Plant feeding by a predatory mite inhabiting cassava

Plant feeding by arthropod predators may strongly affect the dynamics of bi- and tri-trophic interactions. We tested whether a predatory mite, Typhlodromalus aripo, feeds upon its host plant, cassava. This predator species is an effective biological control agent of Monoychellus tanajoa (the cassava green mite or CGM) a herbivorous mite specific to cassava. We developed a technique to detect plant feeding, based on the use of a systemic insecticide. We found that T. aripo feeds upon plant-borne material, while other predatory mite species, Neoseiulus idaeus and Phytoseiulus persimilis, do not. Subsequently, we measured survival of juveniles and adult females of T. aripo and N. idaeus, both cassava-inhabiting predator species, on cassava leaf discs. Survival of T. aripo was higher than that of N. idaeus. Thus, T. aripo was able to withstand longer periods of prey scarcity. Because CGM populations fluctuate yearly and are heterogeneously distributed within plants, plant feeding may facilitate the persistence of populations of T. aripo in cassava fields and its control of CGM outbreaks. This revised version was published online in July 2006 with corrections to the Cover Date.     

Influence of humidity and water availability on the survival ofAmblyseius idaeus andA. anonymus (Acarina: Phytoseiidae)

Amblyseius idaeus (Denmark & Muma) andA. anonymus Chant & Baker are morphologically very similar species of phytoseiids inhabiting areas in South America that have very different levels of humidity. Above 60% RH, nearly all eggs of both species hatch successfully, but below 60% RH the egg hatching rate ofA. anonymus is very poor, whereas eggs ofA. idaeus hatch at humidities as low as 30% RH. The mobile stages ofA. idaeus are better able to survive in absence of food and water than those ofA. anonymus. Water availability promotes survival of both species, but its effect onA. idaeus exceeds that onA. anonymus. These differences in low-humidity tolerance and survival ability are consistent with the climatic origin of these phytoseiid species;Amblyseius ideaus has been reported from very dry and humid areas, andA. anonymus from humid areas only.In comparison with other phytoseiid species, the eggs ofA. idaeus have the highest tolerance to low humidities reported to date, and, among the phytoseiids that are shown to be capable of controllingTetranychus spp., this tolerance appears to be exceptionally high. The impact of this result on the scope of biological control ofTetranychus spp. is discussed.     

Biosystematics of phytoseiid mites (Acari: Phytoseiidae) associated with cassava

Laboratory crossing experiments indicate that populations of A. limonicus sensu lato collected from cassava (Manihot esculenta Crantz) in Brazil (Cruz das Almas) and Colombia (Palmira and Monteria) are conspecific and different from A. limonicus Garman & McGregor sensu stricto collected in Riverside, California, USA and Jaguariuna, Brazil. A. limonicus s.l. did not cross with A. tenuiscutus, A. rapax or A. limonicus s.s.. A. limonicus s.s. did not cross with A. rapax. Populations of A. aerialis, A. anonymus and A. idaeus from Colombia are conspecific with Brazilian populations of these species.     

Effects of prey mite species on life history of the phytoseiid predators Typhlodromalus manihoti and Typhlodromalus aripo

The effects of prey mite suitability on several demographic characteristics of phytoseiid predators and the relationship of these effects to the potential of phytoseiid predators to control herbivorous mite populations are well documented. Evidence has also accumulated in the last 20 years demonstrating that phytoseiid predators utilize herbivorous prey mite-induced plant volatiles as olfactory cues in locating their herbivorous mite prey, but less well established is the predictability of reproductive success from the ability of the predators to utilize olfactory cues to locate their prey, and how these processes are related to the success of the predators as biological control agents of the herbivorous mite. In this study, we determined in laboratory no choice experiments, the development, survivorship and fecundity of the two neotropical phytoseiid predators Typhlodromalus manihoti Moraes and T. aripo DeLeon when feeding on three herbivorous mites, including the key prey species Mononychellus tanajoa (Bondar), and the two alternative prey species Oligonychus gossypii (Zacher) and Tetranychus urticae (Koch). Intrinsic rate of increase (r_m) of T. aripo was 2.1 fold higher on M. tanajoa as prey compared with T. urticae as prey, while it was almost nil on O. gossypii. For T. manihoti, r_m was 2.3 fold higher on M. tanajoa as prey compared with O. gossypii as prey, while reproduction was nil on T. urticae. An independent experiment on odor-related prey preference of the two predator species showed that T. manihoti and T. aripo preferred odors from M. tanajoa-infested leaves to odors from O. gossypii-infested leaves. Moreover, both predator species preferred odors from M. tanajoa-infested leaves over those from T. urticae-infested leaves. As reported here, life history of the two predatory mites matches odor-related prey preference if the key prey species is compared to the two inferior prey species. The implications of our findings for the persistence of T. manihoti and T. aripo and biological control of M. tanajoa in the cassava agroecosystem in Africa are discussed. This revised version was published online in July 2006 with corrections to the Cover Date.     

