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.     

Interactions in an acarine predator guild: impact on Typhlodromalus aripo abundance and biological control of cassava green mite in Benin, West Africa

To determine the impact of an acarine predator guild on the abundance of a shared herbivorous prey and its principal exotic predator, a series of surveys were conducted in ca. 200 cassava fields in swamp and non-swamp areas in southwestern Benin, West Africa. For each field, the surveys provided data on the density of a pest arthropod, the cassava green mite Mononychellus tanajoa (Bondar), of an introduced and successfully established natural enemy, the apex-inhabiting predatory mite Typhlodromalus aripo DeLeon, and on occurrence of other predator species that inhabit the leaves and share the same prey. These other predators included one exotic species, Typhlodromalus manihoti Moraes, that is successfully established mainly in swamp areas, and two indigenous species, Euseius fustis (Pritchard and Baker) and Typhlodromalus saltus (Denmark and Matthysse), that are commonly found on cassava in Africa. Our aim was to assess the association between the density of M. tanajoa and that of T. aripo, the most successful predator in terms of establishment and abundance, and subsequently determine how this association was affected by the presence or absence of the other predator species. No obvious density-dependent relationship was found by inspecting the scattergrams of T. aripo versus M. tanajoa densities, but high T. aripo densities did not occur when M. tanajoa densities were low and--during the dry season in February--the densities of M. tanajoa steeply increased when T. aripo numbers were low. Given the establishment of T. aripo in all fields, the presence of other species of predatory mites (T. manihoti, both in swamp and non-swamp areas; T. saltus in absence--as well as presence--of T. manihoti in swamp areas; E. fustis in absence of T. manihoti in non-swamp areas) reduced the density of M. tanajoa by a factor 2-3. Thus in all these cases, the presence of an exotic or indigenous species of predatory mite in addition to T. aripo was associated with lower M. tanajoa density. The density of T. aripo was usually positively affected by the presence of other predator species except for T. saltus in presence of T. manihoti that negatively affected the density of T. aripo in swamp areas, an effect likely mediated by either intraguild predation or competition for food. Path analysis showed that indigenous phytoseiid species were more important in suppression of M. tanajoa populations in cassava fields than previously thought. We suggest that the lack of negative effects of the predator species complex is likely due to differential niche use by the various species which reduces interference among the predators. Manipulative experiments are, however, needed to provide details on the relative importance in M. tanajoa suppression by each species within this acarine predator guild.     

Models for integrated pest control and their biological implications

Successful integrated pest management (IPM) control programmes depend on many factors which include host-parasitoid ratios, starting densities, timings of parasitoid releases, dosages and timings of insecticide applications and levels of host-feeding and parasitism. Mathematical models can help us to clarify and predict the effects of such factors on the stability of host-parasitoid systems, which we illustrate here by extending the classical continuous and discrete host-parasitoid models to include an IPM control programme. The results indicate that one of three control methods can maintain the host level below the economic threshold (ET) in relation to different ET levels, initial densities of host and parasitoid populations and host-parasitoid ratios. The effects of host intrinsic growth rate and parasitoid searching efficiency on host mean outbreak period can be calculated numerically from the models presented. The instantaneous pest killing rate of an insecticide application is also estimated from the models. The results imply that the modelling methods described can help in the design of appropriate control strategies and assist management decision-making. The results also indicate that a high initial density of parasitoids (such as in inundative releases) and high parasitoid inter-generational survival rates will lead to more frequent host outbreaks and, therefore, greater economic damage. The biological implications of this counter intuitive result are discussed.     

Sex ratios in field populations of Epidinocarsis lopezi, an exotic parasitoid of the cassava mealybug, in Africa

Abstract.

• 1 In cassava fields in Africa, population sex ratios of Epidinocarsis fopezi vaned from 0.44 (males to total parasitoids) at low host densities to highly male-biased ratios of 0.70 at high host densities.
• 2 This variability is caused by the difference in allocation of sons and daughters to hosts of different sizes, through the following mechanisms: (a) small, i.e. second instar, hosts are mainly used for the production of male offspring, whereas in large, i.e. third instar, hosts a variable, female-biased sex ratio is produced; (b) E.fopezi does not selectively oviposit into large hosts but always accepts both small and large hosts for oviposition upon encountering; (c) in the field, this parasitoid is time-limited, and not egg-limited. On the basis of an optimal diet model, such general host acceptance is shown to be the best strategy.
• 3 Thus, sex ratio increases with host density for three reasons: the proportion of small hosts encountered in the field increases with increasing host density, small hosts are used for male production, and hosts are always accepted when encountered.

     

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.     

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.     

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.     

