Polyphagous Spider Mite Research Articles

Are predatory mites effective as biological control agents to suppress Oligonychus ilicis (Acari: Tetranychidae) in blueberry plantings?

Southern red mite, Oligonychus ilicis McGregor (Acari: Tetranychidae), is an important polyphagous spider mite pest that causes economic damage to many ornamentals, coffee, and fruit crops. Blueberry growers in the Southeastern United States, including Florida and Georgia, have experienced severe losses due to outbreaks of O. ilicis. Predatory mites are an important management tool used for controlling spider mites; however, predators have not been studied and successfully evaluated in blueberry systems. Amblyseius swirskii Athias-Henriot, Phytoseiulus persimilis Athias-Henriot, and Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) are among the most economically important arthropod agents used in augmentative biological control worldwide. To evaluate the potential of these 3 commercially available predatory mites for use in blueberry plantings, we conducted experiments under controlled laboratory conditions and in the greenhouse. In preliminary laboratory experiments, P. persimilis and N. californicus significantly reduced the number of O. ilicis motile stages below those found in the untreated control, indicating the potential for these 2 predatory mite species to suppress O. ilicis populations. Amblyseius swirskii did not perform well controlling O. ilicis motiles in the laboratory. Under greenhouse conditions, N. californicus and P. persimilis significantly reduced the number of eggs after 7 days of release and the number of motile stages after 14 days of release. This is the first report of using phytoseiid mites to suppress O. ilicis in blueberry systems in the United States. Further studies on predator behavior, feeding preferences, and acaricide compatibility with predators are required to investigate the possibility of using P. persimilis, and N. californicus as biological control agents of O. ilicis in blueberry systems.

Structural and functional characterization of β-cyanoalanine synthase from Tetranychus urticae

Tetranychus urticae is a polyphagous spider mite that can feed on more than 1100 plant species including cyanogenic plants. The herbivore genome contains a horizontally acquired gene tetur10g01570 (TuCAS) that was previously shown to participate in cyanide detoxification. To understand the structure and determine the function of TuCAS in T. urticae, crystal structures of the protein with lysine conjugated pyridoxal phosphate (PLP) were determined. These structures reveal extensive TuCAS homology with the β-substituted alanine synthase family, and they show that this enzyme utilizes a similar chemical mechanism involving a stable α-aminoacrylate intermediate in β-cyanoalanine and cysteine synthesis. We demonstrate that TuCAS is more efficient in the synthesis of β-cyanoalanine, which is a product of the detoxification reaction between cysteine and cyanide, than in the biosynthesis of cysteine. Also, the enzyme carries additional enzymatic activities that were not previously described. We show that TuCAS can detoxify cyanide using O-acetyl-L-serine as a substrate, leading to the direct formation of β-cyanoalanine. Moreover, it catalyzes the reaction between the TuCAS-bound α-aminoacrylate intermediate and aromatic compounds with a thiol group. In addition, we have tested several compounds as TuCAS inhibitors. Overall, this study identifies additional functions for TuCAS and provides new molecular insight into the xenobiotic metabolism of T. urticae.

Delta class glutathione S-transferase (TuGSTd01) from the two-spotted spider mite Tetranychus urticae is inhibited by abamectin

GSTs (Glutathione S-transferases) are known to catalyze the nucleophilic attack of the sulfhydryl group of reduced glutathione (GSH) on electrophilic centers of xenobiotic compounds, including insecticides and acaricides. Genome analyses of the polyphagous spider mite herbivore Tetranychus urticae (two-spotted spider mite) revealed the presence of a set of 32 genes that code for secreted proteins belonging to the GST family of enzymes. To better understand the role of these proteins in T. urticae, we have functionally characterized TuGSTd01. Moreover, we have modeled the structure of the enzyme in apo form, as well as in the form with bound inhibitor. We demonstrated that this protein is a glutathione S-transferase that can conjugate glutathione to 1-chloro-2,4-dinitrobenzene (CDNB). We have tested TuGSTd01 activity with a range of potential substrates such as cinnamic acid, cumene hydroperoxide, and allyl isothiocyanate; however, the enzyme was unable to process these compounds. Using mutagenesis, we showed that putative active site variants S11A, E66A, S67A, and R68A mutants, which were residues predicted to interact directly with GSH, have no measurable activity, and these residues are required for the enzymatic activity of TuGSTd01. There are several reports that associate some T. urticae acaricide resistance with increased activity of GSTs . However, we found that TuGSTd01 is not able to detoxify abamectin; in fact, the acaricide inhibits the enzyme with Ki = 101 μM. Therefore, we suggest that the increased GST activity observed in abamectin resistant T. urticae field populations is a part of the compensatory feedback loop. In this case, the increased production of GSTs and relatively high concentration of GSH in cells allow GSTs to maintain physiological functions despite the presence of the acaricide.

