1The main climatic constraint for cultivated crops in the tropics is the presence of long periods of drought. Insect densities often increase under such conditions of environmental stress (White, 1974; Mattson & Haack, 1987; Koricheva et al., 1998). Several reasons have been advanced to account for such increases, including improved food quality (White, 1974; 1984), reduced efficiency of natural enemies, and direct effects of the abiotic environment (Mattson & Haack, 1987). Of the above, food quality has received most attention (Mattson & Haack, 1987; Larsson, 1989; Koricheva et al., 1998). Biochemical changes leading to enhanced insect performance have been shown to take place in plants under abiotic stress, for instance increases in concentrations of soluble amino acids (White, 1974; 1984), thus possibly contributing to insect outbreaks (Mattson & Haack, 1987). This hypothesis has been criticized by Larsson (1989) and Koricheva et al. (1998), who suggest that stress from water limitation either has nil or a negative effect on insects. A possible explanation for these inconsistent findings is the fact that insects differ in their feeding modes and should therefore respond differently to changes in food quality under stress conditions (Mattson & Haack, 1987; Larsson, 1989). This is exemplified by the response of phloem-feeding insects, which is stronger (i.e. an enhanced performance) compared to that of chewing and leaf-feeding insects (Larsson, 1989; Larsson & Björkman, 1993; Koricheva et al., 1998).

2In Africa and South America, outbreaks of natural populations of P. manihoti and P. herreni, respectively, occur on cassava every year during the dry season (Fabres, 1981; Bellotti et al., 1983; Noronha, 1990; Le Rü et al., 1991). For example, the number of P. manihoti individuals multiplies within 7 to 10 weeks from less than 10 individuals per plant (the number usually seen in the rainy season) to about 100 per plant. These dramatic changes in number occur together with important modifications in plant physiology (e.g. cessation of development of the plant) at the onset of the period of water stress (Le Rü et al., 1991). These observations suggest that some changes in the trophic quality of cassava positively influence the abundance of mealybugs, expressed as a temporary alteration in resistance against the insect during the dry season. Although it might be thought that the strong decrease of mealybug populations at the beginning of a rainy season is due to the mechanical action of the rain. However, using a rainfall simulator, Le Rü and Iziquel (1990) demonstrated that although rain acts mechanically to produce variations in P. manihoti numbers, it is not a unique cause of the fast decrease in mealybug populations generally observed during the beginning of a rainy season. These authors conclude that the mechanisms responsible are probably numerous and complex, including not only the mechanical action of the rain, but also the impact of disease, the action of natural enemies, and the changes in host-plant physiology.

3To test the hypothesis that the frequently observed increase in mealybug populations on cassava during periods of drought occurs as a result of cassava’s undergoing important modifications in plant nutrients, the physiological modifications of cassava to resist water limitation stress were studied and their influence on mealybug growth and development investigated.

INFLUENCE OF DROUGHT STRESS ON CASSAVA

4Cassava can endure several months of drought during its seasonal cycle. Although some cassava varieties are more tolerant to drought stress than others, Manihot esculenta is generally highly resistant to long dry seasons (El-Sharkawy, 1993). This is achieved by the plant’s reducing its evaporative surface (El-Sharkawy, 1993). Calatayud and colleagues (2000a, b) have shown under laboratory conditions that the stems stop growing from the onset of the period of water limitation stress, while the number of leaves per plant decreases due to a dramatic acceleration of leaf senescence and leaf drop in addition to a substantial decrease in leaf emergence (Figure 4.1); the leaf area that emerges and expands during water limitation is about half of that in the control. All these modifications lead to a substantially reduced leaf canopy.

5Similarly to other plants in general, cassava also resists drought by enhancing water use efficiency through stomatal closure (El-Sharkawy, 1993). Stomatal conductance is very low under water-limiting conditions, whatever the leaf age. A small transitory increase is nevertheless detectable in young leaves at the beginning of the morning, explaining the remaining maintenance photosynthetic rate under water stress conditions (Calatayud et al., 2000a, b). The leaves of cultivated cassava as well as of wild species are predominantly hypostomatic, i.e. with stomata on the lower face of the leaves (P.-A. Calatayud, unpublished observation). A few varieties and species, however, possess amphistomatic leaves with stomata on both the upper and lower surfaces, but with a low stomatal density on the upper face (Figure 4.2). This anatomical characteristic of having stomata mostly on the lower leaf face may contribute to a favourable adaptation of cassava to water stress by limiting evaporation.

