Evaluation of airborne methyl salicylate for improved conservation biological control of two-spotted spider mite and hop aphid in Oregon hop yards

The use of synthetic herbivore-induced plant volatiles (HIPV) to attract natural enemies has received interest as a tool to enhance conservation biological control (CBC). Methyl salicylate (MeSA) is a HIPV that is attractive to several key predators of two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), and hop aphid, Phorodon humuli (Schrank) (Homoptera: Aphididae). A 2-year study was conducted to evaluate the recommended commercial use of MeSA in hop yards in Oregon. Slow-release MeSA dispensers were stapled to supporting poles in 0.5 ha plots and these plots were compared to a paired non-treated plot on each of three farms in 2008 and 2009. Across both years, there was a trend for reduced (range 40–91%) mean seasonal numbers of T. urticae in five of the six MeSA-baited plots. Stethorus spp., key spider mite predators, tended to be more numerous in MeSA-baited plots compared to control plots on a given farm. Mean seasonal densities of hop aphid and other natural enemies (e.g., Orius spp. and Anystis spp.) were similar between MeSA-treated and control plots. Variability among farms in suppression of two-spotted spider mites and attraction of Stethorus spp. suggests that the use of MeSA to enhance CBC of spider mites in commercial hop yards may be influenced by site-specific factors related to the agroecology of individual farms or seasonal effects that require further investigation. The current study also suggests that CBC of hop aphid with MeSA in this environment may be unsatisfactory.     

Cost-benefits of reduced aphicide usage on dwarf hops susceptible and partially resistant to damson-hop aphid

Soil‐applied imidacloprid at full (125 g a.i. ha^?1) and half approved doses gave levels of control of damson‐hop aphid, (Phorodon humuli), similar to that provided by foliar spray(s) of tebufenpyrad on the aphid‐susceptible dwarf hop cvs First Gold and Herald. On those cultivars, aphid control was unreliable on plots treated with quarter dose imidacloprid and was generally no better than on untreated plants. Aphids were virtually eliminated from the leaves by the end of July each year in all treatments consistent with the action of natural enemies. Aphid contamination of cones reflected the numbers on foliage at flowering time, but varied widely between years. Yields and percentage α‐acids content of dried hops were unaffected by the numbers of aphids on leaves early in the season and in cones at harvest, but aphid contamination reduced the economic values of crops by as much as 80%. Few P. humuli colonised the partially aphid‐resistant breeding line 23/90/08 before their numbers were regulated and consistent with natural enemy activity. Yields, percentage α‐acids content, and commercial value of harvested cones were similar in all treatments on 23/90/08 whether or not plants were treated with aphicides. The commercial risks posed by P. humuli preclude substantial reductions in aphicide usage on aphid‐susceptible dwarf hop cultivars, but future cultivars expressing a similar level of partial resistance to aphids as 23/90/08 should not need treatment with aphicides.     

Evaluation of a damage threshold for two-spotted spider mites, Tetranychus urticae Koch (Acari: Tetranychidae), in hop culture

Damage caused by two‐spotted spider mites (Tetranychus urticae) at harvest to yield, quality (measured in percentage α‐acids content) and cone infestation was assessed on hop cvs Hallertauer Magnum, Hallertauer Tradition and Perle. Acaricide‐untreated hop plants with known levels of T. urticae infestation were compared with neighbouring acaricide‐treated plants. Although in 24 of the 36 experimental harvests the untreated hop plants had spider mite infestations of > 100 mites leaf^?1, yields and α‐acids content from the untreated plants were significantly lower than the treated plants in only four instances. However, although mite infestation of cones from untreated hops were significantly higher than acaricide‐treated plants in 27 of the 36 cases, in only one instance did that cause economic loss. Spider mite infestation levels of c. 90 mites leaf^?1 are tolerable at harvest time with little or no risk of causing economic loss to hop growers.     

Vertical dispersal of the two-spotted spider mite Tetranychus urticae, and the predatory mite Phytoseiulus persimilis on dwarf hops

1 The pattern of dispersion within plants of the two-spotted spider mite, Tetranychus urticae, and its predator, the phytoseiid Phytoseiulus persimilis, was studied on the dwarf hop variety First Gold from May to September in 1997 and 1998. 2 Spider mite populations developed on the lower leaves initially but, by late July, as the numbers of mites increased, most were found towards the top of plants. From early August, the numbers of spider mites decreased most rapidly on the upper parts of plants. 3 Where P. persimilis was released, the predator maintained the numbers of T. urticae below those found on non-release plots throughout the season. 4 By early August, the predator’s pattern of dispersion was similar to that of the pest. 5 Predators spread to non-release plots by 20 June in 1997 and 24 July in 1998 and eventually became more numerous than on the plots where they had been released.     

