Hops as a metapopulation landscape for tetranychid-phytoseiid interactions: perspectives of intra- and interplant dispersal

Population densities, distributions and dispersal of Neoseiulus fallacis (Garman) and Tetranychus urticae (Koch) on individual hop plants, Humulus lupulus L. were studied for attributes of metapopulations such as empty patches, asynchrony of subpopulations, extinction of subpopulations, and dispersal of predators and prey among patches. Occupancy of hop leaves by predators or prey was stable over a season with 69–75% of leaves having neither predators nor prey, 4–15% with prey mites only, 9–17% with both predators and prey mites and 6–10% with predaceous mites only. Stability of occupancy classes through time indicated that inherently unstable predator and prey subpopulations developed asynchronously. Flagged hop leaves showed the existence of many empty individual leaves, colonization of some by prey, then by predators, then extinction of both, and then recolonization by spider mites. This illustrated the existence of empty patches, extinction of subpopulations, and dispersal of predators and prey to empty patches. This differed from spider mites and phytoseiid predators on apple foliage where there was a progression of occupancy status, indicating synchronous development of subpopulations on individual plants. Studies of predator and prey dispersal between hop plants showed that removal of basal leaves to 1.5 m high, a common agronomic practice, greatly limited dispersal of the predaceous mites but not the spider mites. Retaining basal leaves facilitated interplant movement of predators and improved the extent and timing of biological control. Through management, N. fallacis dispersal may be adjusted so that the entire hop planting becomes a metapopulation landscape, leading to greater stability and persistence of predator–prey within a season.     

Predatory role of Neoseiulus fallacis (Acari: Phytoseiidae): spatial and temporal dynamics in Washington red raspberry fields

The seasonal abundance of spider mites and their predator Neoseiulus fallacis (Garman) (Acari: Phytoseiidae) was determined during three consecutive years in Washington State red raspberry fields. Tetranychus urticae Koch (Acari: Tetranychidae), Eotetranychus carpini borealis (Ewing) (Acari: Tetranychidae), and N. fallacis were commonly found in Skagit and Whatcom Counties. E. carpini borealis colonized the fruiting canes earlier in the season than T. urticae. The two phytophages overlapped in midseason, but T. urticae entered diapause earlier than E. carpini borealis and N. fallacis. Densities of N. fallacis increased with increase in spider mite densities. However, the numerical response of the predator was more evident for T. urticae than for E. carpini borealis. Nevertheless, the predator was spatially associated with the two prey species. The spatial and seasonal distribution of N. fallacis in relationship to host plant phenology and prey distribution may influence the effectiveness of this predator as a biological control agent against spider mites in red raspberry. Densities of the predator increased too late to prevent spider mite damage. The predatory role of N. fallacis could be enhanced by introducing or conserving predators that are more tolerant to climatic factors that prevail in and around the cane canopy in the beginning of the season.     

Neoseiulus californicus (McGregor) and Neoseiulus fallacis (Garman): larval responsesto prey and humidity, nymphal feeding drive and nymphal predation on phytoseiid eggs

Are Neoseiulus californicus (McGregor) and Neoseiulus fallacis (Garman) both specialized predators of spider mites? As part of a series of studies made to answer this question, responses by larvae were assessed in treatments either with or without prey (Tetranychus urticae Koch) and with either moderate or high relative humidities (a factor that may distinguish between these two morphologically similar species). Neoseiulus fallacis larvae had more feeding, ambulatory activity and jerking (intra– or interspecific communication) in all treatments than N. californicus. The percent egg hatch was less and development took longer for N. fallacis larvae than for N. californicus larvae without prey at moderate humidity levels. The nymphs of both mites showed similar drives to feed 1–2>h after being held 12–48 h without food and then given eggs of T. urticae. Neoseiulus californicus nymphs fed more on the eggs of either phytoseiid and thereafter became adults than did N. fallacis nymphs. These data indicate that N. californicus may be a less specialized predator of spider mites than is N. fallacis.     

