1Cassava, Manihot esculenta Crantz (Euphorbiaceae), is a perennial root crop native to tropical America and introduced into Africa by the Portuguese in the 1600s, and after into Asia. Since that time, cassava has constituted a major food crop for more than 500 million people in the tropical countries of Africa, Asia and Latin America. It is cultivated mainly for its starchy storage roots, but also for its leaves.

2Cassava can endure several months of drought during its seasonal cycle. This is accomplished by a reduction in the plant’s evaporative surface and by enhancement of the efficiency of water use through stomatal closure. Resistance to drought is further achieved by increasing the concentration of cell metabolites (sucrose, free amino acids and organic acids levels) to maintain the osmotic pressure of the cells. These mechanisms of stress avoidance are extremely effective in cassava, explaining the plant’s ability to withstand prolonged periods of drought. The photosynthetic CO₂ assimilation pathway of cassava has been a matter of debate. Early work classified cassava as a C₃-C₄ intermediate. Recently, it was demonstrated that the plant displayed C₃ photosynthesis. In conclusion, cassava does not possess a particular photosynthetic metabolism that enables the plant to resist drought, but it does exhibit efficient mechanisms of drought resistance generally displayed by the C₃ plants.

3In Africa and South America, outbreaks of natural populations of phloem feeder insects, occur on cassava every year during the dry season causing severe damages. The insects are two oligophagous mealybugs species, Phenacoccus manihoti Matile-Ferrero and Phenacoccus herreni Cox & Williams (Sternorrhyncha: Pseudococcidae), displaying a typical phloem-feeding behaviour and a predominance of extracellular pathways of the stylets. Several methodologies (microscopic observations, physiological studies...) have been used to study the mealybug–plant interactions. The third trophic level relative to natural enemies (parasitoids and predators) has been also considered.

4The cassava mealybug, Phenacoccus manihoti, possesses sensilla on its antennae that can detect chemicals released by the plant by olfaction and contact. The presence of contact and olfactory chemoreceptors on the labial tip suggests that by tapping the cassava leaf, information about the chemical nature of the leaf surface can be gathered. Linamarin, a cyanogenic compound present on cassava phylloplane, is involved in host-plant recognition and acceptance by the mealybug mobile stages (crawlers). Electropenetrography (EPG) recordings suggest a possible use of cyanides or cyanogenic compounds as allelochemicals for host recognition during the cell penetration process by P. manihoti.

5As mentioned above the cassava mealybugs are phloemophagous insects, reaching then the phloem sap of cassava. It has been demonstrated for P. herreni that the delay in reaching the phloem by the stylets is less when the insect is located near a major leaf vein, explaining why the mealybugs are usually spaced in areas around a major leaf vein. In the case of P. manihoti, it was observed also that on less preferred host plants, it takes longer for the stylets to reach the phloem; this appears to be related to the higher levels of phenolic acids in the apoplastic compartment of leaf tissues of such plants.

6During the stylets pathway process to reach the phloem sap, P. manihoti secretes pectinolytic salivary enzymes that facilitate intercellular stylet penetration into the host tissues by digesting the constituents of the middle lamellae and primary cell walls. An analysis of the enzymes present in the midgut of P. herreni was carried out, and the intestinal pH was estimated to be between pH 6.8–7.6, close to that of the phloem sap, which ranges between pH 7.2–8.5. As mealybugs are mainly phloemfeeders with a diet of simple food constituents such as free amino acids, only a few enzymes were detected in the midgut. Of 19 enzymes assayed, only alkaline phosphatase, esterase and leucine aminopeptidase activities were evident in the midgut of the insect.

7It has been demonstrated that linamarin (a cyanogenic glucoside) is translocated by the phloem sap of cassava. Although this compound appears to have a limited effect on mealybug development and physiology, it plays an important role in stimulating feeding. In contrast, rutin (a flavonoid glycoside), also translocated by the phloem sap of cassava, affects the growth and the development of the insect. These results have been demonstrated with P. manihoti.

8Phagostimulants play a very important role in cassava mealybugs and in phloemfeeding insects in general. Sucrose has been found to be a strong phagostimulant. Studies on P. herreni showed that certain amino acids, either alone or in combination, act synergistically with sucrose as phagostimulants. Aspartic acid, glutamic acid, valine and alanine are important phagostimulatory factors, whereas lysine, ornithine, asparagine, methionine and histidine have a mainly nutritive function. Other amino acids such as glutamine, cysteine, tryptophan, glycine and arginine play both phagostimulant and nutritional roles. Glutamine, cysteine, tryptophan, lysine, ornithine, asparagine, glycine, methionine and arginine were found to be essential for the development of P. herreni. Other compounds such as vitamins, cholesteryl benzoate and oligoelements also are important constituents of the development of mealybugs.

