Interactions in a tritrophic acarine predator-prey metapopulation system IV: effects of host plant condition on Tetranychus urticae (Acari: Tetranychidae)

Feeding by spider mites can cause severe injury to a host plant and lead to a decreasing per capita growth rate and an increasing per capita emigration rate. Such density-dependent responses to local conditions are important in a metapopulation context because they allow the herbivores to colonize new host plants and thereby prolong the time until regional (metapopulation) extinction. In order to include density-dependent responses of the two-spotted spider mite (Tetranychus urticae) in a realistic metapopulation model, a series of greenhouse experiments was conducted with the purpose to quantify how the condition of bean plants (Phaseolus vulgaris) influences the demographic parameters of T. urticae. Plant age per se reduced the growth rate of the spider mites only slightly, whereas the growth rate declined significantly as the plants were injured by the mites. The relationships between plant condition (expressed by the plant injury index D) and the birth and loss (death + emigration) rates of the mites were quantified so as to predict population growth as a function of D. Maximum per capita growth rate (r) was estimated to be c. 0.21 day⁻¹. The growth rate is expected to be negative when D exceeds 0.8. When mites were allowed to emigrate to neighbouring plants via bridges, the per capita emigration rate increased almost exponentially with D. The proportion of eggs in the population decreased with D while the numerical ratio between immatures to adults and the sex ratio did not change with D. Overall, immatures and adults constituted 74% and 26%, respectively, of the active mites and c. 46% of the adults were males. The bridges that connected a donor plant with the surrounding recipient plants were responsible for the majority of the emigrations from donor plants. Most mites stopped after having crossed a single bridge, but a few crossed two bridges while none crossed three bridges within 24 h. The significance of the results for biological control is discussed. This revised version was published online in July 2006 with corrections to the Cover Date.     

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.     

Host plant-mediated interactions between Tetranychus urticae and Eotetranychus carpini borealis (Acari: Tetranychidae)

Competitive interactions between Tetranychus urticae and Eotetranychus carpini borealis were investigated under laboratory and greenhouse conditions. When placed first to colonize red raspberry leaves, T. urticae caused extinction of E. carpini borealis populations. E. carpini borealis had detrimental effects on T. urticae but did not cause T. urticae population extinction. The area used by E. carpini borealis for egg deposition decreased with an increase in the number of T. urticae eggs. Red raspberry showed an induced response to T. urticae and E. carpini borealis feeding after two weeks of infestation. Population growth of each species was reduced on plants that were previously infested by conspecifics but inducible response by one species had no effects on the other species.     

Evaluation of Vigna angularis (Willd.) Ohwi and Ohashi accessions for resistance to Tetranychus urticae Koch (Acari:Tetranychidae)

Under laboratory conditions 88 azuki bean and three rice bean accessions were evaluated with a leaf-disc technique to select for those which expressed an antibiotic response to the TSSM ovipositional rate. Nine of the most promising accessions determined in the screening and Erimo, a commercial cultivar used as a control, were re-evaluated to determine the ovipositional rate and fecundity. Statistically significant differences between accessions were found: some of the accessions exhibited a reduced TSSM ovipositional rate and fecundity when compared with the susceptible control. The accessions ADZU279 and ADZU514 from Japan and ADZU577 from Ivory Coast demonstrated strong inhibition to TSSM fecundity. These three accessions may possess inherent potential in a breeding programme designed to enhance resistance to T. urticae.     

Genetic distinctness between two forms of Tetranychus urticae Koch (Acari: Tetranychidae) detected by electrophoresis

The genetic relatedness between the green and red forms of the two-spotted spider mite, Tetranychus urticae Koch, was analysed using an allozyme marker, MDH, detected by polyacrylamide gel electrophoresis. Cross experiments showed that each of the two forms had form-specific alleles for MDH. Furthermore, there was no overlapping in the alleles for MDH between the field populations of the two forms, suggesting that no gene flow would occur between them in the field.     

