Direct and indirect cues of predation risk influence behavior and reproduction of prey: a case for acarine interactions

Little is known about the flow of chemical information fromhigher to lower levels within the animal food chain. However,this information may determine the behavior and distributionof many animals (e.g., that of potential prey) when exposedto direct and indirect cues of predation risk. We used herbivorousspider mites, Tetranychus urticae Koch (Tetranychidae) as amodel to examine the foraging and oviposition decisions thatprey make when exposed to these cues. We conducted laboratorytests to determine if the previous presence of predators (directcues) on leaf discs or the presence of injured conspecifics(indirect cues) alters the distribution of adults and eggs ofT. urticae. When given a choice, after 24 h, fewer adults and eggswere found on leaf discs that had previously contained specialistspider mite predators, Phytoseiulus persimilis Athias-Henriot (Phytoseiidae),than on discs unexposed to predators. Also, more T. urticaeemigrated from predator-exposed discs than from unexposed discs orfrom those that had previously contained nonpredatory mites(Tyrophagus putrescentiae, Acaridae). Finally, fewer T. urticaeforaged and laid eggs on predator-exposed discs or on thosewith artificially damaged conspecifics (eggs or dead adults)than on discs with intact conspecifics. Tetranychus urticaeprobably recognizes infochemicals (kairomones) from its predatorsor cues from injured spider mites and consequently avoids feedingor ovipositing in areas exposed to these cues. Recognition and avoidanceof kairomones from specialist predators by this prey are likelyto be hereditary, but avoidance of injured conspecifics maybe an adaptation to avoid predators that are not inherentlyrecognized. We discuss the behavioral and ecological implicationsof our findings.     

Factors influencing the acaricidal activity of flucycloxuron

Contact activities of flucycloxuron on immature stages of the two-spotted spider mite (Tetranychus urticae (Koch)) and the European red mite (Panonychus ulmi (Koch)) gradually decrease in the successive developmental stages. The levels of contact activity of flucycloxuron on larvae and protonymphs ofT. urticae andP. ulmi are of the same order. Deutonymphs ofT. urticae are less susceptible to contact activity than the similar stage ofP. ulmi. In adultT. urticae, the transovarial ovicidal activity was used as an indicator for cuticular penetration. More than 90% of the maximal penetration into adult mites occurs within 8 h. Reversibility of the transovarial activity was not observed after 24 h, but did occur after a subsequent 48 h stay on untreated leaves. The ovo-larvicidal activity of flucycloxuron onP. ulmi after treatment of apple leaves is strongly negatively influenced by leaf age, partly by lower retention of the spray liquid on the leaves. Leaf penetration was measured by application of flucycloxuron on leaf uppersides and assessment of the transovarial activity in mites (P. ulmi orT. urticae) infested on the undersides, one day after treatment. In this test system, leaf penetration was found to be strongly species dependent. Penetration was high in cucumber, moderate in French beans, cotton, roses and strawberry, but low in apple and pepper. Leaf penetration in French bean plants is drastically reduced at increasing leaf age. The overall positive effect of increase in relative air humidity on leaf penetration, is statistically highly significant (P=0.001) for French beans and almost significant (P=0.08) for cucumbers. WithT. urticae on French bean it was found that in this test flucycloxuron needs more than one day for maximal leaf penetration. Although in apple leaves penetration from uppersides was low, penetration from undersides was much higher. The surfactants Arkopal N 130, Silwet L-77 and X2-5309 enhance penetration from leaf under-sides.     