Phytoseiid mites on peppermint and effectiveness of Neoseiulus fallacis to control Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae) in arid growing regions

The humid-adapted species Neoseiulus fallacis (German) was the most common phytoseiid mite collected in either humid (> 100 cm annual rainfall) or arid (20-45 cm annual rainfall) mint growing regions of Washington, Oregon, Montana, Idaho, and California during 1991-1995. In experimental field plots, this predator gave excellent biological control of Tetranychus urticae Koch on mint grown under arid conditions in central Oregon when evaluated by an insecticide check method or by the caging of mites. N. fallacis is effective as a predator in arid areas probably because regular irrigation creates a humid environment in the canopy. The selective miticide propargite, when used in combination with predators, was effective at reducing high spider mite populations to below the treatment threshold faster than did N. fallacis alone.     

Intra- and interspecific predation by adult female Metaseiulus occidentalis and Typhlodromus pyri (Acari: Phytoseiidae) when provisioned with varying densities and ratios of Tetranychus urticae (Acari: Tetranychidae) and phytoseiid larvae

The phytoseiid mites Metaseiulus occidentalis (Nesbitt) and Typhlodromus pyri Schueten are used together and alone as biological control agents against tetranychid pest mites of apple. Their effectiveness as control agents may be impacted by intraguild predation. The effects of prey species and prey density on the rates of inter- and intraspecific predation and oviposition by these two predators were investigated through a series of experiments. Adult female predators were given prey as mixed populations of phytoseiid larvae and larvae of a more preferred species, the spider mite, Tetranychus urticae Koch, at different densities and ratios. Typhlodromus pyri, more of a generalist predator, showed higher rates of predation and cannibalism on phytoseiid immatures at most prey densities and ratios. Manly preference indices indicated that T. pyri switched to feed on phytoseiid larvae at higher prey levels and ratios of T. urticae than M. occidentalis. This greater ability to use phytoseiid larvae as prey may help stabilize T. pyri populations when more preferred prey is unavailable. This may, in part, explain the observed persistence of T. pyri populations when M. occidentalis populations were decreasing in orchard test plots.     

The Effects of Timing and Rates of Release of Phytoseiulus persimilis against Two-spotted Spider Mite Tetranychus urticae on Dwarf Hops

Single inoculative releases of the phytoseiid mite Phytoseiulus persimilis were made against the two-spotted spider mite, Tetranychus urticae, on two varieties of dwarf hops in 1996 and 1997 at means of 20, 10, 5, 2.5 and nil per plant, and at up to three timings. The numbers of spider mites recorded on leaves after the predators were released were related inversely to the rates of release. The earliest releases of the predator maintained spider mites at lower population densities than did those made later in the year. In all treatments the numbers of spider mites decreased when the prey:predator ratio reached approximately 10:1.     

The effect of powdery mildew on the number of prey consumed by Typhlodromus pyri (Acari: Phytoseiidae)

Abstract:  Prey consumption by Typhlodromus pyri Scheuten was studied in the presence and absence of apple powdery mildew, Podosphaera leucotricha (Ell. and Everh.) under constant laboratory conditions. Eggs of Tetranychus urticae Koch were offered to predatory mites as a prey. Seven densities ranging from five to 100 T. urticae eggs per arena were used. Mildew conidia (approximately 0.5 mg) were added to half of the arenas by brushing them from infected apple leaves. A single adult female of T. pyri was introduced onto each arena and number of prey eggs consumed was counted 12 h later when the predator was offered new T. urticae eggs again and the procedure was repeated once. Data showed that predators consumed in both experimental periods nearly all prey in experiments with densities up to 40 eggs per arena and no mildew. However, the number of eggs consumed decreased more than twofold when mildew conidia were supplied, even at high prey densities. Differences in predation rate between treatments with and without mildew were highly significant. The results thus indicate that availability of mildew as an alternative food can reduce prey suppression by T. pyri . Possible implications of these findings in biological control of spider mites by generalist predatory mites are discussed.     