Specificity of a strain ofNeozygites sp. (Zygomycetes: Entomophthorales) toMononychellus tanajoa (Acari: Tetranychidae)

Neozygites sp. is commonly found infecting the cassava green mite,Mononychellus tanajoa (Bondar), in parts of northeast Brazil. The introduction of this fungus into other regions requires the knowledge of its specificity, especially in relation to natural enemies of different cassava pests. Laboratory tests indicated the development of germination tubes ofNeozygites in some females ofTetranychus bastosi Tuttle et al. andT. urticae Koch, with subsequent formation of a reduced number of hyphal bodies in someT. bastosi. No females of the phytoseiid predatorsAmblyseius idaeus (Denmark & Muma) andAmblyseius limonicus Garman & McGregor s.l. were infected byNeozygites sp.     

Cannibalism and Interspecific Predation in a Phytoseiid Predator Guild from Cassava Fields in Africa: Evidence from the Laboratory

Interspecific predation and cannibalism are common types of interaction in phytoseiid predator guilds, but the extent and nature of these interactions have not been determined yet in phytoseiid guilds composed of African native and neotropical exotic phytoseiid predators found in cassava habitat in southern Africa. We determined in laboratory experiments the level of cannibalism and interspecific predation among the three phytoseiid mite species Euseius fustis, Iphiseius degenerans, and Typhlodromalus aripo in the absence of food and in the presence of limited or abundant quantities of two food types – Mononychellus tanajoa and maize pollen – commonly found on cassava in Africa. When confined without food, only two T. aripo females laid each two eggs within 5 days, and this species survived longer than I. degenerans and E. fustis. In the presence of con- or hetero-specific larvae or protonymphs, the three species fed more on the former than on the latter, and more on hetero-specifics than on con-specifics. Oviposition rates of the three species did not exceed 0.7 egg/female/day on con- and hetero-specific immatures. Typhlodromalus aripo and E. fustis survived longer on con-specific and hetero-specific larvae and on hetero-specific protonymphs than in the absence of any food, while T. aripo survived longer than the two other species on the same diets. Provision of limited quantity of food decreased interspecific predation rate by I. degenerans and T. aripo, but not by E. fustis, and increased oviposition rate and longevity of all three species. Provision of abundant food, however, eliminated cannibalism by all three species and further reduced interspecific predation rates, but their oviposition and longevity remained relatively unchanged compared with limited food provision. Potential consequences of cannibalism and interspecific predation among phytoseiid mites on cassava for the biological control of M. tanajoa are discussed.     

Abundance of phytoseiid mites on Vitis species: effects of leaf hairs,domatia, prey abundance and plant phylogeny

We observed the number of predatory mites (Phytoseiidae:Typhlodromus caudiglans) on the foliage of 20 North American species of grapes (Vitis spp) plus the domesticated EuropeanVitis vinifera, all grown in a common garden. We found relatively few phytophagous mites. The numbers of phytophagous mites were not correlated with the plant characteristics that we measured. We found approximately five times as many predatory mites as phytophagous mites and the numbers of these phytoseiid predators were not affected by the availability of prey. Similarly, numbers of phytoseiids were unaffected by plant gender and, hence, the availability of pollen, another source of food. The numbers of phytoseiids were not clustered according to the taxonomic grouping of the tested plant species. Leaf surface characteristics explained over 25% of the variance in the numbers of phytoseiids. Numbers of phytoseiids were positively associated with the density of vein hairs, the density of bristles in leaf axils, and the presence of leaf domatia. These results suggest that sheltered habitats rather than food availability may limit the numbers of phytoseiid mites on grapevines.     

