Do Herbivore-Induced Plant Volatiles Influence Predator Migration and Local Dynamics of Herbivorous and Predatory Mites?

If predators lack information on the prey's position, prey have more chance to escape predation and will therefore reach higher population densities. One of the many possible cues that predators may use to find their prey are herbivore-induced plant volatiles. Although their effects on the behaviour of foraging predators have been well studied, little is known about how these prey-related odours affect predator–prey dynamics on a plant. We hypothesise that herbivore-induced plant volatiles provide the major cue eliciting predator arrestment on prey-infested leaves and that the response to these volatiles ultimately leads to lower prey densities. To test this hypothesis experimentally, we created two types of odour-saturated environments: one with herbivore-induced plant volatiles (treatment), and one with green-leaf volatiles (control). An odour-free environment could not be tested because herbivores require plants for population growth. We measured the rate at which predatory mites (Phytoseiulus persimilis) immigrate, emigrate and exploit a single leaf infested by two-spotted spider mites (Tetranychus urticae). The experiments did not show a significant difference between treatment and control. At best, there was a somewhat higher rate of predator (and possibly also prey) emigration in the treatment. The lack of a pronounced difference between treatment and control indicates that at the spatial scale of the experiments random searching for prey was as effective as directional searching. Alternatively, predators were arrested in the prey patch by responding not merely to herbivore-induced plant volatiles, but also to other prey-related cues, such as web and faeces. Based on our current experience we advocate to increase the spatial scale of the experiment (>1m²) and we provide other suggestions for improving the set-up.     

Resource-Dependent Giving-Up Time of the Predatory Mite, Phytoseiulus persimilis

We examined the effect of prey (Tetranychus urticae) egg density on leaving rate of the predatory mite, Phytoseiulus persimilis, from leaf disks using predators with different feeding experiences and levels of external volatile cues related to their prey. Predators stayed longer on disks with prey eggs than on those without prey eggs. However, at each prey egg density predators stayed longer in the absence of prey-related volatiles from an external source. Starved predators stayed longer in a prey patch than those that had not experienced starvation. At each prey density, starved P. persimilis consumed a greater proportion of prey eggs than satiated predators. The total prey consumption of starved predators appears to be related to their longer residence time on source disks compared to satiated predators and also the per capita consumption rate was greater for starved predators compared to satiated predators.     

Response of predatory mites with different rearing histories to volatiles of uninfested plants

The behavioural response of the predatory mite Phytoseiulus persimilis to volatiles from several host plants of its prey, spider mites in the genus Tetranychus, was investigated in a Y-tube olfactometer. A positive response to volatiles from tomato leaves and Lima bean leaves was recorded, whereas no response was observed to volatiles from cucumber leaves, or leaves of Solanum luteum and Solanum dulcamara.Different results were obtained for predators that differed in rearing history. Predators that were reared on spider mites (Tetranychus urticae) on Lima bean leaves did respond to volatiles from Lima bean leaves, while predators that had been reared on the same spider mite species but with cucumber as host plant did not respond to Lima bean leaf volatiles. This effect is compared with the effect of rearing history on the response of P. persimilis to volatile allelochemicals of prey-infested plant leaves.     

Patch-Leaving Decision of the Predatory Mite Amblyseius womersleyi (Acari: Phytoseiidae) Based on Multiple Signals from Both Inside and Outside a Prey Patch

We compared the emigration rates of Amblyseius womersleyi from prey patches (leaf disks) of different conditions in airflow containing either infested plant volatiles (volatiles airflow) or uninfested plant volatiles (control airflow). Both airflow and prey patch conditions significantly affected the emigration rates. Emigration rates from patches carrying prey products (feces, exuviae, webs, etc.) and prey eggs were significantly lower in control airflow than in volatiles airflow. Under other patch conditions, the rates were lower in control airflow than in volatiles airflow, although the difference was not significant. In both airflows, the lowest emigration rates were observed when predators were in a heavily infested patch. Patches carrying prey products and prey eggs resulted in lower emigration rates than patches carrying eggs alone and patches emitting prey-infested plant volatiles but carrying no prey. Thus, A. womersleyi appears to decide the timing of emigration based on two criteria: prey products in the patch and prey-infested plant volatiles from outside.     

