Patterns, mechanisms and spatial scale of aggregation in generalist and specialist predatory mites (Acari: Phytoseiidae)

Prey species often distribute themselves patchily in their habitats. In response to this spatial variation in prey density, some predator species aggregate in patches of higher prey density. This paper reviews a series of laboratory experiments to demonstrate the patterns of responses by phytoseiid predators (Phytoseiulus persimilis, Typhlodromus occidentalis and Amblyseius andersoni) to spatial variation in the density of their spider mite prey (Tetranychus urticae) and reveal the behavioural mechanisms underlying the observed patterns. In addition, patterns of aggregation were examined at a variety of spatial scales on plants in greenhouses. The patterns, mechanisms and spatial scale of aggregation in three predatory species are discussed in relation to their varying degrees of polyphagy. The results show that a specialist predator species (1) aggregates more strongly than generalist predators, (2) does so not because it finds prey patches of high density more easily but because it remains in these patches longer than generalist predators and (3) tends to aggregate more often at lower levels of spatial scale than generalist predators. It is suggested that these conclusions, based mainly on laboratory studies of a small sample of species, should be tested in the future on a wider selection of specialist and generalist species at different scales in the field. This revised version was published online in November 2006 with corrections to the Cover Date.     

Canalization of body size matters for lifetime reproductive success of male predatory mites (Acari: Phytoseiidae)

The adaptive canalization hypothesis predicts that highly fitness‐relevant traits are canalized via past selection, resulting in low phenotypic plasticity and high robustness to environmental stress. Accordingly, we hypothesized that the level of phenotypic plasticity of male body size of the predatory mites Phytoseiulus persimilis (low plasticity) and Neoseiulus californicus (high plasticity) reflects the effects of body size variation on fitness, especially male lifetime reproductive success (LRS). We first generated small and standard‐sized males of P. persimilis and N. californicus by rearing them to adulthood under limited and ample prey supply, respectively. Then, adult small and standard‐sized males were provided with surplus virgin females throughout life to assess their mating and reproductive traits. Small male body size did not affect male longevity or the number of fertilized females but reduced male LRS of P. persimilis but not N. californicus. Proximately, the lower LRS of small than standard‐sized P. persimilis males correlated with shorter mating durations, probably decreasing the amount of transferred sperm. Ultimately, we suggest that male body size is more strongly canalized in P. persimilis than N. californicus because deviation from standard body size has larger detrimental fitness effects in P. persimilis than N. californicus. © 2014 The Authors. Biological Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 889–899.     

Verified and potential pathogens of predatory mites (Acari: Phytoseiidae)

Several species of phytoseiid mites (Acari: Phytoseiidae), including species of the genera Amblyseius, Galendromus, Metaseiulus, Neoseiulus, Phytoseiulus and Typhlodromus, are currently reared for biological control of various crop pests and/or as model organisms for the study of predator-prey interactions. Pathogen-free phytoseiid mites are important to obtain high efficacy in biological pest control and to get reliable data in mite research, as pathogens may affect the performance of their host or alter their reproduction and behaviour. Potential and verified pathogens have been reported for phytoseiid mites during the past 25 years. The present review provides an overview, including potential pathogens with unknown host effects (17 reports), endosymbiotic Wolbachia (seven reports), other bacteria (including Cardinium and Spiroplasma) (four reports), cases of unidentified diseases (three reports) and cases of verified pathogens (six reports). From the latter group four reports refer to Microsporidia, one to a fungus and one to a bacterium. Only five entities have been studied in detail, including Wolbachia infecting seven predatory mite species, other endosymbiotic bacteria infecting Metaseiulus (Galendromus, Typhlodromus) occidentalis (Nesbitt), the bacterium Acaricomes phytoseiuli infecting Phytoseiulus persimilis Athias-Henriot, the microsporidium Microsporidium phytoseiuli infecting P. persimilis and the microsporidium Oligosproridium occidentalis infecting M. occidentalis. In four cases (Wolbachia, A. phytoseiuli, M. phytoseiuli and O. occidentalis) an infection may be connected with fitness costs of the host. Moreover, infection is not always readily visible as no obvious gross symptoms are present. Monitoring of these entities on a routine and continuous basis should therefore get more attention, especially in commercial mass-production. Special attention should be paid to field-collected mites before introduction into the laboratory or mass rearing, and to mites that are exchanged among rearing facilities. However, at present general pathogen monitoring is not yet practical as effects of many entities are unknown. More research effort is needed concerning verified and potential pathogens of commercially reared arthropods and those used as model organisms in research.     