Infochemical-Mediated Niche Use by the Predatory Mites Typhlodromalus manihoti and T. aripo (Acari: Phytoseiidae)

In Africa, Typhlodromalus manihoti and T. aripo, two introduced predators of the cassava green mite Mononychellus tanajoa, occupy different parts of cassava foliage. In the present study, niche use by these two predators, as mediated by prey-induced infochemicals, was investigated. In response to prey feeding damage, cassava plant parts emit volatile blends, that attract phytoseiidae predators. When given a choice between old cassava leaves infested with M. tanajoa and either apices or young cassava leaves infested with M. tanajoa, T. aripo displayed a marked preference for odors emitted from either infested apices or infested young leaves over infested old leaves but showed no preference for odors from apices versus young leaves, all infested with M. tanajoa. Typhlodromalus manihoti did not discriminate between volatiles from the three infested cassava plant parts. Our data show that T. aripo uses differences in volatile blends released by infested cassava plant parts and restricts its fundamental niche to a realized niche, which enables coexistence with its competitor T. manihoti.     

Reproductive success ofAmblyseius idaeus andA. anonymus on a diet of two-spotted spider mites

Amblyseius idaeus is a drought-resistant predatory mite of tetranychid spider mites. In this paper, life-history parameters ofA. idaeus and a morphologically similar species,A. anonymus, are measured and compared on a diet ofTetranychus urticae. Intrinsic rates of increase of both phytoseiids are similar, and are comparable to rates of phytoseiids that successfully controlTetranychus species. This makes both species promising candidates as biological control agents,A. idaeus especially under dry conditions.     

Interactions Between Two Neotropical Phytoseiid Predators on Cassava Plants and Consequences for Biological Control of a Shared Spider Mite Prey: a Screenhouse Evaluation

The issue of introducing single or multiple natural enemy species for classical biological control has been an area of intense inquiry by ecologists and biological control practitioners. This is particularly relevant to classical biological control of cassava green mite Mononychellus tanajoa (Bondar) (Tetranychidae) in Africa, as this pest mite is shared by several natural enemies in the Neotropics (its area of origin), two of which have been introduced and established widely in Africa. We conducted two screenhouse experiments using the two neotropical phytoseiid predatory mites, Typhlodromalus aripo DeLeon and Typhlodromalus manihoti Moraes, to determine the effects of single and two-predator species on population dynamics of the two predators and on suppression of M. tanajoa populations. The two predators are thought to be complementary in their impact on their shared prey M. tanajoa, due to similarities in their preference for this prey and to differences in their spatial distribution and foraging activities on cassava. The two predator species were released alone or together at low and at high initial densities of M. tanajoa. In all cases, predator releases resulted in significant suppression of M. tanajoa, but the degree of suppression did not differ among single and two-species releases with one exception: at high initial density of M. tanajoa, releases of T. aripo alone had less impact than that of either T. manihoti alone or of the two species together. Typhlodromalus aripo also appeared to be inferior as a competitor of T. manihoti: at low initial density of M. tanajoa, the proportion of T. aripo in the two-predator release treatments gradually declined and was strikingly lower than in the single species release, probably due to intraguild predation on its larvae by T. manihoti. However, T. aripo persisted longer than T. manihoti after elimination of M. tanajoa. On the basis of this study under semi-natural conditions, it appears that either species is sufficient for controlling M. tanajoa populations, with T. manihoti being more efficient at high initial prey densities and T. aripo at low initial prey densities. At high prey density, T. manihoti increased to large numbers and outcompeted T. aripo. Relevance of these findings to larger spatial scale and under natural conditions is discussed.     

Living at the threshold: Where does the neotropical phytoseiid mite Typhlodromalus aripo survive the dry season?

