The effect of the cassava green mite Mononychellus tanajoa on the growth and yield of cassava Manihot esculenta in a seasonally dry area in Kenya

The effect of the cassava green mite Mononychellus tanajoa on the growth and yield of cassava Manihot esculenta was studied over a 10-month period in two field trials near Lake Victoria in Kenya. One plot was maintained free of mites by means of acaricide, while the other was artificially infested.The highest population density of M. tanajoa occurred during the dry season. A maximum leaf area index (LAI) of about 2 was reached at the onset of the dry season. The total leaf area of mite infested plants was reduced compared with uninfested plants during the dry spell. During the following rainy season infested plants recovered and attained the same leaf area as uninfested plants. A multiple regression model predicting the leaf area showed that 58% of the seasonal variation could be explained by plant age, soil water, and leaf injury.The net growth rate of infested plants was lower than that of uninfested plants. Maximum values of 21 (infested plants) and 49 (uninfested plants) g m^-2 week^-1 were attained at the onset of the second rainy season. No difference was found between uninfested and infested plants with respect to net assimilation rates per unit leaf area during the dry season. The net assimilation rates reached a maximum almost at the same time as the growth rates, but the infested plants peaked slightly earlier and at a lower level than the uninfested plants. M. tanajoa did not affect the relative allocation of dry matter into stems and storage roots, but the absolute allocation of dry matter declined with increasing mite injury. Thus, after 10 months the dry matter of infested plants was reduced by 29% and 21% for storage roots and stems, respectively, compared with the uninfested plants.     

Sampling strategies for assessing the overall density of the cassava green mite (Mononychellus tanajoa)

Six different sampling methods to estimate the density of the cassava green mite, Mononychellus tanajoa, are categorized according to whether leaves or leaflets are used as secondary sampling units and whether the number of leaves on the sampled plants are enumerated, estimated from an independent plant sample, or not censused at all. In the last case, sampling can provide information only on the average number of mites per leaf and its variance, while information on stratum sizes is necessary to estimate the mean number of mites per plant as well. It is shown that leaflet-sampling is as reliable as leaf-sampling for the same number of sampling units. When stratum sizes are estimated from a separate plant sample, sampling time may also be reduced, but the estimated mean density and its variance may be biased if mite density and plant size are correlated. Sampling data show that the within-plant variance contributes relatively little to the overall variance of the population density estimates. It points at a sampling strategy in which the number of primary units (plants) is as large as possible at the expense of secondary units (leaflets) per plant. Mean-variance relationships may be applied to estimate sample variances and can be used even when only one leaflet is taken per plant per stratum. An unequal allocation of primary units among strata can increase precision, but the gain is small compared with an equal allocation. Leaf area can be predicted from the length of the longest leaflet and the number of leaflets.     

Sampling strategies for assessing the intra-plant density of the cassava green mite (Mononychellus tanajoa): A case-study

Sampling data from a single cassava plant were used for testing various sampling methods. It was found that the degree of leaf damage was poorly correlated with the number of cassava green mites (CGM) present on a leaf. Sampling of specific mite stages should take into consideration the effect of leaf damage on the age distribution of the mites. Simple random sampling resulted in a high between-leaf variation caused by a vertical gradient in spider-mite abundance. The between-leaf variation could be reduced by stratified sampling. The optimum number of strata was three. Subsampling of leaflets combined with stratification provided the most precise estimates for a given sampling effort.Various regression methods for estimating the area of a cassava leaf from some simple measurements were compared. Combining the length of the longest leaflet with the number of leaflets gave the best prediction, explaining 95.8% of the total variation in observed leaf areas.     

Failure of the mite-pathogenic fungus Neozygites tanajoae and the predatory mite Neoseiulus idaeus to control a population of the cassava green mite, Mononychellus tanajoa

Monitoring of a population of the phytophagous cassava green mite, Mononychellus tanajoa (Bondar), and its natural enemies was undertaken in central Bahia, Brazil, in mid-1996. In spite of the presence of extremely high densities of the predatory phytoseiid mite Neoseiulus idaeus Denmark & Muma, the phytophagous mite population reached such high densities itself that there was total overexploitation of the cassava plants, leading to total leaf loss. Meanwhile, the mite-pathogenic fungus Neozygites tanajoae Delalibera, Humber & Hajek did not affect the M. tanajoa population in its growth phase as there was no inoculum present, even though we predict from a simple regression model that there was the potential for epizootics at that time. Soon after the M. tanajoa population crashed due to defoliation, there could have been an epizootic but there were simply no mite hosts to infect. These data demonstrate the ineffectiveness of one natural enemy (the predator) in terms of prey population regulation and demonstrate the importance of timing in the possible effectiveness of the other (the pathogen). For the pathogen, this probably explains its sporadic effect on host populations as previously reported. We conclude that the fungus is likely to be most useful as an adjunct to biological control with predatory mites other than N. idaeus.     