Effects of soil water stress and twospotted spider mites on net photosynthesis and transpiration of apple leaves

Soil water stress and twospotted spider mites (Tetranychus urticae Koch) were tested for their influence on the content and activity of leaves of greenhouse grown Delicious apple trees. Soil water stress caused reductions in net photosynthesis (Pn), transpiration (Tr), and shoot growth. Leaf water potential was decreased by both water stress and mite feeding. Feeding of 15 adult mites/leaf for 28 days resulted in a 16% reduction in Pn while an initial population of 10 mites leaf/left to develop for 20 days reduced Pn by 27%. Mite feeding reduced leaf nitrogen and non-structural carbohydrate levels when sampled 20 days after placement on the leaf. There was no interaction between the changed physiology of the leaf due to soil water stress and mite feeding.Approved for publication as Journal Article No. 111-80 of the Ohio Agricultural Research and Development Center, Wooster, OH 44691.Associate Professor and Professor, Departments of Horticulture and Entomology, respectively.     

Development of two spotted spider mite (Acari: Tetranychidae) populations on strawberry and raspberry cultivars

Five strawberry (Fragaria sp.) and five raspberry (Rubus ideaus L.) cultivars were evaluated for resistance to two spotted spider mite (Tetranychus urticae Koch.). Two methods of assessing the development of two spotted mite populations using detached leaves were compared. The number of eggs laid and mites which developed were compared. The strawberry cvs Hapil and Pegasus had significantly greater development of two spotted mite populations than the cvs Rhapsody, Symphony and Elsanta. The raspberry cv. Joan Squires had higher populations of two spotted mite whilst the raspberry cv. Leo the least, when compared with cvs Glen Clova, Glen Moy and Glen Prosen. Differences were observed in oviposition sites and mite distribution when comparing raspberries with strawberries. The method of assessing the populations development of two spotted mite which involved maintaining the cut leaf stem in water may be of potential use for studying population dynamics of both two spotted mite and possible predators over extended periods of time.     

No variation for Wolbachia-induced hybrid breakdown in two populations of a spider mite

Wolbachia are cytoplasmically transmitted bacteria that infect several species of mites. In the two-spotted spider mite Tetranychus urticae Koch this symbiont can induce reproductive incompatibility. Wolbachia-induced reproductive incompatibility is observed in crosses between Wolbachia-infected (W) males and uninfected (U) females. This incompatibility is expressed in F1 broods as male-biased sex ratios, an effect called cytoplasmic incompatibility (CI). However, in the two-spotted spider mite, Wolbachia-induced reproductive incompatibility may extend to the F2: broods of virgin F1 females from U×W crosses sometimes suffer increased mortality rates. This F2 effect is called hybrid breakdown (HB). Several isofemale lines derived from mites collected from rose and cucumber plants had been previously tested for CI. Here we report on the results obtained for HB.     

Altered host plant preference of Tetranychus urticae and prey preference of its predator Phytoseiulus persimilis (Acari: Tetranychidae, Phytoseiidae) on transgenic Cry3Bb-eggplants

The behavior of the two-spotted spider mite, Tetranychus urticae Koch and the predatory mite Phytoseiulus persimilis A.-H. was investigated in laboratory experiments with transgenic Bt-eggplants, Solanum melongena L., producing the Cry3Bb toxin and corresponding isogenic, non-transformed eggplants. In bitrophic experiments, dual-choice disc tests were conducted to reveal the effects of transgenic eggplants on host plant preference of T. urticae. Adult spider mite females were individually placed on leaf discs (2 cm diameter) and were observed during five days. Females occurred significantly more frequently on transgenic halves on which also significantly more T. urticae eggs were found. The effects of a Cry3Bb-eggplant fed prey on the feeding preference of P. persimilis were investigated in tritrophic experiments. Sixteen spider mite females, eight of which had been taken from transgenic and eight from isogenic eggplants, were offered to well-fed females of P. persimilis and numbers of respective spider mites consumed were registered 12 h later when the predators were offered new spider mites again. This procedure was repeated six times. The results revealed that predatory mites consumed significantly less Bt-fed spider mites than prey that had been raised on control eggplants. These results indicate that eggplants expressing the Cry3Bb toxin for resistance against the Colorado potato beetle are more preferred by spider mites but are less preferred by their predator P. persimilis. Possible consequences of these findings for biological control of spider mites on eggplants are discussed.     