How Predatory Mites Learn to Cope with Variability in Volatile Plant Signals in the Environment of their Herbivorous Prey

When the chemical cues co-occurring with prey vary in time and space, foraging predators profit from an ability to repeatedly associate chemical cues with the presence of their prey. We demonstrate the ability of a predatory arthropod (the plant-inhabiting mite, Phytoseiulus persimilis) to learn the association of a positive stimulus (herbivorous prey, Tetranychus urticae) or a negative stimulus (hunger) with a chemical cue (herbivore-induced plant volatiles or green leaf volatiles). It has been suggested that the rate at which the integration of information becomes manifest as a change in behaviour, differs between categories of natural enemies (parasitoids versus insect predators; specialist versus generalist predators). We argue that these differences do not necessarily reflect differential learning ability, but rather relate to the ecologically relevant time scale at which the biotic environment changes.     

Anemotactic responses of the predatory mite,Phytoseiulus persimilis Athias-Henriot,and their role in prey finding

Although it is well established that the predatory mite Phytoseiulus persimilis Athias-Henriot responds to odour emanating from leaves infested by its phytophagous prey, the two-spotted spider mite Tetranychus urticae Koch, little is known of the behavioural mechanisms elicited by odour perception and how they contribute to finding the prey. In this paper the influence of prey-related odour on orientation to wind direction is discussed. It was analysed by observing the predator's walking paths in still air and in an air stream uniformly permeated either with or without prey-related odour stimuli. The results show that well-fed predator females move upwind in presence of these stimuli, but downwind otherwise. Starved predators always move upwind. The anemotactic responses observed are therefore both odour-conditioned and (feeding) state-dependent.In an attempt to explain these responses it is argued that the anemotactic responses of well-fed predators may contribute to arrestment within the area marked by a cluster of prey-colonized leaves. The anemotactic responses of starved predators may help them to find clusters of spider mite colonies located upwind. Why predatory mites also move upwind in absence of prey-related odour stimuli, is a question that remains to be answered.     

Phytoseiulus persimilis response to herbivore-induced plant volatiles as a function of mite-days

The predatory mite, Phytoseiulus persimilis (Acari: Phytoseiidae), uses plant volatiles (i.e., airborne chemicals) triggered by feeding of their herbivorous prey, Tetranychus urticae (Acari: Tetranychidae), to help locate prey patches. The olfactory response of P. persimilis to prey-infested plants varies in direct relation to the population growth pattern of T. urticae on the plant; P. persimilis responds to plants until the spider mite population feeding on a plant collapses, after which infested plants do not attract predators. It has been suggested that this represents an early enemy-free period for T. urticae before the next generation of females is produced. We hypothesize that the mechanism behind the diminished response of predators is due to extensive leaf damage caused by T. urticae feeding, which reduces the production of volatiles irrespective of the collapse of T. urticae population on the plant. To test this hypothesis we investigated how the response of P. persimilis to prey-infested plants is affected by: 1) initial density of T. urticae, 2) duration of infestation, and 3) corresponding leaf damage due to T. urticae feeding. Specifically, we assessed the response of P. persimilis to plants infested with two T. urticae densities (20 or 40 per plant) after 2, 4, 6, 8, 10, 12 or 14 days. We also measured leaf damage on these plants. We found that predator response to T. urticae-infested plants can be quantified as a function of mite-days, which is a cumulative measure of the standing adult female mite population sampled and summed over time. That is, response to volatiles increased with increasing numbers of T. urticae per plant or with the length of time plant was infested by T. urticae, at least as long at the leaves were green. Predatory mites were significantly attracted to plants that were infested for 2 days with only 20 spider mites. This suggests that the enemy-free period might only provide a limited window of opportunity for T. urticae because relatively low numbers of T. urticae per plant can attract predators. Leaf damage also increased as a function of mite-days until the entire leaf was blanched. T. urticae populations decreased at this time, but predator response to volatiles dropped before the entire leaf was blanched and before the T. urticae population decreased. This result supports our hypothesis that predator response to plant volatiles is linked to and limited by the degree of leaf damage, and that the quantitative response to T. urticae populations occurs only within a range when plant quality has not been severely compromised.     