Relative contribution of biotic and abiotic factors to the population density of the cassava green mite, Mononychellus tanajoa (Acari: Tetranychidae)

The cassava green mite, Mononychellus tanajoa, is a key pest of cassava, Manihot esculenta Crantz (Euphorbiaceae), and it may be kept in check by naturally occurring predatory mites of the family Phytoseiidae. In addition to predatory mites, abiotic factors may also contribute to regulate pest mite populations in the field. Here, we evaluated the population densities of both M. tanajoa and the generalist predatory mite Euseius ho DeLeon (Acari: Phytoseiidae) over the cultivation cycle (11 months) of cassava in four study sites located around the city of Miranda do Norte, Maranhão, Brazil. The abiotic variables rainfall, temperature and relative humidity were also recorded throughout the cultivation cycle of cassava. We determined the relative importance of biotic (density of E. ho) and abiotic (rainfall, temperature and relative humidity) factors to the density of M. tanajoa. The density of M. tanajoa increased whereas the density of E. ho remained constant throughout time. A hierarchical partitioning analysis revealed that most of the variance for the density of M. tanajoa was explained by rainfall and relative humidity followed by E. ho density and temperature. We conclude that abiotic factors, especially rainfall, were the main mechanisms driving M. tanajoa densities.     

Potential of the mite-pathogenic fungus Neozygites floridana (Entomophthorales: Neozygitaceae) for control of the cassava green mite Mononychellus tanajoa (Acari: Tetranychidae)

The cassava green mite, Mononychellus tanajoa (Bondar), is an exotic pest in Africa and is the target of a classical biological control programme. Field data from the Neotropics, where it is indigenous, are presented for the first time, charting the variation in abundance of M. tanajoa over several seasons. This was highly variable, with a characteristic trough mid-year and a peak at the turn of the year. This pattern corresponded positively with rainfall levels, appearing to fit a phenology also characteristic of African studies, where rainfall at the start of the wet season promotes a leaf flush and so growth in M. tanajoa populations. Analyses implied some impact of leaf-inhabiting predatory mites (predominantly Neoseiulus idaeus Denmark & Muma) and a considerable impact of the fungal pathogen Neozygites floridana Fisher on M. tanajoa populations. This pathogen was not observed in the host population for several (generally dry) periods implying survival outside the host, perhaps as resting spores. This is a particularly desirable characteristic of a biological control agent. It is therefore proposed that N. floridana might be of particular use in drier cassava-growing areas where rainfall at the outset of the wet season is not sufficiently intense to cause heavy M. tanajoa mortality but may be sufficient to stimulate epizootics of the fungal pathogen, protecting the flush of new cassava growth.     

A rapid and non-destructive method to assess leaf injury caused by the cassava green mite,Mononychellus tanajoa (Bondar) (Acarina: Tetranychidae)

A relative scale of Leaf Damage Indices (LDI) from 0 to 5 describes the visible injury to leaves of cassava, Manihot esculenta Crantz caused by the cassava green mite, Mononychellus tanajoa (Bondar). As the scale is ordinal and thus not quantitative, the observed LDIs are converted individually to relative loss of chlorophyll on a ratio scale before an average injury is determined. This calibration is required because the ordinal and the ratio scales are not linearly related. A calibration curve was established on the basis of laboratory experiments to determine the chlorophyll content, c, of leaves representing various leaf damage indices. Several monotonously decreasing functions were fitted to the experimental data yielding the following relation , where c _o is the chlorophyll content of unijured leaf tissue and a is a constant describing the steepness of the curvilinear relation. This means that LDIs could be converted to relative loss of chlorophyll, d, where . The photosynthetically active leaf area of plants can be estimated by combining the relative loss of chlorophyll with leaf area assessments and adds the effects of defoliation and suspended growth to the chlorophyll depletion. The difference in photosynthetically active area that arises between uninjured and injured plants over a period of time provides a measure of spider mite injury that can be related to growth and yield. The method integrates the injury inflicted over a period of time, allows successive observations of the same plants, and is rapid and reasonably precise considering the time savings.     