Diet‐dependent intraguild predation between the predatory mites Neoseiulus californicus and Neoseiulus cucumeris

Based on the hypothesis that matching diets of intraguild (IG) predator and prey indicate strong food competition and thus intensify intraguild predation (IGP) as compared to non‐matching diets, we scrutinized diet‐dependent mutual IGP between the predatory mites Neoseiulus cucumeris and N. californicus. Both are natural enemies of herbivorous mites and insects and used in biological control of spider mites and thrips in various agricultural crops. Both are generalist predators that may also feed on plant‐derived substances such as pollen. Irrespective of diet (pollen or spider mites), N. cucumeris females had higher predation and oviposition rates and shorter attack latencies on IG prey than N. californicus. Predation rates on larvae were unaffected by diet but larvae from pollen‐fed mothers were a more profitable prey than those from spider‐mite fed mothers resulting in higher oviposition rates of IG predator females. Pollen‐fed protonymphs were earlier attacked by IG predator females than spider‐mite fed protonymphs. Spider mite‐fed N. californicus females attacked protonymphs earlier than did pollen‐fed N. californicus females. Overall, our study suggests that predator and prey diet may exert subtle influences on mutual IGP between bio‐control agents. Matching diets did not intensify IGP between N. californicus and N. cucumeris but predator and prey diets proximately influenced IGP through changes in behaviour and/or stoichiometry.     

Downy mildew resistance is genetically mediated by prophylactic production of phenylpropanoids in hop

Downy mildew in hop (Humulus lupulus L.) is caused by Pseudoperonospora humuli and generates significant losses in quality and yield. To identify the biochemical processes that confer natural downy mildew resistance (DMR), a metabolome‐ and genome‐wide association study was performed. Inoculation of a high density genotyped F1 hop population (n = 192) with the obligate biotrophic oomycete P. humuli led to variation in both the levels of thousands of specialized metabolites and DMR. We observed that metabolites of almost all major phytochemical classes were induced 48 hr after inoculation. But only a small number of metabolites were found to be correlated with DMR and these were enriched with phenylpropanoids. These metabolites were also correlated with DMR when measured from the non‐infected control set. A genome‐wide association study revealed co‐localization of the major DMR loci and the phenylpropanoid pathway markers indicating that the major contribution to resistance is mediated by these metabolites in a heritable manner. The application of three putative prophylactic phenylpropanoids led to a reduced degree of leaf infection in susceptible genotypes, confirming their protective activity either directly or as precursors of active compounds.     

Comparative effectiveness of an integrated pest management system and other control tactics for managing the spider mite Tetranychus ludeni (Acari: Tetranychidae) on eggplant

The effect of an integrated pest management (IPM) package, host plantresistance, Chrysoperla carnea predation and neem oil wereevaluated against the spider mite Tetranychus ludeni oneggplant(Solanum melongena L.) fields in 1996 and 1997, byestimating the mite population density and yield levels. Compared with the IPMpackage (Panruti local, C. carnea plus neem oil), thestandard (susceptible) eggplant variety (MDU₁) grown by farmers andtreated with an acaricide (dicofol) had significantly higher mite densities.Thepredator C. carnea was recorded in significantly lowernumbers in plots with the standard variety compared to a resistant variety(panruti local) with the full IPM package. Eggplant yield level and crop valuewere highest in the IPM-treated plots followed by Panruti local plusC. carnea. The standard variety treated with an acaricidehad the lowest yield and value. These results indicated the usefulness of hostplant resistance complemented by biorational control agents, such asC. carnea and neem oil, that these are suitable componentsin an IPM programme for managing the spider mite in endemic areas.     