Arbuscular mycorrhiza enhances preference of ovipositing predatory mites for direct prey‐related cues

Most terrestrial plants are associated with arbuscular mycorrhizal fungi but research on the effects of arbuscular mycorrhizal symbiosis on aboveground plant‐associated organisms is scarcely expanded to tri‐trophic systems. The arbuscular mycorrhizal fungus Glomus mosseae Nicol. & Gerd. enhances fitness of the two‐spotted spider mite Tetranychus urticae Koch and its natural enemy, the predatory mite Phytoseiulus persimilis Athias‐Henriot, via changes in host plant and prey quality, respectively. In the present study, it is hypothesized that gravid P. persimilis are able to recognize arbuscular mycorrhiza‐enhanced prey quality and behave accordingly. In two experiments, on leaf arenas and in cages, P. persimilis is given a choice between prey patches deriving from mycorrhizal and non‐mycorrhizal bean plants (Phaseolus vulgaris L.) as feeding and oviposition sites. The use of cages allows the manipulation of distinct patch components acting as possible cues to guide predator foraging and oviposition behaviours, such as eggs produced and traces (webbing and faeces) left by the spider mite females. Both experiments show that P. persimilis preferentially resides close to prey fed on mycorrhizal plants. The cage experiment reveals that P. persimilis uses direct prey‐related cues, mainly derived from eggs, to discern prey quality and preferentially oviposits close to prey from mycorrhizal plants. This is the first study to document that predators recognize arbuscular mycorrhiza‐induced changes in herbivorous prey quality via direct prey‐related cues.     

Plant—Phytoseiid Interactions Mediated by Herbivore-Induced Plant Volatiles: Variation in Production of Cues and in Responses of Predatory Mites

Phytoseiid mites use herbivore-induced plant volatiles in long-range prey-habitat location and are arrested by these volatiles in a prey patch. The responses of predatory mites to these volatiles are considered to be an important factor in the local extermination of prey populations by phytoseiids such as Phytoseiulus persimilis. Prey-induced plant volatiles are highly detectable and can be reliable indicators of prey presence and prey identity. The composition of herbivore-induced plant volatiles depends on plant species and plant cultivar. Moreover, the composition may also vary with the herbivore species that infests a plant. The responses of phytoseiids to prey-induced plant volatiles from a specific plant-herbivore combination are highly variable. Causal factors include starvation, specific hunger, experience, pathogen infestation and the presence of competitors. Investigating variation in the phytoseiid's behavioural response in relation to these factors is important for understanding how and why behavioural strategies maximize phytoseiid fitness.     

Predator avoidance in phytophagous mites: response to present danger depends on alternative host quality

We studied whether volatiles released by putative host plants affect the antipredator response of an herbivorous mite, Tetranychus urticae, when the patch was invaded by Phytoseiulus persimilis. Tetranychus urticae laid a lower number of eggs on tomato leaves than on lima bean leaves, suggesting that lima bean is a preferred host food source for T. urticae. In addition, T. urticae preferred lima bean plant volatiles to tomato plant volatiles in a Y-tube olfactometer test. To investigate the antipredator response of T. urticae, we examined the migration of T. urticae from a lima bean leaf disc to a neighbouring leaf disc (either a tomato or lima bean leaf disc) when ten predators were introduced into the original lima bean disc. A Parafilm bridge allowed for migration between the leaf discs. No migrations occurred between leaf discs when there were no predators introduced to the original leaf disc. However, when predators were introduced migrations did occur. When the neighbouring leaf disc was upwind of the original disc, the migration rate of the mite from original lima bean leaf disc to a neighbouring tomato leaf disc was significantly lower than that to a neighbouring lima bean leaf disc. By contrast, when the neighbouring leaf disc was downwind of the original leaf disc, there was no difference in the migration rates between lima bean leaf discs and tomato leaf discs. The number of T. urticae killed by P. persimilis for each treatment was not different, and this clearly shows that the danger was the same in all treatments regardless of the decision made by T. urticae. From these results, we conclude that T. urticae change their antipredator response by evaluating the difference in host plant volatiles in the patch they inhabit.     

