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.     

不同猎物及密度对巴氏新小绥螨和拉戈钝绥螨同类相残和集团内捕食作用的影响

明确不同猎物及密度下巴氏新小绥螨Neoseiulus barkeri与拉戈钝绥螨Amblyseius largoensis(Muma)的同类相残和集团内捕食作用,为其协同应用控制橡胶树害螨提供依据.在室温27±1℃、湿度75％±5％、光周期12 L∶12D 条件下,以六点始叶螨 Eotetranvchus sexmac...     

Intraguild Interactions Between the Predatory Mites Neoseiulus californicus and Phytoseiulus persimilis

Species at the same trophic level may interact through competition for food, but can also interact through intraguild predation. Intraguild predation is widespread at the second and third trophic level and the effects may cascade down to the plant level. The effects of intraguild predation can be modified by antipredator behaviour in the intraguild prey. We studied intraguild predation and antipredator behaviour in two species of predatory mite, Neoseiulus californicus and Phytoseiulus persimilis, which are both used for control of the two-spotted spider mite in greenhouse and outdoor crops. Using a Y-tube olfactometer, we assessed in particular whether each of the two predators avoids odours emanating from prey patches occupied by the heterospecific predator. Furthermore, we measured the occurrence and rate of intraguild predation of different developmental stages of P. persimilis and N. californicus on bean leaves in absence or in presence of the shared prey. Neither of the two predator species avoided prey patches with the heterospecific competitor, both when inexperienced with the other predator and when experienced with prey patches occupied by the heterospecific predator. Intraguild experiments showed that N. californicus is a potential intraguild predator of P. persimilis. However, P. persimilis did not suffer much from intraguild predation as long as the shared prey was present. This is probably because N. californicus prefers to feed on two-spotted spider mites rather than on its intraguild prey.     

Prey preference,intraguild predation and population dynamics of an arthropod food web on plants

The theory of intraguild predation (IGP) largely studies effects on equilibrium densities of predators and prey, while experiments mostly concern transient dynamics. We studied the effects of an intraguild (IG) predator, the bug Orius laevigatus, on the population dynamics of IG-prey, the predatory mite Phytoseiulus persimilis, and a shared prey, the phytophagous two-spotted spider mite Tetranychus urticae, as well as on the performance of cucumber plants in a greenhouse. The interaction of the predatory mite and the spider mite is highly unstable, and ends either by herbivores overexploiting the plant or predators exterminating the herbivores. We studied the effect of IGP on the transient dynamics of this system, and compared the dynamics with that predicted by a simple population-dynamical model with IGP added. Behavioural studies showed that the predatory bug and the predatory mite were both attracted to plants infested by spider mites and that the two predators did not avoid plants occupied by the other predator. Observations on foraging behaviour of the predatory bug showed that it attacks and kills large numbers of predatory mites and spider mites. The model predicts strong effects of predation and prey preference by the predatory bugs on the dynamics of predatory mites and spider mites. However, experiments in which the predatory bug was added to populations of predatory mites and spider mites had little or no effect on numbers of both mite species, and cucumber plant and fruit weight.     

Herbivore population suppression by an intermediate predator, <Emphasis Type="Italic">Phytoseiulus macropilis</Emphasis>, is insensitive to the presence of an intraguild predator: an advantage of small body size?

Recent work in terrestrial communities has highlighted a new question: what makes a predator act as a consumer of herbivores versus acting as a consumer of other predators? Here we test three predictions from a model (Rosenheim and Corbett in Ecology 84:2538–2548) that links predator foraging behavior with predator ecology: (1) widely foraging predators have the potential to suppress populations of sedentary herbivores; (2) sit and wait predators are unlikely to suppress populations of sedentary herbivores; and (3) sit and wait predators may act as top predators, suppressing populations of widely foraging intermediate predators and thereby releasing sedentary herbivore populations from control. Manipulative field experiments conducted with the arthropod community found on papaya, Carica papaya, provided support for the first two predictions: (1) the widely foraging predatory mite Phytoseiulus macropilis strongly suppressed populations of a sedentary herbivore, the spider mite Tetranychus cinnabarinus, whereas (2) the tangle-web spider Nesticodes rufipes, a classic sit and wait predator, failed to suppress Tetranychus population growth rates. However, our experiments provided no support for the third hypothesis; the sit and wait predator Nesticodes did not disrupt the suppression of Tetranychus populations by Phytoseiulus. This contrasts with an earlier study that demonstrated that Nesticodes can disrupt control of Tetranychus generated by another widely foraging predator, Stethorus siphonulus. Behavioral observations suggested a simple explanation for the differing sensitivity of Phytoseiulus and Stethorus to Nesticodes predation. Phytoseiulus is a much smaller predator than Stethorus, has a lower rate of prey consumption, and thus has a much smaller requirement to forage across the leaf surface for prey, thereby reducing its probability of encountering Nesticodes webs. Small body size may be a general means by which widely foraging intermediate predators can ameliorate their risk of predation by sit and wait top predators. This effect may partially or fully offset the general expectation from size-structured trophic interactions that smaller predators are subject to more intense intraguild predation.     

