David C. Margolies

Response of a phytoseiid predator to herbivore-induced plant volatiles: selection on attraction and effect on prey exploitation

Bean plants infested with herbivorous spider mites emit volatile chemicals that are attractive toP. persimilis, a predator of spider mites. In Y-tube olfactometer tests we evaluated involvement of a genetic component in predator response to herbivore-induced plant volatiles. Replicated bidirectional selection resulted in a significant increase in attraction after one generation of selection, but no decrease even after three generations of selection, indicating significant, but unbalanced, additive genetic variation in predator perception of, or response to, herbivore-induced plant volatiles. Selected lines responded differently than an unselected population to food deprivation, pointing to an interaction between their internal state and response to plant volatiles. Selected lines also differed from unselected ones in behaviors associated with local prey exploitation, such as residence time, prey consumption, and reproduction. At lower prey densities,P. persimilis from both “+” lines left spider mite-infested leaves more rapidly and consumed fewer prey eggs than an unselected population. Defining olfactory components of predator search behavior is one step in understanding the effect of plant volatiles on predator foraging efficiency. By selecting lines differing in their attraction to herbivore-induced plant volatiles we may experimentally investigate the link between this behavior, predator foraging efficiency, and local and regional predator-prey population dynamics. The impact of significant additive genetic variation in predator response to plant volatiles on evolution in a tritrophic context also remains to be uncovered.

Movement of the twospotted spider mite, Tetranychus urticae, among hosts in a corn‐peanut agroecosystem

A 3 year study of spider mites in a corn‐peanut agroecosystem indicated that the persistance and pest status of mite populations depended on dispersal among a succession of temporarily suitable cultivated and non‐cultivated hosts. In the spring, mites crawled from overwintering sites in vegetation along field margins into both peanut and corn fields, but became established only in corn. Initiation of aerial dispersal from corn was coincident with and appeared dependent upon mites moving to the top of the corn canopy, where they were exposed to the wind. Mites were first observed in peanut immediately following the onset of aerial dispersal from corn, and these aerial dispersers were the primary source of subsequent mite infestations in peanut. As populations grew in peanut, mites dispersed into vegetation along peanut field margins and became the nucleus of populations which persisted over the winter. This pattern of host utilization was reinitiated in the spring if corn was planted adjacent to infested field borders. This pattern commonly occurs since corn is planted following peanut in the predominant crop rotation sequence in this area.

Susceptibility and Detoxifying Enzyme Activity in Two Spider Mite Species (Acari: Tetranychidae) After Selection with Three Insecticides

Abstract Changes in the susceptibility and detoxifying enzyme activity were measured in laboratory strains of Banks grass mite, Oligonychus pratensis (Banks), and twospotted spider mite, Tetranychus urticae Koch, that were repeatedly exposed to three insecticides. Three strains of each mite species were exposed to one of two pyrethroids, bifenthrin, and λ-cyhalothrin, or an organophosphate, dimethoate, for 10 selection cycles at the LC60 for each insecticide. A reference or nonselected strain of each mite species was not exposed to insecticides. After 10 cycles of exposure, susceptibility to the corresponding insecticides, bifenthrin, λ-cyhalothrin, and dimethoate, decreased 4.5-, 5.9-, and 289.2-fold, respectively, relative to the reference strain in the respective O. pratensis strains, and 14.8-, 5.7-, and 104.7-fold, respectively, relative to the reference strain in the respective T. urticae strains. In the bifenthrin-exposed O. pratensis strain, there was a 88.9-fold cross-resistance to dimethoate. In the dimethoate-exposed T. urticae strain, there was a 15.9-fold cross-resistance to bifenthrin. These results suggest that there may be cross-resistance between dimethoate and bifenthrin. The reduced susceptibility to dimethoate remained stable for three months in the absence of selection pressure in both mites. The decrease in susceptibility in the O. pratensis strains exposed to bifenthrin, λ-cyhalothrin, and dimethoate was associated with a 4.7-, 3.0-, and 3.6-fold increase in general esterase activity, respectively. The decrease in susceptibility in the T. urticae strains exposed to bifenthrin and λ-cyhalothrin was associated with a 1.3- and 1.1-fold increase in general esterase activity, respectively. The mean general esterase activity was significantly higher in the pyrethroid-exposed O. pratensis and T. urticae strains than in the nonselected strain. There was no significant increase in esterase activity in the dimethoate-exposed T. urticae strain. The decrease in susceptibility to insecticides was also associated with reduced glutathione S-transferase 1-chloro-2, 4-dinitrobenzene conjugation activity, but this did not appear to be related to changes in insecticide susceptibility. These results suggest that in these mites, the general esterases may play a role in conferring resistance to pyrethroids. However, some other untested mechanism, such as target site insensitivity, must be involved in conferring dimethoate resistance.