The establishment of the neotropical predatory mite Typhlodromalus aripo in sub-Saharan Africa has resulted in broadly successful biological control of the cassava green mite Mononychellus tanajoa throughout the cassava belt of Africa. In some mid-altitude areas and drier lowland savannahs of sub-Saharan Africa, which are characterized by cool or hot long (≥5 months) dry seasons, the predator disappears from its habitat in the cassava apex during the dry season and reappears after the onset of rains. It is not known, however, where the predator remains during this time period. In this study, we conducted a field enclosure experiment of cassava plants with the objectives to determine if (a) T. aripo survives at very low densities in the apex, if (b) it survives in the soil or leaf litter below the cassava plant, and if (c) it recolonizes the cassava plant from the surrounding vegetation. Towards the end of the dry season, when the predators had disappeared from all cassava plants included in the experiment, five treatments were applied: (1) plants without enclosure; (2) plants with enclosure; (3) plants with enclosure, apices removed; (4) plants with enclosure, glue barrier around stem; and (5) plants kept free of T. aripo, without enclosure. Predator (re)appearance on cassava apices was monitored non-destructively at weekly intervals and was expressed as the proportion of plants with at least one apex with T. aripo per total number of plants of the treatment. The predators reappeared first on the plants of the treatments (1), (2), and (4). With a time lag of 7–8 weeks, the predators appeared also on the plants of the treatments (3) and (5). The time pattern of the predator’s (re)appearance in the cassava apex of the different treatments suggests that (a) T. aripo survives the dry season in very low densities in the cassava apex; this result is supported by an assessment of the efficiency of non-destructive visual in-field apex inspections which proved that about 10% of the cassava apices that had T. aripo were not recognized as such; (b) T. aripo does not survive in the soil or leaf litter, but we did document cases in a screenhouse experiment, where few individuals migrated down to the ground and walked over exposed soil until they reached the apex bouquet traps; additionally, microclimate measurements in various cassava plant strata proved that the cassava apex and the cassava stem base are the locations with the highest relative humidity during the dry season—which makes the stem base a potentially interesting refuge; (c) T. aripo does not survive in the surrounding vegetation, which is supported by a vegetation survey, where T. aripo was not found on any other plant species than cassava.     

Within-season dynamics of red palm mite (Raoiella indica) and phytoseiid predators on two host palm species in south-west India

Field surveys were conducted monthly between December 2008 and July 2009 in Kerala, south-west India to compare the population dynamics of the red palm mite Raoiella indica (RPM) on two host plants Areca catechu and Cocos nucifera during one non-monsoon season when, in general, RPM populations increase. The aim was to examine the effects of host plant, host plant locality and the impact of climatic factors on RPM and related phytoseiid predators. There were significantly higher RPM densities on areca in peak season (May/June) compared to coconut; although significantly more coconut sites were infested with RPM than areca. Although no one climatic factor was significantly related to RPM numbers, interactions were found between temperature, humidity and rainfall and the partitioning of host plant locality showed that where conditions were warmer and drier, RPM densities were significantly higher. Specifically on coconut, there was a significant relation between RPM densities and the combined interaction between site temperature, site humidity and phytoseiid densities. There was a marked difference in the density of phytoseiids collected between areca and coconut palms, with significantly more on the latter, in several months. Amblyseius largoensis was the most commonly collected phytoseiid in association with RPM, although Amblyseius tamatavensis species group and Amblyseius largoensis species group were collected in association with RPM also. There was also evidence of a weak numerical response of the combined phytoseiid complex in relation to RPM density the previous month on coconut but this was not observed on areca.     

The profit of senescence in phytoseiid mites

Summary A long post-reproductive period in females under optimal conditions is common among phytoseiid mites which are specialized predators of Tetranychus-species. The resulting long life span provides the possibility to postpone or delay egg production during periods of prey scarcity, theoretically in both virgin and fertilized females. The latter are better as colonists. These specialized predators are also the most prolific phytoseiids. The unusual combination of large reproductive capacity and long life might be explained as an adaptation to widely fluctuating prey densities.     

Non-prey food for subsistence of Amblyseius idaeus (Acari: Phytoseiidae) on cassava in Africa

The nutritional effects of pollen from cassava, oil palm, castor bean, Leucaena leucocephala and a phloem exudate from cassava were tested in the laboratory for their effect on survivorship and oviposition of Amblyseius idaeus (Denmark & Muma). Survival and longevity of even-aged females were enhanced on the aforementioned non-prey diets when compared with the control of no food. Castor bean pollen provided sufficient nutrition to induce an irregular and low ovipositional rate of A. idaeus over a five week interval. Oviposition ceased after 48 h in the presence of the other non-prey foods or free-water only. These studies suggest that A. idaeus is capable of switching or supplementing its diet with non-prey foods during periods when spider mite populations are low.     