The fitness costs of developmental canalization and plasticity

Organisms are capable of an astonishing repertoire of phenotypic responses to the environment, and these often define important adaptive solutions to heterogeneous and unpredictable conditions. The terms ‘phenotypic plasticity’ and ‘canalization’ indicate whether environmental variation has a large or small effect on the phenotype. The evolution of canalization and plasticity is influenced by optimizing selection‐targeting traits within environments, but inherent fitness costs of plasticity may also be important. We present a meta‐analysis of 27 studies (of 16 species of plant and 7 animals) that have measured selection on the degree of plasticity independent of the characters expressed within environments. Costs of plasticity and canalization were equally frequent and usually mild; large costs were observed only in studies with low sample size. We tested the importance of several covariates, but only the degree of environmental stress was marginally positively related to the cost of plasticity. These findings suggest that costs of plasticity are often weak, and may influence phenotypic evolution only under stressful conditions.     

Prey-related odor preference of the predatory mites Typhlodromalus manihoti and Typhlodromalus aripo (Acari: Phytoseiidae)

Typhlodromalus manihoti and Typhlodromalus aripo are exotic predators of the cassava green mite Mononychellus tanajoa in Africa. In an earlier paper, we showed that the two predators were attracted to odors from M. tanajoa-infested cassava leaves. In addition to the key prey species, M. tanajoa, two alternative prey mite species, Oligonychus ossypii and Tetranychus urticae also occur in the cassava agroecosystem. Here, we used a Y-tube olfactometer to determine the attraction of the predators to odors from O. gossypii- or T. urticae-infested cassava leaves and their prey-related odor preference. T. aripo but not T. manihoti was slightly attracted to odors from O. gossypii-infested leaves. Both predator species showed a stronger response to odors from cassava leaves infested by M. tanajoa over odors from cassava leaves infested by O. gossypii. Neither predator species was attracted to odors from T. urticae-infested leaves and the predators preferred the odors from M. tanajoa-infested leaves over those from T. urticae-infested leaves. When O. gossypii was present together with M. tanajoa on the same leaves or on different sets of leaves offered together as an odor source the two predators were attracted. In contrast, after mixing non-attractive odors from T. urticae-infested leaves with attractive odors from M. tanajoa-infested leaves, neither T. aripo nor T. manihoti was attracted. Ecological advantages and disadvantages of the predators’ behavior and possible implications for biological control of M. tanajoa are discussed. This revised version was published online in July 2006 with corrections to the Cover Date.     

Powdery mildew (Ascomycotina: Erysiphales) — an alternative food for the predatory mite Typhlodromus pyri Scheuten (Acari: Phytoseiidae)

The ability of Typhlodromus pyri Scheuten to feed on powdery mildew was investigated. Adult females of T. pyri which had previously been fed on the pollen of Pinus sylvestris L. were offered three powdery mildew species and their feeding behaviour was observed. The females fed readily on the conidia of Erysiphe orontii Cast. from tobacco and Oidium fragariae Harz. from strawberry while no feeding was observed on Erysiphe polygoni DC. from red clover, even after the mites were starved for 2 days. Erysiphe orontii was tested for its effect on the survival, oviposition and development of T. pyri. The results showed that the conidia of E. orontii can supply mites with the water and nutrients necessary for their normal development. Mature females successfully mated and reproduced, although their oviposition rate was low. This revised version was published online in November 2006 with corrections to the Cover Date.     

