Neonicotinoid insecticide imidacloprid causes outbreaks of spider mites on elm trees in urban landscapes

Background

Attempts to eradicate alien arthropods often require pesticide applications. An effort to remove an alien beetle from Central Park in New York City, USA, resulted in widespread treatments of trees with the neonicotinoid insecticide imidacloprid. Imidacloprid''s systemic activity and mode of entry via roots or trunk injections reduce risk of environmental contamination and limit exposure of non-target organisms to pesticide residues. However, unexpected outbreaks of a formerly innocuous herbivore, Tetranychus schoenei (Acari: Tetranychidae), followed imidacloprid applications to elms in Central Park. This undesirable outcome necessitated an assessment of imidacloprid''s impact on communities of arthropods, its effects on predators, and enhancement of the performance of T. schoenei.

Methodology/Principal Findings

By sampling arthropods in elm canopies over three years in two locations, we document changes in the structure of communities following applications of imidacloprid. Differences in community structure were mostly attributable to increases in the abundance of T. schoenei on elms treated with imidacloprid. In laboratory experiments, predators of T. schoenei were poisoned through ingestion of prey exposed to imidacloprid. Imidacloprid''s proclivity to elevate fecundity of T. schoenei also contributed to their elevated densities on treated elms.

Conclusions/Significance

This is the first study to report the effects of pesticide applications on the arthropod communities in urban landscapes and demonstrate that imidacloprid increases spider mite fecundity through a plant-mediated mechanism. Laboratory experiments provide evidence that imidacloprid debilitates insect predators of spider mites suggesting that relaxation of top-down regulation combined with enhanced reproduction promoted a non-target herbivore to pest status. With global commerce accelerating the incidence of arthropod invasions, prophylactic applications of pesticides play a major role in eradication attempts. Widespread use of neonicotinoid insecticides, however, can disrupt ecosystems tipping the ecological balance in favor of herbivores and creating pest outbreaks.     

Physiologic Response of Cotton to the Insecticide Imidacloprid under High-Temperature Stress

The insecticide imidacloprid (tradename Trimax™) has been shown to increase cotton (Gossypium hirsutum L.) yield in the absence of insects, but the explanation for this is not clear. Growth room studies were designed to investigate changes in the physiology and biochemistry of imidacloprid-treated cotton plants and provide information on the mode of action of yield enhancement. Imidacloprid was applied at the pinhead square growth stage at the rate of 52.3 g ai/ha and plants were exposed to day temperatures of 30, 33, 36, and 39°C. Increased levels of photosynthesis and higher values of chlorophyll fluorescence yield, measured two days after imidacloprid application, showed an advantage of imidacloprid-treated over untreated plants. The effect of imidacloprid was greater at the higher temperatures of the growth chamber studies. The results suggested that the imidacloprid-treated plants suffered less temperature stress. This suggestion was supported by findings of reduced glutathione reductase in the imidacloprid-treated plants in the growth chamber, indicating that the untreated plants were experiencing more stress, necessitating the activation of this defense mechanism.     

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.     

Fecundity in twospotted spider mite (Acari: Tetranychidae) is increased by direct and systemic exposure to imidacloprid

The effect of imidacloprid on fecundity in twospotted spider mites, Tetranychus urticae Koch, was investigated in laboratory experiments using individual females on bean leaf discs. Mites were directly exposed to spray formulations of imidacloprid or fed on discs cut from a systemically treated bean plant. Imidacloprid-treated T. urticae produced 10-26% more eggs during the first 12 d of adult life and 19-23% more during adulthood compared with a water-only treatment. Increased egg production occurred immediately after exposure and lasted for about 15 d in sprayed mites. In mites exposed to imidacloprid by ingestion, increased egg production was not apparent until after 6 d and lasted until about day 18. Longevity was significantly greater in mites that ingested imidacloprid but not in sprayed mites. The significance and importance of imidacloprid-stimulation of fecundity in T. urticae to pest management in crop systems like hops, which routinely use this insecticide, is discussed.     

