has undoubtedly affected the considered to be a secondary or minor pest in the movement of cassava pests, although this is not Neotropics (e.g. the cassava mealybug, which is well documented. For example, the lepidopteran found only in limited sites, as mentioned) could stemborer C. clarkei, which has good flight

Table 11.1. Global distribution of important arthropod pests of cassava.

Pest Major species Americas Africa Asia

Mites Mononychellus tanajoa X X Tetranychus urticae X X Mealybugs Phenacoccus manihoti X X Phenacoccus herreni X Whiteflies Aleurotrachelus socialis X Aleurodicus dispersus X X X Aleurothrixus aepim X Bemisia tabaci X X X Bemisia afer X X Hornworm X X Lacebugs X Vatiga manihotae X Burrower bugs Cyrtomenus bergi X Thrips Frankliniella williamsi X X Scirtothrips manihoti X Scales Aonidomytilus albus X X X Fruitflies Anastrepha pickeli X Anastrepha manihoti X Shootflies Neosilba perezi X Silba pendula X Gallmidge Jatrophobia (Eudiplosis) brasiliensis X White grubs Leucopholis rorida X X X Phyllophaga spp. X X X Several others X X X Termites Coptotermes spp. X X X Heterotermes tenuis X Stemborers Chilomima spp. X Coelosternus spp. X Lagochirus spp. X X X Leaf-cutter ants Atta spp. X Acromyrmex spp. X Root mealybugs Pseudococcus mandioca X Stictococcus vayssierei X Grasshoppers elegans X X X X

Source: Adapted from Bellotti et al. (1999).

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212 A.C. Bellotti

capabilities and has spread through many The burrower bug (C. bergi; : regions of Colombia and Venezuela, is not ) is one of the few pests that damage reported west of the westernmost range of the cassava roots directly. Root punctures during Andean mountains, but has been reported from feeding can introduce fungal pathogens that Argentina (B. Lohr, personal communication). reduces root yield and quality (García and Bellotti, 1980). Grubs, millipedes and termites are reported occasionally as feeding on tuberous Crop damage and yield loss roots; however these may be secondary feeders, attacking already damaged and decaying roots. Arthropod damage to cassava is often indirect In general, arthropod pests are most damag- because most pests are foliage or stem feeders, ing to cassava during the dry season and do not reducing leaf area, leaf life or photosynthetic appear to cause significant damage in areas rate. Field studies indicate that pests that attack of considerable and consistent rainfall (Bellotti the crop over prolonged periods (3–6 months) – et al., 1999). The cassava plant is well adapted such as mites, mealybugs, thrips, whiteflies to long periods of limited water, responding to and lacebugs – can cause severe root yield water shortage by reducing its evaporative (leaf) reductions (Table 11.2) as a result of their surface rapidly and efficiently and by closing the feeding on leaf cell fluids and the consequent stomata partially, thereby increasing water use decrease in photosynthesis. Severe attacks can efficiency (Cock et al., 1985; El-Sharkawy et al., induce premature leaf drop and death of the 1992). In water-deprived plants, both the accel- apical meristem. The potential for yield reduc- erated shedding of old leaves and the pronounced tion by these pests is greater than that by decrease in their photosynthetic activity means cyclical pests such as hornworm and leaf-cutter that the younger leaves play a key role in the ants, which cause sporadic defoliation. Never- plant’s carbon nutrition. Given that pests prefer theless, these highly visible pests often cause the younger canopy leaves, dry-season feeding farmers to apply insecticides (Braun et al., tends to cause the greatest yield losses in cassava. 1993). Once the crop enters into a wet cycle (following

Table 11.2. Yield losses due to major cassava pests.

Pest Yield losses References

Hornworm In farmers’ fields, natural attack resulted Arias and Bellotti (1984); (Erinnyis ello) in 18% yield loss; simulated damage Bellotti et al. (1992) studies resulted in 0–64% loss, depending on no. of attacks, plant age and soil fertility. Mites 21, 25 and 53% yield loss during a 3-, 4- Bellotti et al. (1983b); Byrne (Mononychellus and 6-month attack, resp.; 73% for et al. (1982); Herren and tanajoa) susceptible cultivars compared with 15% Neuenschwander (1991); for resistant cultivars; 13–80% in Africa. Yaninek and Herren (1988) Whiteflies 1-, 6-, 11-month attacks resulted in 5, 42 Bellotti et al. (1983b, 1999); (Aleurotrachelus socialis) and 79% yield loss, respectively. Vargas and Bellotti (1981) Mealybugs 68–88% loss depending on cultivar Herren and Neuenschwander (Phenacoccus herreni, susceptibility (in Colombia); in Africa (1991); Schulthess (1987); Phenacoccus manihoti) yield losses of ≈ 80% are reported. Vargas and Bellotti (1984) Burrower bugs Brown-to-black lesions render roots Arias and Bellotti (1985); (Cyrtomenus bergi) commercially unacceptable; > 50% Bellotti et al. (1999); Castaño reduction in starch content. et al. (1985) Lacebugs Field trials with A. machalana and CIAT (1990) (Vatiga manihoti, V. manihoti resulted in 39% yield loss. Amblystira machalana) Stemborers (Chilomima In Colombia, 45–62% loss when stem Lohr (1983) clarkei) breakage exceeds 35%.

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Arthropod Pests 213

rain or irrigation), it has the potential to recover and Neuenschwander, 1991; Skovgård et al., and compensate for yield losses from severe 1993). drought, as well as from pest attack, because CGM populations feed preferentially on of the formation of a new leaf canopy and the undersides of young emerging leaves, which the higher photosynthetic rate in newly formed develop a mottled whitish-to-yellow appearance; leaves (El-Sharkawy, 1993). andtheymaybecomedeformedorreducedinsize (Byrne et al., 1983). The CGM is a serious prob- lem only in dry regions, where heavy infestations Major Pests; Bioecology Damage cause defoliation which begins at the top of and Management the plant, often killing apical buds and shoots. Regrowth may occur but if the rains are scarce, Cassava mites this new flush of leaves will also be attacked (Yaninek and Animashaun, 1987). Mites are a universal pest of cassava, causing serious yield losses in the Americas and Africa Control (Herren and Neuenschwander, 1991; Bellotti et al., 1999). Of the > 40 species reported feed- Research into the control of M. tanajoa has had ing on cassava (Byrne et al., 1983), the most two main thrusts: host plant resistance (HPR) frequent are Mononychellus tanajoa (syn = Mono- and biological control (Table 11.3). These two nychellus progresivus), Mononychellus carrib- complementary strategies promise to reduce beanae, Tetranychus cinnabarinus and Tetranychus CGM populations below economic injury levels. urticae (also reported as Tetranychus bimaculatus The continual use of acaricides is not feasible and Tetranychus telarius). Cassava is the major for low-income farmers. Moreover, such use is host for the Mononychellus species, whereas the not recommended because of adverse effects on Tetranychus species have a wide host range. natural enemies. Other mite species (e.g. Oligonychus peruvianus, Oligonychus biharensis, Eutetranychus banksi or HPR. Substantial efforts have been made by Mononychellus mcgregori) are not important both international research centres which have economically and feed on cassava only a mandate for cassava [Centro Internacional de sporadically (Byrne et al., 1983). Agricultura Tropical (CIAT) and International CGM, the most important species, is reported Institute for Tropical Agriculture (IITA)] and causing crop losses in the Americas and Africa by national research programmes [e.g. Centro (Herren and Neuenschwander, 1991; Bellotti Nacional de Pesquisa en Mandioca y Fruticul- et al., 1999), especially in seasonally dry regions tura (CNPMF)/Empresa Brasileira de Pesquisa of the lowland tropics (Yaninek and Anima- Agropecuaria (EMBRAPA)] to identify cassava shaun, 1987; Braun et al., 1989). In experimen- cultivars and develop hybrids with resistance tal trials fresh root yields were reduced by 21, 25 to CGM (Byrne et al., 1983; Bellotti et al., 1987; and 53% following 3-, 4- and 6-month attacks, Hershey, 1987). Of nearly 5000 landrace respectively (Bellotti et al., 1983b). Under field cultivars in the CIAT cassava germplasm bank conditions with higher mite populations, there that were evaluated for CGM resistance, only was a 15% yield reduction in resistant cultivars c. 6% (300 cultivars) have been identified as compared with a ≤ 73% loss in susceptible having low-to-moderate levels of resistance cultivars; 67% of the stem-cutting planting (CIAT, 1999). After substantial effort, cultivars material was damaged (Byrne et al., 1982, with moderate levels of resistance have been 1983). developed and released to farmers. M. tanajoa is native to the Neotropics and it CIAT’s mite-resistance research has tradi- was first reported from northeast Brazil in 1938. tionally been carried out at two sites: (i) CIAT, It first appeared in Africa (Uganda) in 1971 Palmira, located in the mid-altitude (1000 m) and by 1985 it had spread across most of the Andean highlands, where mite populations are cassavabelt,occurringin27countries(Yaninek, moderate; and (ii) Pivijay, Magdalena, on the 1988) and causing estimated root yield losses Colombian Atlantic Coast, in the lowland tropics of 13–80% (Yaninek and Herren, 1988; Herren with a prolonged (4–6 months) dry season and

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214 A.C. Bellotti

Table 11.3. Control options for major cassava pests.

