Flexible antipredator behaviour in herbivorous mites through vertical migration in a plant (original) (raw)
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When predation risk varies in space and time and with predator species, successful prey defence requires specific responses to each predator. In cassava fields in Africa, the herbivorous cassava green mite (Mononychellus tanajoa) is attacked by three predatory mite species that are segregated within the plant: the leaf-dwelling Typhlodromalus manihoti and Euseius fustis occur on the middle leaves, whereas the apex-inhabiting T. aripo migrates from the apex to the top leaves only during the night. We found that differential distributions of these predators allow prey to escape predation by vertical migration to other plant strata. We studied the role of odours in the underlying prey behaviour on predator-free plants placed downwind from plants with predators and prey or with prey only. Prey showed increased vertical migration in response to predator-related odours. Moreover, these responses were specific: when exposed to odours associated with T. manihoti, prey migrated upwards, irrespective of the plant stratum where they were placed. Odours associated with T. aripo triggered a flexible response: prey on the top leaves migrated downwards, whereas prey on the middle leaves migrated upwards. Odours associated with E. fustis, a low-risk predator, did not elicit vertical migration. Further experiments revealed that: (1) prey migrate up or down depending on the stratum where they are located, and (2) prey discrimination among predators is based upon the perception of predator species-specific body odours. Thus, at the scale of a single plant, odour-based enemy specification allows herbivorous mites to escape predation by vertical migration.
Journal of Chemical Ecology, 2010
Plants infested with herbivores release specific volatile compounds that are known to recruit natural enemies. The response of natural enemies to these volatiles may be either learned or genetically determined. We asked whether there is genetic variation in the response of the predatory mite Phytoseiulus persimilis to methyl salicylate (MeSa). MeSa is a volatile compound consistently produced by plants being attacked by the two-spotted spider mite, the prey of P. persimilis. We predicted that predators express genetically determined responses during longdistance migration where previously learned associations may have less value. Additionally, we asked whether these responses depend on odors from uninfested plants as a background to MeSa. To infer a genetic basis, we analyzed the variation in response to MeSa among iso-female lines of P. persimilis by using choice-tests that involved either (1) MeSa presented as a single compound or (2) MeSa with background-odor from uninfested lima bean plants. These tests were conducted for starved and satiated predators, i.e., two physiological states, one that approximates migration and another that mimics local patch exploration. We found variation among iso-female lines in the responses to MeSa, thus showing genetic variation for this behavior. The variation was more pronounced in the starved predators, thus indicating that P. persimilis relies on innate preferences when migrating. Background volatiles of uninfested plants changed the predators' responses to MeSa in a manner that depended on physiological state and iso-female line. Thus, it is possible to select for context-dependent behavioral responses of natural enemies to plant volatiles.
Predatory mites learn to discriminate between plant volatiles induced by prey and nonprey herbivores
Animal Behaviour, 2005
Many carnivorous arthropods can use chemical information from plants to locate their herbivorous prey. The composition of blends of herbivore-induced plant volatiles can vary with plant and herbivore species and thus carnivores are confronted with variable information about the presence of their prey. Such environmental variation is expected to favour learning. We investigated the learning ability of the predatory mite Phytoseiulus persimilis, a specialized natural enemy of polyphagous spider mites. We reared mites on different plant species, and subsequently tested their preference for volatiles from lima bean plants infested with either the prey herbivore Tetranychus urticae or the nonprey caterpillar Spodoptera exigua in a Y-tube olfactometer. Predators reared on lima bean preferred the volatiles induced by T. urticae, whereas predators reared on cucumber did not. We also investigated the foraging behaviour of mites after a nonrewarding experience during the adult phase (i.e. food deprivation in the presence of S. exiguainduced volatiles from lima bean) or after a rewarding experience (i.e. feeding in the presence of T. urticaeinduced volatiles). The rewarding experience had a much larger impact on the foraging responses. Predatory mites with multiple experiences (i.e. a nonrewarding experience followed by a rewarding experience) had the strongest preference for T. urticae-induced versus S. exigua-induced volatiles. We conclude that these learning abilities enable the predatory mites to forage in an environment where their prey can feed on a different plant species than the one on which the predator developed, and where nonprey caterpillars are also present.
Journal of Insect Behavior, 2009
Under attack by herbivores, plants produce a blend of "herbivore-induced plant volatiles (HIPV)" that help natural enemies of herbivores locating their prey, thereby helping plants to reduce damage from herbivory. The amount of HIPV emitted by plants increases with herbivore density and is positively correlated with the intensity of the olfactory response of natural enemies. In this study, we determined the effects of density or within-plant distribution of the herbivorous mite Mononychellus tanajoa on movement of the predatory mite Typhlodromalus aripo out of apices of cassava plants. Proportions of T. aripo that migrated out of apex, and distances traveled were significantly higher when M. tanajoa was further away from the apex-i.e. on middle or bottom leaves of cassava plants-than when present on top leaves, or absent from the plant. This supports previous field observations that T. aripo is not a sit-and-wait predator but uses HIPV to search and locate its prey within cassava plant.