Identifying inter‐ and intra‐guild feeding activity of an arthropod predator assemblage

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Diet‐dependent intraguild predation between the predatory mites Neoseiulus californicus and Neoseiulus cucumeris

Based on the hypothesis that matching diets of intraguild (IG) predator and prey indicate strong food competition and thus intensify intraguild predation (IGP) as compared to non‐matching diets, we scrutinized diet‐dependent mutual IGP between the predatory mites Neoseiulus cucumeris and N. californicus. Both are natural enemies of herbivorous mites and insects and used in biological control of spider mites and thrips in various agricultural crops. Both are generalist predators that may also feed on plant‐derived substances such as pollen. Irrespective of diet (pollen or spider mites), N. cucumeris females had higher predation and oviposition rates and shorter attack latencies on IG prey than N. californicus. Predation rates on larvae were unaffected by diet but larvae from pollen‐fed mothers were a more profitable prey than those from spider‐mite fed mothers resulting in higher oviposition rates of IG predator females. Pollen‐fed protonymphs were earlier attacked by IG predator females than spider‐mite fed protonymphs. Spider mite‐fed N. californicus females attacked protonymphs earlier than did pollen‐fed N. californicus females. Overall, our study suggests that predator and prey diet may exert subtle influences on mutual IGP between bio‐control agents. Matching diets did not intensify IGP between N. californicus and N. cucumeris but predator and prey diets proximately influenced IGP through changes in behaviour and/or stoichiometry.     

Combined versus Single Species Release of Predaceous Mites: Predator–Predator Interactions and Pest Suppression

Interactions such as competition, intraguild predation (IGP), and cannibalism affect the development and coexistence of predator populations and can have significance for biological control of commonly exploited pest organisms. We studied the consequences of combined versus single release of two predaceous mite species (Phytoseiidae), with differing degrees of diet specialization, on their population dynamics and the suppression of the carmine spider mite, Tetranychus cinnabarinus Boisduval (Tetranychidae), on greenhouse-grown gerbera. Population growth of the specialist predator Phytoseiulus persimilis Athias-Henriot was greater and population decline steeper when released in combination with the generalist Neoseiulus californicus McGregor than when released alone. In contrast, the N. californicus population grew and declined more gradually when released in combination with P. persimilis, compared to the single species release. The differential impact on each other's population dynamics can be primarily attributed to contrasting properties in competition, IGP, and cannibalism. At the same overall predator density and as long as prey was abundant, the specialist P. persimilis was more strongly affected by intraspecific competition than by interspecific competition with the generalist N. californicus. In contrast, interspecific competition with P. persimilis had a greater impact on N. californicus than intraspecific competition. After prey depletion, the generalist predator N. californicus was more likely to engage in IGP than was the specialist predator P. persimilis. Overall, the study demonstrates that prey specificity has significance for the quality and intensity of predator–predator interactions and indicates potential implications for biological control of spider mites. All predator releases (i.e., either species alone and both species in combination) resulted in reduction of the spider mite population to zero density. Individual release of the specialist P. persimilis led to the most rapid spider mite suppression. Nonetheless, in perennial greenhouse-grown crops P. persimilis and N. californicus could have complementary effects and a combination of the two predators could enhance long-term biological control of spider mites. The potential risks and benefits associated with the release of both species are discussed.     