Artificial overwintering chambers for green lacewings: results of international trials and implications for pest control

Lacewing overwintering chambers placed correctly in the field may be colonized by large numbers of adult common green lacewings ( Chrysoperla carnea ). This paper reports field results collected over 2 years from chambers placed in a number of European locations. Considerable variation was found in the success rates of the chambers from different areas and some suggestions are made as to why this might be. An experiment was conducted to investigate the potential use of overwintered lacewings in pest control. This attempt was not successful and possible reasons why are discussed.     

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.     

外来害虫蔗扁蛾的寄主范围

综述了我国近年传入的害虫蔗扁蛾的寄主植物范围 :到目前为止 ,蔗扁蛾Opogonasacchari(Bo jer)的寄主植物已达 2 8科 87种 8变种 ;其中国外已报导的为 2 4科 4 6种 4变种 ,中国已查到 1 4科 5 5种 2变种 ,且不断发现新的寄主植物 ,有蔓延到多种行道绿化树木和园林花卉植物上的趋势 ,须引起充分关注。     

Effects of the entomopathogenic fungus Neozygites tanajoae and the predatory mite Typhlodromalus aripo on cassava green mite densities: screenhouse experiments

To improve biocontrol of the cassava green mite, Mononychellus tanajoa, a series of screenhouse experiments were conducted on cassava to determine the effects of single and combined releases of the predatory mite Typhlodromalus aripo and the entomopathogenic fungus Neozygites tanajoae on the suppression of M. tanajoa. We showed that, separately or in combination, T. aripo and N. tanajoae significantly reduced M. tanajoa populations. Moreover, combined release of T. aripo and N. tanajoae on the same cassava plants improved M. tanajoa control. However, our data suggest between T. aripo and N. tanajoae an asymmetric competition that significantly affected N. tanajoae only. This interference is indirect, probably mediated by their common prey or host mite, M. tanajoa since N. tanajoae is not pathogenic to T. aripo. We conclude that adding N. tanajoae to T. aripo populations in Africa would not negatively affect T. aripo and would further promote biocontrol of M. tanajoa.     

The dynamics of the cassava green mite Mononychellus tanajoa in a seasonally dry area in Kenya

The population dynamics of the cassava green mite Mononychellus tanajoa was studied on cassava during 35 weeks (early March to first of November 1989) in an experimental field near Lake Victoria in Western Kenya. The mite population peaked at the onset of the long dry season with 1,100 mites/leaf, declined sharply to a level of about 300 individuals/leaf, not to increase again until the next rainy season commenced. An indigenous phytoseiid predator Iphiseius degenerans was abundant during the dry spell with a maximum about 9 predators/leaf.A nonlinear regression analysis revealed that food depletion in combination with I. degenerans predation limited the population growth of the mites, whereas rain intensity had no effect. The predator exhibited no aggregative response to high densities of M. tanajoa and stayed mainly in the lower part of the canopy while the spider mites preferred the top, indicating that I. degenerans is a generalist predator without capacity to control M. tanajoa alone. However, in combination with another density dependent factor, such as food depletion, the predator may have prevented the spider mites from causing complete defoliation during the dry season.     

Patterns of parasitoid host utilization and development across a range of temperatures: implications for biological control of an invasive forest pest

Although climate change frequently has been linked to observed shifts in the distributions or phenologies of species, little is known about the potential effects of varying temperatures on parasitoids and their relationships with hosts. Using the egg parasitoid Oobius agrili (Hymenoptera: Encyrtidae) we examined host utilization patterns of this species across a range of temperatures (20–35 °C) to explore how changing climate could affect the interaction with its host—the emerald ash borer (EAB) (Coleoptera: Buprestidae), a serious invasive forest pest that has killed tens of millions of ash (Fraxinus spp.) trees in North America. Results from our study showed that the window of host susceptibility to O. agrili parasitism declined significantly from 14.8 to 2.6 days in an inverse second-order relationship with increasing exposure temperatures from 20 to 35 °C. In contrast, parasitoid host attack rate changed in a bell-shaped second-order relationship—i.e., increased with temperatures from 20 to 25 °C, but decreased at about the same rate when temperatures increased from 30 to 35 °C. This range of temperatures also significantly affected the development and mortality of immature parasitoids with 35 °C resulting in 100 % mortality. There was little mortality (0–4.5 %) and no significant differences in the percentage (20.9–34.9 %) of immature O. agrili that entered diapause (as mature larvae) at 20, 25, and 30 °C. However, there were significant differences in the time event of adult wasp emergence within this temperature range. The median time for 50 % of immature O. agrili emerging as adults at 20, 25, and 30 °C were 38, 18, and 17 days after parental wasp oviposition, respectively. Together these findings indicate that the non-linear and unequal temperature effects on these host utilization parameters are likely to result in differential host parasitism rates, and thus could reduce the efficacy of this parasitoid in suppressing host populations due to climate change (global warming and extreme heat).     