Control of phytoseiids in a spider mite mass-rearing system (Acari: Phytoseiidae,Tetranychidae)

Phytoseiid mites which contaminated the spider mite colony and interfered with the mass-rearing of spider mites were controlled by dipping in hot water. Immersion for 60 s in water of 50°C killed all stages ofAmblyseius fallacis (Garman),A. womersleyi Schicha andPhytoseiulus persimilis (Athias-Henriot) (Acari: Phytoseiidae). Only approximately 0.3% of theA. womersleyi eggs hatched, and this seems negligible. The populations ofTetranychus kanzawai Kishida andT. urticae (Koch) (Acari: Tetranychidae) were reduced. However, they recovered well. Although this treatment resulted in the withering of some soybean seedlings, the next trifoliate leaf to be produced was normal. A very satisfactory result was obtained when this technique was applied to the mass-rearing system.     

Within-leaf differences in nutritive value and defence mechanism in chrysanthemum to the two-spotted spider mite (Tetranychus urticae)

Some chrysanthemum leaf characteristics were evaluated to determine their importance as nutrition for, and as factors of resistance to,Tetranychus urticae Koch. These characteristics were: leaf age and chemical composition, content of phenolic substances, total nitrogen, and soluble protein.Mite density was lower on young leaves than on mature ones. Young leaves appear to be protected againstT. urticae by a higher concentration of mono-and polyphenols, although they contained higher levels of nutrients than mature ones. After mite infestation, the most valuable young leaves were also the best-protected leaves on their shoots. Content of phenolic compounds increased only in young chrysanthemum leaves after mite feeding.     

A single nucleotide polymorphism in the acetylcholinesterase gene of the predatory mite Kampimodromus aberrans (Acari: Phytoseiidae) is associated with chlorpyrifos resistance

The predatory mite Kampimodromus aberrans (Oudemans) (Acari: Phytoseiidae) is one of the most important biocontrol agents of herbivorous mites in European perennial crops. The use of pesticides, such as organophosphate insecticides (OPs), is a major threat to the success of biocontrol strategies based on predatory mites in these cropping systems. However, resistance to OPs in K. aberrans has recently been reported. The present study investigated the target site resistance mechanisms that are potentially involved in OP insensitivity. In the herbivorous mite Tetranychus urticae Koch (Acari: Tetranychidae), resistance to OPs is due to a modified and insensitive acetylcholinesterase (AChE; EC: 3.1.1.7) that bears amino acid substitution F331W (AChE Torpedo numbering). To determine whether the predators and prey have evolved analogous molecular mechanisms to withstand the same selective pressure, the AChE cDNA from a putative orthologous gene was cloned and sequenced from susceptible and resistant strains of K. aberrans. No synonymous mutation coding for a G119S substitution was determined to be strongly associated with the resistant phenotype instead of the alternative F331W. Because the same mutation in T. urticae AChE was not associated with comparable levels of chlorpyrifos resistance, the role of the G119S substitution in defining insensitive AChE in K. aberrans remains unclear. G119S AChE genotyping can be useful in ecological studies that trace the fate of resistant strains after field release or in marker-assisted selection of improved populations of K. aberrans to achieve multiple resistance phenotypes through gene pyramiding. The latent complexity of the target site resistance in K. aberrans vs. that of T. urticae is also discussed in the context of data from the genome project of the predatory mite Metaseiulus occidentalis (Nesbitt) (Acari: Phytoseiidae).     