The effect of host plants on Tetranychus evansi, Tetranychus urticae (Acari: Tetranychidae) and on their fungal pathogen Neozygites floridana (Entomophthorales: Neozygitaceae)

In a series of tritrophic-level interaction experiments, the effect of selected host plants of the spider mites, Tetranychus evansi and Tetranychus urticae, on Neozygites floridana was studied by evaluating the attachment of capilliconidia, presence of hyphal bodies in the infected mites, mortality from fungal infection, mummification and sporulation from fungus-killed mite cadavers. Host plants tested for T. evansi were tomato, cherry tomato, eggplant, nightshade, and pepper while host plants tested for T. urticae were strawberry, jack bean, cotton and Gerbera. Oviposition rate of the mites on each plant was determined to infer host plant suitability while host-switching determined antibiosis effect on fungal activity. T. evansi had a high oviposition on eggplant, tomato and nightshade but not on cherry tomato and pepper. T. urticae on jack bean resulted in a higher oviposition than on strawberry, cotton and Gerbera. Attachment of capilliconidia to the T. evansi body, presence of hyphal bodies in infected T. evansi and mortality from fungal infection were significantly higher on pepper, nightshade and tomato. The highest level of T. evansi mummification was observed on tomato. T. evansi cadavers from tomato and eggplant produced more primary conidia than those from cherry tomato, nightshade and pepper. Switching N. floridana infected T. evansi from one of five Solanaceous host plants to tomato had no prominent effect on N. floridana performance. For T. urticae, strawberry and jack bean provided the best N. floridana performance when considering all measured parameters. Strawberry also had the highest primary conidia production. This study shows that performance of N. floridana can vary with host plants and may be an important factor for the development of N. floridana epizootics.     

Interactions in a trirophic acarine predator-prey metapopulation system: effects of Tetranychus urticae on the dispersal rates of Phytoseiulus persimilis (Acarina: Tetranychidae, Phytoseiidae)

The dispersal behaviour of the predatory mite Phytoseiulus persimilis Athias-Henriot between bean plants was studied in a greenhouse. The aim of the study was to estimate the rate of predator emigration affected by different densities of Tetranychus urticae Koch and different numbers of between-plant connections (bridges). The results show that predators emigrate from a plant almost exclusively as a response to the local prey density whereas the loss rate (the per capita rate at which predators disappear from the system) also depends on the prey density on the surrounding plants, provided they are connected to the central plant by bridges. © Rapid Science Ltd. 1998     

Behavioural response and winter survival of mated and unmated diapausing females of the Tetranychus atlanticus-urticae complex (Acari, Tetranychidae)

Behavioural responses were studied in mated and unmated females of a Dutch strain of the spider mite Tetranychus urticae which were destined to enter diapause. Observations were confined to the period between acquirement of the winter coloration by the females (a few days after the last moult) and their entering of artificial hibernation sites offered to the mites on the host leaves. Unmated females were found to stay longer on the leaf surface than mated females; they entered the hibernation sites significantly later than mated females. The delay in the search for hibernation sites shown by unmated females may be seen as a behavioural adaptation to enhance the chance of being fertilized before hibernation. Winter survival of mated and unmated diapausing females of the same strain of mites was studied both in the laboratory at a constant temperature of 2±1°C and outdoors under natural climatic conditions in Amsterdam during the winter of 1990–1991. Survival was high under both conditions for mated as well as unmated females; no significant differences in survival were found between both types of female. Observations on post-diapause females of Tetranychus atlanticus (a mite belonging to the T. urticae complex) sampled from strawberry fields near Moscow in spring, showed that at most 10% of the females of this natural spider mite population were unmated. Both mated and unmated females had survived winter temperatures of -28 to -30°C.     