Structural and functional characterization of an intradiol ring-cleavage dioxygenase from the polyphagous spider mite herbivore Tetranychus urticae Koch

Genome analyses of the polyphagous spider mite herbivore Tetranychus urticae (two-spotted spider mite) revealed the presence of a set of 17 genes that code for secreted proteins belonging to the “intradiol dioxygenase-like” subgroup. Phylogenetic analyses indicate that this novel enzyme family has been acquired by horizontal gene transfer. In order to better understand the role of these proteins in T. urticae, we have structurally and functionally characterized one paralog (tetur07g02040). It was demonstrated that this protein is indeed an intradiol ring-cleavage dioxygenase, as the enzyme is able to cleave catechol between two hydroxyl-groups using atmospheric dioxygen. The enzyme was characterized functionally and structurally. The active site of the T. urticae enzyme contains an Fe3+ cofactor that is coordinated by two histidine and two tyrosine residues, an arrangement that is similar to those observed in bacterial homologs. However, the active site is significantly more solvent exposed than in bacterial proteins. Moreover, the mite enzyme is monomeric, while almost all structurally characterized bacterial homologs form oligomeric assemblies. Tetur07g02040 is not only the first spider mite dioxygenase that has been characterized at the molecular level, but is also the first structurally characterized intradiol ring-cleavage dioxygenase originating from a eukaryote.

Dehydration Stress Contributes to the Enhancement of Plant Defense Response and Mite Performance on Barley.

Under natural conditions, plants suffer different stresses simultaneously or in a sequential way. At present, the combined effect of biotic and abiotic stressors is one of the most important threats to crop production. Understanding how plants deal with the panoply of potential stresses affecting them is crucial to develop biotechnological tools to protect plants. As well as for drought stress, the economic importance of the spider mite on agriculture is expected to increase due to climate change. Barley is a host of the polyphagous spider mite Tetranychus urticae and drought produces important yield losses. To obtain insights on the combined effect of drought and mite stresses on the defensive response of this cereal, we have analyzed the transcriptomic responses of barley plants subjected to dehydration (water-deficit) treatment, spider mite attack, or to the combined dehydration-spider mite stress. The expression patterns of mite-induced responsive genes included many jasmonic acid responsive genes and were quickly induced. In contrast, genes related to dehydration tolerance were later up-regulated. Besides, a higher up-regulation of mite-induced defenses was showed by the combined dehydration and mite treatment than by the individual mite stress. On the other hand, the performance of the mite in dehydration stressed and well-watered plants was tested. Despite the stronger defensive response in plants that suffer dehydration and mite stresses, the spider mite demonstrates a better performance under dehydration condition than in well-watered plants. These results highlight the complexity of the regulatory events leading to the response to a combination of stresses and emphasize the difficulties to predict their consequences on crop production.

Enormous expansion of the chemosensory gene repertoire in the omnivorous German cockroach Blattella germanica.