Spatial distribution of predators and prey affect biological control of twospotted spider mites by Phytoseiulus persimilis in greenhouses

We evaluated the effects of predator release pattern and prey distribution on rate of suppression of the twospotted spider mite, Tetranychus urticae Koch (Acari, Tetranychidae) and visual damage to the ornamental plant, Impatiens wallerana Hook.f., in a greenhouse. Sixteen impatiens plants were arranged in a square and infested with the same total number of spider mites distributed either evenly (equal numbers on all plants) or clumped (divided equally among the 4 central plants), simulating a “hot spot.” The predatory mite, Phytoseiulus persimilis Athias-Henriot, was released at a 1:4 predator:prey ratio based on total spider mites in the experimental unit, but the pattern of release was either even or clumped, which simulated broadcast or point-release strategies, respectively. Nine days after predator release, spider mite populations were reduced in all treatments, but only in the clumped pest-clumped predator treatment were spider mites undetectable. Poorest pest suppression occurred in the clumped spider mite-even predator treatment. Eighteen days after predator release, spider mites were eliminated in all treatments, but a reduction in average plant damage occurred only in treatments in which the predator release pattern matched the spider mite distribution (i.e., even-even or clumped-clumped) with the greatest reduction in the even-even treatment. Results suggest that there is an advantage to releasing predators in “hot spots” provided that the recommended predator:prey ratio is maintained within infested patches. If more uniform predator releases are planned, overall predator numbers need to be kept sufficiently high so that the predator:prey ratio of 1:4 shown to prevent damage on impatiens is achieved in higher-density spider mite patches.     

Potential of the predatory mite Phytoseius finitimus (Acari: Phytoseiidae) to feed and reproduce on greenhouse pests

Phytoseiid mites of the genus Phytoseius are natural enemies of tetranychid and eriophyid herbivorous mites mostly found on hairy plants where they feed on prey, as well as on pollen. Nevertheless, the nutritional ecology and the role of these predators in biological pest control are only rarely addressed. In the present study, we evaluated the potential of Phytoseius finitimus to feed and reproduce on three major greenhouse pests, the two-spotted spider mite, the greenhouse whitefly and the western flower thrips. Additionally, we estimated the effect of cattail pollen when provided to the predator alone or in mixed diets with prey. Contrary to thrips larvae, both spider mite larvae and whitefly crawlers sustained the development of P. finitimus. In addition, females consumed more spider mite eggs and larvae, as well as whitefly crawlers than thrips larvae, but laid eggs when feeding on all prey. When provided alone, cattail pollen sustained the development and reproduction of the predator. The addition of pollen in mixed diets with prey reduced prey consumption, though it increased the predator’s egg production. We discuss the implications of our findings for biological pest control.     

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.     

Biocontrol of Two-spotted Spider Mite Tetranychus urticae on Dwarf Hops by the Phytoseiid Mites Phytoseiulus persimilis and Neoseiulus californicus

Two female Phytoseiulus persimilis and their offspring eliminated two-spotted spider mite Tetranychus urticae from hop leaf discs faster than two female Neoseiulus californicus and their offspring at 25°C. A combination of one female of each species and their offspring eliminated spider mites faster than the N. californicus alone, but slower than P. persimilis alone. Air relative humidities of 55% and 93% had no effect on predation. Both predator species cannibalised eggs and juveniles when spider mite numbers were low. In field experiments in 1996, fewer spider mites were recorded where P. persimilis was released, irrespective of the presence of N. californicus. Pest numbers on cv. 'First Gold' were lower than on cv. 'Herald'. No differences were recorded between the numbers of spider mite eggs in predator release treatments on 'First Gold', but fewer active stages of spider mites were recorded on plots with P. persimilis than controls soon after the time of peak pest population densities. On 'Herald', fewer spider mite active stages and eggs were recorded where predators were released than on untreated controls.     

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.     