Evaluation of predatory mite (Acari: Phytoseiidae) releases to suppress spruce spider mites, Oligonychus ununguis (Acari: Tetranychidae), on juniper

A laboratory trial evaluated four phytoseiid species for their potential as biological control agents of spruce spider mite, Oligonychus ununguis (Jacobi) (Acari: Tetranychidae). An augmentative biological control approach, using the predatory mites Neoseiulus fallacis Garman and Galendromus occidentalis Nesbitt (Acari: Phytoseiidae), was evaluated for reducing pest mite densities and injury, and economic costs on Juniperus chinensis 'Sargentii' A. Henry (Cupressaceae) in an outdoor nursery. Sequential releases of predator species, individually and in combination, were tested and compared with two commonly used miticides, a low-toxicity miticide, horticultural oil, and a conventional miticide, hexythiazox. Timing of treatments was based on grower-determined need, and predator release rates were based on guidelines in literature received from producers of beneficial organisms. Predator releases were more expensive and provided less effective suppression of spruce spider mites, resulting in greater spider mite injury to plants, compared with conventional pesticides. However, spider mite damage to plants did not differ in an economically meaningful way between treatments. Unsatisfactory levels of control seem related to under estimations of actual spider mite abundance based on grower perceptions and the beat sampling technique used to estimate predator release rates. These data suggest that when initial populations of spruce spider mite are high, it is unlikely that sequential releases of predator species, individually or in combination, will suppress spider mite populations. In this trial, augmentative biological control control was 2.5-7 times more expensive than chemical controls.     

Survival, horizontal distribution, and economics of releasing predatory mites (Acari: Phytoseiidae) using mechanical blowers

The predatory mites Phytoseiulus persimilis and Amblyseius cucumeris are commonly used in commercial greenhouses for augmentative biological control of spider mites and thrips, respectively. One disincentive for growers to use biological control is the cost of manually distributing predators. Therefore, we tested the efficiency of two types of mechanical blowers for dispensing predatory mites. One blower had a metering device to control the flow of material (MBWMD); the other had no metering device (MBWOMD). Predator survival was measured at various distances after dispensing them with blowers. Survival also was compared with a manual-sprinkling method. When blowers were held horizontally, the distribution of predators was uneven for both blowers. For P. persimilis, 77% were found at 1.52 and 2.44 m with the MBWOMD, whereas 75% were located at 2.44, 3.35, and 4.27 m with the MBWMD. For A. cucumeris, 97% were found at 1.52, 2.44, and 3.35 m with the MBWOMD, while 81% landed at 2.44 and 3.35 m with the MBWMD. Percentages of live P. persimilis found using the MBWMD, MBWOMD, and manual-sprinkling were 31 ± 4, 49 ± 3, and 68 ± 8%, respectively. For A. cucumeris, percentages of survival were 61 ± 4, 79 ± 4, and 83 ± 7%, respectively. The MBWOMD dispensed P. persimilis 22 and 44 times faster than the MBWMD and manual-sprinkling, respectively. Mechanical blowers have the advantage of better coverage, substantially less labor, and estimated total costs to growers that are approximately half that of the manual release method.     

Evaluation of astigmatid mites as factitious food for rearing four predaceous phytoseiid mites (Acari: Astigmatina; Phytoseiidae)

Phytoseiids are possibly the most important mites used in biological control and are usually produced using a tritrophic system that, although efficient, is expensive and laborious. Mites of the cohort Astigmatina (Sarcoptiformes) have been used as factitious prey in the mass rearing of phytoseiids and may allow a much simpler production system. This research evaluated the potential of ten Astigmatina species to serve as factitious food sources for Euseius concordis (Chant), Iphiseiodes zuluagai Denmark and Muma, Neoseiulus barkeri Hughes and Neoseiulus californicus McGregor, all phytoseiid species commonly found in different countries. The high fecundity and survival rates obtained suggest that Thyreophagus n. sp. is a suitable prey for rearing N. barkeri and that Austroglycyphagus lukoschusi (Fain) and Blomia tropicalis is suitable for rearing N. californicus. Oviposition by E. concordis was negligible, but survivorship was high on most prey species, suggesting that these species may be useful for maintenance of the predator. I. zuluagai had low fecundity and survival on all the astigmatid species evaluated and none were suitable for its rearing.     