The acquisition of genome sequences from a wide range of insects and other arthropods has revealed a broad positive correlation between the complexity of their chemical ecology and the size of their chemosensory gene repertoire. The German cockroach Blattella germanica is an extreme omnivore and has the largest chemosensory gene repertoire known for an arthropod, exceeding even the highly polyphagous spider mite Tetranychus urticae. While the Odorant Receptor family is not particularly large, with 123 genes potentially encoding 134 receptors (105 intact), the Gustatory Receptor family is greatly expanded to 431 genes potentially encoding 545 receptors (483 intact), the largest known for insects and second only to the spider mite. The Ionotropic Receptor family of olfactory and gustatory receptors is vastly expanded to at least 897 genes (604 intact), the largest size known in arthropods, far surpassing the 150 known from the dampwood termite Zootermopsis nevadensis. Commensurately, the Odorant Binding Protein family is expanded to the largest known for insects at 109 genes (all intact). Comparison with the far more specialized, but phylogenetically related termite, within the Dictyoptera, reveals considerable gene losses from the termite, and massive species‐specific gene expansions in the cockroach. The cockroach has lost function of 11%–41% of these three chemoreceptor gene families to pseudogenization, and most of these are young events, implying rapid turnover of genes along with these major expansions, presumably in response to changes in its chemical ecology.

Effects of host plant on life-history traits in the polyphagous spider mite Tetranychus urticae.

Studying antagonistic coevolution between host plants and herbivores is particularly relevant for polyphagous species that can experience a great diversity of host plants with a large range of defenses. Here, we performed experimental evolution with the polyphagous spider mite Tetranychus urticae to detect how mites can exploit host plants. We thus compared on a same host the performance of replicated populations from an ancestral one reared for hundreds of generations on cucumber plants that were shifted to either tomato or cucumber plants. We controlled for maternal effects by rearing females from all replicated populations on either tomato or cucumber leaves, crossing this factor with the host plant in a factorial design. About 24 generations after the host shift and for all individual mites, we measured the following fitness components on tomato leaf fragments: survival at all stages, acceptance of the host plant by juvenile and adult mites, longevity, and female fecundity. The host plant on which mite populations had evolved did not affect the performance of the mites, but only affected their sex ratio. Females that lived on tomato plants for circa 24 generations produced a higher proportion of daughters than did females that lived on cucumber plants. In contrast, maternal effects influenced juvenile survival, acceptance of the host plant by adult mites and female fecundity. Independently of the host plant species on which their population had evolved, females reared on the tomato maternal environment produced offspring that survived better on tomato as juveniles, but accepted less this host plant as adults and had a lower fecundity than did females reared on the cucumber maternal environment. We also found that temporal blocks affected mite dispersal and both female longevity and fecundity. Taken together, our results show that the host plant species can affect critical parameters of population dynamics, and most importantly that maternal and environmental conditions can facilitate colonization and exploitation of a novel host in the polyphagous T. urticae, by affecting dispersal behavior (host acceptance) and female fecundity.

A link between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae.

Plants produce a wide range of allelochemicals to defend against herbivore attack, and generalist herbivores have evolved mechanisms to avoid, sequester, or detoxify a broad spectrum of natural defense compounds. Successful arthropod pests have also developed resistance to diverse classes of pesticides and this adaptation is of critical importance to agriculture. To test whether mechanisms to overcome plant defenses predispose the development of pesticide resistance, we examined adaptation of the generalist two-spotted spider mite, Tetranychus urticae, to host plant transfer and pesticides. T. urticae is an extreme polyphagous pest with more than 1,100 documented hosts and has an extraordinary ability to develop pesticide resistance. When mites from a pesticide-susceptible strain propagated on bean were adapted to a challenging host (tomato), transcriptional responses increased over time with ~7.5% of genes differentially expressed after five generations. Whereas many genes with altered expression belonged to known detoxification families (like P450 monooxygenases), new gene families not previously associated with detoxification in other herbivores showed a striking response, including ring-splitting dioxygenase genes acquired by horizontal gene transfer. Strikingly, transcriptional profiles of tomato-adapted mites resembled those of multipesticide-resistant strains, and adaptation to tomato decreased the susceptibility to unrelated pesticide classes. Our findings suggest key roles for both an expanded environmental response gene repertoire and transcriptional regulation in the life history of generalist herbivores. They also support a model whereby selection for the ability to mount a broad response to the diverse defense chemistry of plants predisposes the evolution of pesticide resistance in generalists.