Sublethal effects of esfenvalerate residues on pyrethroid resistant Typhlodromus pyri (Acari: Phytoseiidae) and its prey Panonychus ulmi and Tetranychus urticae (Acari: Tetranychidae)

The effect of residues of esfenvalerate on oviposition of the resistant strain of the predatory mite Typhlodromus pyri and its main prey, European red mite Panonychus ulmi and two-spotted spider mite Tetranychus urticae, were investigated. T. pyri showed a significant linear reduction in oviposition after 24h in the presence of increasing levels of esfenvalerate residue applied at the field rate. Furthermore, when given a choice, T. pyri preferred to lay eggs on residue-free surfaces. Of the two prey species, only P. ulmi showed significant avoidance of increasing levels of residues of the field rate concentration of esfenvalerate, as measured by runoff mortality, however both P. ulmi and T. urticae, when given a choice, showed a preference for esfenvalerate-free surfaces. As with the predatory mite T. pyri, both prey species showed a significant linear reduction of oviposition with increasing esfenvalerate residues and a preference to lay eggs on esfenvalerate-free surfaces. Esfenvalerate residues as high as 15X field rate were not repellent to pyrethroid-resistant T. pyri. The possible effects of these sublethal effects on predator-prey dynamics and implications for integrated mite control programmes in apple orchards are discussed.     

Prey stage preference and functional response of Euseius hibisci to Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae)

The aims of this study were: (a) determine the prey stage preference of female Euseius hibisci (Chant) (Phytoseiidae) at constant densities of different stages of Tetranychus urticae Koch (Tetranychidae), (b) assess the functional response of the predator females to the varying densities of eggs, larvae, or protonymphs of T. urticae, and (c) estimate the functional response of E. hibisci when pollen of Ligustrum ovalifolium was present as well. We conducted experiments on excised pieces of strawberry leaf arenas (Fragaria ananassa) under laboratory conditions of 25 ± 2 °C, 60 ± 5% RH and 12 h photophase. Our results indicated that the predator consumed significantly more prey eggs than other prey stages. Consumption of prey deutonymphs and adults was so low that they were excluded from the non-choice functional response experiments. The functional response on all food items was of type II. The two parameters of the functional response were estimated for each prey type by means of the adjusted non-linear regression model. The highest estimated value a (instantaneous rate of discovery) and the lowest value of T_h (handling time, including digestion) were found for the predator feeding on prey eggs, and a was lowest and T_h highest when fed protonymphs. Using the jack-knife method, the values for the functional response parameters were estimated. The values of a and T_h produced by the model were similar among all prey types except for the eggs, which were different. Using pollen simultaneously with prey larvae decreased the consumption of the latter over the full range of prey densities The suitability of this predator for biological control of T. urticae on strawberry is discussed.     

Microsatellite markers reveal spatial genetic structure of Tetranychus urticae (Acari: Tetranychidae) populations along a latitudinal gradient in Europe

The genetic structure of populations of the two-spotted spider mite Tetranychus urticae was investigated along a south–north European transect spanning from southern France to The Netherlands. Mites were collected on Urtica dioica in 6 sampling zones. Microsatellite variation at 5 loci revealed considerable genetic variation with an average heterozygozity of 0.49. Significant heterozygote deficiency was found in 7 populations out of the 18 samples analyzed and one of them was completely monomorphic. Tetranychus urticae populations show some level of genetic structuring. First, genetic differentiation between localities (F _ST estimates) was significant for all comparisons. Second, the analysis of molecular variance, AMOVA, indicates that there is an effect, albeit low (9%), of the locality in accounting for allele frequency variance. Geographic distance emerges as a factor responsible for this genetic structure. The results are discussed in relation to the biological features of the species and the known patterns of migration. Related agronomical issues are addressed.     