Susceptibility to deltamethrin in the predatory mites Neoseiulus californicus and Phytoseiulus macropilis (Acari: Phytoseiidae) populations in protected ornamental crops in Brazil

Knowledge of inter and intra-specific variation in the susceptibility of natural enemies to pesticides could help to better design integrated pest management strategies. The objective of this research was to evaluate the susceptibility to deltamethrin in populations of the predatory mites Neoseiulus californicus (McGregor) and Phytoseiulus macropilis (Banks) populations collected from protected ornamental crops in Brazil. The susceptibility to deltamethrin was characterized against immature and adult stages of both species. The impact of this insecticide was also measured by estimating the intrinsic rate of increase (r _i). The immature and adult stages of N. californicus were approximately 3,600 and 3,000-fold more tolerant to deltamethrin than those of P. macropilis. However, high variability in the susceptibility to this insecticide was detected among P. macropilis populations, with resistance ratios of up to 3,500-fold. The selection of deltamethrin-resistant strains of P. macropilis could be exploited in applied biological control programs.     

Morphological variation and reproductive incompatibility of three coconut-mite-associated populations of predatory mites identified as Neoseiulus paspalivorus (Acari: Phytoseiidae)

Predatory mites identified as Neoseiulus paspalivorus DeLeon (Phytoseiidae) have been considered as agents for classical biological control of the coconut mite, Aceria guerreronis Keifer (Eriophyidae), in Africa and elsewhere. Preliminary identification of geographically distinct populations as belonging to the same species (N. paspalivorus) was based on their morphological similarity. However, laboratory studies recently conducted have shown large differences in feeding behaviors and biological characteristics among individuals collected from three geographic origins: Brazil (South America), Benin and Ghana (West Africa). As morphologically similar specimens do not necessarily belong to the same species, we evaluated under laboratory conditions, reproductive compatibility between the specimens from three geographic locations to ascertain their conspecificity. Morphological measurements were also made to determine whether there is a means of discriminating between them. Inter-population crosses showed complete reproductive isolation between the three geographic populations, but interpopulation discontinuities in morphometric characters were absent. These results indicate that the tested specimens are distinct biological entities despite morphological similarity. Further molecular genetic studies are therefore proposed, including screening for endosymbionts and assessment of genetic differentiation, to determine the cause of reproductive incompatibility and to clarify the taxonomic relationship between those populations.     

Phenotypic plasticity, heterochrony and ontogenetic repatterning during juvenile development of divergent Arctic charr (Salvelinus alpinus)

Phenotypic plasticity is a developmental process that plays a role as a source of variation for evolution. Models of adaptive divergence make the prediction that increasing ecological specialization should be associated with lower levels of plasticity. We tested for differences in the magnitude, rate and trajectory of morphological plasticity in two lake populations of Arctic charr (Salvelinus alpinus) that exhibited variation in the degree of resource polymorphism. We reared offspring on diet treatments that mimicked benthic and pelagic prey. Offspring from the more divergent population had lower levels of morphological plasticity. Allometry influenced the rate of shape change over ontogeny, with differences in rate among ecomorphs being minimal when allometric variation was removed. However, plasticity in the spatial trajectory of development was extensive across ecomorphs, both with and without the inclusion of allometric variation, suggesting that different aspects of shape development can evolve independently.     

Risk assessment of Cry toxins of Bacillus thuringiensis on the predatory mites Euseius concordis and Neoseiulus californicus (Acari: Phytoseiidae)

Genetically modified plants carrying Cry toxins of Bacillus thuringiensis (Bt) are widely used for pest control. Possible adverse effects as a result of the use of this control technique to non-target organisms is still a concern; however, few studies have addressed the effects of Bt crops on phytoseiid predatory mites. Phytoseiids are important for the natural control of phytophagous mites, but they can also feed on pollen, plant exudates, etc. Thus, phytoseiids may ingest Bt toxins through several pathways. In this paper, we evaluate the direct effect of Bt-toxins by feeding the predators on Bt cell suspensions, on solution of a Bt toxin and the tri-trophic effect by Bt expressed in transgenic plants. We present a method of conducting toxicological tests with Phytoseiidae which can be useful in studies of risk analysis of toxins to be expressed by genetically engineered plants. This method was used to evaluate the potential effect of ingestion of suspensions of Bt (1.25 × 10⁸ spores/ml) and of purified protein Cry1Ia12 (0.006 mg/ml and 0.018 mg/ml) on Euseius concordis, a predatory mite that develops and reproduces best on pollen. The effects of genetically modified Bollgard^® cotton, which carries the Cry1Ac protein, on Neoseiulus californicus, a selective predator that feeds more on spider mites than on pollen or insects, was determined by feeding them with Tetranychus urticae reared in Bollgard^® cotton and on the non-transgenic isoline. When E. concordis was fed with suspension of Bt isolate derived from product Dipel^® PM, no significant effects were detected. Similarly, Cry1Ia12 Bt toxin, at a concentration of 0.006 mg/ml, did not affect E. concordis. At a concentration of 0.018 mg/ml, however, the intake of this protein reduced the reproduction of E. concordis. There were no effects of Bollgard^® cotton on the biological traits and on the predatory capacity of N. californicus. Results indicate that the Cry toxins of B. thuringiensis studied, at the concentrations used in the field or expressed in transgenic plants, should not affect the predatory mites E. concordis and N. californicus.     