The predatory mite Typhlodromalus aripo prefers green-mite induced plant odours from pubescent cassava varieties

It is well known that plant-inhabiting predators use herbivore-induced plant volatiles to locate herbivores being their prey. Much less known, however, is the phenomenon that genotypes of the same host plant species vary in the attractiveness of these induced chemical signals, whereas they also differ in characteristics that affect the predator’s foraging success, such as leaf pubescence. In a series of two-choice experiments (using a Y-tube olfactometer) we determined the preference of Typhlodromalus aripo for pubescent versus glabrous cassava cultivars infested with the cassava green mite Mononychellus tanajoa and also the preference for cultivars within each of the two groups. We found that when offered a choice between pubescent and glabrous cassava cultivars (either apex or leaves), T. aripo was significantly more attracted to pubescent cultivars. For each cultivar, M. tanajoa infested leaves and apices were equally attractive to T. aripo. There was however some variation in the response of T. aripo to M. tanajoa-infested plant parts within the group of pubescent cultivars, as well as within the group of glabrous cultivars. Our study confirms not only that T. aripo uses herbivore-induced plant volatiles to search for prey in cassava fields, but it also shows that it can discriminate between glabrous and pubescent cultivars and prefers the latter. This knowledge can be useful in selecting cultivars that are attractive and suitable to T. aripo, which, in turn, may promote biological control of the cassava green mite.     

Phytoseiid mites (Acari: Phytoseiidae) on apple trees and in surrounding vegetation in southern Finland. Densities and species composition

Leaf samples were collected from sprayed (n=29) and unsprayed (n=19) apple orchards, from the surrounding vegetation (n=58) and from one arboretum (n=12), altogether from 46 plant species (1–5 samples each). The density of phytoseiid mites averaged 1.2 mites/leaf on unsprayed apple trees, but only 0.06 mites/leaf on sprayed trees. The phytoseiid density exceeded 1/leaf onAesculus hippocastani, Aristolochia macrophylla, Corylus avellana, Fragaria vesca, Frxinus excelsior, Juglans cinerea, Pterocarya rhoifolia, Ribes nigrum, Rubus odoratus, Sorbus aucuparia, S. thuringiaca, Tilia×euchlora andUlmus glabra. Other common trees and bushes inhabited by phytoseiids wereCrataegus coccinea (0.2 mites/leaf),Prunus padus (0.7),Salix caprea (0.4), andTilia cordata (0.9).Twelve species of phytoseiid mites were found, of which ten occurred on unsprayed apple trees. The most widely distributed species on apple trees werePhytoseius macropilis (in 79% of unsprayed samples),Euseius finlandicus (74%),Paraseiulus soleiger (53%),Paraseiulus triporus (37%),Amblyseius canadensis (26%) andAnthoseius rhenanus (26%). The highest densities on apple trees were found in populations ofE. finlandicus (mean 0.7 mites/leaf),Ph. macropilis (0.5) andA. canadensis (0.5). On sprayed apple trees,E. finlandicus, Pa. soleiger andPh. macropilis occurred most commonly, but their mean densities were under 0.1/leaf. Almost no phytoseiids were found in orchards sprayed with oxydemetonmethyl before blooming of apple.On other plants,E. finlandicus occurred most commonly (on 33 plant species) and in the highest densities, followed byPh. macropilis (14),Pa. soleiger (12),Pa. triporus (12) andAn. rhenanus (7).Seiulus aceri andParaseiulus talbii were identified as new phytoseiid species in Finland. It is concluded that deciduous trees and bushes in forest margins around orchards can serve as important reservoirs for phytoseiid mites, and that the dominant species in these plants would migrate into and colonize the orchards if the use of harmful chemicals were restricted.     

Establishment of the neotropical predator Amblyseius idaeus (Acari: Phytoseiidae) in Benin,West Africa

Populations of the phytoseiid predator Amblyseius(=Neoseiulus) idaeus (Denmark & Muma) from northeastern Brazil, have been successfully introduced into Benin, West Africa, as part of a classical biological control campaign to control the exotic cassava green mite Mononychellus tanajoa (Bondar). Monthly follow‐up surveys revealed the presence of A. idaeus in most release sites. Some populations have persisted for at least 18 months, including two cycles of potentially limiting wet and dry season conditions. In some sites A. idaeus has been the numerically dominant phytoseiid predator on cassava Manihot esculenta, where it is associated with the tetranychids M. tanajoa and Oligonychus gossypii Zacher. During periods of low M. tanajoa densities A. idaeus disappeared from cassava, but were found on weeds with O. gossypii until prey densities on cassava increased.     