The impact of insecticides applied in apple orchards on the predatory mite Kampimodromus aberrans (Acari: Phytoseiidae)

Kampimodromus aberrans is an effective predatory mite in fruit orchards. The side-effects of insecticides on this species have been little studied. Field and laboratory experiments were conducted to evaluate the effects of insecticides on K. aberrans. Field experiments showed the detrimental effects of etofenprox, tau-fluvalinate and spinosad on predatory mites. Spider mite (Panonychus ulmi) populations reached higher densities on plots treated with etofenprox and tau-fluvalinate than in the other treatments. Single or multiple applications of neonicotinoids caused no detrimental effects on predatory mites. In the laboratory, spinosad and tau-fluvalinate caused 100 % mortality. Etofenprox caused a significant mortality and reduced fecundity. The remaining insecticides did not affect female survival except for imidacloprid. Thiamethoxam, clothianidin, thiacloprid, chlorpyrifos, lufenuron and methoxyfenozide were associated with a significant reduction in fecundity. No effect on fecundity was found for indoxacarb or acetamiprid. Escape rate of K. aberrans in laboratory was relatively high for etofenprox and spinosad, and to a lesser extent thiacloprid. The use of etofenprox, tau-fluvalinate and spinosad was detrimental for K. aberrans and the first two insecticides induced spider mite population increases. The remaining insecticides caused no negative effects on predatory mites in field trials. Some of them (reduced fecundity and repellence) should be considered with caution in integrated pest management programs.     

Systemic Imidacloprid Affects Intraguild Parasitoids Differently

Toxoneuron nigriceps (Viereck) (Hymenoptera, Braconidae) and Campoletis sonorensis (Cameron) (Hymenoptera, Ichneumonidae) are solitary endoparasitoids of the tobacco budworm, Heliothis virescens (Fabricius) (Lepidoptera, Noctuidae). They provide biological control of H. virescens populations in Southeastern US agricultural production systems. Field and greenhouse experiments conducted from 2011–2014 compared parasitism rates of parasitoids that developed inside H. virescens larvae fed on tobacco plants treated with and without imidacloprid. The parasitoids in our study did not have a similar response. Toxoneuron nigriceps had reduced parasitism rates, but parasitism rates of C. sonorensis were unaffected. Preliminary data indicate that adult female lifespans of T. nigriceps are also reduced. ELISA was used to measure concentrations of neonicotinoids, imidacloprid and imidacloprid metabolites in H. virescens larvae that fed on imidacloprid-treated plants and in the parasitoids that fed on these larvae. Concentrations were detectable in the whole bodies of parasitized H. virescens larvae, T. nigriceps larvae and T. nigriceps adults, but not in C. sonorensis larvae and adults. These findings suggest that there are effects of imidacloprid on multiple trophic levels, and that insecticide use may differentially affect natural enemies with similar feeding niches.     

Spatial distribution of predators and prey affect biological control of twospotted spider mites by Phytoseiulus persimilis in greenhouses

We evaluated the effects of predator release pattern and prey distribution on rate of suppression of the twospotted spider mite, Tetranychus urticae Koch (Acari, Tetranychidae) and visual damage to the ornamental plant, Impatiens wallerana Hook.f., in a greenhouse. Sixteen impatiens plants were arranged in a square and infested with the same total number of spider mites distributed either evenly (equal numbers on all plants) or clumped (divided equally among the 4 central plants), simulating a “hot spot.” The predatory mite, Phytoseiulus persimilis Athias-Henriot, was released at a 1:4 predator:prey ratio based on total spider mites in the experimental unit, but the pattern of release was either even or clumped, which simulated broadcast or point-release strategies, respectively. Nine days after predator release, spider mite populations were reduced in all treatments, but only in the clumped pest-clumped predator treatment were spider mites undetectable. Poorest pest suppression occurred in the clumped spider mite-even predator treatment. Eighteen days after predator release, spider mites were eliminated in all treatments, but a reduction in average plant damage occurred only in treatments in which the predator release pattern matched the spider mite distribution (i.e., even-even or clumped-clumped) with the greatest reduction in the even-even treatment. Results suggest that there is an advantage to releasing predators in “hot spots” provided that the recommended predator:prey ratio is maintained within infested patches. If more uniform predator releases are planned, overall predator numbers need to be kept sufficiently high so that the predator:prey ratio of 1:4 shown to prevent damage on impatiens is achieved in higher-density spider mite patches.     