Eotetranychus lewisi

<i>Eotetranychus lewisi</i>

Development and Oviposition of Tetranychus pueraricola Ehara and Gotoh (Acari: Tetranychidae) on Various Plants

The spider mite Tetranychus pueraricola is widely distributed throughout Japan and it is common on kudzu vine but not on crops. Because this species has the second highest rm-value among tetranychid mites studied so far, there is a real possibility that T. pueraricola will get out of hand after invasion of agricultural crops. To better evaluate its potential severity as a pest, we examined the host range of five populations collected from kudzu vine. On leaf discs juvenile survival to adulthood was assessed, as well as egg production of young females over a period of five days. Out of 23 potential host plant species in 12 families tested, 70% or more larvae attained maturity and 15 or more eggs were subsequently laid by mites of all five populations on nine plantspecies (soybean, lima bean, kidney bean, kudzu vine, cowpea, spinach, apricot, rose and mulberry), whereas no or few larvae attained maturity on another four species (cucumber, tomato, chrysanthemum and Satsuma mandarin). On watermelon, strawberry and eggplant four of the five populations performed well. These results indicate that T. pueraricola has a broad potential host plant range, just like other polyphagous spider mite species, which are all serious pests. Its broad host range plus the second highest rm-value among Tetranychus species, suggest that this species has the potential to become a serious pest on agricultural crops.

Density dependent population growth of the two‐spotted spider mite, Tetranychus urticae, on the host plant Leonurus cardiaca

We observed Tetranychus urticae (Koch), a polyphagous spider mite herbivore, on Leonurus cardiaca (L.) at several sites in eastern North America at variable density, ranging from extremely dense to sparse. To understand the nature of T. urticae's population dynamics we experimentally manipulated population densities on L. cardiaca and assessed per capita growth after 1 to 2 generations in laboratory and field experiments. In particular, we took a ‘bottom‐up’ approach, manipulating both plant size and quality to examine effects on mite dynamics. Per capita growth was strongly dependent on the initial density of the mite population. Spider mite populations grew (1) in a negatively density dependent manner on small plants and (2) unhindered by density dependence on large plants. Mean per capita growth was 59% higher on small plants compared to large plants, irrespective of mite density. We also found evidence for density dependent induced susceptibility to spider mites in small plants and density dependent induced resistance in large plants. Hence, spider mite populations grew at a relatively fast rate on small plants, and this was associated with negative density dependence due to factors that depress population growth, such as food deterioration or limitation. On large plants, spider mite populations grew at a relatively slow rate, apparently resulting in herbivore densities that may not have been high enough to cause intraspecific competition or other forms of negative density dependence.

Induction of Preference and Performance after Acclimation to Novel Hosts in a Phytophagous Spider Mite: Adaptive Plasticity?

We examined induction of preference and performance on novel host plants for two laboratory populations of the polyphagous spider mite Tetranychus urticae, with one population adapted to bean and the other population adapted to tomato. We bred four isofemale lines of the bean population only and used them in all the assays. The bean population had a 30% lower fecundity on tomato than on bean, while the tomato population had equal fecundity on both host plants. Acclimation of adult females to the novel host plant for both populations increased acceptability of that novel host but did not increase rejection of the original host. The bean population experienced a 60% benefit and a 30% cost in terms of egg production for acclimating to tomato, thus exemplifying adaptive plasticity. The tomato population showed a 23% benefit for acclimating to bean but no cost. Mites from the bean population that were acclimated to tomato fed more on tomato than did mites that were not acclimated to tomato. When these mites were fed inhibitors of cytochrome P-450 detoxification enzymes, their performance was severely depressed (84%) on tomato but not on bean. However, mites that were fed inhibitors of P-450 enzymes did not reduce their acceptance of tomato as a host. Thus, performance on novel hosts (but not preference) in this species is likely correlated with the induction of detoxifying enzymes. Spider mites are known to form host races rapidly on novel hosts. Induction of preference and physiological acclimation via detoxification enzymes may enhance performance and, thus, strongly contribute to initial stages of host race formation.