Pest/species Control options References

Hornworm Biological control. Baculovirus biopesticide; Bellotti et al. (1992, 1999); Braun (Erinnyis ello) monitoring of hornworm populations with light et al. (1993); Schmitt (1988) traps and field scouting. Mites (Mononychellus Host plant resistance (HPR). Moderate levels of Bellotti et al. (1994); Braun et al. tanajoa, resistance available in cassava clones; effective (1989); Byrne et al. (1982, 1983); Mononychellus breeding programme needed to incorporate CIAT (1999) caribbeanae) resistance into commercial cultivars. Biological control. Large predator Bellotti et al. (1999); Yaninek and complex associated with mite complex that Herren (1988) reduces mite populations effectively; fungal pathogen (Neozygites) and virus disease identified. HPR. Several highly resistant varieties and Arias (1995); Bellotti et al. (1994, (Aleurotrachelus hybrids available; natural enemies, especially 1999); Castillo (1996); CIAT (1999) socialis) being surveyed and evaluated. Mealybugs Adequate HPR not available in cassava Bellotti et al. (1983a, 1999); Van (Phenacoccus germplasm. Several natural enemies identified: Driesche et al. (1990) herreni) 3 species (Acerophagus cocois, Aenasius vexans and Apoanagyrus diversicornis) give good control. (Phenacoccus Parasite species Apoanagyrus lopezi provides Herren and Neuenschwander manihoti) good control in most regions of Africa. (1991); Neuenschwander (1994a) Thrips (Frankliniella HPR. Pubescent cultivars have effective Bellotti and Kawano (1980); Bellotti williamsi) resistance and are available to farmers. and van Schoonhoven (1978a,b); van Schoonhoven (1974) Burrower bug High-HCN cultivars less damaged than others. Barberena and Bellotti (1998); (Cyrtomenus bergi) Several biological control agents including Bellotti and Riis (1994); Bellotti entomopathogenic nematodes and fungal et al. (1999); Caicedo and Bellotti pathogens give promising results in lab studies. (1994); Riis (1997) Intercropping with Crotalaria sp. reduces damage. Stemborers Cultural practices; maintain clean fields, destroy Bellotti and van Schoonhoven (Chilomima clarkei) infested stems. HPR being investigated. Possible (1978a,b); Gold et al. (1990); Lohr use of transgenic cultivars (Bt) being evaluated. (1983) Lacebugs (Vatiga HPR evaluations have given some promising Bellotti et al. (1987, 1999); manihotae, Vatiga results. Natural enemies identified but not Calvacante and Ciociola (1993); illuden, Amblystira thoroughly investigated. CIAT (1990); Farias (1985) machalana)

high mite populations. Low-to-moderate levels a shorter development time, a longer adult life of resistance are indicated by a 0–3.5 damage span and lower larval and nymphal mortality rating on a 0–6 evaluation scale. than those feeding on resistant cultivars (Byrne Of the 300 cultivars selected as promising et al., 1983). In more recent laboratory studies, for mite resistance over several years (two to M. tanajoa displayed a strong ovipositional seven field cycles), 72 have consistently had preference for susceptible cultivars. When paired damage ratings < 3.0 (CIAT, 1999). Most of with the resistant cultivars M Ecu 72, M Per these cultivars were collected from Brazil, 611 and M Ecu 64 in free-choice tests, 95, 91 Colombia, Venezuela, Peru and Ecuador, but and 88%, respectively, of the eggs were ovi- there are also several hybrids. posited on CMC 40, the susceptible cultivar Mechanisms of mite resistance have usually (CIAT, 1999). been expressed as antixenosis (preference versus non-preference) or antibiosis (Byrne et al., BIOLOGICAL CONTROL. Extensive surveys of cas- 1982). Mites feeding on susceptible cultivars sava fields and experimental data indicate that had greater fecundity, greater acceptability, although CGM is present throughout much

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of the lowland Neotropics, severe outbreaks Data from field experiments in Colombia causing significant yield losses are rare, except in (Braun et al., 1989) demonstrated the value parts of Brazil. From 1983–1990 extensive eval- and effect of the richness of phytoseiid species uations of the natural enemy complex associated associated with CGM. Fresh and dry root yields in with cassava mites were carried out at 2400 sites Colombia were reduced by 33% when natural in 14 countries of the Americas (Byrne et al., enemies were eliminated, whereas applications 1983;Bellottietal.,1987).Thisledtotheidentifi- of acaricides did not increase yields, indicating cation of the phytoseiid predator complex associ- good natural biological control. ated with the mites. The current predator mite Since 1984 numerous species of phytoseiids reference collection held at CIAT conserves pri- have been shipped from Colombia and Brazil marily those predators related to phytophagous to Africa. Despite massive releases, none of mites found on cassava. Collecting zones were the Colombian species became established, but usually chosen for their similarity to ecological three of the Brazilian species did (T. manihoti, homologues in Africa and Brazil. Of the 87 spe- T. aripo and N. idaeus; Yaninek et al., 1992, 1993; cies collected and stored, 25 are new or unre- Bellotti et al., 1999). T. aripo appears to be the corded species; 76% (66 species) were collected most successful of the three species. It has spread from cassava. A taxonomic key on phytoseiid rapidly and is now in more than 14 countries. species associated with cassava is being prepared On-farm field trials indicate that T. aripo reduces as part of a collaborative project with Brazilian CGM populations by 35–60% and increases fresh colleagues. The CIAT-Brazil collection is now root yields by 30–37%. organized into a true reference collection with Neozygites cf. floridana, a fungal pathogen accompanying database and can be used readily (Zygomycetes: Entomophthorales), causes irreg- for species description or redescription, where ular or periodic mortality of mite populations in types and paratypes may be found. Colombia and northeast Brazil (Delalibera et al., Of the 66 phytoseiid species collected on 1992). The pathogen has been found on mites cassava, 13 occur frequently. Typhlodromalus throughout many cassava-growing regions of manihoti was collected most frequently, being the Neotropics. Some strains appear to be specific found in > 50% of the fields surveyed. This was to the genus Mononychellus (de Moraes et al., followed by Neoseiulus idaeus, Typhlodromalus 1990). The pathogen has also been found in aripo, Galendromus annectens, concordis CGM in Africa, but epizootics have not been and Euseius ho, T. aripo and N. idaeus have played observed (Yaninek et al., 1996), indicating that an important role in the successful control Brazilian strains may be more virulent than the of M. tanajoa in Africa (Yaninek et al., 1992, African strains. Molecular techniques are being 1993). used to determine taxonomic identification of Explorations also revealed several fungal strains, and in vitro methodologies for predators of CGM, especially the staphylinid rearing the pathogen are being developed. This Oligota minuta and the coccinellid Stethorus sp. fungus, which shows considerable promise for These phytoseiids and insect predators have been biological control of CGM, is being evaluated in studied extensively in the laboratory and field Africa. (Table 11.4). It is generally agreed that the phytoseiid predators are more efficient than the insect predators at controlling mites occurring in Cassava mealybugs low densities (Byrne et al., 1983). Survey data also showed that CGM densities More than 15 species of mealybugs are reported were much higher in northeast Brazil than in feeding on cassava in Africa and South America. Colombia and that the richness of phytoseiid spe- P. herreni, P. manihoti, Phenococcus madeirensis, cies was considerably higher in Colombia than in Ferrisia virgata and Pseudococcus mandio are all Brazil. Of the fields surveyed in Colombia, 92% reported from the Americas (Bellotti et al., were uninfested or had low CGM densities (< 25 1983a; Williams and Granara de Willink, 1992). mites per leaf) whereas in Brazilian fields only Only P. herreni and P. manihoti, both of neotropi- 12% were uninfested and 25% had intermediate cal origin, are important economically (Table or high densities (Bellotti et al., 1994). 11.2). P. manihoti was introduced inadvertently

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216 A.C. Bellotti c

Tu 88 81 84 79 62 58 66 85 70

Mt 74 75 73 70 78 73 64 74 75 ) and % Females

Mc (

c Mc 20.9 16.1 27.8 12.0 19.0 27.7 (days) 6.6 Longevity Tu 14.0 21.6 39.1 14.2 23.0 d d d 3.5 Mc 13.0 16.1 12.5 23.4 19.4 27.7 23.0 31.0 d d d c d d d

Mononychellus caribbeanae – Tu 2.5 8.0 ), 13.0 19.0 32.3 43.7 12.0 34.4 d d d

Mt ( Fecundity d d d

Mt 6.0 14.2 32.0 13.8 34.8 14.5 18.7 22.4 12.7 d d d

Mc 5.5 6.8 5.7 5.1 7.7 5.8 5.2 c

Tu 4.1 5.8 4.6 4.4 5.4 5.1 7.0 6.1 5.0

Mononychellus tanajoa time (days) Development

Mt 4.9 5.8 4.6 4.7 5.0 4.7 7.4 5.7 5.7 b .4 Egg 68 45.4 26.8 26.5 17.8 (24 h) consumption b + + + + ++ ++ +++ to RH Tolerance Egg eclosion a 9 7 5 1 4 5 6 1 31 20 No. colony 1986–1999 strains/species ).