Phenotypic plasticity in anti-intraguild predator strategies: mite larvae adjust their behaviours according to vulnerability and predation risk

Interspecific threat-sensitivity allows prey to maximize the net benefit of antipredator strategies by adjusting the type and intensity of their response to the level of predation risk. This is well documented for classical prey-predator interactions but less so for intraguild predation (IGP). We examined threat-sensitivity in antipredator behaviour of larvae in a predatory mite guild sharing spider mites as prey. The guild consisted of the highly vulnerable intraguild (IG) prey and weak IG predator Phytoseiulus persimilis, the moderately vulnerable IG prey and moderate IG predator Neoseiulus californicus and the little vulnerable IG prey and strong IG predator Amblyseius andersoni. We videotaped the behaviour of the IG prey larvae of the three species in presence of either a low- or a high-risk IG predator female or predator absence and analysed time, distance, path shape and interaction parameters of predators and prey. The least vulnerable IG prey A. andersoni was insensitive to differing IGP risks but the moderately vulnerable IG prey N. californicus and the highly vulnerable IG prey P. persimilis responded in a threat-sensitive manner. Predator presence triggered threat-sensitive behavioural changes in one out of ten measured traits in N. californicus larvae but in four traits in P. persimilis larvae. Low-risk IG predator presence induced a typical escape response in P. persimilis larvae, whereas they reduced their activity in the high-risk IG predator presence. We argue that interspecific threat-sensitivity may promote co-existence of IG predators and IG prey and should be common in predator guilds with long co-evolutionary history.     

Geotaxis and leaf-surface preferences mitigate negative effects of a predatory mite on an herbivorous mite

Reproductive success and population growth of an herbivorous mite are limited by activities of phytoseiid predators. However, occurrences on upper versus lower leaf surfaces are sometimes mismatched between these prey and predators. The mismatch potentially mitigates predation risk for the prey species. We assessed factors that affect mite distributions on leaf surfaces, testing whether the presence of the phytoseiid mite Phytoseius nipponicus alters the leaf-surface distribution and reproductive success of the herbivorous false spider mite Brevipalpus obovatus. The host plant was Viburnum erosum var. punctatum (Adoxaceae). Leaves were set in natural (TRUE) and reversed (upside down; INVERTED) orientations using experimental devices. Both surfaces were accessible to mites. We detected lower and abaxial leaf-surface preferences in P. nipponicus. In contrast, upper and adaxial surfaces were preferred by B. obovatus. Thus, prey and predatory mites accumulated on different sides of leaves. Presence of the predator also indirectly decreased egg production in B. obovatus. Brevipalpus obovatus females actively avoided leaf surfaces with elevated predator numbers; these females shifted their distributions and changed oviposition sites to leaf surfaces with fewer predators. In consequence, B. obovatus eggs on the upper sides of leaves were less frequently preyed upon than were those on lower sides. We suggest that upper leaf-surface exploitation in this particular herbivorous mite species mitigates predation risk from phytoseiid mites, which prefer lower leaf surfaces.     

Factors affecting biological control of apple mites by mixed populations ofMetaseiulus occidentalis andTyphlodromus pyri

Metaseiulus occidentalis (Nesbitt) andTyphlodromus pyri Scheuten have complementary features/ traits that enable them to control effectively plant-feeding mites on apple. Populations of both predators gave as good or better biological control of the apple rust mite (Aculus schlechtendali Nalepa), European red mite (Panonychus ulmi Koch) and two-spotted spider mite (Tetranychus urticae (Koch)) than single-predator populations. With mixed predators,M. occidentalis provided better control of spider mites the first season after release, butT. pyri gave better control in the second season. Several factors affected the ability of predators to provide biological control: When prey were dense,M. occidentalis rapidly increased during the warm mid-summer, whileT. pyri provided greater predation when it was cool at the start or end of the growing season. When few prey were present, searching byM. occidentalis was more confined on individual apple leaves, but it migrated between leaves and trees more often. Pollen feeding, cannibalism and interspecific predation were more common byT. pyri. In fall, oviposition byM. occidentalis stopped sooner and in the following spring,T. pyri reproduced beforeM. occidentalis. Research needs and management of mixed-predator populations are discussed.     