Induction of Preference and Performance after Acclimation to Novel Hosts in a Phytophagous Spider Mite: Adaptive Plasticity?

We examined induction of preference and performance on novel host plants for two laboratory populations of the polyphagous spider mite Tetranychus urticae, with one population adapted to bean and the other population adapted to tomato. We bred four isofemale lines of the bean population only and used them in all the assays. The bean population had a 30% lower fecundity on tomato than on bean, while the tomato population had equal fecundity on both host plants. Acclimation of adult females to the novel host plant for both populations increased acceptability of that novel host but did not increase rejection of the original host. The bean population experienced a 60% benefit and a 30% cost in terms of egg production for acclimating to tomato, thus exemplifying adaptive plasticity. The tomato population showed a 23% benefit for acclimating to bean but no cost. Mites from the bean population that were acclimated to tomato fed more on tomato than did mites that were not acclimated to tomato. When these mites were fed inhibitors of cytochrome P‐450 detoxification enzymes, their performance was severely depressed (84%) on tomato but not on bean. However, mites that were fed inhibitors of P‐450 enzymes did not reduce their acceptance of tomato as a host. Thus, performance on novel hosts (but not preference) in this species is likely correlated with the induction of detoxifying enzymes. Spider mites are known to form host races rapidly on novel hosts. Induction of preference and physiological acclimation via detoxification enzymes may enhance performance and, thus, strongly contribute to initial stages of host race formation.

Host-related differences in diapause characteristics of different geographical populations of the Kanzawa spider mite, Tetranychus kanzawai Kishida(Acari: Tetranychidae), in Japan.

The incidence of diapause in the polyphagous spider mite Tetranychus kanzawai was determined for 65 populations derived from deciduous and herbaceous hosts and for 33 populations from tea, at 3 temperatures under short-day conditions. Most populations on the four main islands of Japan, irrespective of the host species on which they occurred, expressed more than 90% diapause at 15°C, whereas populations on the Okinawa islands exhibited a very low incidence or no diapause. The incidence of diapause decreased when temperature was increased from 18 to 20°C in populations from warmer areas such as southern Kyushu and Honshu. This temperature-dependent decline in diapause incidence was most conspicuous in populations from Tanegashima and Yakushima Islands. The incidence of diapause at 20°C tended to be lower in populations derived from tea than those from deciduous hosts in the same, warmer areas, showing that the former have a lower capacity for diapause. The present results, together with previously published data for T. urticae, showed that the lower temperature threshold for diapause induction was higher in T. kanzawai than in T. urticae and thus the clinal decrease in diapause percentage occurred at much lower latitudes in the former at 20°C.

Host-Range Evolution: Adaptation and Trade-Offs in Fitness of Mites on Alternative Hosts

Trade-offs in fitness on different host plants has been a central hypothesis in explaining the evolutionary specialization of herbivores. Surprisingly, only a few studies have documented such trade-offs. In this paper, I present results from a selection experiment that demonstrates trade-offs in host plant use for a polyphagous spider mite. Although adaptation to a novel poor-quality host did not result in detectable costs on a favorable host, spider mites that had adapted to a poor-quality host lost their ability to tolerate the poor-quality host when they were reverted to the favorable host for several generations. Trade-offs in fitness on alternative hosts among herbivorous spider mites remains one of the classic empirical examples of constraints on the evolution of host range. Adaptation to the novel poor-quality host was not associated with adaptation to a related host-plant species or to particular host-plant chemicals that I assayed. Thus, the complexity of host-plant defenses may restrict host shifts to single species of novel host plants, and adaptive zone shifts onto entire groups of plants predicted by the Ehrlich and Raven Model may be rare. Spider mite performance was genetically associated with host-plant preference. Mites from the control population showed a significant preference for the favorable host plant, whereas mites adapted to the novel host plant showed no preference. Finally, although induced plant responses to herbivory in the poor-quality host decreased the fitness of unselected mites, induced responses resulted in higher fitness of adapted mites. These results suggest that spider mites that rapidly adapt to particular host plants can overcome constitutive and inducible plant defenses.