Variable fitness and reproductive effects of Wolbachia infection in populations of the two-spotted spider mite Tetranychus urticae Koch in China

Maternally inherited Wolbachia bacteria are widely distributed among insects, and their presence usually causes modifications of the host. To understand the evolutionary history of diverse host-Wolbachia associations, we investigated the symbiosis between Wolbachia and the two-spotted spider mite Tetranychus urticae Koch in China. The cytoplasmic incompatibility (CI) level, fecundity, female ratio, host longevity and host development time were examined. Our results indicate that Wolbachia bacteria had variable effects on the reproduction and fitness of Chinese populations of T. urticae. Variability of CI expression within T. urticae ranged from no CI to a strong level of CI in spite of the low variability of the wsp gene. Relative to uninfected mites, infected females in one of the three populations showed enhanced fecundity associated with the infection of Wolbachia. This is the first report of a Wolbachia infection promoting the fecundity of infected females in T. urticae. Furthermore, we found both positive and negative effects of Wolbachia infection on longevity and the development time. The differences in ecological characters may be attributed to both Wolbachia and host genotype.     

Lima bean�Clady beetle interactions: spider mite mediates sublethal effects of its host plant on growth and development of its predator

Cultivated plants can have negative effects on natural enemies that attack spider mites. In this study, we tested the hypothesis that spider mites mediate effects of a lima bean, Phaseolus lunatus L., cultivar on the life history of a lady beetle Stethorus punctillum Weise. We provisioned laboratory arenas with two-spotted spider mites, Tetranychus urticae Koch, from planters containing Henderson Bush Bean or Fordhook 242 lima bean plants and monitored the growth, development, larval survival, fecundity, and adult life span of predators. We determined the protein content and the linamarin (a cyanogenic glycoside) content in foliage, spider mites, and predators. Predators took longer to develop and were smaller sized when consuming mites from the Henderson foliage. There was no significant mite-mediated effect of cultivar on predator fecundity or life span. Although soluble protein was greater in foliage of the Henderson than the Fordhook cultivar, mites contained less protein when reared on the Henderson, and predators contained less protein when fed with mites from the Henderson. Linamarin content was greater in Henderson than Fordhook foliage, and greater in spider mites and predators in the Henderson treatment. Linamarin in Henderson foliage may reduce the ability of spider mites to utilize plant protein. As a result, prey quality is reduced and predators that feed on these prey (from the Henderson treatment) grow at a slower rate and are smaller sized than their cohorts (from the Fordhook treatment). In conclusion, T. urticae mediates the effects of the Henderson cultivar on S. punctillum development but not fecundity or life span.     

Incidence of resistance to neonicotinoid insecticides in greenhouse populations of the whitefly, Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) from Greece

The greenhouse whitefly, Trialeurodes vaporariorum Westwood, is an important pest of field and greenhouse crops of horticultural and ornamental plants. In integrated pest management programs its control is mainly based on the release of biological control agents and application of chemical insecticides. Neonicotinoids are relatively new chemicals currently applied for the chemical control of T. vaporariorum. However, cases of development of insecticide resistance to neonicotinoids have already been reported. The state of resistance to neonicotinoid insecticides for populations of the greenhouse whitefly in Greece is currently unknown. The objective of our study was to screen a number of whitefly populations for resistance to the neonicotinoids imidacloprid and thiacloprid. Seven whitefly populations were collected from tomato greenhouse crops from different areas of central and northern Greece. LC₅₀ values were estimated for all populations following the method proposed by the Insecticide Resistance Action Committee (IRAC). The development of resistance to both neonicotinoids was confirmed for all tested populations with resistance ratios ranging from 1.5 to 4.4-fold and from 1.4 to 12.2-fold for imidacloprid and thiacloprid, respectively. We discuss our results with regard to the development of neonicotinoid resistance in T. vaporariorum populations and its implications for whitefly control.     

Interactions of two natural enemies of Tetranychus urticae,the fungal entomopathogen Beauveria bassiana and the predatory mite,Phytoseiulus persimilis