6Another physiological response of cassava to long periods of drought is an increase in cell metabolite concentrations, which probably works to maintain the osmotic pressure of the tissues for protection of cellular structures (Calatayud et al., 2000a). The total amount of glucose, fructose and sucrose in leaf tissues increases following water limitation. In addition, the free amino acid level increases, with serine, glutamic acid, glutamine and arginine concentrations reaching very high levels. An increase in the levels of some organic acids such as malate, succinate and citrate was also observed. The increase in the levels of sucrose and organic acids in leaves of water-depressed plants is associated with higher activities of sucrose phosphate synthase and phosphoenolpyruvate carboxylase (PEP case), respectively.

7All of these mechanisms of stress avoidance (reduction of the evaporative surface, efficient stomatal closure and increase in cell metabolite concentration to maintain cell osmotic pressure) are the main mechanisms commonly used by plants. However, they are extremely effective in cassava, explaining in part why this plant is highly resistant to long periods of drought.

PHOTOSYNTHESIS IN CASSAVA

8Atmospheric carbon dioxide (CO₂) is generally assimilated into 3- or 4-carbon compounds by plants, giving rise to type C₃ or C₄ photosynthetic plants. Since in C₄ photosynthetic plants water-use efficiency is increased and photorespiration is suppressed, C₄ plants are often more competitive than C₃ plants in drought areas and in warm environments (Edwards & Ku, 1987). In cultivated cassava, the photosynthetic CO₂ assimilation pathway has been a matter of debate (Angelov et al., 1993). Early work classified cassava as a C₃-C₄ intermediate (El-Sharkawy & Cock, 1987). Later, it was demonstrated that the plant displayed C₃ photosynthesis (Edwards et al., 1990). Nevertheless, leaves of Manihot species have distinct green bundle sheath cells (cells with chloroplasts immediately surrounding the phloem cells, a typical anatomical feature of C₄ plants) which are unusual in type C₃ leaves (Angelov et al., 1993) (Figure 4.3).

9The difficulty in determining the photosynthetic CO₂ assimilation pathway in cassava could be due to the fact that M. esculenta is thought to be derived from wild species possessing C₄ photosynthesis. Studies by Calatayud and co-workers (2002b), however, have demonstrated that most of the Manihot species, including M. flabellifolia—considered to be the wild progenitor of cultivated cassava, M. esculenta (Fregene et al., 1994; Roa et al., 1997)—exhibit typical C₃ characteristics. This is evidence that cultivated cassava is not derived from wild species possessing C₄ photosynthesis.

10In conclusion, cassava does not possess a particular photosynthetic metabolism that enables the plant to resist drought, but it does exhibit efficient mechanisms limiting evapo-transpiration and water loss, as well as maintaining the osmotic pressure of the leaf tissues.

INFLUENCE OF WATER LIMITATION ON PLANT–MEALYBUG INTERACTIONS

11Under controlled environmental conditions, P. manihoti exhibits the highest intrinsic rate of increase of plants under drought stress, indicating that cassava grown under water shortage enhances P. manihoti performance (Fabres & Le Rü, 1988). Water limitation induces changes in cassava physiology that also favour P. herreni development and reproduction (Calatayud et al., 2002c). The fecundity and adult weight of mealybug females are higher on plants under water stress. The insects also grow faster and the maturation of females (evidenced by the start of egg-laying into an ovisac) is faster on plants under water limitation stress, as illustrated in Figure 4.4.

12The faster development of P. herreni on water-stressed plants can be related to nutritional factors. An increase in the level of sucrose and free amino acids in the artificial diet favours mealybug growth (P.-A. Calatayud, unpublished data). Moreover, some amino acids such as glutamine and arginine, whose levels increase strongly in cassava leaves under water limitation, play an important role in the development of the P. herreni female; for example, when these constituents are absent in the diet, the insect does not grow to the adult stage (Calatayud et al., 2002c). This demonstrates the importance to mealybug growth of increased levels of free amino acids such as glutamine and arginine in the mesophyll cells, and consequently in the phloem sap, of cassava leaves under water limitation.

Accumulated percentage of mature female (i.e. beginning to form ovisac) of Phenacoccus herreni reared on cassava (var. CMC 40) grown with normal (N) or low (L) water availability

13The molar ratio of sucrose to free amino acids in cassava leaves has been shown to decrease by half under conditions of low water availability (Calatayud et al., 2000a). Studies using artificial diets with two distinct sucrose/total free amino acids ratios (5 and 2.5), showed that the 2.5 diet ratio (corresponding to the molar ratio found in cassava leaves under low water availability) favours mealybug growth (Table 4.1) (CIAT, 1999). The weight of adult females was significantly higher on this diet, and this is due to a more balanced ratio of sucrose to free amino acids.