Mix‐planting pubescent and glabrous cassava affects abundance of Typhlodromalus aripo and its prey mite Mononychellus tanajoa

There is an increasing awareness that vegetation diversity can affect herbivore and natural enemy abundance and that plants can play a major role in directly manipulating natural enemy abundance for protection against herbivore attacks. Using data from cassava fields, we aimed at (i) testing the capacity of the predatory mite Typhlodromalus aripo to control the herbivorous mite Mononychellus tanajoa in a chemical exclusion trial; and (ii) testing, based on the differential preference by T. aripo for cassava cultivars, how combinations of two morphologically different cassava cultivars with differential suitability to the predator can improve its population densities on the non‐favourable cultivar, thereby reducing M. tanajoa densities with subsequent increases in cassava yield. The study was conducted in a cassava field in Benin, West Africa. The experiments confirmed that T. aripo effectively suppresses M. tanajoa populations on both cultivars and showed, in the no‐predator‐exclusion experiments, that cultivar combinations have significant effects on M. tanajoa and T. aripo densities. Indeed, T. aripo load on the non‐preferred cultivar was lowest in subplots where the proportion of T. aripo‐preferred cultivar was also low, while, and as expected, M. tanajoa load on the non‐preferred cultivar showed decreasing trends with increasing T. aripo densities. The possible mechanisms by which cultivar mixing could increase predator load on the non‐favourable cultivar were discussed. Our data showed that appropriate cultivar combinations effectively compensate for morphologically related differences in natural enemy abundance on a normally predator‐deficient cultivar, resulting in lower pest densities on the non‐favourable cultivar. In practical terms, this strategy could, in part, enhance adoption of cultivars that do not support sufficient levels of natural enemies for pest control.     

Importance of ambient saturation deficits in an epizootic of the fungus Neozygites floridana in cassava green mites (Mononychellus tanajoa)

The mite-pathogenic fungus Neozygites floridana Fisher (Entomophthorales: Neozygitaceae) is considered to have potential for the biological control of the cassava green mite, Mononychellus tanajoa (Bondar). However, its activity is sporadic and laboratory data suggest a strong dependence on night-time saturation deficits for transmission. We report on an epizootic of this fungus in a mite population in northeastern Brazil. During the epizootic, host populations appeared to be limited by a combination of the pathogen and a predatory mite Neoseiulus idaeus (Acari: Phytoseiidae). When temperatures increased, the epizootic finished and the host population began to grow. Abiotic conditions could not explain the variation in host mortality following pickup of infective propagules in this epizootic. However, night-time saturation did help to explain the variation in transmission from infective cadavers to newly killed hosts. This supports laboratory observations that horizontal transmission between hosts is determined mainly by saturation deficits, while the process of infection is little affected by abiotic conditions. A further field observation was the near-absence of resting spores in dead mites (ca. 0.1% of cadavers), suggesting that the pathogen population was unsuccessful in producing inoculum to infect future M. tanajoa populations. The implications are that this pathogen will only be effective as a biological control agent in periods of high relative humidity, and establishment in new areas may be limited by resting spore formation. This revised version was published online in July 2006 with corrections to the Cover Date.     

Functional responses of Iphiseius degenerans and Neoseiulus teke (Acari: Phytoseiidae) to changes in the density of the cassava green mite, Mononychellus tanajoa (Acari: Tetranychidae)

The functional responses of protonymph and adult female Iphiseius degenerans and Neoseiulus teke to increasing density of three stages of their prey, the cassava green mite (CGM), Mononychellus tanajoa, were studied on excised cassava leaf discs under laboratory conditions. The responses obtained were predominantly sigmoid type III curves with the highest plateau when both stages of I. degenerans and N. teke were preying on CGM eggs. In all cases, the predation rate of the former species exceeded that of the latter. The empirical data were fitted by four different models. From the models, the attack coefficient (a) and handling time (T _h) were estimated. For a given predator stage (protonymph or adult female), the predator's attack coefficient declines and handling time increases as the prey gets larger. For a given prey stage, the predator's attack coefficient increases and handling time decreases as the predator stage becomes larger.     

Reproductive responses of Iphiseius degenerans and Neoseiulus teke (Acari: Phytoseiidae) to changes in the density of the cassava green mite, Mononychellus tanajoa (Acari: Tetranychidae)

We assessed the reproductive responses of adult female Iphiseius degenerans and Neoseiulus teke to increasing density of three stages of their prey, Mononychellus tanajoa, on cassava leaf discs under laboratory conditions. The oviposition rates increased with number of prey consumed per predator per day with a maximum of approximately two eggs per day for I. degenerans and four eggs per day for N. teke. The oviposition rate of N. teke was higher when consuming eggs than other prey stages. Neoseiulus teke was more efficient than I. degenerans in converting consumed prey into egg production. The data were adequately described by simple mathematical models.     