Predation by Allothrombium pulvinum on the spider mites Tetranychus urticae and Amphitetranychus viennensis: Predation Rate, Prey Preference and Functional Response

The deutonymphs of Allothrombium pulvinum Ewing (Acari: Trombidiidae) are among the most important natural enemies of spider mites in North, North East and West Iran. In this study, maximum predation rate and preference experiments were conducted with A. pulvinum deutonymphs on apple leaf discs, to determine their preference for either of two spider mite species: Amphitetranychus viennensis (Zacher) and Tetranychus urticae Koch (Acari: Tetranychidae). Maximum predation rate tests showed that the predatory mite consumed more eggs and females of T. urticae than of A. viennensis. Furthermore, the Manly’s preference index for eggs and females of T. urticae confirmed that T. urticae were the preferred prey. The functional response of A. pulvinum deutonymphs on females of T. urticae was examined over a 24-h period. Predation of A. pulvinum deutonymphs presented with females of T. urticae followed a type III functional response. Estimated handling time for the predatory mites was 4.51 h and attack coefficient b, which describes the changes in attack rate with prey densities in a type III functional response, was 0.021.     

Voluntary Falling in Spider Mites in Response to Different Ecological Conditions at Landing Points

We examined voluntary-falling behaviour by adult females of the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) and one of its major predators Neoseiulus californicus McGregor (Acari: Phytoseiidae). Experiments were conducted using a setup in which mites could only move onto one of two landing points by falling. Significantly more T. urticae females fell onto available food leaves compared to non-food or heavily infested leaves, whereas significantly fewer females fell onto leaves with the predatory mite N. californicus compared to leaves without the predator. This suggests that spider mites can actively choose on which patch to land on the basis of food quality and predation risk on the patch. Using the same experimental setup, starved N. californicus females never fell, suggesting that falling T. urticae females gain the potential advantage of predator avoidance.     

Resistance status of the carmine spider mite,Tetranychus cinnabarinus and the twospotted spider mite,Tetranychus urticae to selected acaricides on strawberries

The carmine spider mite, Tetranychus cinnabarinus (Boisduval) and the twospotted spider mite, Tetranychus urticae Koch, are serious pests of strawberries and many other horticultural crops. Control of these pests has been heavily dependent upon chemical acaricides. Objectives of this study were to determine the resistance status of these two pest species to commonly used acaricides on strawberries in a year‐round intensive horticultural production region. LC₉₀ of abamectin for adult carmine spider mites was 4% whereas that for adult twospotted spider mites was 24% of the top label rate. LC_90s of spiromesifen, etoxazole, hexythiazox and bifenazate were 0.5%, 0.5%, 1.4% and 83% of their respective highest label rates for carmine spider mite eggs, 0.7%, 2.7%, 12.1% and 347% of their respective highest label rates for the nymphs. LC_90s of spiromesifen, etoxazole, hexythiazox and bifenazate were 4.6%, 11.1%, 310% and 62% of their respective highest label rates for twospotted spider mite eggs, 3%, 13%, 432,214% and 15% of their respective highest label rates for the nymphs. Our results suggest that T. cinnabarinus have developed resistance to bifenazate and that the T. urticae have developed resistance to hexythiazox. These results strongly emphasize the need to develop resistance management strategies in the region.     

Yield loss to corn from feeding by the Banks grass mite and two-spotted spider mite (Acari: Tetranychidae)

Our research was designed to determine the effects of a mite complex consisting of the Banks grass mite (BGM),Oligonychus pratensis (Banks), and the two-spotted spider mites (TSM),Tetranychus urticae Koch, on corn yield and plant lodging. For BGM, mite days and damage rating for the whole plant and leaves in the lower third of a corn plant had the best correlation with corn yield. The best correlation with yield for TSM was plant damage ratings. The percentage loss per unit for most independent variables (mite densities, mite days, or percentage of the leaf area damaged on a plant) was very similar for BGM and TSM. Therefore, the same economic threshold can be used for either mite species. When TSM fed on corn in the dent growth stage, yield was not reduced, and their feeding did not influence corn plant lodging.     