Spider mite (Acari: Tetranychidae) mitochondrial COI phylogeny reviewed: host plant relationships,phylogeography, reproductive parasites and barcoding

The past 15 years have witnessed a number of molecular studies that aimed to resolve issues of species delineation and phylogeny of mites in the family Tetranychidae. The central part of the mitochondrial COI region has frequently been used for investigating intra- and interspecific variation. All these studies combined yield an extensive database of sequence information of the family Tetranychidae. We assembled this information in a single alignment and performed an overall phylogenetic analysis. The resulting phylogeny shows that important patterns have been overlooked in previous studies, whereas others disappear. It also reveals that mistakes were made in submitting the data to GenBank, which further disturbed interpretation of the data. Our total analysis clearly shows three clades that most likely correspond to the species T. urticae, T. kanzawai and T. truncatus. Intraspecific variation is very high, possibly due to selective sweeps caused by reproductive parasites. We found no evidence for host plant associations and phylogeographic patterns in T. urticae are absent. Finally we evaluate the application of DNA barcoding.     

The effect of non-pathogenic phylloplane fungi on life-history traits of urticae (Acari: Tetranychidae)

The direct effect of three common non-pathogenic phylloplane fungi on the life-history traits of Tetranychus urticae Koch was investigated on intact leaves of the garden bean Phaseolus vulgaris L. (var. Tendergreen Improved), under conditions of low and high water-deficit stress. The survival rate of T. urticae was always reduced by an increase in water-deficit stress, whereas the effect of the fungi depended in part on the watering regime. On two of the three fungi tested, Alternaria alternata (Fr.) Keissler and Epicoccum nigrum Link, the mites showed a significant increase in net reproduction compared to those reared under control (i.e. no fungi added) conditions, independent of water-deficit stress, resulting in a higher intrinsic rate of increase. The third fungus tested, Cladosporium cladosporioides (Fres.) de Vries, had a similar response with respect to net reproduction when reared under low water-deficit stress but not when reared under a high water-deficit stress. There was, however, no evidence of an interactive effect with water-deficit stress and presence or absence of fungus affecting the net reproduction of the mites, for any of the three fungal species tested. An interactive effect between fungal species and water-deficit stress was observed for the intrinsic rate of increase of the mites. It is suspected that the fungi are acting as a source of an otherwise limiting resource and the differences observed between the fungal treatments is due to differences in consumption, based on the different sizes of their conidia.     

Local variation in diapause characteristics of Tetranychus urticae Koch (Acarina: Tetranychidae)

Summary Diapause characteristics of nine local populations of Tetranychus urticae Koch (Acarina: Tetranychidae) occurring on rose in central Japan were investigated. The percentage of females that entered diapause at 18° C and 9L: 15D photoperiod ranged between 0 and 77%. In addition, both photoperiodic and temperature responses varied widely among these populations. We suggest that temperature response might be a better trait than photoperiodic response for selection among local populations. Females in diapause survived –24° C better than those that were not. However, no difference in cold hardiness among these populations was found. The mite responded rapidly to artificial selection for low and high diapause percentage. The response was asymmetrical, being easier in the direction of low diapause percentage. Reciprocal and back crosses using selected low and high diapause percentage cultures showed that the genetic control of diapause was complicated. Neither the lowdiapause nor the high-diapause trait dominated over the other. However, the low-diapause trait seemed to be stronger. The results of this study suggest that variation in diapause response is maintained by (1) adaptation to local environments and (2) the complexity of the genetics of diapause. Such variation may provide the genetic raw material for natural selection and is a prerequisite for the extension of ecological range.     

Potentiation of a propargite and fenpyroximate mixture against two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae)

Using susceptible and resistant reference strains and standard bioassay methods a new miticide product was screened for efficacy and cross-resistance against two-spotted spider mite, Tetranychus urticae Koch. Experimental product NN1 850.0 EW (fenpyroximate and propargite 3:10 ratio) was significantly (P<0.05) more toxic than either compound tested alone (co-toxicity index 1029). Non-overlapping 95% CIs at the LC₅₀ and LC₉₉ level suggest that there is no cross-resistance to NN1 850.0 EW from existing organophosphate and pyrethroid resistance. NN1 850.0 EW is worthy of further development for T. urticae control.     