The role of resting spores in the survival of the mite-pathogenic fungus Neozygites floridana from Mononychellus tanajoa during dry periods in Brazil

Survival of pathogens during long periods of unfavorable conditions can be critical to their ecology and to their use in biological control. In northeastern Brazil, the mite pathogen Neozygites floridana must survive hot and dry conditions between wet seasons when it infects the cassava green mite Mononychellus tanajoa. We report on large numbers of mite cadavers bearing resting spores towards the end of epizootics in mid-1995. High within-leaf variability indicated that local factors may be important in determining resting spore formation. These spores remain in the host cadaver on a leaf until the cadaver breaks up, whereupon the spores fall freely to the soil, there to remain dormant. Laboratory simulation of field conditions led to ca. 25% of mycosed individuals bearing resting spores. Mummies (without resting spores) kept in hot and dry conditions showed little or no viability within 2 months, implying no role for survival over extended dry periods. It is proposed that resting spores form the principal means by which this pathogen survives the dry season in the study area. This has implications for its introduction to new areas in classical biological control.     

Effect of cassava exudate and prey densities on the survival and reproduction of Typhlodromalus limonicus (Garman & McGregor) s.l. (Acari: Phytoseiidae), a predator of the cassava green mite,Mononychellus tanajoa (Bondar) (Acari: Tetranychidae)

The effects of cassava exudate and prey densities on reproduction and survival of the predatory mite, Typhlodromalus limonicus (Garman & McGregor) (Acari: Phytoseiidae), were investigated in the laboratory. Females were provided either cassava exudate ad lib. daily, low or high numbers of the cassava green mite prey, Mononychellus tanajoa (Bondar) (Acari: Tetranychidae) daily, or exudate for 5 or 10 days before switching to a low or high prey diet. Females fed only exudate laid no eggs. Females fed exudate before prey experienced a significant decrease (30%) in the number of eggs laid compared to females fed high numbers of prey daily. The reduction in fecundity was the result of prolonged preoviposition periods (2.0 days on prey daily vs 4.0 days on exudate before prey) and reduced number of eggs laid per female per day (1.7 eggs per female per day on prey daily vs 0.4 eggs per female per day on exudate before prey). Females fed only exudate had a greater survival rate and longevity than females fed prey daily or females fed exudate before a diet of prey. These results suggest that T. limonicus can survice for a limited period on cassava exudate during periods of low prey availability, but requires prey to complete oögenesis and propagate the population.     

Photosynthesis and yield performance of cassava in seasonally dry and semiarid environments

Two field trials with two groups of cassava (Manihot esculenta Crantz) cultivars were conducted under rainfed conditions in seasonally dry and semiarid environments at the northern coast of Colombia, South America, to evaluate the genetic diversity in photosynthesis and productivity, and to determine their interrelationship. There were significant differences among cultivars in both environments, in average net photosynthetic rates (P _N ) of upper canopy leaves and in final dry root yields. Both P _N and dry root yields were much higher in the seasonally dry environment than in the semiarid one. Highly significant correlation (r ² = 0.90, p < 0.001) between leaf P _N and dry root yield was observed across environments, suggesting that selection in parental plants for high photosynthesis might lead to high yields if combined with other yield determinants, such as leaf area duration, high harvest index and strong root sink. This revised version was published online in August 2006 with corrections to the Cover Date.     

Host specificity of the cassava green mite pathogen Neozygites floridana

Tests were conducted on the hostspecificity of a Brazilian isolate of thefungus Neozygites floridana, a potentialbiological control agent for the cassava greenmite, Mononychellus tanajoa, in Africa.Five insect and two mite species, mostly fromthe cassava agroecosystem, were evaluated forsusceptibility to N. floridana, namelyEuseius concordis, E. citrifolius, Phenacoccus herreni, Stethorus sp., Aleurothrixus aepim, Apoanagyrusdiversicornis, and Bombyx mori.Individuals of each species were exposed tocapilliconidia (the infective stage of thefungus). None of the tested individuals wasfound with hyphal bodies (the vegetative stageof the fungus), whereas 73 to 94% of thecassava green mites in the controls becameinfected. Non-germinated capilliconidia were,however, found attached to several individualsin most species. N. floridana appears tobe safe for exportation. Further evaluation ofits performance against M. tanajoa inAfrica is therefore desirable.     