Influence of prey density, species and developmental stages on the predatory behaviour ofAmblyseius longispinosus (Acari: Phytoseiidae)

The influence of prey density, species and developmental stages on the predatory behaviour ofAmblyseius longispinosus (Evans) was studied. A 24 h exposure revealed that gravid females were more voracious compared to young females. The trends in the number of eggs and larvae consumed by each young and gravid female predator were about the same, showing an increase with density of the red and the yellow strains ofT. urticae levelling off at a prey density of 40 per predator. The highest mean number of eggs consumed in 24 h was 16.7 for the young female and 33.3 for the gravid female, and a mean high of 17 larvae in 24 h for the young female and 27.8 for the gravid female. With adult prey, however, the predators reached satiation point at a lower density of five to ten adult prey per female. In general, the response curves were adequately described by the Holling’s Type II model. Under continuous exposure for five days, a significant reduction in consumption was observed with the gravid female from the second day onwards, to a level similar to the number of eggs and larvae consumed by a young female predator.     

Population dynamics of phytophagous and predatory mites (Acari: Tetranychidae, Eriophyidae, Phytoseiidae) on bamboo plants in Fujian, China

The seasonal cycle and population dynamics of Schizotetranychus nanjingensis Ma and Yuan, Aponychus corpuzae Rimando (Tetranychidae), Aculus bambusae Kuang (Eriophyidae) and their natural enemy Typhlodromus bambusae Ehara (Phytoseiidae) were studied during 1996–1998 in moso bamboo forests in Nanping, Fujian, China. Damage to bamboo leaves was often caused by mixed populations of the three phytophagous species, which displayed different seasonal dynamics: S. nanjingensis fed actively and reproduced in May and from late July to late October (aestivating from June to mid July), Ap. corpuzae was active and reproduced from mid July to late November, and Ac. bambusae from July to next February. During Spring S. nanjingensis was the dominant species with the greatest niche width, but in Summer Ac. bambusae and Ap. corpuzae became dominant and had greater niche widths. In Autumn, Ac. bambusae decreased but both S. nanjingensis and Ap. corpuzae mites increased and the latter became dominant. In winter all species decreased sharply in number. The two spider mite species (S. nanjingensis and Ap. corpuzae) had high niche overlaps in all four seasons. Niche overlaps between the eriophyid Ac. bambusae and the two spider mites were similarly high except during the spring when Ac. bambusae was absent. The predatory mite (T. bambusae) had higher niche overlap with Ap. corpuzae than with others during Autumn and Winter, but during Spring and Summer niche overlap was higher with S. nanjingensis.     

Different colonization patterns of phytophagous and predatory mites (Acari: Tetranychidae, Phytoseiidae) on three grape varieties: a case study