The effect of either untreated or treated adults of the spider mite, Tetranychus urticae Koch (Acari: Tetranychidae) by Beauveria bassiana (Bals.) Vuillemin (Ascomycota: Hypocreales) DEBI008 at 1×10⁶ (conidia/ml) was investigated on developmental stages and life table parameters of Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae) under laboratory conditions. Four time intervals (0, 24, 48 and 72 h post-inoculation of spider mites) were considered for studying the predator characteristics as different treatments. Duration of each life stage, longevity, reproduction rate, intrinsic rate of natural increase (r _m ), net reproductive rate (R ₀), mean generation time (T) and finite rate of increase (λ) of the P. persimilis were calculated on both untreated and B. bassiana treated spider mite adults. Data analysis showed that longevity and fecundity of predatory mites fed on untreated and treated mites (time interval 0) were higher in comparison with other time intervals after inoculation. The entomopathogenic fungus adversely affected longevity and fecundity of the predatory mite. Fertility life table parameters of predatory mites fed on T. urticae treated by B. bassiana at different time intervals showed that T, R ₀, λ and r _m are strongly affected by the fungus presence and these parameters had significant differences among time treatments. The least r _m value was observed in the time interval of 72 h post-inoculation. The fitness of T. urticae was affected by B. bassiana 24, 48 and 72 h post-inoculation of mite adults, and consequently it caused decreased longevity of P. persimilis and accordingly a decrease in the intrinsic rate of natural increase of the predator.     

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.     

Phytoseiid predator of whitefly feeds on plant tissue

Predatory mites of the family Phytoseiidae feed on herbivorous mites and insects but they also use a variety of non-prey food items, such as pollen and nectar. Plant tissue is another potential food source. We investigated whether plant feeding occurs in the two phytoseiids Euseius scutalis (Athias-Henriot) and Typhlodromips swirskii (Athias-Henriot), which are natural enemies of whiteflies. These predatory mites can suppress populations of Bemisia tabaci (Gennadius) on isolated plants and are candidates for biological control of this pest. Both species can be reared on a diet of pollen, but E. scutalis requires a leaf tissue substrate, suggesting that this species might feed on plant tissue. To test this hypothesis, we applied a systemic insecticide (aldicarb) to cucumber plants and assessed the survival of predatory mites on leaves from insecticide-treated plants and untreated plants, both in presence and absence of pollen. The survival of T. swirskii was not affected by the presence of systemic insecticide in the plant. However, the survival of E. scutalis on leaves from insecticide-treated plants was 10 times lower than on leaves from untreated plants. Since the two species showed similar sensitivity to the insecticide when applied in a slide-dip test, this suggests that E. scutalis ingested insecticide through feeding on the leaf tissue. Mortality on treated leaves was observed both in absence and presence of pollen, suggesting that plant feeding is indispensable for E. scutalis. The extent to which plants are used as food by E. scutalis requires further analysis.     

PCR-based identification of the pathogenic bacterium, Acaricomes phytoseiuli, in the biological control agent Phytoseiulus persimilis (Acari: Phytoseiidae)

The predatory mite, Phytoseiulus persimilis is an important biological control agent of herbivorous spider mites. This species is also intensively used in the study of tritrophic effects of plant volatiles in interactions involving plants, herbivores, and their natural enemies. Recently, a novel pathogenic bacterium, Acaricomes phytoseiuli, has been isolated from adult P. persimilis females. This pathogen causes a characteristic disease syndrome with dramatic changes in longevity, fecundity, and behavior. Healthy P. persimilis use spider mite-induced volatiles to locate prey patches. Infection with A. phytoseiuli strongly reduces the attraction to herbivore-induced plant volatiles. The loss of response to herbivore-induced plant volatiles along with the other disease symptoms can have a serious impact on the success of biological control of spider mites. In this study, we have developed a molecular tool (PCR) to detect the pathogenic bacterium in individual predatory mites. PCR primers specific for A. phytoseiuli were developed based on 16S ribosomal DNA of the bacterium. The PCR test was validated with DNA extracted from predatory mites that had been exposed to A. phytoseiuli. A survey on different P. persimilis populations as well as other predatory mite species from several companies that rear predatory mites for biological control revealed that the disease is widespread in Europe and is restricted to P. persimilis. The possibility that the predatory mites get infected via their prey Tetranychus urticae could be eliminated since the PCR test run on prey gave a negative result.     