HOST-RANGE EVOLUTION: ADAPTATION AND TRADE-OFFS IN FITNESS OF MITES ON ALTERNATIVE HOSTS

Trade-offs in fitness on different host plants has been a central hypothesis in explaining the evolutionary specialization of herbivores. Surprisingly, only a few studies have documented such trade-offs. In this paper, I present results from a selection experiment that demonstrates trade-offs in host plant use for a polyphagous spider mite. Although adaptation to a novel poor-quality host did not result in detectable costs on a favorable host, spider mites that had adapted to a poor-quality host lost their ability to tolerate the poor-quality host when they were reverted to the favorable host for several generations. Trade-offs in fitness on alternative hosts among herbivorous spider mites remains one of the classic empirical examples of constraints on the evolution of host range. Adaptation to the novel poor-quality host was not associated with adaptation to a related host-plant species or to particular host-plant chemicals that I assayed. Thus, the complexity of host-plant defenses may restrict host shifts to single species of novel host plants, and adaptive zone shifts onto entire groups of plants predicted by the Ehrlich and Raven Model may be rare. Spider mite performance was genetically associated with host-plant preference. Mites from the control population showed a significant preference for the favorable host plant, whereas mites adapted to the novel host plant showed no preference. Finally, although induced plant responses to herbivory in the poor-quality host decreased the fitness of unselected mites, induced responses resulted in higher fitness of adapted mites. These results suggest that spider mites that rapidly adapt to particular host plants can overcome constitutive and inducible plant defenses.

Interaction between life stages in a phytoseiid predator: western flower thrips prey killed by adults as food for protonymphs of Amblyseius cucumeris

Alternative feeding strategies are important in determining the lifestyle of polyphagous spider mite prodators, and could play a key role in their use for biocontrol of prey such as thrips. The small size of Amblyseius cucumeris relative to western flower thrips, Frankliniella occidentalis, limits its survival and development when this prey is the only food available. We show that when A. cucumeris nymphs were reared either alone or with a gravid female on live larvae of F. occidentalis as the only source of food, survival was increased and development was accelerated by the presence of the adult. Similar performance by predator nymphs reared alone on freshly killed thrips larvae indicated that those nymphs reared on live prey with an adult were benefiting from feeding on prey killed by the adult. Variation of the period when an adult female was present with the nymph showed that food provided as a result of the adult's preying activities was beneficial until approximately one third through nymphal development, after which protonymphs became independent predators, with good survival and rapid development when provided only with live F. occidentalis larvae. The results are discussed in relation to adult dispersal in specialist as opposed to generalist phytoseiids, and its potential manipulation in using A. cucumeris for thrips biocontrol.

Life History and Population Dynamics of Tetranychus tumidus in Florida (Acarina: Tetranychidae)

Tetranychus tumidus Banks, is a polyphagous spider mite that can thrive in the laboratory on over 70 host plants of various families, especially on many belonging to the Leguminosae, Malvaceae, Compositae and Gramineae; those in the Solanaceae appear unpalatable. The female mite developed slowly at 19@* C and required 21.5 days (20 for male) as compared to its development at 29@* C which required 8 days (7.5 days for male). At 24@* C the average daily rate of oviposition (4.21 eggs) and average number of eggs per female lifespan (49.67 eggs) were both higher than at 19 and 29@* C. Optimal temperatures appeared to be closer to 24 than to 29@* C. Field populations appeared in spring once morning low temperatures climbed into the upper teens and day-time highs into the twenties. Populations decreased in early summer and virtually disappeared when rains appearing in May and June established, together with the high temperature, optimal conditions for a spider mite fungus, Entomophthora, epidemic. Precipitation also reduced the population mechanically if occurring at 3 in. or more per 24 hr. The population remained practically negligible until early autumn when precipitation ceased. The 2nd population growth in autumn was halted and its decline commenced once temperatures dropped in October, or if prior to that, optimal conditions for fungus infection were established again. Phytoseiulus macropilis (Banks) was the only predator found in significant numbers among several predatory species recorded.