Plant-related factors influence the effectiveness of Neoseiulus fallacis (Acari: Phytoseiidae), a biological control agent of spider mites on landscape ornamental plants

The predatory mite Neoseiulus fallacis (Garman) was evaluated as a biological control agent of herbivorous mites on outdoor-grown ornamental landscape plants. To elucidate factors that may affect predator efficiency, replicated tests were conducted on 30 ornamental plant cultivars that varied in relationship to their generalized morphology (e.g., conifers, shade trees, evergreen shrubs, deciduous shrubs, and herbaceous perennials), production method (potted or field grown), canopy density, and the prey species present on each. Plant morphological grouping and foliar density appeared to be the most influential factors in predicting successful biological control. Among plant morphological groups, N. fallacis was most effective on shrubs and herbaceous perennials and less effective on conifers and shade trees. N. fallacis was equally effective at controlling spider mites on containerized (potted) and field grown plants, and there was no difference in control of mites on plants with Tetranychus spp. versus those with Oligonychus or Schizotetranychus spp. Moderate to unsuccessful control of spider mites by N. fallacis occurred mostly on tall, vertical plants with sparse canopies. Acceptable spider mite control occurred in four large-scale releases of N. fallacis into production plantings of Abies procera, Thuja occidentalis 'Emerald', Malus rootstock, and Viburnum plicatum 'Newport'. These data suggest that N. fallacis can be an effective biological control agent of multiple spider mite species in a range of low-growing and selected higher growing ornamental plants.     

Spider Mites Avoid Plants with Predators

While searching for food, prey can use cues associated with their predators to select patches with a reduced predation risk. In many cases, odours indicate the presence of both food and predators. Spider mites are known to use odours to locate food and mates, but also to avoid interspecific competitors. We studied the response of the two-spotted spider mite, Tetranychus urticae, to cues associated with the presence of their predators, the phytoseiid Phytoseiulus persimilis. We found that the spider mites strongly avoid plants defended by this predator, but do not avoid plants with another predatory mite, Neoseiulus californicus. Since P. persimilis is commonly used in the greenhouse where our strain of T. urticae was collected and strains of this pest are known to adapt to greenhouse environments, we hypothesize that there has been selection on the pest to recognize its enemy. We further hypothesize that there has been no selection to recognize N. californicus, as it has not been used against two-spotted spider mites in the greenhouse where our spider mites were collected. We discuss the implications of avoidance of predation by spider mites and non-lethal effects of predators for biological control of this pest in greenhouses.     

Effect of tomato leaf hairiness on functional and numerical response of Neoseiulus californicus (Acari: Phytoseiidae)

The objective of this study was to determine whether differences in hairiness of tomato plants affect the functional and numerical response of the predator Neoseiulus californicus McGregor attacking the two-spotted spider mite, Tetranychus urticae Koch. Two tomato hybrids with different density of glandular hairs were used. The functional response was measured by offering eggs and adults of T urticae at densities ranging from 4 to 64 items per tomato leaflet (surface ca. 6.3 cm2); eggs were offered to predator protonymphs and deutonymphs, adult spider mites to adult predators. The number of spider mites eaten as a function of initial density was fitted to the disc equation. Predator densities were regressed against initial prey densities to analyze the numerical response. The number of eggs and adults of T. urticae eaten by N. californicus was extremely low in both hybrids. The nymphal stage of N. californicus and prey density had a significant effect on the number of T urticae eggs eaten by the predator, while hybrid had no effect. The functional response fitted reasonably well to the Holling model. The handling time (Th) and the attack rate (a) were very similar among the two hybrids. The numerical response indicated that the absolute density of predators increased with changes in spider mite densities but the relative predator/prey density decreased in both hybrids. Tomato hairiness prevented N. californicus from exhibiting a strong numerical response and the predator functional response was much lower than observed in other host plants and other phytoseiids. This result shows the need to consider plant attributes as an essential and interactive component of biological control practices.     

东亚小花蝽对西方花蓟马和二斑叶螨的捕食选择性

多食性天敌对猎物的捕食选择性及猎物密度对天敌捕食的干扰作用直接影响到天敌对不同猎物的控制作用.在实验室条件下研究了东亚小花蝽对西方花蓟马和/或二斑叶螨不同虫态的捕食选择性,以及两猎物中一种猎物的密度变化对小花蝽取食另一种猎物的影响.结果如下:东亚小花蝽5龄若虫和成虫对西方花蓟马2龄若虫的捕食选择性均强于对其成虫,对二斑叶螨的选择性为雌成螨>若螨>幼螨.实验中西方花蓟马2龄若虫是东亚小花蝽最喜好的虫态.二斑叶螨雌成螨密度固定为60头/19.63cm2,西方花蓟马若虫密度从10增加到60时显著地减少了东亚小花蝽对二斑叶螨的取食.反之,固定西方花蓟马同样密度,增加二斑叶螨密度却没有显著改变小花蝽对西方花蓟马的取食.此结果进一步表明,西方花蓟马是东亚小花蝽更喜好的猎物.     