Odour-mediated responses of phytophagous mites to conspecific and heterospecific competitors
Oecologia, 1997
Plants under herbivore attack produce volatiles, thus attracting natural enemies of the herbivores. However, in doing so, the plant becomes more conspicuous to other herbivores. Herbivores may use the odours as a cue to refrain from visiting plants that are already infested, thereby avoiding competition for food, or, alternatively, to visit plants with defences weakened by earlier attacks. We investigated the response of one species of herbivore (the spider mite Tetranychus urticae) to odours emanating from cucumber plants infested by conspecific or heterospecific (the western flower thrips, Frankliniella occidentalis) herbivores. Olfactometer experiments in the laboratory showed that spider mites have a slight, but significant, preference for plants infested with conspecifics, but strongly avoid plants with thrips. These results were substantiated with greenhouse experiments. We released spider mites on the soil in the centre of a circle of six plants, half of which were infested with either conspecifics or heterospecifics (thrips), whereas the other half were uninfested. It was found that 60-70% of the mites were recaptured on the plants within 5 h after release. Results of these experiments were in agreement with results of the olfactometer experiments: (1) significantly fewer spider mites were found on plants infested with thrips than on uninfested plants and (2) more mites were found on plants with conspecifics than on clean plants (although this difference was not significant). From a functional point of view it makes sense that spider mites prefer clean plants over thrips-infested plants, since thrips are not only competitors, but are also known as intraguild predators of spider mites. Possible reasons for the slight attraction of spider mites to plants infested with conspecifics are discussed.
Experimental & applied acarology, 2000
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.
Entomologia Experimentalis et Applicata, 1999
Arthropods use odours associated with the presence of their food, enemies and competitors when searching for patches. Responses to these odours therefore determine the spatial distribution of animals, and are decisive for the occurrence and strength of interactions among species. Therefore, a logical first step in studying food web interactions is the analysis of behaviour of individuals that are searching for patches of food. We followed this approach when studying interactions in an artificial food web occurring on greenhouse cucumber in the Netherlands. In an earlier paper we found that one of the predators of the food web, the predatory mite Phytoseiulus persimilis Athias-Henriot, used to control spider mites, discriminates between odours from plants with spider mites, Tetranychus urticae Koch, and plants with spider mites plus conspecific predators. The odours used for discrimination are produced by adult prey in response to the presence of predators, and probably serve as an alarm pheromone to warn related spider mites. Other predator species may also trigger production of this alarm pheromone, which P. persimilis could use in turn to avoid plants with heterospecific predators. We therefore studied the response of the latter to odours from plants with spider mites and 3 other predator species, i.e. the generalist predatory bug Orius laevigatus (Fieber), the polyphagous thrips Frankliniella occidentalis and the spider-mite predator Neoseiulus californicus (McGregor). Both olfactometer and greenhouse release experiments yielded no evidence that P. persimilis avoids plants with any of the 3 heterospecific predators. This suggests that these predators do not elicit production of alarm pheromones in spider mites, and we argue that this is caused by a lack of coevolutionary history. The consequences of the lack of avoidance of heterospecific predators for interactions in food webs and biological control are discussed.
Innate responses of the predatory mite Phytoseiulus persimilis to a herbivore-induced plant volatile
Experimental and Applied Acarology, 2011
The responses of the predatory mite P. persimilis to herbivore-induced plant volatiles are at least partly genetically determined. Thus, there is potential for the evolution of this behaviour by natural selection. We tested whether distinct predator genotypes with contrasting responses to a specific herbivore-induced plant volatile, i.e. methyl salicylate (MeSa), could be found in a base population collected in the field (Sicily). To this end, we imposed purifying selection on individuals within iso-female lines of P. persimilis such that the lines were propagated only via the individual that showed either a preference or avoidance of MeSa. The responses of the lines were characterized as the mean proportion of individuals choosing MeSa when given a choice between MeSa and clean air. Significant variation in predator responses was detected among iso-female lines, thus confirming the presence of a genetic component for this behaviour. Nevertheless, we did not find a significant difference in the response to MeSa between the lines that were selected to avoid MeSa and the lines selected to prefer MeSa. Instead, in the course of selection the lines selected to avoid MeSa shifted their mean response towards a preference for MeSa. An inverse, albeit weaker, shift was detected for the lines selected to prefer MeSa. We discuss the factors that may have caused the apparent lack of a response to selection within isofemale line in this study and propose experimental approaches that address them.
Entomologia Experimentalis et Applicata, 2006
To clarify the prey-finding behavior of the predatory mite Neoseiulus womersleyi (Schicha) (Acari: Phytoseiidae), we studied its olfactory responses to volatiles from the prey-infested plant on which the mites had been collected. We used a local N. womersleyi population called Kanaya collected from tea (Camellia sinensis L.) (Theaceae) plants infested by Tetranychus kanzawai Kishida (Acari: Tetranychidae) in Kanaya City, Japan. Neoseiulus womersleyi (Kanaya population) were more attracted to volatiles from tea plants infested with five female T. kanzawai per leaf for 7 days than to intact tea leaves in a Y-tube olfactometer. Tetranychus kanzawai-induced tea leaf volatiles were identified as (E)-β-ocimene, (E)-4,8-dimethyl-1,3,7-nonatriene, and (E,E)-α-farnesene. As olfactory responses are known to differ among local populations of N. womersleyi , we compared the responses of the Kanaya population with those of a Kikugawa population collected from tea plants infested by T. kanzawai in Kikugawa City. To test the influence of previous predation experience, we reared the two populations on tea plants infested by T. kanzawai or on kidney bean plants (Phaseolus vulgaris) infested by Tetranychus urticae Koch. The Kanaya population was more attracted to the volatiles from infested plants on which they had been reared. Because the Kanaya population was not attracted to the plant volatiles they had not previously experienced, the positive response to previously experienced volatiles might be the result of learning. By contrast, the Kikugawa population showed no preference for previously experienced volatiles from infested plants. The implications of this flexibility in foraging behavior are discussed.
Experimental & applied acarology, 2002
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 gossypii 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-infeste...