Tu ; + = 75%; ++ = 60%; +++ = 40–50%. ( Life table data on selected Phytoseiidae predators of the cassava mites . (1996).

et al CIAT (1994). CIAT (1999). Cuéllar CIAT (1990). Table 11.4. Tetranychus urticae Phytoseiidae species Typhlodromalus manihoti Typhlodromalus aripo Typhlodromalus tenuiscutus Neoseiulus idaeus Neoseiulus californicus Typhlodromalus rapax Neoseiulus anonymus Galendromus helveolus Galendromus annectens Euseius concordis RH, relative humidity a b c d

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into Africa in the early 1970s, where it spread cultivars from the CIAT cassava germplasm rapidly, causing considerable yield loss. It has bank screened for resistance to P. herreni, only been the object of a successful biological control low levels of resistance or tolerance were identi- programme (Herren and Neuenschwander, fied (Porter, 1988). Resistance studies at IITA 1991). In the Americas, P. manihoti is confined in Africa and at ORSTOM have given similar to Paraguay, certain areas of Bolivia and Mato results. Partial or low-to-weak levels of resis- Grosso do Sul State of Brazil, causing no eco- tance have been reported in germplasm evalua- nomic damage (Lohr and Varela, 1990). tions with P. manihoti (Le Ru and Calatayud, P. herreni is distributed throughout north- 1994; Neuenschwander, 1994a). It is sug- ern South America and northeast Brazil, where gested, however, that even low levels of plant high populations can cause considerable yield resistance could enhance the impact of natural losses (Table 11.2). Damage caused by both enemies in a biological control programme. species is similar: feeding by nymphs and adults causes leaf yellowing, curling and cabbage-like BIOLOGICAL CONTROL. Management of cassava malformation of the growing points. High mealybugs is a well-documented example of densities lead to leaf necrosis, defoliation, classical biological control, especially in Africa stem distortion and shoot death. Reductions where P. manihoti is being controlled successfully in photosynthetic rate, transpiration and meso- through the introduction of the parasitoid Apo- phyll efficiency – together with moderate anagyrus lopezi from the Neotropics. Although increases in water pressure deficit, internal CO2 P. herreni is distributed throughout northern and leaf temperature – were found in infested South America, it causes serious yield losses only plants (CIAT, 1992). in northeast Brazil. Thus P. herreni may be an P. manihoti is parthenogenic, whereas males exotic pest in this region, probably coming from are required for reproduction of P. herreni. P. northern South America (Williams and Granara herreni females deposit ovisacs containing de Willink, 1992). several hundred eggs on the underside of the Approximately 70 species of parasites, leaves, or around the apical bud. Eggs hatch in predators and entomopathogens of P. herreni 6–8 days and there are four nymphal instars; the have been identified in the Neotropics. Many fourth instar is the adult stage. Males have four of these are generalist predators that feed upon nymphal instars plus the adult stage. The third numerous mealybug species. Nevertheless, sev- and fourth instars occur in a cocoon, from which eral parasitoids show a specificity or preference the winged adult emerges. Adult males live only for P. herreni. Parasitoids identified from north- 2–4 days; the average life cycle of the female is ern South America include Acerophagus coccois, 49.5 days, that of the male, 29.5. The optimal Apoanagyrus diversicornis, Anagyrus putonophilu, temperature for female development is 25–30°C Anagyrus insolitus, Apoanagyrus elegeri and (Herrera et al., 1989). Aenasius vexans. The three encyrtid parasitoids P. herreni populations peak during the dry (Ap. diversicornis, Ac. coccois and Ae. vexans) season. The onset of rains reduces pest popula- have been identified as effective parasitoids of tions and permits crop recovery. (Herrera et al., P. herreni (Van Driesche et al., 1988, 1990). 1989). Recent research shows that when the Ae. vexans and Ap. diversicornis display a water supply is limited, the cassava leaves pro- marked preference for parasitizing P. herreni, duce increased amounts of metabolites, which although laboratory studies show they will also could favour mealybug growth and decrease parasitize other mealybug species (Bellotti et al., parasitoid efficacy (CIAT, 1999; Polanía et al., 1983a, 1994; Bertschy et al., 1997). Ac. coccois 1999; Calatayud et al., 2002). These results showed equal preference for both P. herreni could help explain the rapid mealybug popula- and P. madeirensis. All three parasitoids were tion increases during the dry season. attracted to P. herreni infestations (Bertschy et al., 1997). Comparative studies on the life cycles of the three parasitoid species show that each Control would complete two cycles for each cycle of P. Considerable effort has been made to identify herreni, which is a favourable ratio for biological resistance to cassava mealybugs. Of > 3000 control.

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Ap. diversicornis prefers third instar nymphs, dispersus, Paraleyrodes sp., Aleuronudus sp. and whereas the much smaller Ac. coccois can para- Tetraleurodes sp. (Bellotti et al., 1994, 1999; sitize male cocoons, adult females and second Castillo, 1996; França et al., 1996). A. socialis instar nymphs with equal frequency. Oviposition is the predominant species in northern South by Ap. diversicornis caused 13% mortality of first America, where it causes considerable crop nymphal instars (Van Driesche et al., 1990). Ae. damage, but it is also found, to a lesser extent, vexans prefers second and third instar nymphs in Brazil (Farias, 1994). B. tuberculata and T. and adult females with equal frequency (CIAT, variabilis are reported in low populations from 1990). Field studies with natural populations Brazil, Colombia, Venezuela and several other of Ap. diversicornis and Ac. coccois determined countries (Farias, 1990a; Bellotti et al., 1999). percentage parasitism by using trap plants with The spiralling whitefly A. dispersus is reported mealybug hosts set out in cassava fields (Van causing conspicuous damage on cassava Driesche et al., 1988). P. herreni mortality was in West Africa (Neuenschwander, 1994b; estimated at 55% for the combined action of the D’Almeida et al., 1998); Bemisia afer occurs in two parasitoids (Van Driesche et al., 1990). Kenya (Munthali, 1992) and the Côte d’Ivoire Through the combined efforts of CIAT and and in other countries of sub-Saharan Africa EMBRAPA, Ap. diversicornis, Ac. coccois and Ae. (J. Legg, personal communication). vexans were exported from CIAT and released B. tabaci has a pantropical distribution, feed- in northeast Brazil, primarily in the states of ing on cassava throughout Africa and several Bahia and Pernambuco from 1994 to 1996. countries in Asia including India (Lal and Pillai, Prior to introduction, EMBRAPA scientists had 1981) and Malaysia. Before 1990, the B. tabaci conducted field surveys to measure damage and biotypes found in the Americas did not feed on collect natural enemies. By the end of 1996, cassava. Whiteflies are known to transmit the > 35,000 individuals of the three parasitoid viruses causing two diseases of cassava: species had been released. In Bahia Ap. divers- • cassava mosaic disease (CMD) in Africa, icornis dispersed 130 km in 6 months, 234 km India and Sri Lanka, caused by gemini- in 14 months and 304 km in 21 months after viruses that are transmitted by B. tabaci release. Ac. coccois also became established and (Thresh et al., 1998; see Chapter 11). was recovered in high numbers at ≤ 180 km • B. tuberculata is the reported vector of from its release site 9 months later. Ae. vexans, cassava frog skin disease in the Neotropics although being consistently recaptured at its (Angel et al., 1990; see Chapter 11). release site in Pernambuco, dispersed only 40 km in 5 months (Bellotti et al., 1999; Bento It has been speculated that the absence of CMD et al., 1999). Subsequently, personal observa- in the Americas may be related to the inability of tions indicate that mealybug populations have its vector, B. tabaci, to colonize cassava. Since been reduced considerably and that cassava the early 1990s a new biotype (B) of B. tabaci, cultivation has returned to areas where it had regarded by some as a separate species (B. been previously abandoned due to P. herreni argentifolii), has been found feeding on cassava outbreaks. in the Neotropics. It is considered that CMD now poses a more serious threat to cassava produc- tion given that most traditional cultivars in the Whiteflies Neotropics are highly susceptible to the disease. In addition the B. tabaci biotype complex is the Whiteflies cause major damage in cassava- vector of several viruses of crops often grown in based agroecosystems in the Americas, Africa association with or near cassava. The possibility and, to a lesser degree, in Asia as direct feeding of viruses moving between these crops or the pests and virus vectors. There is a large complex appearance of new viruses presents a potential in the Neotropics, where 11 species are reported threat. on cassava: Al. socialis, variabilis, Al. Whiteflies cause direct damage to cassava aepim, Bemisia tuberculata, Bemisia tabaci, Bemisia by feeding on the phloem of leaves, inducing argentifolii, Trialeurodes abutiloneus, Aleurodicus leaf chlorosis and abscission, which results in