Overview of a classical biological control project directed against the red palm mite in Florida

Information is provided on the steps involved in classical biological control programs, with an outline of the steps achieved in the classical biological control of the red palm mite, Raoiella indica (Acari: Tenuipalpidae), in Florida. An overview is provided of the results and an accompanying paper by Bowman and Hoy (2012) describes the molecular analyses conducted to characterize phytoseiid predators of the red palm mite collected from Mauritius. The Mauritius phytoseiids were identified as Amblyseius largoensis, using morphological criteria, and compared to four populations of A. largoensis from Florida. The difficulties encountered in the systematics, rearing, and evaluation of the Mauritius phytoseiids are described. A method was tested for obtaining DNA from single mites without destroying the body so that voucher specimens can be maintained. Ultimately, the project was terminated due to constraints expected in obtaining permission to make releases.     

Mites (Acari) associated to Myrtaceae in areas of Cerrado in the State of São Paulo with faunistic analysis of families Tarsonemidae and Phytoseiidae

The objective of this study was to determine and to analyse the diversity of mites on native Myrtaceae of the "Cerrado" vegetation type of the State of S?o Paulo, with particular attention to the families Phytoseiidae and Tarsonemidae. In the year 2000, mites were collected from Myrtaceae species in three "Cerrado" areas in the State of S?o Paulo. Samples of leaves, flowers and fruits were taken from three plant of each species in each site. Mites of 49 genera belonging to 14 families were found. Fourteen phytoseiid species of nine genera and 19 tarsonemid species of six genera were collected. The most abundant phytoseiids were Euseius citrifolius Denmark & Muma, Transeius bellottii (Moraes & Mesa) and Amblyseius acalyphus Denmark & Muma. The most abundant tarsonemids were Daidalotarsonemus tesselatus DeLeon, Daidalotarsonemus folisetae Lofego & Ochoa and Metatarsonemus megasolenidii Lofego & Ochoa. The highest indexes of diversity of phytoseiids and tarsonemids were observed in the fall; the lowest indexes were found in the winter for phytoseiids and in the spring for tarsonemids. Taking into consideration the total number of phytoseiids and tarsonemids collected in this work, the corresponding indexes of diversity (Shannon) were similar and close to 2.0. Different predatory mite species prevailed on distinct plant species, indicating the complementariness of the latter as reservoirs of the former.     

Pest management systems affect composition but not abundance of phytoseiid mites (Acari: Phytoseiidae) in apple orchards

We examined the faunal composition and abundance of phytoseiid mites (Acari: Phytoseiidae) in apple orchards under different pest management systems in Hungary. A total of 30 apple orchards were surveyed, including abandoned and organic orchards and orchards where integrated pest management (IPM) or broad spectrum insecticides (conventional pest management) were applied. A total of 18 phytoseiid species were found in the canopy of apple trees. Species richness was greatest in the organic orchards (mean: 3.3 species/400 leaves) and the least in the conventional orchards (1.4), with IPM (2.1) and abandoned (2.7) orchards showing intermediate values. The phytoseiid community’s Rényi diversity displayed a similar pattern. However, the total phytoseiid abundance in the orchards with different pest management systems did not differ, with abundance varying between 1.8 and 2.6 phytoseiids/10 leaves. Amblyseius andersoni, Euseius finlandicus, and Typhlodromus pyri were the three most common species. The relative abundance of A. andersoni increased with the pesticide load of the orchards whereas the relative abundance of E. finlandicus decreased. The abundance of T. pyri did not change in the apple orchards under different pest management strategies; regardless of the type of applied treatment, they only displayed greater abundance in five of the orchards. The remaining 15 phytoseiid species only occurred in small numbers, mostly from the abandoned and organic orchards. We identified a negative correlation between the abundance of T. pyri and the other phytoseiids in the abandoned and organic orchards. However, we did not find any similar link between the abundance of A. andersoni and E. finlandicus.