Migration of specialist insect predators to exploit patchily distributed spider mites

It is believed that specialist predators of spider mites often migrate by flight or aerial transport to exploit patchily distributed prey. The migration is an important factor in determining the seasonal occurrence of the predators in a field. Several species of specialist insect predators, such as Oligota kashmirica benefica (Coleoptera: Staphylinidae) and Scolothrips takahashii (Thysanoptera: Thripidae), migrate between orchard trees and plants near the trees (e.g., groundcover, weeds, or windbreaks) to exploit abundant spider mites. This migration is at least partly triggered by prey scarcity in the original local habitats. Although these predators are tiny insects, they have flight abilities. For example, adult O. kashmirica benefica (body length, ∼1 mm) could move at least 5–16 m in one flight. Presumably, migration of the insect predators between prey-infested plants occurs mainly by flights. Predatory mites, such as Amblyseius fallacis and Amblyseius womersleyi (Acari: Phytoseiidae), migrated to spider mite-infested plants outside an orchard by aerial transport when they suffered from prey scarcity in the orchard. S. takahashii can use plant volatiles from lima bean plants induced by the spider mite Tetranychus urticae as cues for prey location during migration in Satsuma mandarin groves. However, it remains unknown how far from the trap boxes S. takahashii could respond to herbivore-induced plant volatiles in the groves. Received: August 25, 2000 / Accepted: February 1, 2001     

How predatory mites find plants with whitefly prey

We investigated the searching behaviour of two species of predatory mites, Typhlodromips swirskii (Athias-Henriot) and Euseius scutalis (Athias-Henriot), both known to feed on immature stages of the whitefly Bemisia tabaci Gennadius. When released in a greenhouse inside a circle of cucumber plants that were alternatingly clean or infested with immature whiteflies, the mites took several days to find plants. Both species were recaptured significantly more on plants with whiteflies. This suggests that the mites are able to discriminate between plants with and without whiteflies. The predators may either have been attracted to plants with whiteflies from a distance or arrested on plants with whiteflies. Typhlodromips swirskii that had previously fed on whitefly immatures on cucumber leaves were significantly attracted by volatiles from cucumber plants with whiteflies in a Y-tube olfactometer. This suggests that the mites use volatile cues to discriminate between infested and clean plants. However, this response waned rapidly; if predators, experienced as above, were starved for 3–4 h in absence of cucumber leaves, they no longer preferred volatiles of infested plants to clean plants. Furthermore, T. swirskii that had no experience with immature whiteflies on cucumber plants also did not prefer odours of infested plants to those of clean plants. Because the release experiment with this species in the greenhouse was done with inexperienced predators, this suggests that the aggregation of mites on plants with whiteflies was mainly caused by differential arrestment of mites on plants with prey and clean plants. For T. swirskii, this was in agreement with the finding that the fraction of predators on plants with prey increased with time to levels higher than 70%. A less clear trend was found for E. scutalis, for which the fraction of predators on plants with prey stabilized soon after release to levels from 54–70%. Hence, the predatory mites may find plants with prey by random searching, but they are subsequently arrested on these plants. An earlier study showed that 87% of all whiteflies released in a set-up as used here were recaptured within 1 day. Hence, the effectiveness with which predatory mites locate plants with whiteflies is low compared with that of their prey. We expect this to generate spatial patterns in the dynamics of predator and prey and this may have consequences for biological control of whiteflies with predatory mites.     

Of mites and movement: the effects of plant connectedness and temperature on movement of Phytoseiulus persimilis

Simulation modelling studies on the biological control of Tetranychus urticae Koch in ornamental crops suggest that the dispersal of the predatory mite Phytoseiulus persimilis Athias-Henriot in the absence of food is important in determining its ability to locate sparsely distributed patches of prey (Skirvin et al., 2002). Experimental work to examine factors influencing dispersal of P. persimilis has shown that ground substrate affects the movement of the predator, and that the greater the number of connections between adjacent plants the greater the number of mites moving. In addition, P. persimilis are able to move across as many as 10 plant–plant connections within 24 h, although the majority of predators tracked moved less than this. Temperature has a significant impact on dispersal of P. persimilis, with more mites leaving release points as temperature increases up to 25 °C, but decreasing above this temperature. This work highlights the importance of understanding how the plant canopy and temperature influence the dispersal of predatory mites. The importance of these results for biological control in ornamental crops is discussed.     