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considerable reduction in root yield if feeding is populations (Gold, 1993), indicating that this prolonged. Yield losses of this type are common technique can depend on the intercropped due to Al. socialis and At. aepim. There is a correla- species for success, thereby limiting its effective- tion between duration of whitefly attack and root ness and acceptance by farmers. However, it is a yield loss (Table 11.2). promising means of reducing pest populations Research efforts in the Neotropics have con- for small-scale farmers. centrated on Al. socialis and At. aepim. Popula- tions of both species are highest during the rainy HPR. Stable HPR offers a practical, low-cost, season, but may occur throughout the crop cycle long-term solution for maintaining reduced (Farias et al., 1991; Gold et al., 1991). Al. socialis whitefly populations. Whitefly resistance in agri- females oviposit individual banana-shaped eggs cultural crops is rare, although several good on the undersides of apical leaves. Eggs hatch sources of resistance have been identified and in c. 10 days and pass through three feeding high-yielding, whitefly-resistant cassava hybrids nymphal instars and a pupal stage (fourth instar) are being developed. HPR studies initiated at before reaching the winged adult stage. During CIAT > 15 years ago are evaluating systemati- the third instar, the body colour changes from cally the 6000 cultivars in the germplasm bank beige to black, surrounded by abundant waxy for whitefly resistance (CIAT, 1999), especially white cerosine. The black pupal stage makes this to Al. socialis. In Brazil some HPR research has species easy to distinguish from other whitefly been done with At. aepim (Farias, 1990a). species feeding on cassava. Egg-to-adult develop- Several sources of resistance to Al. socialis ment time of Al. socialis in the growth chamber have been identified. The clone M Ecu 72 (28 ± 1°C, 70% relative humidity (RH)) was 32 has consistently expressed the highest level days (Arias, 1995). of resistance. Additional cultivars expressing moderate-to-high levels of resistance include M Ecu 64, M Per 335, M Per 415, M Per 317, M Control Per 216, M Per 221, M Per 265, M Per 266 and HPR and biological control agents are accepted M Per 365. Based on these results, Al. socialis increasingly as complementary pest-control resistance appears to be concentrated in tactics that reduce environmental contamina- germplasm originating from Ecuador and Peru, tion and other disadvantages that arise from but this phenomenon needs to be investigated the excessive use of chemical pesticides. further. Research on cassava whitefly control in the M Ecu 72 and M Bra 12 (an agronomically Neotropics initially emphasized activities in desirable clone with field tolerance to white- HPR and cultural practices. More recently, a flies) were used in a crossing programme to concentrated effort is being made to identify and provide high-yielding, whitefly-resistant clones evaluate the use of natural enemies in an IPM that showed no significant differences in yield context. between insecticide-treated and untreated plots (CIAT, 1992; Bellotti et al., 1999). Greenhouse CULTURAL CONTROL. In traditional cropping and field studies showed that Al. socialis feeding systems, cassava is often intercropped, a practice on resistant clones had less oviposition, longer that has been shown to reduce populations development periods, reduced size and higher of many pests (Leihner, 1983). Intercropping mortality than those feeding on susceptible ones. cassava with reduced egg populations of Al. socialis nymphal instars feeding on M Ecu Al. socialis and T. variabilis, compared to those in 72 suffered 73% mortality, mostly in the early monoculture (Gold et al., 1990). These effects instars (CIAT, 1994; Arias, 1995; Fig. 11.1). The were residual and persisted up to 6 months after progeny (CG 489–34, CG 489–4, CG 489–31 harvest. Yield losses in cassava/maize, cassava and CG 489–23) selected from the M Ecu 72 × M monoculture and mixed cultivar systems were Bra 12 cross have consistently displayed moder- c. 60%; whereas in cassava/cowpea intercrops, ate levels of whitefly resistance. Three of these yield losses were only 12% (Gold et al., 1989a). hybrids are currently being evaluated for release Intercropping with maize did not reduce egg to producers in Colombia.

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Fig. 11.1. Whitefly (Aleurotrachelus socialis) nymphal development and mortality on resistant and susceptible cassava clones. Source: Arias, 1995.

Resistance screening using natural Al. repeat (SSR) markers with bulk segregant socialis populations is done in the field at two sites analysis (BSA), are being used to locate markers in Colombia: linked with resistance for mapping and ultimately cloning the resistant genes. • Nataima, Tolima, in cooperation with Co-segregating AFLP bands with resistance to CORPOICA, the Colombian Agricultural Al. socialis have been identified and are being Research Corporation. Al. socialis popula- sequenced to generate sequence-characterized tions at Nataima have consistently been at amplified region (SCARs) markers. The PCR- moderate to high levels for nearly 15 years, based marker will be the basis for the molecular offering the opportunity for sustained mapping and used in breeding. research over a long period. • CIAT, Palmira, Valle del Cauca. Initially, BIOLOGICAL CONTROL. Surveys in recent years Al. socialis populations at CIAT were low; in the Neotropics – especially in Colombia, however, since 1994, populations have Venezuela, Ecuador and Brazil – have identified increased dramatically and are presently a considerable number of natural enemies asso- higher than in Tolima. The reason for this ciated with the cassava whitefly complex. Gaps sudden increase in Al. socialis populations in knowledge about the natural enemy complex is not understood, but is evidence of associated with the different whitefly species the dynamics of cassava pest eruptions, have limited their effectiveness in biological con- emphasizing the present and potential trol programmes. Although a large complex of severity of whiteflies as cassava pests. parasitoids has been identified, there is limited Research is also being done at CIAT to identify knowledge about levels of parasitism, parasitism molecular markers linked to genes conferring rates for individual species, host specificity and resistance to Al. socialis in order to evaluate their overall effect on regulating whitefly further and understand the genetics of whitefly populations. resistance in cassava. Different breeding popu- Since 1994, CIAT has carried out surveys lations have been obtained from crosses between in northern South America for natural enemies. resistant (CG 489–34) and susceptible (M Col The most representative group is the micro- 2026) genotypes. Amplified fragment length hymenopteran parasitoids (Gold et al., 1989c; polymorphism (AFLP) and simple sequence Castillo, 1996; Evans and Castillo, 1998). In

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Colombia, species richness – primarily from the genera Encarsia, Eretmocerus and Amitus – was most frequently associated with Al. socialis, Several species of Lepidoptera feed on cassava, B. tuberculata and T. variabilis (Castillo, 1996). including E. ello (L), Erinnyis alope, Chilomima More than ten species – several unrecorded – clarkei (Amsel), Chilozela bifilalis (Hampson), were collected. Three of the Encarsia spp. were Phyctaenodes fibilialis, Agrotis ipsilon, Prodenia identified as Encarsia hispida, Encarsia pergandiella eridania and Phoenicoprocta sanguinea (Bellotti and Encarsia bellottii (Evans and Castillo, 1998). and van Schoonhoven, 1978a,b; Bellotti et al., None of the Eretmocerus and only one Amitus 1999). The stemborer Cm. clarkei causes break- (Amitus macgowni) have been identified. The age of cassava stems. A. ipsilon and Pr. eridania predominant species were E. hispida, Amitus sp. attack recently planted stem cuttings, resulting and Eretmocerus sp. The highest levels of para- in poor establishment; Ph. sanguinea is a leaf sitism observed for Al. socialis, B. tuberculata and feeder. Yield reductions attributable to these T. variabilis were 15, 14 and 12%, respectively, last three species have not been documented. although this varied according to geographic Attacks by E. ello and Cm. clarkei can reduce region (Castillo, 1996). Parasitism was higher in yields and are discussed in detail. the Andean zone than in the coastal and eastern plains regions of Colombia. In surveys conducted Cassava hornworms between 1997 and 1999 in Colombia, Encarsia was the genus most frequently collected from the E. ello () is one of the most serious Andean highlands, while Eretmocerus predomi- pests of cassava in the Neotropics (Bellotti et al., nated at lower altitudes on the Caribbean coast 1992, 1999). It has a broad geographic range, (CIAT, 1999). Moreover, the parasitoid species extending from southern Brazil, Argentina and complex associated with each whitefly species Paraguay to the Caribbean basin and the can be influenced by geographic area. On the southern USA. The migratory flight capacity of Caribbean coast, Al. socialis was most frequently E. ello, its broad climatic adaptation and wide parasitized by Eretmocerus, while in the Andean host range probably account for its wide distri- highlands it was Encarsia. In Valle del Cauca bution and sporadic attacks (Janzen, 1987). (1000 m altitude), 99.6% of the parasitism Several other species of Erinnyis feed on cassava. of Al. socialis was by Encarsia and 0.4% by The subspecies E. ello ello and E. ello encantado Eretmocerus. The most numerous complex of and the closely related species E. alope are all parasitoids species was found associated with reported from the Neotropics. B. tuberculata. Hornworm larvae feed on cassava leaves Greenhouse studies with E. hispida parasitiz- of all ages as well as on young, tender stems and ing Al. socialis show that the third whitefly instar leaf buds. Severe attacks cause complete plant is preferred. Parasitism rates reached 75% in the defoliation, bulk root loss and poor root quality third instar and 16, 45 and 43% in the first, sec- (Table 11.2). Although yield losses may be ond and fourth instars, respectively. The average severe, complete defoliation due to hornworm parasitism rate was 45%, and peak parasitism attack, or even repeated attacks, do not kill occurred 72–96 h after exposure (CIAT, 1999). cassava. The carbohydrates stored in the roots E. hispida is the most frequent parasitoid observed enable the plant to recover, especially under the when there are high populations of Al. socialis, more favourable conditions of the tropical rainy but its effectiveness in regulating the populations season. Repeated attacks are most common in the field is not known. when ill-timed pesticide applications destroy The influence of Al. socialis-resistant cas- natural enemies, but not fifth instar larvae or sava cultivars on parasitoid behaviour has prepupae of the pest (Braun et al., 1993). More- also been evaluated. Survival of E. hispida was over, large plantations of cassava are more prone not adversely affected by resistant genotypes. to frequent and repeated hornworm attacks. Parasitoid emergence was, however, consider- E. ello adults are grey nocturnal that ably lower from pupae of Al. socialis that fed oviposit small, round, light green-to-yellow eggs on the resistant cultivar M Ecu 72 than on the individually on the upper surface of cassava susceptible CMC 40 (CIAT, 1999). leaves. In field cage studies as many as 1850