Cell Membrane Stability and Leaf Surface Wax Content as Affected by Increasing Water Deficits in Maize

A field experiment was conducted with a water-stressed treatmentand well-watered control using eight maize (Zea mays L.) cultivars.Effects of water deficits on cell membrane stability (CMS) measuredby the polyethylene glycol (PEG) test, leaf surface wax content,and relative growth rate were investigated. Cytoplasmic lipidcontent was also analysed. Cell membrane stability and leaf surface wax content increasedwith the degrees of stress. Tolerance to drought evaluated asincrease in CMS under water deficit conditions was well differentiatedbetween cultivars and was well correlated with a reduction inrelative growth rate under stress. A negative correlation wasfound between percentage injury in the PEG test and leaf surfacewax content. High phospholipid contents were observed in tissuesof drought tolerant cultivars under water deficit conditions. Key words: Cell membrane stability, cytoplasmic lipid, drought tolerance, leaf surface wax, relative growth rate     

Allocating time between feeding, resting and moving by the two-spotted spider mite, Tetranychus urticae and its predator Phytoseiulus persimilis

This study characterizes the timing of feeding, moving and resting for the two-spotted spider mite, Tetranychus urticae Koch and a phytoseiid predator, Phytoseiulus persimilis Athias-Henriot. Feeding is the interaction between T. urticae and plants, and between P. persimilis and T. urticae. Movement plays a key role in locating new food resources. Both activities are closely related to survival and reproduction. We measured the time allocated to these behaviours at four ages of the spider mite (juveniles, adult females immediately after moult and adult females 1 and 3 days after moult) and two ages of the predatory mite (juveniles and adult females). We also examined the effect of previous spider mite-inflicted leaf damage on the spider mite behaviour. Juveniles of both the spider mite and the predatory mite moved around less than their adult counterparts. Newly emerged adult female spider mites spent most of their time moving, stopping only to feed. This represents the teneral phase, during which adult female spider mites are most likely to disperse. With the exception of this age group, spider mites moved more and fed less on previously damaged than on clean leaves. Because of this, the spider mite behaviour was initially more variable on damaged leaves. Phytoseiulus persimilis rested at all stages for a much larger percentage of the time and spent less time feeding than did T. urticae; the predators invariably rested in close proximity to the prey. Compared to adult predators, juveniles spent approximately four times as long handling a prey egg. The predator-prey interaction is dependent upon the local movement of both the predators and prey. These details of individual behaviours in a multispecies environment can provide an understanding of population dynamics.     

Functional response of Neoseiulus barkeri Hughes on two-spotted spider mite (Acari: Tetranychidae)

Generalist predatory mites are the common phytoseiid fauna in many agroecosystems, but little attention has been paid to their potential as biological control agents. In this study, we determined the functional responses of adult females of the generalist predator Neoseiulus barkeri Hughes on eggs, larvae, and adults of the two-spotted spider mite, Tetranychus urticae Koch, in the laboratory. Predation experiments were conducted on pepper leaf discs over a 24 h period at 25±1°C, 70–80% RH and 16L:8D photoperiod. Prey densities ranged 5 to 80 eggs, or 5 to 40 larvae, or 1 to 8 female adults of T. urticae per disc. The predation rate of N. barkeri adult females on T. urticae eggs was the same as on its larvae, but the predation rate on adult females was much lower. The role of generalist predatory mites in integrated and biological control of greenhouse pests was discussed.     

Effects of mating status and age on dispersal behavior in the twospotted spider mite, Tetranychus urticae in response to fenvalerate-treated leaf surfaces

Effects of variation in age and mating status on dispersal of the twospotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), from fenvalerate-treated leaf surfaces were investigated. Unmated and mated female mites, 1 to 6 days in age, were scored for walkoff and spindown dispersal response on bean leaves treated with a sub-lethal, residual dose of fenvalerate. Variation in mite age did not have a pronounced effect on dispersal response. Significant differences in dispersal response due to mating type were observed, yet the mean differences in dispersal response between unmated and mated females was generally small. Our data suggest that the current practice of using mated female mites of unknown age when testing for among-population differences in dispersal response, in most cases, provides an adequate estimate of population response when differences among treatments in dispersal response are large. However, when testing for within-population differences in dispersal response, small treatment effects may be more easily measured using a single age class of mites, because this could decrease within-treatment variance.     