Effects of mite age, mite density, and host quality on aerial dispersal behavior in the twospotted spider mite

Mite age, population density, and host leaf quality affect various life history traits in spider mites. We investigated the effects of these factors on the aerial dispersal behavior of adult female twospotted spider mites, Tetranychus urticae Koch (Acari: Tetranychidae). The proportion of adult females exhibiting the dispersal behavior dropped significantly with age following adult emergence, particularly in the first 3 days. Sixty to eighty percent of female mites 2‐days old or younger displayed the behavior under test conditions, whereas less than 20% of female mites older than 3‐days‐old showed the behavior. Younger adult females also exhibited shorter latency for the behavior, although this trend was not as clear. Leaf quality experienced during deutonymph development had no effect on the behavior adults subsequently displayed. On the other hand, adult females that fed on poor quality leaves after emergence were twice as likely to display the behavior (90% vs. 45%), and with shorter latency (37 vs. 77 min), than those that fed on high quality leaves. When newly emerged adult females encountered high mite density and dry leaves, the incidence of the behavior increased (69% vs. 47%) and latency decreased (69 vs. 93 min) compared to mites that encountered low density on well watered leaves. Our results suggest that both starvation and desiccation of adult females may enhance their dispersal behavior.

Responses to direct and indirect selection on aerial dispersal behaviour in Tetranychus urticae

Dispersal within and between hosts is an important element of arthropod life histories. This study was designed to assess adaptability of traits related to dispersal and colonization in the twospotted spider mite, Tetranychus urticae. Defining the flexibility of mite dispersal and life-history is necessary to understand the response of mites to changes in the spatial and temporal structure of their environment. We found significant direct response to bidirectional selection on aerial dispersal behaviour after eight and five generations of selection. The realized heritability estimated from these lines (h2=0.28) was in close agreement with that estimated in a previous sib-analysis on the base population. As predicted from the sib-analysis, there were no correlated responses in fecundity or sex ratio. Crosses between selected lines indicated that the dispersal behaviour was under weak maternal influence and that non-dispersal may be a slightly dominant trait. Mite sensitivity or resistance to starvation or desiccation, the major environmental cues triggering their behaviour, changed in response to selection. Results suggest that variation in aerial dispersal behaviour is largely attributed to different sensitivity or resistance to environmental stress and that genetic variation in this behaviour may be maintained by selection for dispersal when food resources become depleted and against when food is abundant. The dispersal behaviour itself, although not correlated with reproductive traits, may increase mite fitness in temporally and spatially fluctuating environments.

Host plant-induced changes in detoxification enzymes and susceptibility to pesticides in the twospotted spider mite (Acari: Tetranychidae).

Abstract Adult female twospotted spider mites, Tetranychus urticae Koch, reared on lima bean plants were moved to cucumber, maize, or new lima bean plants (the latter being a control) and evaluated after 24 h or 7 d for changes in susceptibility to three pesticides and in levels of related detoxification enzymes. The largest and most consistent changes were observed in mites feeding on cucumber. Susceptibility of mites on cucumber to the synthetic pyrethroids bifenthrin and λ-cyhalothrin was greater than that of mites reared on lima bean and maize after only 24 h on the plants, and remained higher after 7 d. Mites on cucumber also were more susceptible to the organophosphate dimethoate than were mites on lima bean, but only after 7 d on the host. Susceptibility was inversely related to activities of both general esterase and glutathione S-transferase (GST) in mites on cucumber; general esterase and GST activities were 60 and 25% lower, respectively, than activities of twospotted spider mite on lima bean after 7 d of feeding. Mites on maize were slightly but significantly more susceptible than those on lima bean to bifenthrin, but not to λ-cyhalothrin, after 7 d and to dimethoate after 24 h but not after 7 d. General esterase and GST activities in twospotted spider mite fed on maize for 24 h were 20 and 16% higher, respectively, than activities in twospotted spider mite on lima bean, but general esterase activity was 30% lower than lima bean-fed mites and GST was not different after 7 d. Thus, plant-induced changes in general esterase activity, perhaps in combination with GST activity, in twospotted spider mite appear to be inversely related to, and possibly responsible for, changes in susceptibility of twospotted spider mite to several pesticides, particularly the synthetic pyrethroids. General esterases appear to play less of a role in the detoxification of the organophosphate insecticide dimethoate.