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eggs were laid per female. This high oviposition, Trichogramma and Telenomus are the most impor- combined with the migratory behaviour of tant. Tachinid flies are the most important group adults, helps explain the rapid build-up of horn- among the dipteran larvae parasitoids; the worm populations and their sporadic occurrence , particularly Cotesia spp., are the (Janzen, 1987; Bellotti et al., 1992). During most important hymenopteran (Bellotti et al., the larval period, each hornworm consumes 1992, 1994). The commonest egg predators are c. 1100 cm2 of leaf foliage; c. 75% of this during Chrysopa spp. Important larval predators include the fifth instar. At 15, 20, 25 and 30°C the Polistes spp. (Hymenoptera: Vespidae), Podisus mean duration of the larval stage is 105, 52, 29 spp. (Hemiptera: Pentatomidae) and several and 23 days, respectively, indicating that peak spider species (Bellotti et al., 1992). Important hornworm activity may occur at lower altitudes entomopathogens include Cordyceps sp. (Acony- (< 1200 m), or during the summer in the cetes: Clavicipitaceae), a soil-borne fungus that subtropics (Bellotti and Arias, 1988). invades hornworm pupae, causing mortality. More recently, isolates of Beauveria sp. and CONTROL. E. ello’s strong flight abilities and Metarhizium sp. were found to cause high larval migratory flight capacity, combined with its mortality in laboratory studies (Múnera et al., broad climatic adaptation and wide host range 1999). (Janzen, 1986, 1987), often make effective con- The key to the effective use of biological con- trol difficult to achieve. Pesticides give adequate trol agents is the ability to synchronize the control if hornworm populations are detected release of large numbers of predators or parasites and treated while at the first three instar stages. during the early stages, preferably the egg or the However, farmers often react to attacks with first to third larval instars. Predator and parasite excessive, ill-timed applications of pesticides, effectiveness is limited by poor functional res- leading to repeated and more severe attacks ponse during hornworm outbreaks, which are (LaBerry, 1997). Larval populations in the of short duration (15 days). Successful control, fourth and fifth instar stages are not only diffi- therefore, requires monitoring of field popula- cult to control but also uneconomical, because tions to detect immigrant adults or larvae in the considerable defoliation has already occurred. early instars. This can be done with black lights Pesticide use also disrupts natural enemy popu- (Type T20T12BLT), which trap flying adults, or lations, leading to more frequent attacks (Urias by scouting for the presence of eggs or larvae López et al., 1987). (Braun et al., 1993). The complexities of syn- An extensive complex of natural enemies chronizing inundative releases of parasites and is associated with E. ello. Nevertheless, their predators with peak pest populations, suggests effectiveness is limited, most likely because of the theneedforacheap,storablebiologicalpesticide. migratory behaviour of the hornworm adults. A granulosis virus species of the family Adults migrating en masse will oviposit a consid- Baculoviridae was found attacking E. ello in cas- erable number of eggs in cassava fields (up to 600 sava fields at CIAT in the early 1970s. Pathoge- per plant), where natural enemy populations are nicity studies in the laboratory and field resulted too low to prevent an explosion of hornworm in nearly 100% mortality of hornworm larvae larvae, which can cause severe crop defoliation. (Bellotti et al., 1992; Braun et al., 1993; Table Because their rate of reproduction is limited, pre- 11.3). Infested larvae are collected from the dators and parasites cannot usually compensate field, macerated in a blender, filtered through sufficiently quickly to suppress dramatic horn- cheesecloth, mixed with water and applied to worm eruptions (Bellotti et al., 1992). hornworm-infested fields. Studies on the effect of Approximately 35 species of parasites, pred- virus concentration on mortality of larval instars ators and pathogens of the egg, larval and pupal showed a sigmoidal relationship for the first, stages have been recorded and reviewed exten- second and fourth instars. LC50 studies indicate sively (Bellotti and van Schoonhoven, 1978a,b; that progressively higher concentrations are Schmitt, 1983; Farias, 1990b; Bellotti et al., needed for adequate control of each succeeding 1992, 1999). Eight microhymenopteran species larval instar. Most fifth instar larvae reached of the families Trichogrammatidae, Scelionidae the prepupal state, but few female adults and Encyrtidae are egg parasites, of which emerged and those that did had wing deformities

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and died without producing progeny (Bellotti mobile and search for an appropriate feeding site, et al., 1992). generally around axillary buds. They form a pro- The hornworm baculovirus can be man- tective web, under which the first four instars aged by cassava growers themselves. They can feed, enlarging the web with each instar. In the collect and macerate diseased larvae and apply fifth instar the larvae penetrate the stem, where the virus suspension to their fields. The virus can they complete their cycle (6–12 instars), pupate be stored at low cost by refrigeration and and emerge as winged adults (Lohr, 1983). The wettable powder formulations of the virus are larval stage lasts 32–64 days; the pupal stage being developed. Hornworm management with within the stem is 12–17 days. Female adults live the virus was first implemented in southern 5–6 days (males 4–5 days), each ovipositing an Brazil, where light traps were used to detect adult average of 229 eggs. movement and invasions. Virus applications, Ch. clarkei populations occur throughout made when populations were in their early the year but are highest during the rainy season. instars, resulted in almost complete control From 4–6 overlapping cycles can occur during (Schmitt, 1988) and pesticide applications were the 1-year crop cycle, increasing potential dam- reduced by 60%. age and making control more difficult. Extensive The hornworm virus is an especially attrac- tunnelling by the larvae (> 20 can be found in tive option for use on large cassava plantations, one stem) cause stem breakage, leading to stem where pesticide applications have proved ineffec- rot and a reduction in the quality and quantity tive. In Venezuela, where the hornworm is of planting material (Table 11.3). Field studies endemic, the virus preparation was applied show that when > 35% of the plants suffer (70 ml ha−1) to 7000 ha via overhead sprinkler stem breakage, significant yield loss can occur irrigation systems when larvae were in the first (45–62%) (Lohr, 1983). On the Colombia and second instars, resulting in 100% control. Caribbean coast, 85% of the cassava fields had The virus has replaced pesticides and the cost of Ch. clarkei damage (Vides et al., 1996). gathering, processing, storing and applying it is only US$4 ha−1 (LaBerry, 1997). CONTROL. Once larvae enter the stem, control is very difficult. Moreover the web that covers the early larval instars offers protection from both Stemborers natural enemies and pesticide applications. The A complex of arthropod stemborers, which highly mobile early-instar larvae are more includes both coleopteran and lepidopteran spe- vulnerable and can be controlled by Bacillus cies, feed on and damage cassava. Long-horned thuringiensis [Bt]. Given the overlapping genera- beetles (Lagochirus spp.) are distributed world- tions, however, several applications would be wide, but do not appear to cause yield losses. necessary and they would be too costly for Stemborers are most important in the Neo- producers to adopt. Field research by Gold et al. tropics, especially in Colombia, Venezuela and (1990) showed that intercropping with maize Brazil. Seven species of Coelosternus (Coleoptera: reduced stemborer populations until the inter- Curculionidae) are reported reducing cassava crop was harvested. yields and quality of planting material in Brazil. Several natural enemies have been identi- However, the damage is generally sporadic or fied, including the hymenopteran parasitoids localized and does not significantly reduce yield Bracon sp., Apanteles sp. and Brachymeria sp. (Bellotti and van Schoonhoven, 1978a,b). (Lohr, 1983). More recently emphasis has been Populations of the stemborer C. clarkei placed on identifying resistant cassava germ- (Lepidoptera:Pyralidae)haveincreaseddramati- plasm. Approximately 1000 clones have been cally in Colombia and Venezuela in recent years evaluated on the Colombia Caribbean coast, and the species is now a major pest of cassava where Ch. clarkei populations are high. Evalua- (Vides et al., 1996). The nocturnal adult females tions are based on the number of Ch. clarkei holes oviposit in cassava stems, usually around the and tunnels in the stems and percentage stem bud or node. The egg stage is ~6 days (28°C). breakage. A number of clones with only 0–1 Upon hatching, first instar larvae feed on the hole per stem have been identified, indicating outer bark or stem epidermis. They are very varietal influence (CIAT, 1999). Nevertheless,