On gene flow between Tetranychus urticae Koch, 1836 and Tetranychus cinnabarinus (Boisduval) Boudreaux, 1956 (Acari: Tetranychidae): Sononomy between the two species

It was found that the reproductive separation between the two-spotted spider mite (Tetranychus urticae Koch) and the carmine spider mite (Tetranychus cinnabarinus (Boisduval) is far from complete. Hybrid strains were established which possessed the morphological characteristics of T. cinnabarinus, but which were homozygous for a marker gene originating from T. urtica. In addition, short-day treatment leads to diapause not only in the species from cold climates (T. urticae), but also in a population of T. cinnabarinus. It is questioned whether T. cinnabarinus deserves ranking at species level.

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Résumé Ce travail montre que l'isolement reproductif entre Tetranychus uriticae Koch et Tetranychus cinnabarinus (Boisduval), est loin d'être complet. L'auteur a obtenu des souches hybrides présentant les caractéristiques morphologiques de T. cinnabarinus, mais homozygotes pour un gêne marqueur provenant de T. urticae. De plus, une diminution de la photopériode entraîne l'entrée en diapause des espèces provenant de régions à climat froid (T. urticae), mais aussi d'une population de T. cinnabarinus.Il est finalemant proposé de considérer Tetranychus cinnabarinus (Boisduval) Boudreaux, 1956, comme un synonyme de Tetranychus urticae Koch, 1836.

     

The presence of webbing affects the oviposition rate of two-spotted spider mites, <Emphasis Type="Italic">Tetranychus urticae</Emphasis> (Acari: Tetranychidae)

Several species of tetranychid mites including Tetranychus urticae Koch (Acari: Tetranychidae) construct complicated three-dimensional webs on plant leaves. These webs provide protection against biotic and abiotic stress. As producing web is likely to entail a cost, mites that arrive on a leaf with web are expected to refrain from producing it, because they will gain the benefit of protection from the existing web. Mites that produce less web may then allocate resources that are not spent on web construction to other fitness-enhancing activities, such as laying eggs. To test this, the oviposition rate of T. urticae adult females was examined on leaves with web. As a control, we used leaves where the web had been removed, hence both types of leaves had been exposed to conspecifics previously and were thus damaged. On leaves with web, the oviposition rate of T. urticae females was higher than on leaves where the web had been removed. Therefore, the presence of web constructed by conspecifics enhanced the oviposition rate of T. urticae females. This provides indirect evidence that mites use the web constructed by conspecifics and thereby save resources that can be allocated to other traits that enhance reproductive success.     

Effect of water stress on abundance of twospotted spider mite on soybeans under greenhouse conditions

A rope wick technique was used to establish different levels of water stress in potted, greenhouse-grown soybean, Glycine max (L.) Merrill, plants. Water stress reduced, within a single generation, the overall abundance (number of mites/cm² leaf) of the twospotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae) and particularly influenced female mites and eggs. Mites were most numerous in the upper strata of soybean plants on youger and possibly more nutritious leaves.

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Influence de l'arrosage sur l'abondance de Tetranychus urticae sur soja, Glycine max en serre

Résumé Un arrosage par capillarité contrôlé a été utilisé pour maintenir différentes teneurs en eau dans des pieds empotés de G. max. Le stress hydrique a réduit, en une génération, la densité de T. urticae (nombre d'acariens/cm² de feuille), et particulièrement celle des femelles et des oeufs. Les acariens étaient plus nombreux sur les feuilles les plus jeunes et peut-être les plus nutritives des strates supérieures des pieds de soja.