9As mentioned above, outbreaks of natural populations of cassava mealybugs occur on cassava every year during the dry season in Africa and South America. Since in drought-stressed cassava nutrients such as sucrose and amino acids are either more concentrated or better balanced, such plants are more suitable for the development and reproduction of mealybugs. This has been demonstrated with P. herreni. Simultaneously, it has been demonstrated with P. manihoti that the partial resistance of cassava (both antixenosis and antibiosis) decreases during the dry season. All the above-mentioned conditions combine to ensure that drought-stressed plants are physiologically more favourable for infestation by the cassava mealybugs, and serve to enhance mealybug infestation build-up during long dry seasons in the field.

10Cassava resistance to mealybugs involves both intrinsic mechanisms (antixenosis, antibiosis and tolerance) and extrinsic mechanisms, which are related to the interactions between mealybug-infested plants and natural enemies. Antixenosis of cassava to P. manihoti involves chemical factors such as linamarin for initial host recognition and for phagostimulation of larvae and adults, suggesting that cassava varieties with high levels of linamarin are the most preferred by the pests.

11Rutin in cassava disrupts P. manihoti growth and development by having an anti-nutritive effect, delaying the insect’s development into the adult rather than having a toxic effect, as no toxicity was observed. This compound participates in the antibiosis resistance of cassava to P. manihoti, or is at least linked to an induced (defensive?) reaction of cassava towards the insect. This defensive reaction is manifested by an increase in the levels of rutin and also of total phenolic compounds (mostly flavonoids) after mealybug infestation.

12All cassava varieties studied to date are tolerant to P. manihoti infestation. Although different levels of partial resistance (antixenosis and antibiosis) are evident, total resistance (complete absence of mealybugs) has not been found in M. esculenta. Jatropha gossypiifolia (Euphorbiaceae), a species closely related to Manihot esculenta, has been shown recently to display total resistance to P. herreni by both antixenosis and antibiosis mechanisms, resulting in a 100% mortality shortly after infestation. Therefore, the use of J. gossypiifolia in a breeding programme might afford an opportunity for obtaining hybrid plants resistant to the cassava mealybugs.

13It has been demonstrated with P. manihoti and its natural enemies that mealybug infested cassava plants have been shown to be a source of volatiles that attract at long distances both female parasitoids and coccinellids to the microhabitat of the herbivore. This emission of volatiles does not appear to be limited to the infested parts of the plant, but occurs systemically throughout the plant. After landing on an infested plant, the mealybug-derived chemicals such as the O-caffeoylserine from the body surface of the insect, play a role in host location for the parasitoid. This last result has been demonstrated with P. herreni and its associated parasitoids.

14The above results on resistance mechanisms of cassava to mealybugs show clearly that different types of mechanism are involved in cassava resistance towards the insects. Current plant breeding programmes to improve the resistance of plants to insects generally consider only intrinsic resistance mechanisms but not extrinsic mechanisms (i.e. effects of plants on the third trophic level). Future cassava breeding programmes should consider a more holistic approach by integrating the different resistance mechanisms reported here.

15After more than 30 years of intensive research on the cassava mealybugs, some questions have never been resolved, among them the reasons for the year-to-year regional fluctuations in P. manihoti infestations in Africa and the inefficiency of the introduced parasitoid Apoanagyrus lopezi in a number of ecological conditions. Both P. manihoti and A. lopezi originate from a restricted area of 100,000 km² in Paraguay, where the insect population is naturally well regulated by the parasitoid, but where the ecological conditions are quite different from those in Africa where both species are now distributed over an area of about 8 million km². The new and highly variable ecological conditions in the new area of distribution might have caused the differentiation of geographical populations of mealybugs, and as a consequence might have modified the cassava–mealybug interactions and the suitability of the mealybug to A. lopezi, its main natural enemy. This is likely because both the second (P. manihoti) and third (A. lopezi) trophic levels are highly specialized.

16Cassava was introduced into Africa four centuries ago by the Portuguese, while the introduction of the cassava mealybug and its parasitoid occurred more recently, 35 and 20 years ago, respectively. The three trophic levels have evolved separately under different abiotic and biotic constraints. Future prospects on cassava–mealybug–natural enemies interactions should consider the population variability of the three trophic levels at both phenotypic (phenotypic plasticity) and genetic (modification of the genome under selection pressure) levels. Understanding how cassava–mealybug–natural enemy interactions evolved should help in developing a more effective strategy for integrated management of the cassava mealybugs, pests which have the potential to wreak havoc on the food security of peoples in the tropics who rely on this crop as a vital food staple.