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field evaluations of germplasm using natural black lesions begin to develop on the roots within populations of a highly mobile pest can often give 24 h after feeding is initiated, resulting in starch misleading results due to ‘escapes’ (plants that reduction and a serious loss in commercial value have avoided damage by chance). Thus these (Table 11.2). As damage is not detected until cultivars will need to be evaluated over several roots are harvested and peeled, producers can cycles. lose the value of the crop and also labour, time CIAT has initiated research based on and land use. introducing insect-resistant Bt genes through C. bergi has five nymphal instars; nymphs Agrobacterium-mediated transformation into and adults can live for more than 1 year feeding cassava embryonic tissue to develop Ch. clarkei- on cassava roots (García and Bellotti, 1980). resistant cultivars. Initial results are promising C. bergi had a lifespan of 286–523 days when fed (CIAT, 1999). on slices of low-HCN cassava roots in the labora- tory (23°C, 65 ± 5% RH). Egg eclosion averaged 13.5 days; mean development time of the five Cassava burrower bug: C. bergi nymphal stages was 111 days; mean longevity C. bergi is one of the few arthropod pests that feed for adults was 293 days. directly on the tuberous roots of cassava, but C. bergi populations occur in the soil this polyphagous species has not co-evolved throughout the crop cycle and root damage with cassava. It was first recorded as a cassava starts in the first month of plant growth. Feeding pest in Colombia in 1980 (García and Bellotti, can continue throughout the crop cycle and can 1980) and more recently it has been reported result in 70–80% total root damage and > 50% causing commercial losses in Panama, Costa reduction in total starch content. C. bergi can Rica and Venezuela (Riis, 1997). C. bergi is cause serious economic damage, even if popula- probably present in many other areas of the tions are not high (Arias and Bellotti, 1985). Riis Neotropics, but feeding on other hosts including (1990) showed that even when populations onion, groundnut, maize, potato, Arachis pintoi were very low (~0), 22% of the roots were dam- (forage groundnut), sorghum, sugarcane, cof- aged. The economic injury threshold – the point fee, coriander, asparagus, beans, pea, pastures where cassava root purchasers will reject a con- and numerous weeds (Riis, 1997; Bellotti et al., signment – is when 20–30% of the roots are 1999). damaged, given that the ‘cosmetic’ damage of rot Some hosts are strongly preferred over spots is not acceptable for the fresh food market. others. Laboratory experiments indicate that C. bergi is strongly attracted to moist soil; cassava is not the optimal host. C. bergi develops it will migrate when soil moisture content is faster on maize and groundnut than on cassava below 22% and is most persistent when it exceeds and prefers maize to cassava (78 versus 22%) in 31%. The rainy season greatly favours adult free-choice feeding tests. The LD50 for adults was and nymphal survival, behaviour and dispersal; 95 days on maize, 69 on onion and 66 and 64 whereas low soil water content during the dry days, respectively, on sweet (CMC 40) and bitter season restricts adult burrowing and migration (M Col 1684) cassava (Riis, 1990). Optimal and increases nymphal mortality (Riis, 1997). fecundity, survival and intrinsic rate of popula- Field trials and laboratory studies strongly tion increase occurred on groundnut and pea- suggest that feeding preferences of C. bergi may nut, not on maize. Sweet cassava, sorghum and be related to the levels of cyanogenic glucosides onions were not favourable hosts and C. bergi in cassava roots. Adults and nymphs that fed could not complete its life cycle on bitter cassava on a high-HCN (> 100 mg kg−1 HCN) cultivar (Riis, 1997). had longer nymphal development, reduced egg C. bergi nymphs and adults feed on cassava production and increased mortality. Oviposition roots by penetrating the peel and parenchyma on CMC 40 (43 mg kg−1 HCN) was 51 eggs per with a thin strong stylet. This feeding action female versus only 1.3 on M Col 1684 (627 mg can introduce several soil-borne pathogens HCN equivalent kg−1). Adult longevity on CMC (e.g. Aspergillus, Diplodia, Fusarium, Genicularia, 40 (235 days) was more than twice that on M Col Phytophthora and Pythium spp.) into the root 1684 (112 days; Bellotti and Riis, 1994). Riis parenchyma (Bellotti and Riis, 1994). Brown-to- (1997) showed that oviposition on clones with a

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cyanogenic potential (CNP) of < 45 p.p.m. (fresh C. bergi feeding and damage. However, in many weight) was significantly higher than on clones cassava-producing regions, low CNP or ‘sweet’ with a CNP > 150 p.p.m., while oviposition var- cultivars are preferred, especially for fresh ied considerably on clones with CNPs between consumption. Recent studies indicate a potential 45–150 p.p.m. Additional studies indicate that resistance/tolerance to C. bergi in 15 low-CNP the earliest instars are most susceptible to root cultivars (Riis, 1997). The potential employment CNP. Due to the short length of the stylet, feeding of this resistance justifies research on pest behav- during the first two nymphal instars is confined iour, resistance mechanisms, biochemistry and mainly to the root peel (Riis, 1990; Riis et al., genetics. 1995), whereas third to fifth instars can feed The potential for biological control of C. bergi on the root parenchyma. CMC 40 has a low is being investigated and recent studies with cyanogen level in the root parenchyma, but a entomopathogenic nematodes and fungi indi- high level in the root peel (707 mg kg−1 HCN). cate a possible solution. This research, however, Laboratory feeding experiments resulted in 56% has been done only in the laboratory/green- mortality of first and second instar nymphs house and field studies are required before feeding on CMC 40 and 82% for those feeding on acceptable technologies can be recommended. M Col 1684. The high cyanogen level in the peel The nematode Steinernema carpocapsae suc- of CMC 40 is probably responsible for the high cessfully parasitized C. bergi in the laboratory, mortality rate (Bellotti and Riis, 1994). infecting it 5–8 days after exposure. The adult Feeding preference studies carried out in was most sensitive to infection (59% parasitism cassava fields in Colombia resulted in consider- after 10 days); the least sensitive were the first ably more damage to CMC 40 (the low-HCN and second instars, with 17 and 31%, respec- clone) than to M Col 1684. M Mex 59, with an tively (Caicedo and Bellotti, 1994). A native intermediate cyanogen content (106 mg kg−1 species, Heterorhabditis bacteriophora, found HCN) suffered moderate damage. These data parasitizing C. bergi in the field in Colombia, indicate that CNP may act as a feeding deterrent resulted in 84% parasitism of the instars and the C. bergi damage should not be a problem (Barberena and Bellotti, 1998). Isolates of the where cassava clones with high CNP are culti- entomopathogenic fungus Metarhizium anisoplae vated (i.e. northeast Brazil and many parts of have been recovered parasitizing C. bergi in the Africa; Bellotti and Riis, 1994). field. In laboratory studies mortality was highest (61%) during the fifth instar, overall average CONTROL. Control of C. bergi is difficult due to mortality was 33% (CIAT, 1994). the polyphagous nature of the pest and its adap- tation to the soil environment. Measures should be taken early in the crop growth cycle, either Cassava lacebugs during planting or within the first 2 months, Lacebugs (Hemiptera: ) are neotropical given the fact that initial damage can occur dur- cassava pests. Froeschner (1993) identified five ing this period. Pesticide applications can reduce Vatiga species that show a decided preference pestpopulationsanddamage.However,frequent for cassava: Vatiga illudens, Vatiga manihotae, applications may be required, and these are Vatiga pauxilla, Vatiga varianta and Vatiga cassiae. costly, environmentally hazardous, and often fail The first two are the most widely distributed. to reduce damage below economic injury levels V. illudens predominates in Brazil, but also (Castaño et al., 1985). Intercropping cassava occurs throughout the Caribbean area. V. mani- with Crotalaria sp. (sunn hemp) reduced root hotae predominates in Colombia and Venezuela, damage to ~4% compared to 61% damage in but is also reported from Cuba, Trinidad, Peru, cassava monoculture (Table 11.3). However, Ecuador, Paraguay, Argentina and Brazil. V. cassava yields were reduced by 22% when varianta is reported from Brazil and Colombia, intercropped and as Crotalaria has little commer- V. cassiae from Brazil, and V. pauxilla from cial value, producers are reluctant to adopt this Argentina. Moreover, A. machalana, referred technology. to as the black lacebug, damages cassava Experimental data and field observations in Colombia, Venezuela and Ecuador (CIAT, show that high CNP cultivars are resistant to 1990).