Orientation behaviour of the predatory hemipteran Perillus bioculatus to plant and prey odours

The pentatomid predator P. bioculatus responded by positive odour-conditioned anemotaxis when exposed to airborne volatiles emitted by potato plants damaged by Colorado potato beetle larvae, whereas intact potato plants and non-feeding larvae as odour sources failed to elicit anemotaxis. Walking tracks of adult predators had higher values of straightness and upwind fixation when odours emanating from mechanically damaged plants were encountered than tracks registered in response to air carrying volatiles from intact plants, but these parameters returned to control values within 1–2 h after damage was caused. In contrast, air led over plants damaged by beetle larvae elicited orientation responses at least 3 hours after feeding damage ceased. The combination of chemical data on headspace composition, olfactory sensitivity established in electro-antennogram studies and behavioural data presented here imply a role of sesquiterpenoid plant volatiles as odorous cues eliciting attraction of this predator to damaged potato plants.     

捕食螨化学生态研究进展

捕食螨是重要的生物防治因子。早在20世纪70年代就发现了捕食螨的性信息素,许多研究证明植物挥发物在捕食螨向猎物定位过程中发挥着至关重要的作用,影响捕食螨寻找猎物的植物挥发物来源于未受害植物、机械损伤植物、猎物危害植物、非猎物危害植物。人工合成的植物挥发物组分对捕食螨具有引诱作用,但引诱活性低于虫害诱导植物释放的挥发性混合物。捕食螨的饲养条件、饥饿程度、学习与经验行为等会影响捕食螨对植物挥发物的反应。介绍了信息素与植物挥发物对捕食螨的作用,并讨论了目前存在的问题和研究前景。     

Induced production of extrafloral nectar in intact lima bean plants in response to volatiles from spider mite-infested conspecific plants as a possible indirect defense against spider mites

We found that intact lima bean plants increased the secretion of extrafloral nectar (EFN) after exposure to Tetranychus urticae-induced plant volatiles. Predatory mites, Phytoseiulus persimilis, dispersed more slowly from an exposed intact plant than from a control plant (plant exposed to volatiles from intact conspecific). The predators also dispersed more slowly from those plants that were provided with extra EFN than from untreated plants. We further show that EFN was a potential alternative food source for P. persimilis. From these results, we concluded that increased EFN was involved in the slow dispersal of P. persimilis from the plants exposed to herbivore-induced plant volatiles. Our data suggest that the increase of EFN in an HIPV-exposed intact plant could be an induced indirect defense against spider mites.     

Genetic variation in foraging traits among inbred lines of a predatory mite

Response of predators to herbivore-induced plant volatiles can affect the length of time a predator spends in a prey patch and the probability of a predator finding a new prey patch. Variation in response to herbivore-induced plant volatiles may lead to different foraging decisions among individuals, thereby affecting both within-patch dynamics and between-patch dispersal. We found significant phenotypic and additive genetic variation in two behavioral assays of response to herbivore-induced plant volatiles among inbred isofemale lines of the predatory mite, Phytoseiulus persimilis. In wind-tunnel tests to measure patch residence time, adult female predators from certain lines left prey patches sooner than others when a distant source of herbivore-induced plant volatiles was presented; whereas such variation disappeared when no distant volatiles were presented. In a measure of patch location, certain lines were more likely than others to locate a prey-infested leaf disc; again there was no difference when uninfested leaf discs were used. Patch location was negatively correlated with patch residence. That is, lines that were more likely to leave a prey patch in the presence of distant volatiles were also more likely to find an odor source (ie, prey patch) from a distance of 20 cm. These two foraging-related behaviors are heritable. A continuous distribution of both behaviors indicated that several to many loci may be responsible for these behavioral traits. Our line-crossing experiments suggested that maternal influence could be excluded. Substantial phenotypic variation in two other foraging-related traits, consumption and oviposition, were also detected among inbred lines. Consumption and oviposition were positively correlated; however, the relationship (slope) varied among inbred lines, suggesting that predatory mites vary in food conversion efficiency. A relationship was detected between patch residence and consumption. Patch location, as one important foraging trait, appeared to be negatively related to consumption, suggesting a trade-off between searching for patches and reproduction.     