In a vineyard having three varieties of grape (Merlot, Trebbiano and Garganega) differently colonized by two phytoseiid species,Typhlodromus pyri Scheuten andAmblyseius andersoni (Chant), the dynamics of mite populations were monitored over 5 years (1989–1993) in order to study their colonization, interspecific competition and the control of spider mites, i.e.Panonychus ulmi (Koch). These aspects were also investigated by releasingT. pyri, A. andersoni andAmblyseius aberrans (Oudemans) on some of the above varieties. In most of the experimental years (1989–1992), selective pesticides were used in order to allow a successful release of phytoseiids, in particularA. aberrans. The use of non-selective insecticides was re-established during 1993 in order to test its effect on the new mite communities originating from 1989 onwards. In the first years of the experiments an apparent relationship between grape variety and phytoseiid species was observed: in the control plots,A. andersoni occurred on Merlot whereT. pyri was rare, while the latter species was largely dominant overA. andersoni on Trebbiano and Garganega.Panonychus ulmi populations reached moderate levels only on Merlot and in the first part of experiments. The variety-phytoseiid species relationship was temporary as, at the end of experiments,T. pyri was completely dominant on all varieties. This new situation started when prey occurrence and interspecific competition decreased in importance. The moderate success of theT. pyri release on Merlot contrasts with the results of previous experiments. Two factors could be involved in this phenomenon: low interspecific competition by phytoseiids and predation by macropredators.Amblyseius aberrans was able to displaceA. andersoni andT. pyri on grape varieties where the two species were more abundant and reached higher population densities on varieties with pubescent leaf undersurfaces. In the first experimental year, spider mite densities were reduced more effectively inA. aberrans release plots than in the control or inT. pyri release plots. One year later,P. ulmi reached lower levels in the release treatments than in the control.Typhlodromus pyri andA. aberrans persisted in conditions of prey scarcity. The high competitivity ofA. aberrans over the remaining two phytoseiid species constitutes a major factor in selecting predatory species for inoculative releases in vineyards.     

Efficacy of indigenous predatory mites (Acari: Phytoseiidae) against the citrus rust mite Phyllocoptruta oleivora (Acari: Eriophyidae): augmentation and conservation biological control in Israeli citrus orchards

The citrus rust mite (CRM), Phyllocoptruta oleivora (Acari: Eriophyidae) is a cosmopolitan key pest of citrus, inflicting severe economic damage if not controlled. In Israel, CRM damages all citrus cultivars. International regulation and increasing control failures of CRM led growers to seek sustainable biological control solutions such as acarine biological control agents. Laboratory studies conducted in Israel have indicated that the indigenous predator species Amblyseius swirskii, Iphiseius degenerans, Typhlodromus athiasae and Euseius scutalis (all Acari: Phytoseiidae) can potentially control CRM. Our general objective in the present study was to bridge the gap of knowledge between laboratory studies and the lack of control efficacy of these species in commercial orchards. Predator augmentation in the field showed that although predator populations increased immediately following releases they later decreased and did not affect CRM populations. When A. swirskii augmentation was combined with a series of maize pollen applications, A. swirskii populations were enhanced substantially and continuously but again CRM populations were not affected. Growth chamber studies with CRM-infested seedlings, with or without a maize pollen supplement, indicated that pollen provisioning led to population increase of E. scutalis and A. swirskii but only E. scutalis significantly lowered CRM populations. Control with E. scutalis was confirmed in the field on CRM infested seedlings with pollen provisioned by adjacent flowering Rhodes grass. While experiments in mature citrus orchard showed that pollen supplement usually increased predator populations they also indicated that other factors such as intraguild interactions and pesticide treatments should be taken into account when devising CRM biological control programs.     

Morphological change and phenotypic plasticity in native and non‐native pumpkinseed sunfish in response to sustained water velocities

Phenotypic plasticity can contribute to the proliferation and invasion success of nonindigenous species by promoting phenotypic changes that increase fitness, facilitate range expansion and improve survival. In this study, differences in phenotypic plasticity were investigated using young‐of‐year pumpkinseed sunfish from colonies established with lentic and lotic populations originating in Canada (native) and Spain (non‐native). Individuals were subjected to static and flowing water treatments for 80 days. Inter‐ and intra‐population differences were tested using ancova and discriminant function analysis, and differences in phenotypic plasticity were tested through a manova of discriminant function scores. Differences between Iberian and North American populations were observed in dorsal fin length, pectoral fin position and caudal peduncle length. Phenotypic plasticity had less influence on morphology than genetic factors, regardless of population origin. Contrary to predictions, Iberian pumpkinseed exhibited lower levels of phenotypic plasticity than native populations, suggesting that canalization may have occurred in the non‐native populations during the processes of introduction and range expansion.