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A prolonged dry period is favourable for CONTROL. Lacebug control appears to be increasing lacebug populations (Salick, 1983). difficult as few natural enemies have been Adults and nymphs feed on the undersurface observed (Borrero and Bellotti, 1983; Salick, of lower leaves. Initially, white feeding spots 1983; Farias, 1985). Preliminary screening of appear, increasing in number and area until the cassava germplasm indicates that HPR may be leaf centres turn white and eventually darken. available (CIAT, 1990; Calvacante and Ciociola, High lacebug populations will cause leaves to 1993), but considerable research is still required curl and die. Younger plants (4–5 months old) before implementation is possible. attract higher populations, which tend to decline on older plants (Salick, 1983). The relationship between damage, popula- Secondary pests tion density and duration is unknown. A field trial at CIAT with natural populations The cassava arthropod pest complex includes of A. machalana resulted in 39% yield reduction numerous species that feed on cassava but they compared with pesticide-treated plots (CIAT, do not generally cause major economic damage 1990). to the crop. These ‘occasional’ or ‘incidental’ Field observations in Colombia indicate a pests either occur sporadically or at such shift in populations of lacebug species. In CIAT low population levels that yield is unaffected. cassava fields V. manihotae predominated until Outbreaks may occur in localized areas, and the mid-1980s. By 1990, A. machalana popula- populations may increase to the point where tions were considerably higher than V. manihotae they cause yield reductions. Moreover, changes and remained so for several years. Currently, V. in agronomic practices or varietal selection manihotae is again the predominant species and could influence pest populations, causing more it is difficult to find A. machalana in Colombian crop damage (Table 11.5). cassava fields (B. Arias, personal observation). ThethripsF.williamsicanreducecropyields The cause of this shift in populations is not under- of cassava by 5–28%, depending on varietal stood. In Ecuador populations of A. machalana susceptibility (Bellotti and van Schoonhoven, remain high. 1978a,b), especially in the seasonally dry Lacebugs are the least studied of the impor- tropics having a dry season of at least 3 months. tant cassava pests. Populations of V. illudens in F. williamsi can be controlled easily by using Brazil are endemic and appear to be causing yield the resistant pubescent cultivars that are readily losses, especially in the central Campo Cerrado available and commonly grown in these areas region and more recently in the south. Neverthe- (van Schoonhoven, 1974). If non-pubescent less, a sustained research effort has not been cultivars are introduced, thrips populations and attempted in order to understand fully the damage increases, resulting in yield losses. dynamics of lacebug populations, yield losses The fruitflies A. pickeli and A. manihoti nor- and control. Considering the present and poten- mally attack cassava fruit. This is a problem for tial importance of lacebugs, there is a dearth of plant breeders, but of no concern to producers. In published information. certain areas during the rainy season, however, females will oviposit in the tender upper portion BIOLOGY. The egg stage of V. manihotae is 8–15 of the cassava stem. The larvae tunnel into the days, followed by five nymphal stages averaging stem, providing an entrance for soft rot bacteria 16–17 days. Adult longevity under field condi- such as Erwinia carotovora. The bacteria can tions averages 40 days (Borrero and Bellotti, cause severe rotting of the stem tissue, resulting 1983). Laboratory studies with V. illudens in in apical dieback. Yield losses due to this damage Brazil show a nymphal duration of 13.5 days and have not been reported, although there is a an average adult longevity of 27 days (Farias, reduction in the quality of planting material, 1987). In laboratory studies with A. machalana, which may result in decreased establishment the egg stage averaged 8.2 days, the five and yield in the subsequent crop cycle (Bellotti nymphal instars 14 days and adult longevity and van Schoonhoven, 1978a,b). was 18 and 22 days for females and males, Shootfly (N. perezi) damage to the growing respectively (CIAT, 1990). points of cassava breaks apical dominance,

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Arthropod Pests 227 .

et al . (1988); . (1981); . (1986);

et al

et al et al . (1981); Bellotti and . (1981)

et al et al . (1981) . (1990); Modder (1994) Bellotti and van Schoonhoven (1978a,b); Frison and Feliu (1991); Lozano Peña (1978); Bellotti and van Schoonhoven (1978a,b); Lozano Bellotti and van Schoonhoven (1978a,b); Lozano References Bellotti and van Schoonhoven (1978a,b); Cock (1978); Lozano Bellotti and Kawano (1980); Bellotti and van Schoonhoven (1978a,b); van Schoonhoven (1974) Samways (1980) Bellotti and van Schoonhoven (1978a,b); Lal and Pillai (1981);and Peña Waddill (1982) Bellotti and van Schoonhoven (1978a,b); Lal and Pillai (1981); Lozano Samways (1980) Villegas and Bellotti (1985) Bellotti and van Schoonhoven (1978a,b); Diehl-Fleig (1981); Peña and Waddill (1982) Bellotti and van Schoonhoven (1978a,b); Lozano et al Samways (1980) Bellotti and Riis (1994); Bellottivan and Schoonhoven (1978a,b); Lomer et al Destroy infested stems; use scale-free planting material Use of damage-free planting material None required None required Soil pesticide treatment at planting Dusting of planting material with pesticide Cultural practices to maintain clean fields; destroy infested stems Toxic baits Entomopathogens being investigated Host plant resistance Control strategy < 20% fresh root yields; 50–60% loss in stem cutting 0–30% when infested stems used as planting material Not reported; reduced quality of planting material Not reported 95% loss in germination 46–100% loss of planting material Unknown Unknown Unknown Unknown 17–25% Reported yield loss Attack stems causing leaf fall; use of infested stems reduces establishment Bore fruit (seed) and stems, causing rotting of pith area Larvae kill apical buds, retarding plant growth, inducing lateral branching Yellowish green to red galls on upper leaf surface Feed on planting material, roots Tunnel in planting material, roots, stems, swollen roots Tunnel stems, stem breakage Tunnel stems, stem breakage Foliage removed Defoliation, stripping of bark Leaf distortion, bud reduction Type of damage Region Americas, Africa, Asia Americas, Costa Rica, Panama, Venezuela, Colombia, Brazil, Peru Americas Americas All regions All regions Americas, Brazil All regions Americas Mainly Africa, occasionally Americas Americas, Africa ) , , , , , spp. Eudiplosis spp., ( sp.

Acromyrmex spp., several others Important species Aonidomytilus albus Saissetia miranda Anastrepha pickeli Anastrepha manihoti Neosilba perezi Jatrophobia brasiliensis Leucopholis rorida Phyllophaga Coptotermes voltkevi Coptotermes paradoxis Coelosternus Lagochirus Atta spp. Zonocerus elegans Zonocerus variegatus Frankliniella williamsi Occasional and incidental pests of cassava. Table 11.5 Common name Scales Fruitflies Shootflies Gallmidges White grubs Termites Stemborers Leaf-cutting ants Grasshoppers Thrips

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228 A.C. Bellotti

retards plant growth and causes excessive season. This population will attack cassava branching. When younger plants are attacked, toward the latter part of the dry season when there is a reduction in the growth of the stems preferred herbaceous food plants become scarce used as planting material, but seldom in yield. (Modder, 1994). Experiments show that grass- If plants are being grown for quality cutting hoppers are deterred from feeding on cassava by production, then the crop needs to be protected the production of large amounts of HCN. The only during the first 3 months of growth. Usually early instars (I-IV) will not consume growing one timely pesticide application suffices to cassava and instars V and VI will eat growing protect the crop. cassava only if they have been deprived of food Mealybugs feeding on and damaging for a considerable period. Wilted cassava leaves cassava roots have been reported in recent years are readily eaten by all stages and result in high from two continents. In South America, P. grasshopper growth rate and high oviposition mandio has been reported from southern Brazil, (Bernays et al., 1977; Bellotti and Riis, 1994). Paraguay and Bolivia (Williams, 1985; Pegoraro Chemical control of grasshoppers has been and Bellotti, 1994), and Stictococcus vayssierei attempted in Africa. Although feasible, it does is reported from the Cameroon, Africa (Ngeve, not appear to be financially or ecologically 1995). Mealybug feeding can result in reduced sustainable, and in the mid-to-long term is not quality of tuberous roots and some plant defol- effective (Modder, 1994). iation. P. mandio females have three nymphal Biological control using entomopathogens instars and adults oviposit an average of 300 offers a more practical, safer and effective long- eggs, accounting for rapid population build-ups. term solution for grasshopper control. The ento- The life cycle from oviposition to adult was 25 mopathogens Metarhizium flavoviride, Beauveria days for females and 30 for males (Pegoraro bassiana and Entomophaga grylli have been and Bellotti, 1994). Yield losses of 17% have identified infecting Z. variegatus. Currently, a been reported; control through crop rotation is considerable effort is being made to develop suggested. effective biopesticides and application tech- Severe attacks of white grubs (Scara- nologies for grasshopper control. Results to date baeidae) and termites can destroy the cuttings are encouraging, especially with M. flavoviride used to establish new plantations (Bellotti and (Lomer et al., 1990; Modder, 1994; Langewald van Schoonhoven, 1978a,b). Populations of et al., 1997). scale , normally under natural biological control, can occasionally increase rapidly, espe- cially if infested stakes are planted, causing yield Trends in Pest Management losses and reduced availability of stems for use as planting material. Leaf-cutting ants can defoliate A successful integrated pest management (IPM) part or all of small plantations, possibly reducing programme in cassava will depend on having yields. effective, environmentally sound, low-cost pest Grasshopper (Zonocerus elegans, Zonocerus management technologies available to cassava variegatus) attacks in Africa are reported as farmers in developing countries. Currently causing severe crop damage, but reliable data available biotechnology tools offer the potential on actual root yield loss are scarce. Several coun- to develop improved pest-resistant cultivars and tries including Nigeria, Congo, Benin, Uganda, to enhance the effectiveness of natural control Côte d’Ivoire and Ghana report thousands of organisms, including parasitoids and entomo- hectares of cassava defoliated in some years, pro- pathogens. The new generation of genetic pest bably causing yield reductions (Modder, 1994). management technologies presently being inte- Simulated damage studies indicate a reduction in grated with traditional IPM offers alternative root yield (Toye, 1982) and in Nigeria, > 50% of technologies for controlling stemborers, leaf- the cassava crop is estimated to be lost in years of cutting ants, grasshoppers, white grubs and high grasshopper populations (Modder, 1994). other pests that are difficult to control. Research In Nigeria grasshopper oviposition usually activities in these areas are already under way occurs at the onset of the wet season and eggs and recommendations should soon be available hatch 6–7 months later, at the start of the dry to farmers.