Relative impact of spider predation and cover crop on population dynamics of Erythroneura variabilis in a raisin grape vineyard

Experimental and correlative evidence has steadily mounted over the past 30 years implicating spiders in the suppression of insect herbivore pests in crop fields. A large body of evidence has also shown that increasing agroecosystem vegetation diversity often influences the abundance of herbivores and their natural enemies. In previous experiments, the abundance of several species of spiders on grapevines in a raisin grape vineyard was twofold enhanced in vineyard plots vegetationally diversified with a cover crop. A concomitant reduction in the abundance of the leafhopper pest Erythroneura variabilis Beamer was observed on grapevines in the diversified plots, but a causal relationship was not established. In the present study, we simultaneously manipulated spider densities (in open‐vine spider exclusion and vine‐shoot enclosures) and ground cover to determine their relative impact on E. variabilis population dynamics. Open‐vine spider exclusion resulted in an average 35% increase in the density of E. variabilis the greatest effect with occurring during the first and second leafhopper generations. The negative impact of spiders on E. variabilis densities was corroborated with vine‐shoot enclosure experiments. Under the conditions of the present study, the cover crop per se did not affect the dynamics of E. variabilis populations on grapevines, despite a 1.6‐fold increase in spider densities on vines in cover crop plots, compared with vines in bare ground plots, probably due to insufficient spider enhancement and low overall E. variabilis abundance during the summer months. The cover crop had little effect on vine macronutrient status (and presumably vine water status). While this study provided further support for the hypothesis that vegetation diversity can enhance spider abundance, this enhancement does not always lead to lower pest densities, thus underscoring the complexity and variability that exists in interactions involving cover crop, spiders, and crop plants and their herbivore pests.     

Inter‐ and intraspecific variation of spider mite susceptibility to fungal infections: Implications for the long‐term success of biological control

Spider mites are severe pests of several annual and perennial crops worldwide, often causing important economic damages. As rapid evolution of pesticide resistance in this group hampers the efficiency of chemical control, alternative control strategies, such as the use of entomopathogenic fungi, are being developed. However, while several studies have focused on the evaluation of the control potential of different fungal species and/or isolates as well as their compatibility with other control methods (e.g., predators or chemical pesticides), knowledge on the extent of inter‐ and intraspecific variation in spider mite susceptibility to fungal infection is as yet incipient. Here, we measured the mortality induced by two generalist fungi, Beauveria bassiana and Metarhizium brunneum, in 12 spider mite populations belonging to different Tetranychus species: T. evansi, T. ludeni, and T. urticae (green and red form), within a full factorial experiment. We found that spider mite species differed in their susceptibility to infection by both fungal species. Moreover, we also found important intraspecific variation for this trait. These results draw caution on the development of single strains as biocontrol agents. Indeed, the high level of intraspecific variation suggests that (a) the one‐size‐fits‐all strategy may fail to control spider mite populations and (b) hosts resistance to infection may evolve at a rapid pace. Finally, we propose future directions to better understand this system and improve the long‐term success of spider mite control strategies based on entomopathogenic fungi.     

Pest species diversity enhances control of spider mites and whiteflies by a generalist phytoseiid predator

To test the hypothesis that pest species diversity enhances biological pest control with generalist predators, we studied the dynamics of three major pest species on greenhouse cucumber: Western flower thrips, Frankliniella occidentalis (Pergande), greenhouse whitefly, Trialeurodes vaporariorum (Westwood), and two-spotted spider mites, Tetranychus urticae Koch in combination with the predator species Amblyseius swirskii Athias-Henriot. When spider mites infested plants prior to predator release, predatory mites were not capable of controlling spider mite populations in the absence of other pest species. A laboratory experiment showed that predators were hindered by the webbing of spider mites. In a greenhouse experiment, spider mite leaf damage was lower in the presence of thrips and predators than in the presence of whiteflies and predators, but damage was lowest in the presence of thrips, whiteflies and predators. Whitefly control was also improved in the presence of thrips. The lower levels of spider mite leaf damage probably resulted from (1) a strong numerical response of the predator (up to 50 times higher densities) when a second and third pest species were present in addition to spider mites, and (2) from A. swirskii attacking mobile spider mite stages outside or near the edges of the spider mite webbing. Interactions of spider mites with thrips and whiteflies might also result in suppression of spider mites. However, when predators were released prior to spider mite infestations in the absence of other pest species, but with pollen as food for the predators, we found increased suppression of spider mites with increased numbers of predators released, confirming the role of predators in spider mite control. Thus, our study provides evidence that diversity of pest species can enhance biological control through increased predator densities.     

Host plant recognition in monophagous weevils: Specialization ofCeutorhynchus inaffectatus to glucosinolates from its host plantHesperis matronalis

Several aphid honeydews were incorporated into sucrose solutions and presented to hop aphids, Phorodon humuli (Schrank), as artificial diets in free-choice bioassays. Small additions of honeydew collected from two species of aphid feeding on hop, Humulus lupulus L., arrested the searching behavior of the hop aphid and appeared to stimulate prolonged periods of ingestion. This effect was more dependent on the host plant honeydew source than the species of aphid that produced the honeydew. Aphid honeydews collected from plants other than hop (non-hosts to P. humuli) contained hop aphid phagostimulants that were less effective. Our results indicate that analysis of aphid honeydew could help describe chemical cues involved in the recognition of appropriate host plants by aphid species.     