Evaluation of the predacious mite Hemicheyletia wellsina (Acari: Cheyletidae) as a predator of arthropod pests of orchids

The cheyletid predator Hemicheyletia wellsina was found in association with orchid pests in a Florida greenhouse. The life history of H. wellsina was determined using the two-spotted spider mite, Tetranychus urticae, as prey in the laboratory. Hemicheyletia wellsina is arrhenotokous, with mated females producing a female-biased sex ratio of 3.4:1. Adult longevity averaged 30.2 days, with females producing an average of 18.5 eggs. Adult females live up to 17 days without food, surviving an average of 9.7 days. Hemicheyletia wellsina will readily feed on the phytoseiid Metaseiulus occidentalis, suggesting intraguild predation by H. wellsina on phytoseiids could be important in pest management programs. The average prey consumption of H. wellsina is 1.5 T. urticae females per day. The results of this study provide information on an under-studied group of mite predators. Although H. wellsina does not have the qualities that would be necessary for its use in an augmentative or classical biological control program, its use in naturally occurring biological control could be beneficial.     

Effect of pollen supplement on intraguild predatory interactions between two omnivores: The importance of spatial dynamics

Arthropods often engage in complex trophic interactions such as intraguild predation (IGP), true omnivory (i.e., feeding on plants and prey), and apparent competition. Theoretical treatments of the effects of such interactions on herbivore populations have been concerned almost entirely with equilibrium conditions. Yet these interactions are common in non-equilibrium settings such as agroecosystems, where they are likely to have a strong influence on pest populations. We therefore tested short-term effects of IGP and food supplementation on interactions between two predators (the phytoseiid mite Neoseiulus cucumeris and the anthocorid bug Orius laevigatus) and their shared prey, Frankliniella occidentalis, on strawberry plants. All three consumers feed on strawberry pollen, both mites and bugs prey on thrips, and the bug also feeds on the mites (IGP). Strong IGP on mites (IG prey) by the bugs (IG predator) was recorded in structurally-simple arenas. In a more complex setting (whole-plants), however, the intensity of IGP differed among plant structures. Likewise, pollen supplementation reduced both IGP and predation on thrips in a structurally simple setting. In the whole-plant experiment, IGP was more intense on pollen-bearing than pollen-free flowers. The study illustrated how spatial dynamics, generated when consumers track food sources differently in the habitat and possibly when herbivorous and IG prey alter their distribution to escape predation, led to site-specific configuration of interacting populations. The intensity of resulting trophic interactions was weakened by food supplementation and by increased complexity of the habitat.     

Predator biodiversity increases the survivorship of juvenile predators

When predator biodiversity strengthens herbivore suppression, the pattern generally is attributed to interspecific complementarity. However, the relaxation of intraspecific interference within diverse communities has received less attention as an underlying factor, and most experiments to date span much less than one predator generation. Here, working with a community of aphid predators, we compared the survivorship of juvenile predators embedded within diverse versus single-species communities of adult predators. We found that greater predator diversity improved juvenile survivorship for three of four predator taxa (the lady beetles Hippodamia convergens and Coccinella septempunctata, and the bug Nabis alternatus; but not the small bug Geocoris bullatus), whereas survivorship was relatively low when juveniles foraged among only conspecific adults. When aphid densities differed they were lowest for the diverse treatment, and so resource availability could not explain differences in juvenile survivorship. Instead, feeding trials indicated that cannibalism generally posed a greater risk to juveniles than did intraguild predation (with Geocoris again the exception). Our results suggest that the dilution of intraspecific interference may play an important, and perhaps underappreciated, role in shaping predator diversity effects. Furthermore, relatively strong cannibalism but weak intraguild predation has the potential to project diversity effects forward into subsequent generations.     

Spider mite web mediates anti-predator behaviour

Herbivores suffer significant mortality from predation and are therefore subject to natural selection on traits promoting predator avoidance and resistance. They can employ an array of strategies to reduce predation, for example through changes in behaviour, morphology and life history. So far, the anti-predator response studied most intensively in spider mites has been the avoidance of patches with high predation risk. Less attention has been given to the dense web produced by spider mites, which is a complex structure of silken threads that is thought to hinder predators. Here, we investigate the effects of the web produced by the red spider mite, Tetranychus evansi Baker & Pritchard, on its interactions with the predatory mite, Phytoseiulus longipes Evans. We tested whether female spider mites recognize predator cues and whether these can induce the spider mites to produce denser web. We found that the prey did not produce denser web in response to such cues, but laid more eggs suspended in the web, away from the leaf surface. These suspended eggs suffered less from predation by P. longipes than eggs that were laid on the leaf surface under the web. Thus, by altering their oviposition behaviour in response to predator cues, females of T. evansi protect their offspring.