Effect of Temperature on Plant Resistance to Arthropod Pests.

Temperature has a strong influence on the development, survival, and fecundity of herbivorous arthropods, and it plays a key role in regulating the growth and development of their host plants. In addition, temperature affects the production of plant secondary chemicals as well as structural characteristics used for defense against herbivores. Thus, temperature has potentially important implications for host plant resistance. Because temperature directly impacts arthropod pests, both positively and negatively, distinguishing direct effects from indirect effects mediated through host plants poses a challenge for researchers and practitioners. A more comprehensive understanding of how temperature affects plant resistance specifically, and arthropod pests in general, would lead to better predictions of pest populations, and more effective use of plant resistance as a management tactic. Therefore, the goals of this paper are to 1) review and update knowledge about temperature effects on plant resistance, 2) evaluate alternative experimental approaches for separating direct from plant-mediated indirect effects of temperature on pests, including benefits and limitations of each approach, and 3) offer recommendations for future research.

Tomato Spotted Wilt Virus Benefits Its Thrips Vector by Modulating Metabolic and Plant Defense Pathways in Tomato.

Several plant viruses modulate vector fitness and behavior in ways that may enhance virus transmission. Previous studies have documented indirect, plant-mediated effects of tomato spotted wilt virus (TSWV) infection on the fecundity, growth and survival of its principal thrips vector, Frankliniella occidentalis, the western flower thrips. We conducted thrips performance and preference experiments combined with plant gene expression, phytohormone and total free amino acid analyses to determine if systemically-infected tomato plants modulate primary metabolic and defense-related pathways to culminate into a more favorable environment for the vector. In a greenhouse setting, we documented a significant increase in the number of offspring produced by F. occidentalis on TSWV-infected tomato plants compared to mock-inoculated plants, and in choice test assays, females exhibited enhanced settling on TSWV-infected leaves. Microarray analysis combined with phytohormone signaling pathway analysis revealed reciprocal modulation of key phytohormone pathways under dual attack, possibly indicating a coordinated and dampening defense against the vector on infected plants. TSWV infection, alone or in combination with thrips, suppressed genes associated with photosynthesis and chloroplast function thereby significantly impacting primary metabolism of the host plant, and hierarchical cluster and network analyses revealed that many of these genes were co-regulated with phytohormone defense signaling genes. TSWV infection increased expression of genes related to protein synthesis and degradation which was reflected in the increased total free amino acid content in virus-infected plants that harbored higher thrips populations. These results suggest coordinated gene networks that regulate plant primary metabolism and defense responses rendering virus-infected plants more conducive for vector colonization, an outcome that is potentially beneficial to the vector and the virus when considered within the context of the complex transmission biology of TSWV. To our knowledge this is the first study to identify global transcriptional networks that underlie the TSWV-thrips interaction as compared to a single mechanistic approach. Findings of this study increase our fundamental knowledge of host plant-virus-vector interactions and identifies underlying mechanisms of induced host susceptibility to the insect vector.

The Effect of Temperature and Host Plant Resistance on Population Growth of the Soybean Aphid Biotype 1 (Hemiptera: Aphididae).

A laboratory experiment was conducted to evaluate direct and indirect effects of temperature on demographic traits and population growth of biotype 1 of the soybean aphid, Aphis glycines Matsumura. Our objectives were to better understand how temperature influences the expression of host plant resistance, quantify the individual and interactive effects of plant resistance and temperature on soybean aphid population growth, and generate thermal constants for predicting temperature-dependent development on both susceptible and resistant soybeans. To assess indirect (plant-mediated) effects, soybean aphids were reared under a range of temperatures (15-30 °C) on soybean seedlings from a line expressing a Rag1 gene for resistance, and life history traits were quantified and compared to those obtained for soybean aphids on a susceptible soybean line. Direct effects of temperature were obtained by comparing relative differences in the magnitude of life-history traits among temperatures on susceptible soybeans. We predicted that temperature and host plant resistance would have a combined, but asymmetrical, effect on soybean aphid fitness and population growth. Results showed that temperature and plant resistance influenced preimaginal development and survival, progeny produced, and adult longevity. There also appeared to be a complex interaction between temperature and plant resistance for survival and developmental rate. Evidence suggested that the level of plant resistance increased at higher, but not lower, temperature. Soybean aphids required about the same number of degree-days to develop on resistant and susceptible plants. Our results will be useful for making predictions of soybean aphid population growth on resistant plants under different seasonal temperatures.

Tomato spotted wilt virus benefits a non-vector arthropod, Tetranychus urticae, by modulating different plant responses in tomato.