Physiological effect of the host plant on the suitability ofTetranychus urticae as prey forPhytoseiulus persimilis [Acari: Tetranychidae,Phytoseiidae]

Weight gain of adult femalesPhytoseiulus persimilis Athias-Henriot was determined after they were fed eggs or adult females ofTetranychus urticae Koch reared on either Lima bean (Phaseolus vulgaris L.) or nightshade (Solanum douglasii Dunal). No significant difference was found when the predator was fed eggs ofT. urticae reared on either host. Predators were heavier when fed adult femaleT. urticae reared on bean. Apparently, a factor determining the prey's suitability is incorporated into its hemolymph or tissues and is not restricted to its gut content.      

Microbial diversity in the predatory mite Metaseiulus occidentalis (Acari: Phytoseiidae) and its prey, Tetranychus urticae (Acari: Tetranychidae)

Microorganisms associated with the predatory mite Metaseiulus (=Typhlodromus or Galendromus) occidentalis (Nesbitt) and its prey, the two-spotted spider mite Tetranychus urticae (Koch), were assessed using a high-fidelity polymerase chain reaction (PCR) protocol and primers designed to identify Eubacteria, Archaeabacteria, iridoviruses, Helicosporidia, Cytophaga-like microorganisms, Wolbachia and its bacteriophage WO, fungi and yeast-like organisms. Sequences from four bacterial species related to Wolbachia (α-Proteobacteria), Cardinium, Bacteroidetes, and Enterobacter (γ-Proteobacteria) were obtained from M. occidentalis, and three sequences related to Wolbachia, Rickettsia, and Caulobacter (α-Proteobacteria) were obtained from T. urticae. No nucleotide differences were detected between the 16S rRNA, wspA or wspB Wolbachia sequences obtained from M. occidentalis and T. urticae, which suggest that horizontal transfer of Wolbachia could have occurred. Southern blot analyses of genomic DNA from both M. occidentalis and T. urticae using wspA probes were negative, indicating that this Wolbachia sequence is not integrated into the nuclear genome of either species. Two of the T. urticae colonies tested contained the WO bacteriophage, but none of the six M. occidentalis populations were infected. New M. occidentalis-specific forward and reverse 16S rRNA primers based on the Wolbachia, Cardinium, Bacteroidetes, and Enterobacter sequences obtained were designed and used to amplify PCR products from each of two laboratory and four field-collected samples of M. occidentalis females and eggs, indicating that these infections are widespread. Likewise, species-specific primers for T. urticae were designed for the Wolbachia, Rickettsia, and Caulobacter sequences obtained and used to evaluate T. urticae from strawberries, wine grapes, hops, almonds, and cherries from California, Washington, and Florida; all were positive for Wolbachia and Caulobacter but two of the six were negative for Rickettsia. None of the M. occidentalis colonies tested were positive for the microsporidium Oligosporidium occidentalis, which previously had been associated with a pathogenic condition in some of our laboratory colonies. The Gainesville colonies of M. occidentalis and T. urticae were negative for iridovirus, Archaeabacteria, fungi, Helicosporidia, and yeast-like organisms. So far, Wolbachia is the only symbiont that is shared by this predator and its prey.     

Coexistence of Tetranychus urticae (Acarina: Tetranychidae) with different capacities for diapause: comparative life-history traits