Continent-wide releases of neotropical phytoseiids against the exotic cassava green mite in Africa

Since the initiation of the classical biological control campaign by the International Institute of Tropical Agriculture to control the exotic mite, Mononychellus tanajoa, 11 species (18 distinct populations) of neotropical phytoseiids have been selected and shipped to Africa for experimental releases. Initially, natural enemies were selected because of their abundance and frequency on cassava. Between 1984 and 1988, more than 5.2 million phytoseiids belonging to 7 species of Colombian origin were imported to Africa and released in 348 sites in 10 countries. None of these species and populations ever became established in the wide range of agronomic and ecological conditions tested, apparently because of inadequate alternative food sources when M. tanajoa densities were low and extended periods of low relative humidity. Foreign exploration was adjusted in 1988 to focus on Neotropical regions that were agrometeorologically homologous to areas in Africa where the potential for severe M. tanajoa damage exists. Natural enemies associated temporally and spatially with M. tanajoa and capable of surviving periods of low M. tanajoa densities on alternative food sources in the new exploration sites were given selection priority. Several natural enemy candidates were immediately identified in Northeast Brazil and shipped to Africa. Approximately 1.9 million phytoseiids of the species Neoseiulus idaeus and Typhlodromalus limonicus of Brazilian origin were released in 133 sites in 6 countries in 1989 and 1990. N. idaeus has since become established in Benin, while T. limonicus may be established in Benin, Burundi, and Ghana.     

Maintenance and mass rearing of phytoseiid predators of the cassava green mite

The cassava green mite Mononychellus tanajoa (Bondar), accidentally introduced from South America into Africa, has spread across the cassava belt and is causing severe yield losses to cassava. Biological control was recognized as the most promising and sustainable strategy against this pest. Among the different stages of a biological control program, mass rearing of beneficials is often a major bottleneck. The different rearing systems used by the International Institute of Tropical Agriculture are described. A mother culture system maintains pure and high quality colonies and provides inoculum to start mass production. Twenty biotypes are maintained separately and no contamination has been found in the cultures. Oligophagous species are reared in the insectary on artificial substrate, using alternative prey as a food source. For phytoseiid species specific to M. tanajoa, an on plant system is used in a greenhouse. Advantages and disadvantages of the two different systems are discussed as well as general requirements and constraints in rearing phytoseiids.     

Fresh and dry wei ghts of Mononychellus tanajoa (Acari: Tetranychidae): A functional description of biomass accumulation

The fresh and dry weights of each life stage of Mononychellus tanajoa (Bondar) were determined using grouped samples. The eggs, larvae and protonymphs averaged 0.637, 0.625 and 1.013 μg fresh weight, respectively. Male and female deutonymphs averaged 1.209 and 2.715 μg, while male and female adults averaged 1.633 and 7.035 μg fresh weight, respectively. The dry matter content of M. tanajoa across all life stages for both sexes averaged 31%. The accumulation of biomass in male and female M. tanajoa is adequately described by logistic growth functions (with 87 and 98% explained variation, respectively). Maximum growth rates of 0.026 and 0.598 μg dry matter per day for males and females, respectively, were estimated using these fitted functions.     

Interactions between the predatory mite Typhlodromalus aripo and the entomopathogenic fungus Neozygites tanajoae and consequences for the suppression of their shared prey/host Mononychellus tanajoa

The predatory mite Typhlodromalus aripo and the entomopathogenic fungus Neozygites tanajoae, both introduced from Brazil for control of the cassava green mite (CGM) Mononychellus tanajoa, now co-occur in cassava fields in Benin. However, studies on interactions between these two natural enemies and how they might affect CGM biological control are lacking. We determined in screenhouse experiments the effects of single and combined releases of N. tanajoae and T. aripo on CGM suppression. In the single natural enemy treatment, both T. aripo and N. tanajoae significantly reduced CGM densities, but the results of the predator (T. aripo) are more quickly measurable than those of the pathogen (N. tanajoae) in our short-term experiment. The level of CGM suppression in the combined natural enemy treatment was reduced considerably compared with T. aripo-alone, but only slightly when compared with N. tanajoae alone, with a simultaneous reduction in T. aripo and N. tanajoae abundance or prevalence. In a laboratory experiment, T. aripo fed more on N. tanajoae-infected CGM than on healthy CGM and its oviposition and survival were reduced when fed on the former compared with the latter, which can help in explaining the reduction in numbers of T. aripo and consequently the considerable loss in suppression of CGM in the combined natural enemy treatment in the screenhouse experiment. Together, the screenhouse and the laboratory experiments predicted negative interactions between the two natural enemies with negative consequences for CGM biological control. Long-term field observations and rigorous field experiments that simultaneously manipulate T. aripo and N. tanajoae abundance and prevalence are needed to validate the prediction of this study.