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Pesticides Biological control

Pesticide use in traditional cassava agroeco- Classical biological control has been highly systems is minimal due to their prohibitive costs successful in Africa against introduced pests. and the long crop cycle of cassava, which may Management of many cassava pests in the necessitate several applications. Farmers in the Neotropics will require greater farmer involve- Neotropics, however, may respond to pest out- ment for the effective implementation of solu- breaks with pesticides. As cassava production tions (Bellotti et al., 1999). Numerous surveys shifts to larger plantations, there may be a of cassava fields in various regions of the Neo- greater tendency to apply pesticides to control tropics have revealed a species-rich complex of outbreaks, as already occurring in certain areas natural enemies of important cassava pests (see of Colombia, Venezuela and Brazil (Bellotti et al., sections on individual pests). CIAT maintains 1990). a taxonomic and working collection, with an There is considerable potential for the use accompanying computerized database, for of biopesticides to replace chemical pesticides cassava pests and their natural enemies. This in cassava pest management. The effectiveness information is available to producers and staff of the hornworm baculovirus and its successful of national agricultural research and extension implementation, especially on large plantations programmes, taxonomists and museums (LaBerry, 1997), exemplifies this possible trend. (Hernández et al., 1995). Entomopathogens have been identified for mites, Results from explorations and surveys indi- mealybugs, whiteflies, hornworms, burrower cate that considerable natural biological control bugs, white grubs, grasshoppers and others. Fur- may be occurring in the Neotropics. This is to ther research is required to develop biopesticides be expected because in many cropping systems, and methodologies for their effective implemen- cassava is grown as a functional perennial and tation. This will probably require a link to and certain pests and associated natural enemies collaboration with the biopesticide industry. This may be in equilibrium. A disruption of this has been initiated already in Colombia. system by, for example, the use of pesticides could cause pest outbreaks. As previously described, the CGM populations in northern South America Cultural practices appear to be regulated by a complex of phytoseiid predators, which, if disturbed, results in reduced Traditional farmers in most cassava-growing yields (Braun et al., 1989). The potential for regions have relied on an array of cultural prac- enhancing the effectiveness or virulence of tices that have often been effective in reducing natural enemies through genetic engineering pest populations (Lozano and Bellotti, 1985). offers further exploitation of this rich complex. Intercropping, as commonly practised by small farmers, has been shown to reduce populations and damage of whiteflies, hornworm and bur- Host plant resistance rower bugs (Castaño et al., 1985; Gold et al., 1989b, 1990). Farmers may, however, be reluc- CIAT’s germplasm bank of more than 6000 tant to adopt this practice if the intercrop species landrace cassava cultivars offers entomologists has little or no commercial value, or if cassava and breeders a potential pool of pest-resistance yields are reduced considerably (see ‘cassava genes. As previously described, differing levels burrower bug’). On larger plantations where of resistance have been identified for mites, mechanization is a standard practice, there may whiteflies, thrips, burrower bugs, lacebugs and be a reluctance to adopt intercropping. Addi- stemborers. The novel biotechnology tools now tional cultural practices that can reduce pest available facilitate access to resistance genes populations include use of varietal mixtures, and more efficient, quicker manipulation at destruction (burning) of plant debris, crop rota- the molecular level. A considerable portion of tion, changed planting dates and high-quality, this germplasm bank is grown continually in pest-free planting material (Lozano and Bellotti, the field and is available for systematic 1985). evaluation for pest resistance. Techniques and

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methodologies are now available for mass rear- References ing of most major cassava pests and damage and population scales have been described to identify Allem, A.C. (1994) The origin of Manihot esculenta resistant and susceptible germplasm. Accurate Crantz (Euphorbiaceae). Genetic Resources and germplasm evaluation needs to be done in the Crop Evaluation 41, 133–150. field using natural or artificial infestations. Angel, J.C., Pineda, B.L., Nolt, B. and Velasco, A.C. Damage symptoms of most cassava pests are (1990) Mosca blanca (Homoptera: Aleyrodidae) not expressed accurately on plants grown in asociadas a transmisión de virus en yuca. Fito- patología Colombiana 13, 65–71. the greenhouse or screen house, resulting in the Arias, B. (1995) Estudio sobre el comportamiento de la misidentification of resistance. ‘mosca blanca’ Aleurotrachellus socialis Bondar Cultivars that possess multiple resistance (Homoptera: Aleyrodidae) en diferentes geno- (i.e. to more than one pest) have also been identi- tipos de yuca, Manihot esculenta Crantz. MS thesis. fied. For example, M Ecu 72 has high levels of Universidad Nacional de Colombia, Palmira. resistance to whiteflies and thrips, and moderate Arias, B. and Bellotti, A.C. (1984) Pérdidas en rendi- levels to mites. One of the challenges confronting miento (daño simulado) causadas por Erinnyis geneticists and plant breeders will be to include ello (L.) y niveles críticos de población en difer- both disease and arthropod pest resistance in the entes etapas de desarrollo en tres clones de yuca. same cultivar. Revista Colombiana de Entomología 10, 28–35. Arias, B. and Bellotti, A.C. (1985) Aspectos ecológicos Perhaps the greatest source of pest resis- y de manejo de Cyrtomenus bergi Froeschner, tance is contained in wild Manihot species. More chinche de la viruela en el cultivo de la yuca than 100 of these species have been identified (Manihot esculenta Crantz). Revista Colombiana de (Allem, 1994) and small collections exist at Entomología 11, 42–46. several locations including CIAT, EMBRAPA/ Barberena, M.F. and Bellotti, A.C. (1998) Parasitismo Brazil and IITA. The cassava molecular genetic de dos razas del nemátodo Heterorhabditis map has been developed (Fregene et al., 1997), bacteriofora sobre la chinche Cyrtomenus bergi and this should provide a useful tool for develop- (Hemiptera: Cydnidae) en el laboratorio. Revista ing transgenic cassava plants (using other Colombiana de Entomología 24, 7–11. Manihot species) having pest resistance. Bellotti, A.C. and Arias, B. (1988) Manejo Integrado de Erinnyis ello (L.).Centro Internacional de Agri- Cassava IPM projects are few and the cultura Tropical (CIAT), Cali, Colombia. decision-making guides and strategies required Bellotti, A.C. and Kawano, K. (1980) Breeding for appropriate implementation of control approaches in cassava. In: Maxwell, F.G. and options are seldom available to small farmers Jennings, P.R. (eds) Breeding Plants Resistant to in traditional production systems (Bellotti et al., Insects. Wiley, New York, pp. 314–335. 1999). It is felt strongly that for large cassava Bellotti, A.C. and Peña, J.E. (1978) Studies on the plantation systems to succeed – especially in the cassava fruit fly Anastrepha spp. In: Brekelbaum, Neotropics where there is a large complex of T., Bellotti, A.C. and Lozano, J.C. (eds) Proceed- arthropod pests and diseases – the implementa- ings, Cassava Protection Workshop. Centro Inter- tion of an effective IPM system based on bio- nacional de Agricultura Tropical (CIAT), Cali, Colombia, pp. 203–208. logical control and varietal resistance is critical Bellotti, A.C. and Riis, L. (1994) Cassava cyanogenic for sustaining high yields. A promising approach potentialandresistancetopestsanddiseases.Acta to overcome the slow technology diffusion inher- Horticulturae 375, 141–151. ent with cassava producers is through the use of Bellotti, A.C. and van Schoonhoven, A. (1978a) farmer participatory methods and the inclusion Cassava Pests and Their Control. CIAT, Cali, of the private sector in setting the research Colombia. agenda and objectives. The successful imple- Bellotti, A.C. and van Schoonhoven, A. (1978b) Mite mentation of an integrated crop and pest man- and insect pests of cassava. Annual Review of agement pilot project with traditional farmers Entomology 23, 39–67. in northeast Brazil (Bellotti et al., 1999; Ospina Bellotti, A.C., Reyes, J.A. and Varela, A.M. (1983a) Observaciones de los piojos harinosos de la yuca et al., 1999) provides an example of how this can en las Américas; su biología, ecología y enemigos be accomplished. naturales. In: Reyes, J.A. (ed.) Yuca: Control

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