Summary Individuals of the two-spotted spider mite, Tetranychus urticae Koch (Acarina: Tetranychidae), with and without a capacity for diapause, coexist in central Japan. Diapause appears to be adaptive because females in diapause suffered less mortality than non-diapausing individuals when frozen at –24°C for more than 4 h. However non-diapausing females showed good survival up to 4 h of freezing. Active non-diapausing mites survived on rose leaves in Kyoto (35°N) throughout the winters of 1988–1989 and 1989–1990. Cultures of mites with low (LD) and high (HD) diapause capacities at 18°C and 9L-15D photoperiod were successfully selected from the rose population and from a population on chrysanthemum in Nara (34.4°N). Their life-history traits at 15, 20, 25 and 30°C were characterized. HD and LD mites from both populations were of similar ages at first reproduction at 15–30° C. However, at temperatures 20° C, HD individuals produced more eggs than LD individuals, resulting in higher fecundity and intrinsic rate of natural increase. These traits allow HD individuals, which stop breeding between October and April, to increase faster in summer than LD individuals. This provides a mechanism, together with climatic fluctuations, in maintaining the coexistence of diapausing and non-diapausing T. urticae in Kyoto where winter conditions are rarely lethal to the non-diapausing individuals.     

The locomotor activities on sites covered by silk produced by related and unrelated spider mites in Tetranychus urticae (Acari: Tetranychidae)

The two-spotted spider mite Tetranychus urticae is a silk producer known to live in groups with a common silk web that can cover entire plants and protect mites against predators, rain and wind. Silk also plays an important role during collective migration by aerial dispersal or by walking. In this context, we studied the locomotor activity i.e. time in movement, in resting, and in static exploration (probing behaviour) of an individual confronted to clean places and/or places covered by silk coming from its own population or from another. Two populations were tested, one of the red form (Tunisia) and another of the green form (Belgium). The experimental results showed that the presence or the absence of silk did not influence the relative proportion of each behavioural item either for the red or the green population. Individuals of the green form population spent more time moving and less time resting than individuals of the red form population and this, whatever the substrate (red/green silk, clean). Moreover, the silk from the red form population attracted individuals from both populations, whereas the silk produced by the green form population did not attract any individual either from the red or the green form. This surprising result might have been due to a difference in the quantity and/or quality of silk woven by the two forms. We discuss how the differences observed in the behaviour of these two populations may result from differences in their strategy to rapidly increase the population of the colony and reinforce the silk nest.     

Life history of the predatory mite <Emphasis Type="Italic">Phytoseiulus fragariae</Emphasis> on <Emphasis Type="Italic">Tetranychus evansi</Emphasis> and <Emphasis Type="Italic">Tetranychus urticae</Emphasis> (Acari: Phytoseiidae,Tetranychidae) at five temperatures

Tetranychus evansi Baker and Pritchard and Tetranychus urticae Koch (Acari: Tetranychidae) are important pests of Solanaceae in many countries. Several studies have demonstrated that T. urticae is an acceptable prey to many predatory mites, although the suitability of this prey depends on the host plant. T. evansi, has been shown to be an unfavorable prey to most predatory mites that have been tested against it. The predator Phytoseiulus fragariae Denmark and Schicha (Acari: Phytoseiidae) has been found in association with the two species in Brazil. The objective of this work was to compare biological parameters of P. fragariae on T. evansi and on T. urticae as prey. The study was conducted under laboratory conditions at 10, 15, 20, 25 and 30°C. At all temperatures, survivorship was lower on T. evansi than on T. urticae. No predator reached adulthood at 10°C on the former species; even on the latter species, only about 36% of the predators reached adulthood at 10°C. For both prey, in general, duration of each life stage was shorter, total fecundity was lower and intrinsic rate of population increase (r _m ) was higher with increasing temperatures. The slower rate of development of P. fragariae on T. evansi resulted in a slightly higher thermal requirement (103.9 degree-days) on that prey than on T. urticae (97.1 degree-days). The values of net reproduction rate (R ₀), intrinsic rate of increase (r _m ) and finite rate of increase (λ) were significantly higher on T. urticae, indicating faster population increase of the predator on this prey species. The highest value of r _m of the predator was 0.154 and 0.337 female per female per day on T. evansi and on T. urticae, respectively. The results suggested that P. fragariae cannot be considered a good predator of T. evansi.