Benefits and risks of exotic biological control agents

The use of exotic (=alien) arthropods in classical and augmentative biological control programs has yielded huge economic and ecological benefits. Exotic species of arthropods have contributed to the suppression of key pests in agriculture and forestry or have aided in restoring natural systems affected by adventive species. However, adverse non-target effects of exotic biological control agents have been observed in a number of projects. Non-target effects range from very small effects, e.g. 2% parasitization on a non-target insect on a local level, to massive effects on a large scale. Until now, no consensus on how to judge the magnitude of non-target effects and whether these effects can be tolerated or are unacceptable has emerged. In this paper, we briefly review both the benefits of biological control as well as the associated risks including to human and animal health, plant health and particularly the environment. We also make an attempt at identifying the major challenges for assessing risks and for balancing benefits and risks. There is general agreement that sound risk assessment procedures should precede the release of exotic invertebrate biological control agents and a recent shift??especially for arthropod biological control??from introductions done without meaningful risk assessment studies to projects conducting thorough host range testing can be observed. However, overly stringent regulations that would preclude promising agents from being developed must be avoided.     

Effects of mite age, mite density, and host quality on aerial dispersal behavior in the twospotted spider mite

Mite age, population density, and host leaf quality affect various life history traits in spider mites. We investigated the effects of these factors on the aerial dispersal behavior of adult female twospotted spider mites,Tetranychus urticae Koch (Acari: Tetranychidae). The proportion of adult females exhibiting the dispersal behavior dropped significantly with age following adult emergence, particularly in the first 3 days. Sixty to eighty percent of female mites 2-days old or younger displayed the behavior under test conditions, whereas less than 20% of female mites older than 3-days-old showed the behavior. Younger adult females also exhibited shorter latency for the behavior, although this trend was not as clear. Leaf quality experienced during deutonymph development had no effect on the behavior adults subsequently displayed. On the other hand, adult females that fed on poor quality leaves after emergence were twice as likely to display the behavior (90% vs. 45%), and with shorter latency (37 vs. 77 min), than those that fed on high quality leaves. When newly emerged adult females encountered high mite density and dry leaves, the incidence of the behavior increased (69% vs. 47%) and latency decreased (69 vs. 93 min) compared to mites that encountered low density on well watered leaves. Our results suggest that both starvation and desiccation of adult females may enhance their dispersal behavior.     

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.     

Spider mite resistance to miticides in South Carolina strawberry and implications for improved integrated pest management

Tetranychus urticae Koch (Acari: Tetranychidae), twospotted spider mite, is a major secondary pest of strawberry and can cause significant yield loss. Tetranychus urticae is typically controlled using miticides, which has led to rapid resistance development. In South Carolina (USA), extension agents and growers have reported field failures of miticides (inadequate pest suppression), but resistance has not been quantitatively determined. In 2018, we determined the level of miticide resistance of six T. urticae populations found on strawberry across South Carolina. We examined efficacy of all miticides registered for use on US strawberry by conducting an initial diagnostic bioassay at 20% of the maximum labeled field rate. Any population?×?active ingredient combination resulting in?<?55% mortality was identified as ‘potentially resistant’ and concentration–response bioassays were then conducted to calculate LC₅₀ values for an individual population. These values were compared with those of a known-susceptible laboratory population to calculate resistance ratios (RR). Our results indicate that examined South Carolina populations of T. urticae from strawberry were highly resistant to bifenthrin (RR?=?100–60,000) and there was reduced susceptibility to fenbutatin-oxide (RR?=?25–123). The 'Sardinia' population had decreased abamectin susceptibility (RR?=?25). No resistance to hexythiazox, etoxazole, acequinocyl, bifenazate, fenpyroximate, spiromesifen, or cyflumetofen was found. Based on available data, it appears that miticide resistance is not a likely cause of field failures and issues related to application error and coverage should be investigated. Overall, this work supports the need to reduce the use of broad-spectrum pesticides and older products, in favor of newer miticide chemistries due to resistance issues.

     

Alternative plant habitats for common phytoseiid predators of the cassava green mite (Acari: Phytoseiidae,Tetranychidae) in northeast Brazil

A survey was conducted to identify possible alternative plant habitats of the most common phytoseiid predators associated with the cassava green mite, Mononychellus tanajoa (Bondar), in their native environment in northeast Brazil. Thirty-two phytoseiid species were collected, including Amblyseius aripo (DeLeon), Amblyseius idaeus (Denmark and Muma) and Amblyseius limonicus Garman and McGregor s.l., the three predators previously shown as the most common on cassava. In increasing order, A. idaeus, Phytoseius guianensis DeLeon and A. aripo were the most common phytoseiids collected on the plant habitats examined. A. limonicus s.l. was one of the least common phytoseiids on plants other than cassava. Altermative plant habitats seem important in harboring A. aripo and A. idaeus, but not A. limonicus s.l..