Response of Neoseiulus fallacis Garmen and Galendromus occidentalis Nesbitt (Acari: Phytoseiidae) to Tetranychus urticae Koch (Acari: Tetranychidae)-Damaged Hop Humulus lupulus (L.) (Urticales: Cannabaceae)

Abstract 1 The response of Neoseiulus fallacis Garmen and Galendromus occidentalis (Acari: Phytoseiidae) to Tetranychus urticae Koch (Acari: Tetranychidae)‐damaged and undamaged hop, Humulus lupulus (L.), plants was tested using a Y‐tube olfactometer. 2 Neoseiulus fallacis but not G. occidentalis was attracted to volatiles from T. urticae‐damaged hop plants when paired with undamaged plants. 3 The response of N. fallacis to these volatiles was stronger for plants severed at the soil surface than for intact plants. 4 There was no difference in the response of N. fallacis to severed or intact hop plants that had no spider mite damage, indicating that artificial wounding by severing alone does not elicit the production of attractive volatiles detectable to N. fallacis. These results are consistent with the existence of cross‐talk between signalling pathways initiated by feeding damage and artificial wounding that result in elevated levels of predator‐attracting volatiles.     

Optimum release times for biological control of the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) by Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseidae) on the strawberry in greenhouses

The effectiveness of the predatory mite Phytoseiulus persimilis Athias‐Henriot (Acari: Phytoseidae) in controlling the two‐spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) was evaluated in commercial strawberry greenhouses in two areas of Korea. Optimum release times for P. persimilis were investigated by case studies. Control effects of the two‐spotted spider mite by release of the predatory mite were shown. There was mostly good control by the release of P. persimilis when there were fewer than 0.9 T. urticae per leaf. We recommend it would be ideal to release P. persimilis twice in December and once in February for very early strawberry harvest, and three times from February to March (after overwintering) for early harvest.     

The microbiota in spider mite feces potentially reflects intestinal bacterial communities in the host

Microorganisms provide many physiological functions to herbivorous hosts. Spider mites (genus Tetranychus) are important agricultural pests throughout the world; however, the composition of the spider mite microbial community, especially gut microbiome, remains unclear. Here, we investigated the bacterial community in five spider mite species and their associated feces by deep sequencing of the 16S rRNA gene. The composition of the bacterial community was significantly different among the five prevalent spider mite species, and some bacterial symbionts showed host‐species specificity. Moreover, the abundance of the bacterial community in spider mite feces was significantly higher than that in the corresponding spider mite samples. However, Flavobacterium was detected in all samples, and represent a “core microbiome”. Remarkably, the maternally inherited endosymbiont Wolbachia was detected in both spider mite and feces. Overall, these results offer insight into the complex community of symbionts in spider mites, and give a new direction for future studies.     

Epigeic spiders are not affected by the genetically modified maize MON 88017

The genetically modified (GM) maize MON 88017 facilitates weed management owing to its tolerance to glyphosate, and resists western corn rootworm (WCR), Diabrotica virgifera virgifera, owing to the expression of Cry3Bb1 toxin. MON 88017 could therefore contribute to the solution of two major problems of European agriculture: continuous WCR spreading and high use of herbicides. To assess possible unwanted environmental impacts of MON 88017, we compared communities of spiders in plots planted in three successive years with this maize, its near isogenic non‐GM cultivar treated or not treated with an insecticide and two unrelated maize cultivars. Each of the five treatments was applied on five 0.5 ha plots in a 14 ha field. Spiders were collected in five pitfall traps per plot five times per year. Upon reaching the waxy ripening stage, all plants of first‐year cultivation were shredded to small pieces and ploughed into the soil in the respective plot, whereas in the 2nd and 3rd year the harvest was used for biogas production and only digestate was returned to the field. Out of 79 spider species, Pardosa agrestis, Pachygnatha degeeri and Oedothorax apicatus made up 28%, 25% and 23% of the total spider count in the 1st year of study; 2%, 8% and 84% in the 2nd; and 40%, 8% and 35% in the 3rd year. Statistical analysis did not reveal any influence of GM maize on the spider abundance and biodiversity. The abundance, and in two years also the species diversity, was insignificantly higher on the plots with GM maize than on plots with the insecticide‐treated non‐GM maize. The composition and size of spider community varied year to year, probably reflecting weather conditions and differences in field fertilization with organic matter.     