Interactions in a trirophic acarine predator-prey metapopulation system: effects of Tetranychus urticae on the dispersal rates of Phytoseiulus persimilis (Acarina: Tetranychidae, Phytoseiidae)

The dispersal behaviour of the predatory mite Phytoseiulus persimilis Athias-Henriot between bean plants was studied in a greenhouse. The aim of the study was to estimate the rate of predator emigration affected by different densities of Tetranychus urticae Koch and different numbers of between-plant connections (bridges). The results show that predators emigrate from a plant almost exclusively as a response to the local prey density whereas the loss rate (the per capita rate at which predators disappear from the system) also depends on the prey density on the surrounding plants, provided they are connected to the central plant by bridges. © Rapid Science Ltd. 1998     

Pest species diversity enhances control of spider mites and whiteflies by a generalist phytoseiid predator

To test the hypothesis that pest species diversity enhances biological pest control with generalist predators, we studied the dynamics of three major pest species on greenhouse cucumber: Western flower thrips, Frankliniella occidentalis (Pergande), greenhouse whitefly, Trialeurodes vaporariorum (Westwood), and two-spotted spider mites, Tetranychus urticae Koch in combination with the predator species Amblyseius swirskii Athias-Henriot. When spider mites infested plants prior to predator release, predatory mites were not capable of controlling spider mite populations in the absence of other pest species. A laboratory experiment showed that predators were hindered by the webbing of spider mites. In a greenhouse experiment, spider mite leaf damage was lower in the presence of thrips and predators than in the presence of whiteflies and predators, but damage was lowest in the presence of thrips, whiteflies and predators. Whitefly control was also improved in the presence of thrips. The lower levels of spider mite leaf damage probably resulted from (1) a strong numerical response of the predator (up to 50 times higher densities) when a second and third pest species were present in addition to spider mites, and (2) from A. swirskii attacking mobile spider mite stages outside or near the edges of the spider mite webbing. Interactions of spider mites with thrips and whiteflies might also result in suppression of spider mites. However, when predators were released prior to spider mite infestations in the absence of other pest species, but with pollen as food for the predators, we found increased suppression of spider mites with increased numbers of predators released, confirming the role of predators in spider mite control. Thus, our study provides evidence that diversity of pest species can enhance biological control through increased predator densities.     

Differential Effects of Plant Species on a Mite Pest (Tetranychus Urticae) and its Predator (Phytoseiulus Persimilis): Implications for Biological Control

The influence of plant species on the population dynamics of the spider mite pest, Tetranychus urticae, and its predator, Phytoseiulus persimilis, was examined as a prerequisite to effective biological control on ornamental nursery stock. Experiments have been done to investigate how the development, fecundity and movement of T. urticae, and the movement of P. persimilis were affected by plant species. A novel experimental method, which incorporates plant structure, was used to investigate the functional response of P. persimilis. Development times for T. urticae were consistent with published data and did not differ with plant species in a biologically meaningful way. Plant species was shown to have a major influence on fecundity (P < 0.001) and movement of the pest mite (P < 0.01), but no influence on the movement of the predator. The movement of both pest and predator was shown to be related to the density of the adult pest mites on the plant (P < 0.001). Plant structure affected the functional response, particularly in relation to the ability of the predator to locate prey at low densities. The impact of these findings on the effective use of biological control on ornamental nursery stock is discussed.     