The interaction between plant viruses and non-vector arthropod herbivores is poorly understood. However, there is accumulating evidence that plant viruses can impact fitness of non-vector herbivores. In this study, we used oligonucleotide microarrays, phytohormone, and total free amino acid analyses to characterize the molecular mechanisms underlying the interaction between Tomato spotted wilt virus (TSWV) and a non-vector arthropod, twospotted spider mite (Tetranychusurticae), on tomato plants, Solanumlycopersicum. Twospotted spider mites showed increased preference for and fecundity on TSWV-infected plants compared to mock-inoculated plants. Transcriptome profiles of TSWV-infected plants indicated significant up-regulation of salicylic acid (SA)-related genes, but no apparent down-regulation of jasmonic acid (JA)-related genes which could potentially confer induced resistance against TSM. This suggests that there was no antagonistic crosstalk between the signaling pathways to influence the interaction between TSWV and spider mites. In fact, SA- and JA-related genes were up-regulated when plants were challenged with both TSWV and the herbivore. TSWV infection resulted in down-regulation of cell wall-related genes and photosynthesis-associated genes, which may contribute to host plant susceptibility. There was a three-fold increase in total free amino acid content in virus-infected plants compared to mock-inoculated plants. Total free amino acid content is critical for arthropod nutrition and may, in part, explain the apparent positive indirect effect of TSWV on spider mites. Taken together, these data suggest that the mechanism(s) of increased host suitability of TSWV-infected plants to non-vector herbivores is complex and likely involves several plant biochemical processes.

Plant architecture and prey distribution influence foraging behavior of the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae).

The arrangement, number, and size of plant parts may influence predator foraging behavior, either directly, by altering the rate or pattern of predator movement, or, indirectly, by affecting the distribution and abundance of prey. We report on the effects of both plant architecture and prey distribution on foraging by the predatory mite, Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae), on cucumber (Cucumis sativus L.). Plants differed in leaf number (2- or 6-leafed), and there were associated differences in leaf size, plant height, and relative proportions of plant parts; but all had the same total surface area. The prey, the twospotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae), were distributed either on the basal leaf or on all leaves. The effect of plant architecture on predator foraging behavior varied depending on prey distribution. The dimensions of individual plant parts affected time allocated to moving and feeding, but they did not appear to influence the frequency with which predators moved among different plant parts. Overall, P. persimilis moved less, and fed upon prey longer, on 6-leafed plants with prey on all leaves than on plants representing other treatment combinations. Our findings suggest that both plant architecture and pattern of prey distribution should be considered, along with other factors such as herbivore-induced plant volatiles, in augmentative biological control programs.

Foraging on and consumption of two species of papaya pest mites, Tetranychus kanzawai and Panonychus citri (Acari: Tetranychidae), by Mallada basalis (Neuroptera: Chrysopidae).

Tetranychus kanzawai Kishida and Panonychus citri (McGregor) are two major acarine pests of the principal papaya variety in Taiwan, and they often co-occur in the same papaya screenhouses. This study measured prey acceptability, foraging schedule, short-term consumption rate, and handling time of larvae of a domesticated line of the green lacewing, Mallada basalis (Walker), in no-choice tests with different life stages of these two mite pests. After a period of prey deprivation, all three larval instars of M. basalis exhibited a high rate of acceptance of all life stages of both T. kanzawai and P. citri. In 2-h trials, second- and third-instar predators foraged actively most of the time, whereas first instars spent approximately 40% of the time at rest. Consumption increased and prey handling time decreased as predator life stage advanced and prey stage decreased. Third-instar lacewings consumed an average of 311.4 T. kanzawai eggs (handling time: 6.7 s/egg) and 68.2 adults (handling time: 58.8 s/adult), whereas first instars consumed 19.6 eggs (handling time: 23.6 s/egg) and 4.0 adults (handling time: 633.4 s/adult). M. basalis generally consumed more P. citri than T. kanzawai. Except for prey eggs, handling times of T. kanzawai were generally longer than those of P. citri by all M. basalis instars. Handling times were shorter, and consumption were greater, at the higher P. citri density than at the lower one, whereas there were generally no significant differences in prey acceptability and foraging time between those two densities. This study suggests that M. basalis larvae may have high potential for augmentative biological control of mites on papayas.

Comparing chemical and biological control strategies for twospotted spider mites (Acari: Tetranychidae) in commercial greenhouse production of bedding plants.

Efficacy, costs, and impact on crop salability of various biological and chemical control strategies for Tetranychus urticae Koch (Acari: Tetranychidae) were evaluated on mixed plantings of impatiens, Impatiens wallerana Hook.f (Ericales: Balsaminaceae), and ivy geranium, Pelargonium peltatum (1.) L'Hér. Ex Aiton (Geraniales: Geraniaceae), cultivars in commercial greenhouses. Chemical control consisting of the miticide bifenazate (Floramite) was compared with two biological control strategies using the predatory mite Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae). Treatments were 1) a single, early application of bifenazate; 2) a single, early release of predatory mites at a 1:4 predator:pest ratio based on leaf samples to estimate pest density; 3) a weekly release of predatory mites at numbers based on the area covered by the crop; and 4) an untreated control. T. urticae populations were monitored for 3 wk after the earliest treatment. When plants were ready for market, their salability was estimated. Bifenazate and density-based P. persimilis treatments effectively reduced T. urticae numbers starting 1 wk after plants had been treated, whereas the scheduled, area-based P. persimilis treatment had little or no effect. The percentage of flats that could be sold at the highest market wholesale price ranged from 15 to 33%, 44 to 86%, 84 to 95%, and 92 to 100%, in the control, weekly area-based P. persimilis, bifenazate, and single density-based P. persimilis treatments, respectively. We have shown that in commercial greenhouse production of herbaceous ornamental bedding plants, estimating pest density to determine the appropriate number of predators to release is as effective and offers nearly the same economic benefit as prophylactic use of pesticides.