Variation between biotype E clones of Schizaphis graminum (Homoptera: Aphididae)

Phenotypic and genotypic variation was investigated between biotype E clones of the greenbug, Schizaphis graminum (Rondani). S. graminum was collected from wheat and sorghum fields in seven Kansas counties, USA. Colonies representing single maternal lineages (clones) were initiated and maintained in an insectary, and were verified as biotype E. An allozyme survey among clones did not detect any polymorphism at 24 enzymatic loci. We were unable to detect interclonal variation for nymphal survivorship, age at first reproduction, fecundity, and reproductive lifespan. Variation among genetically homogeneous daughters within clones was as great as variation among different clones for the above parameters, due to microenvironmental effects. However, by using the intergenic spacer in the rDNA cistron as a molecular fingerprinting tool, we identified 56 unique maternal lineages among 61 clones tested. The length of the intergenic spacer varied within individual S. graminum , and different maternal lineages had unique sets of spacer sizes. However, S. graminum within a single clone shared the same sets of spacer sizes. Extensive molecular genetic variation was found among biotype E clones, despite a lack of variation in additive genetic traits. Thus, biotype E populations are made up of many genetically distinct clones and do not represent an asexual proliferation of one or a few maternal lineages.

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.

Local and distant prey-related cues influence when an acarine predator leaves a prey patch

Over relatively long distances, the predatory mite Phytoseiulus persimilis is able to detect volatiles produced by bean plants that are infested by its prey, Tetranychus urticae, the twospotted spider mite. Our investigation examined the separate and combined effects of prey, their products, and prey‐induced plant volatiles on when P. persimilis left a potential prey host plant. In wind tunnels, we assessed the relative importance of and interaction among local and distant prey‐related cues. The examination of local cues included: (1) all local cues (prey eggs, webbing, and prey‐induced plant volatiles), (2) food (prey eggs) and webbing only, (3) plant volatiles only, and (4) no prey‐related cues. The examination of distant cues involved the presence or absence of prey‐induced plant volatiles from upwind plants. External volatile cues, produced by placing prey‐infested plants upwind in the wind tunnel, resulted in more predators leaving downwind plants, and leaving sooner, than when clean plants were upwind, regardless of the availability of prey or prey‐related cues on the local plant. However, local cues, especially the presence of food/webbing, had a greater effect than distant cues on timing of predator leaving. Predators remained in larger numbers and for longer times on prey‐infested plants. However, the presence of either locally‐produced plant volatiles or food/webbing alone still reduced the number of predators leaving a plant in the first hour compared to clean plants. After the first hour, the number of predators leaving was primarily driven by the presence of food/webbing. When no food/webbing was available, predators left plants rapidly; if food/webbing was available, some predatory mites remained on plants at least 24 hours. Even if no food/webbing was available, predators presented with local volatiles remained on plants for several hours longer than on clean plants without local volatiles. These small changes in leaving rates may lead to differences in local population dynamics, and possibly regional persistence, of the predator‐prey interaction in patchy environments.

Temperature-induced changes in spider mite fitness: offsetting effects of development time, fecundity, and sex ratio

Temperature affects many life history parameters in poikilotherms. Temperature clearly affects development time and fecundity, which affect the intrinsic rate of increase. In haplodiploid mites, ambient temperature may also affect offspring sex ratio which, in turn, affects intrinsic rate of increase. The combined effect of all these processes determines the fitness of individual females. However, sex ratio also affects mating structure and, potentially, rate of local adaptation. We investigated the direct effect of temperature variation on sex ratio, development time, and fecundity in the twospotted spider mite (Tetyranychus urticae), and calculated the effect of their interaction on mite intrinsic rate of increase. We conducted experiments at 2 temperatures and designed the experiment to separate pre‐adult and adult sensitivity to temperature variation. Mites were reared from eggs to adult ecdysis at either 22 °C or 32 °C. Upon emergence as adults, these 2 groups were each split between 22 °C and 32 °C and allowed to oviposit. Not surprisingly, development from egg to adult was accelerated when mites were exposed to the higher temperature during offspring development, regardless of the temperature experienced by the mother during her development. Fecundity and the proportion of female offspring were affected by temperature only when mothers were exposed during both development and oviposition. About 12 offspring were gained and female bias was increased by 26% when the mothers development occurred at 22 °C, whereas oviposition at 22 °C added only 6 more offspring and increased female bias by only 7%. There was no correlation between sex ratio and fecundity; both were related to temperature but not to each other. Furthermore, development time, not fecundity or sex ratio, appeared to the main factor affecting the intrinsic rate of increase. Our results support other evidence that sex ratio varies independently of development time and fecundity.