Interactions among phytophagous mites, and introduced and naturally occurring predatory mites, on strawberry in the UK

In choice test experiments on strawberry leaf disc arenas the phytoseiid mites Neoseiulus californicus and N. cucumeris were more effective than Typhlodromus pyri as predators of the phytophagous mites Tetranychus urticae and Phytonemus pallidus. There were no preferences shown for either prey by any of these predators. In multiple predator leaf disc experiments both Phytoseiulus persimilis and N. cucumeris significantly reduced numbers of T. urticae eggs and active stages; this effect was seen when the two species were present alone or in combination with other predator species. Neoseiulus californicus was less effective at reducing T. urticae numbers, and T. pyri was not effective; no interaction between predator species was detected in these experiments. When T. urticae alone was present as prey on potted plants, P. persimilis and N. californicus were the only phytoseiids to significantly reduce T. urticae numbers. These two predator species provided effective control of T. urticae when P. pallidus was also present; however, none of the predators reduced numbers of P. pallidus. There were no significant negative interactions when different species of predators were present together on these potted plants. In field experiments, releases of both P. persimilis and N. cucumeris significantly reduced T. urticae numbers. However, there was a significant interaction between these predator species, leading to poorer control of T. urticae when both species were released together. These results show the importance of conducting predator/prey feeding tests at different spatial scales.     

Regional persistence of locally unstable predator/prey populations

Phytoseiid mites are efficient predators capable of completely destroying colonies of spider mites. Thus, coexistence of phytoseiids and their tetranychid prey at a local scale (typically an individual plant) is not likely for more than a single predator/prey cycle. However, the species may coexist at a regional scale, i.e. in a complex environment consisting of many plants, provided local colonisations, extinctions and recolonisations occur asynchronously. This review investigates some of the factors responsible for establishing and maintaining spatial asynchrony between local populations of prey and predators, such as dispersal, environmental heterogeneity and demographic stochasticity. Existing predator/prey models are considered in order to find agreement between theory and empirical data. Based on our current knowledge of spatial processes and their importance for the overall dynamics and persistence of predator/prey interactions, some consequences and aspects for biological control of crop pests by means of natural enemies are outlined.     

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 (rm) 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, rm 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 (Gnanvossou et al. 2002) 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.     

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.     

Effects of nutrients and predators on an old-field food chain: interactions of top-down and bottom-up processes

In theory, selection favours predators that select prey in order to maximise reproductive success. We studied the association between preference and performance of the generalist predator Orius laevigatus with respect to two prey species: spider mites ( Tetranychus urticae ) and western flower thrips ( Frankliniella occidentalis ). Under ample prey supply, the predators had higher maximum reproductive success (measured as intrinsic population growth rate r ) on thrips than on spider mites; hence thrips represent a higher prey quality to the bugs. This was at odds with the observed preference of the predatory bug for plants (patches) with high densities of spider mites to plants with moderate densities of thrips in release-recapture experiments. Thus, prey quality does not suffice to explain the preference of predators for plants with prey. The quality of a patch as an oviposition site (i.e. the number of eggs produced on a patch per bug per day) also did not match preference patterns. Hence, patch preference was not correlated to prey quality or oviposition rate on prey patches. However, patch productivity, i.e. the total number of offspring surviving until adulthood that can be produced by one female on a patch, was correlated with preference. This was further tested by offering the predators a choice between plants with high densities of spider mites and plants with high densities of thrips in an independent set of release-recapture experiments. These two types of prey patches were found equivalent in terms of patch productivity. Indeed, the predators showed no preference for either of the two types of patches, which is in agreement with our predictions. This suggests that the predatory bugs select patches based on patch productivity rather than on prey quality or oviposition rate on a patch.     

An acarine predator-prey metapopulation system inhabiting greenhouse cucumbers

The two-spotted spider mite ( Tetranychus urticae ) is a serious pest on greenhouse cucumbers, but can be controlled by the phytoseiid predator Phytoseiulus persimilis. The two mite species exhibit considerable fluctuations in overall population densities but within acceptable limits. The system appears to be persistent at a regional (greenhouse) scale in spite of frequent local extinctions (e.g. at individual plants). Experimental evidence indicates that the mites form a metapopulation system characterized by 'shifting mosaic' dynamics. A stochastic simulation model is used to analyse the role played by dispersal in the dynamics and persistence of the system. It shows that demographic stochasticity generates sufficient endogenous 'noise' to counteract the synchronizing effect of density-dependent dispersal, provided dispersal rates are not too high and the system is not too small. Low dispersal rates, on the other hand, increase the risk of local outbreaks of spider mites that may cause destruction of plants.