Twospotted spider mite population level, distribution, and damage on ivy geranium in response to different nitrogen and phosphorus fertilization regimes.

The influence of plant nutrition on arthropod pests has often been studied by comparing plants provided suboptimal nutrients with those provided sufficient or luxurious nutrients, but such results have limited applicability to commercially produced crops because nitrogen (N) and phosphorus (P) are almost never limiting in greenhouse production. We conducted a series of experiments with ivy geranium, Pelargonium peltatum (L.) L'Hr. ex Aiton 'Amethyst 96' to determine the response of twospotted spider mite, Tetranychus urticae Koch (Acarina: Tetranychidae), to six combinations of N (8 or 24 mM) and P (0.32, 0.64, or 1.28 mM) that reflected commercial production practices. All six combinations resulted in saleable plants when plants were free of spider mites, but tissue N and P concentrations among fertilizer combinations were different. On mite-infested plants, no difference in mite numbers or plant damage was found in response to N fertilization rates. Phosphorus had no effect on mite population level until week 8, at which time plants fertilized with 0.64 mM P had slightly more mites than plants fertilized with 0.32 mM. However, overall quality and dry weight of plants fertilized by 0.32 mM P was lower than that of 0.64 and 1.28 mM, which suggests that ivy geranium plants fertilized with the higher P rates may better compensate for mite feeding damage. Positive correlations were found between within-plant distribution of mites and the corresponding tissue N and P concentrations in three foliage strata, suggesting that tissue nutrient content may influence mite selection of feeding sites.

Testing for non-target effects of spinosad on twospotted spider mites and their predator Phytoseiulus persimilis under greenhouse conditions.

The compatibility of the selective insecticide spinosad (Conserve SC), at rates recommended for thrips control in greenhouses, with release of the predatory mite Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae) to control spider mites, was investigated in a crop of ivy geranium Pelargonium peltatum, cultivar 'Amethyst 96.' Plants were inoculated with twospotted spider mites, Tetranychus urticae Koch (Acari: Tetranychidae), 2 weeks before treatments were applied. There were three treatment variables, each at two levels: predators (released or not), spray application (water or Conserve SC at 2 ml/3.79 l), and timing of spray (1 day before or after predators were released). Twospotted spider mite populations then were sampled twice each week over a three-week period. The application or timing of spinosad had no effect on the ability of the predator to reduce the population of spider mites. Spider mite populations in the no-predator treatment continued to expand over the course of the experiment, while those in the predator-release treatment declined. We conclude that P. persimilis can be used in conjunction with spinosad on ivy geraniums without causing obvious detrimental effects to this predator or leading to a reduction in biological control.

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.

Susceptibility and detoxifying enzyme activity in two spider mite species (Acari: Tetranychidae) after selection with three insecticides.

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 lambda-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, lambda-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, lambda-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 lambda-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.

Is host plant choice by a clytrine leaf beetle mediated through interactions with the ant Crematogaster lineolata?

In the grasslands of northeastern Kansas, adult populations of Anomoea flavokansiensis, an oligophagous leaf beetle (subfamily Clytrinae), specialize on Illinois bundleflower (Desmanthus illinoensis) even though other reported host species commonly occur and are simultaneously available. We performed choice feeding tests to examine whether A. flavokansiensis adults have a fixed feeding preference for bundleflower. In choice tests, beetles ate similar amounts of bundleflower and honey locust (Gleditsia triacanthos). In addition, we measured fecundity and longevity of adults in no-choice tests to determine if adults were adapted solely to bundleflower. In no-choice tests, fecundity and longevity were no different for adults feeding on bundleflower and honey locust. We next examined the influence of host plant on the attractiveness of beetle eggs to ants. In northeastern Kansas, Crematogaster lineolata ants are attracted to A. flavokansiensis eggs and carry them into their nests where the larvae hatch and apparently reside as inquilines. C. lineolata exhibited a strong preference for eggs from female A. flavokansiensis that fed exclusively on bundleflower compared to eggs from females that fed exclusively on honey locust. Local populations of A. flavokansiensis in northeastern Kansas may specialize on bundleflower to increase the chances of their eggs being transported by C. lineolata ants into their nests. C. lineolata nests may serve as a predator-free and sheltered environment in which A. flavokansiensis eggs undergo embryogenesis.