Effects of plant spacing and interplanting with oilseed rape on colonisation of dwarf hops by the damson-hop aphid, Phorodon humuli

The pattern of colonisation of dwarf hops (Humulus lupulus) by damson-hop aphid (Phorodon humuli (Schrank)) migrating from Prunus spp. was investigated at six plant spacings and where some of the hops were replaced by oilseed rape (Brassica napus L.), a non-host of the aphid. The number of migrant aphids that accumulated on hop stems (bines) increased with increasing bine size and density. The numbers of aphids that colonised hops interplanted with oilseed rape reflected the density of the hop plants only and not the overall plant density. As the physical size of the wind shadow within which flying aphids can manoeuvre and land was unimportant unless provided by a host plant, the finding supports the theory that flying aphids respond to olfactory stimuli associated with their hosts. Variation in bine height (as a measure of plant size) explained 29–93% of the variance in aphid counts during the 3 years' study and bine density 1–14%. Standardising the data as the numbers of aphids per metre of bine and taking a square-root transformation of these standardised counts improved the precision of the analyses and, by stabilising variances, facilitated comparisons between years as growth became more vigorous as the plants matured. Each year, the rate of increase in numbers of aphids settling on plots of hops declined curvilinearly with increasing bine density. Maximum colonisation by P. humuli occurred at a bine density of five per metre row, a density similar to that used commercially by growers of dwarf hops.     

Biology of the hop cyst nematode Heterodera humuli

In an intensively sampled English hop garden, cysts of Heterodera humuli were found in every sample taken. Most occurred in the top 15 cm of soil, decreasing in number by half with every 15 cm in depth. Numbers of second-stage juveniles fluctuated during the vegetative period in a pattern which indicated that more than one generation, possibly two to three, were produced. The generation time was about 1.5 months. In pot experiments under controlled conditions (20°C; 16 h light/day) the life cycle lasted 40 days. The optimal temperature was 20°C for the development of H. humuli in the roots of its host Humulus lupulus. Most H. humuli juveniles invaded hop roots at 15°C, but egg hatch was greatest at 20°C. In moist soil, second-stage juveniles survived for at least 54 days and thereafter invaded roots and reproduced.     

Different colonization patterns of phytophagous and predatory mites (Acari: Tetranychidae, Phytoseiidae) on three grape varieties: a case study

In a vineyard having three varieties of grape (Merlot, Trebbiano and Garganega) differently colonized by two phytoseiid species,Typhlodromus pyri Scheuten andAmblyseius andersoni (Chant), the dynamics of mite populations were monitored over 5 years (1989–1993) in order to study their colonization, interspecific competition and the control of spider mites, i.e.Panonychus ulmi (Koch). These aspects were also investigated by releasingT. pyri, A. andersoni andAmblyseius aberrans (Oudemans) on some of the above varieties. In most of the experimental years (1989–1992), selective pesticides were used in order to allow a successful release of phytoseiids, in particularA. aberrans. The use of non-selective insecticides was re-established during 1993 in order to test its effect on the new mite communities originating from 1989 onwards. In the first years of the experiments an apparent relationship between grape variety and phytoseiid species was observed: in the control plots,A. andersoni occurred on Merlot whereT. pyri was rare, while the latter species was largely dominant overA. andersoni on Trebbiano and Garganega.Panonychus ulmi populations reached moderate levels only on Merlot and in the first part of experiments. The variety-phytoseiid species relationship was temporary as, at the end of experiments,T. pyri was completely dominant on all varieties. This new situation started when prey occurrence and interspecific competition decreased in importance. The moderate success of theT. pyri release on Merlot contrasts with the results of previous experiments. Two factors could be involved in this phenomenon: low interspecific competition by phytoseiids and predation by macropredators.Amblyseius aberrans was able to displaceA. andersoni andT. pyri on grape varieties where the two species were more abundant and reached higher population densities on varieties with pubescent leaf undersurfaces. In the first experimental year, spider mite densities were reduced more effectively inA. aberrans release plots than in the control or inT. pyri release plots. One year later,P. ulmi reached lower levels in the release treatments than in the control.Typhlodromus pyri andA. aberrans persisted in conditions of prey scarcity. The high competitivity ofA. aberrans over the remaining two phytoseiid species constitutes a major factor in selecting predatory species for inoculative releases in vineyards.     

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.     

Positive association between thrips and spider mites in seedling cotton

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