Interactions in a tritrophic acarine predator-prey metapopulation system V: Within-plant dynamics of Phytoseiulus persimilis and Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae)

To investigate the relative contributions of bottom-up (plant condition) and top-down (predatory mites) factors on the dynamics of the two-spotted spider mite (Tetranychus urticae), a series of experiments were conducted in which spider mites and predatory mites were released on bean plants. Plants inoculated with 2, 4, 8, 16, and 32 adult female T. urticae were either left untreated or were inoculated with 3 or 5 adult female predators (Phytoseiulus persimilis) one week after the introduction of spider mites. Plant area, densities of T. urticae and P. persimilis, and plant injury were assessed by weekly sampling. Data were analysed by a combination of statistical methods and a tri-trophic mechanistic simulation model partly parameterised from the current experiments and partly from previous data. The results showed a clear effect of predators on the density of spider mites and on the plant injury they cause. Plant injury increased with the initial number of spider mites and decreased with the initial number of predators. Extinction of T. urticae, followed by extinction of P. persimilis, was the most likely outcome for most initial combinations of prey and predators. Eggs constituted a relatively smaller part of the prey population as plant injury increased and of the predator population as prey density decreased. We did not find statistical evidence of P. persimilis having preference for feeding on T. urticae eggs. The simulation model demonstrated that bottom-up and top-down factors interact synergistically to reduce the density of spider mites. This may have important implications for biological control of spider mites by means of predatory mites.     

Odour-mediated responses of a predatory mirid bug and its prey, the two-spotted spider mite

It has been shown that many natural enemies of herbivorous arthropods use herbivore induced plant volatiles (HIPVs) to locate their prey. Herbivores can also exploit cues emitted by plants infested with heterospecifics or conspecifics. A study was conducted to test whether green bean HIPVs as well as odours emitted directly by spider mites influenced the orientation behaviour of the predatory mirid bug, Macrolophus caliginosus and its prey, Tetranychus urticae in a Y-tube olfactometer. Our results show that both spider mites and M. caliginosus preferred spider mite infested green bean plants to uninfested plants. For M. caliginosus this response was mediated by HIPVs whereas for T. urticae it was mediated through a composite response to both HIPVs and odours emitted directly by the conspecifics (and their associated products). The results may be of use in practical biocontrol situations, through e.g., plant breeding for improved HIPV production, conditioning of mass-reared predators to appropriate cues, and employment of “push–pull-strategies” by using HIPVs.     

Attraction of a predator to chemical information related to nonprey: when can it be adaptive?

Information specificity can be important to animals in makingoptimal decisions. However, it is not always necessary to useevery level of specificity. We analyzed the response of thepredatory mite Phytoseiulus persimilis to plant-produced informationrelated to a nonprey herbivore. This predator is a specialistfeeding on spider mites in the genus Tetranychus. Caterpillarsof Spodoptera exigua cannot serve as prey. Plants respond toan infestation by herbivores with the emission of volatilesthat attract carnivorous enemies of the herbivores. Conspecific plants infested with different herbivore species can emit blendsthat are qualitatively identical, while differing in the ratiosof blend components. However, different plant species emitvolatile blends that differ qualitatively. We demonstratedthat the predator P. persimilis is attracted to volatiles frombean plants infested with S. exigua caterpillars, but thatthis attraction is affected by predator starvation and host-plantexperience. One-hour and 24-h starved predators were made to represent predators that just lost a prey patch versus predatorsthat have totally lost a prey patch. Predators reared on spidermites on bean were attracted to bean plants infested with caterpillarswhen starved for 1 h but not when starved for 24 h. Both predatorgroups were attracted to bean plants infested with prey (i.e.,spider mites). One-hour starved predators can use the odorto relocate the rewarding prey patch they just lost contactwith, and using a general olfactory representation of the blendis sufficient for relocation. In contrast, for 24-h starvedpredators, the perception of a plant's odor blend is unlikelyto represent the prey patch lost, and discriminating betweenan odor blend representing prey or nonprey will avoid investingtime in finding a nonprey herbivore. In contrast, predatorsthat had been reared on spider mites on cucumber and thus hadexperienced a qualitatively different odor blend were not attractedto volatiles from caterpillar-infested bean plants. They wereattracted to spider mite-infested bean plants, irrespectiveof starvation level. To cucumber-experienced predators, theperception of bean plant odor cannot represent the prey patch lost, but only a new prey patch. Being discriminative and onlyresponding to prey-infested plants is adaptive in this situation.Our results are discussed in the context of optimal informationprocessing.