Attraction of a generalist predator towards herbivore-infested plants

The occurrence and strength of interactions among natural enemies and herbivores depend on their foraging decisions, and several of these decisions are based on odours. To investigate interactions among arthropods in a greenhouse cropping system, we studied the behavioural response of the predatory bug Orius laevigatus (Fieber) (Hemiptera: Anthocoridae) towards cucumber plants infested either with thrips (Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae)) or with spider mites (Tetranychus urticae Koch (Acari: Tetranychidae)). In greenhouse release-recapture experiments, the predatory bug showed a significant preference for both thrips-infested plants and spider mite-infested plants over clean plants. Predatory bugs preferred plants infested with spider mites to plants with thrips. Experience with spider mites on cucumber leaves prior to their release in the greenhouse had no effect on the preference of the predatory bugs. However, this experience did increase the percentage of predators recaptured. Y-tube olfactometer experiments showed that O. laevigatus was more attracted to odours from plants infested with spider mites than to odours from clean plants. Thus, O. laevigatus is able to perceive odours and may use them to find plants with prey in more natural conditions. The consequences of the searching behaviour for pest control are discussed.     

Effects of spring imidacloprid application for white grub control on parasitism of Japanese beetle (Coleoptera: Scarabaeidae) by Tiphia vernalis (Hymenoptera: Tiphiidae)

Imidacloprid, a relatively long residual neonicotinoid soil insecticide, is often applied to lawns and golf courses in spring for preventive control of root-feeding white grubs. We evaluated effects of such applications on spring parasitism of the overwintered third-instar Japanese beetle, Popillia japonica Newman, by Tiphia vernalis Rohwer, an introduced solitary ectoparasitoid. Natural rates of parasitism on a golf course rough were significantly lower in plots treated with full or one-half label rates of imidacloprid in early May compared with untreated turf. Parasitism also was reduced when female T. vernalis were exposed to imidacloprid residues on turf cores in the laboratory. Such exposures did not affect wasp mortality, longevity, survival, or developmental period of Tiphia larvae feeding on hosts in treated turf. They did, however, reduce wasps' ability to parasitize hosts in nontreated soil for at least 1-2 wk postexposure. In Y-trail choice tests, wasps that previously had been exposed to treated turf failed to respond normally to host frass trails in the soil. Female wasps did not avoid imidacloprid residues, imidacloprid-treated host frass, or host grubs that had previously been exposed to treated soil. This study indicates that applying imidacloprid in early spring can interfere with biological control by T. vernalis, whereas postponing preventive grub treatments until June or July, after the wasps' flight period, will help to conserve T. vernalis populations.     

Reproduction and survival of the predatory bugOrius albidipennis on various arthropod prey

The daily rate of oviposition, fecundity, survival and adult longevity ofOrius albidipennis (Reuter) (Hemiptera: Anthocoridae) were studied in the laboratory in Israel. These parameters were compared on three arthropod prey species: the two-spotted spider mite,Tetranychus urticae Koch; the onion thrips,Thrips tabaci Lindeman; and eggs of the almond moth,Ephestia cautella Walker. The fecundity and survival on the thrips diet (217.2 eggs/female and 98.7%, respectively) and on moth eggs (184.1 eggs/female and 84.6%, respectively) were significantly higher than on the spider mite diet (110.9 eggs/female and 40.4%, respectively). Female longevity was significantly higher onEphestia eggs (63.0 days) than on thrips (45.1 days) and mites (35.1 days). There were no significant differences in male longevity among the three diets (57.5, 64.1 and 54.5 days, respectively).     

The toxic effect of greenhouse insecticides on the predatory bugs <Emphasis Type="Italic">Nesidiocoris tenuis</Emphasis> Reuter and <Emphasis Type="Italic">Macrolophus pygmaeus</Emphasis> H.-S. (Heteroptera,Miridae)

The study reports the results of toxicity tests for several insecticides which are allowed to be used on greenhouse plants (Admiral, Mospilan, Spintor, and BT), as applied to different developmental stages of the predatory bugs Nesidiocoris tenuis Reuter and Macrolophus pygmaeus H.-S. (family Miridae), which feed on whiteflies, aphids, thrips, and spider mites. The juvenoid Admiral is found to be the least toxic to these species, whereas the spinosyn Spintor is most toxic. The neonicotinoid Mospilan and a microbiological insecticide BT are intermediate in their effects. The timing of application of insecticides most favorable to the predatory mirids when both pest management methods are used together is discussed.     

Potential of the predatory mite Phytoseius finitimus (Acari: Phytoseiidae) to feed and reproduce on greenhouse pests

Phytoseiid mites of the genus Phytoseius are natural enemies of tetranychid and eriophyid herbivorous mites mostly found on hairy plants where they feed on prey, as well as on pollen. Nevertheless, the nutritional ecology and the role of these predators in biological pest control are only rarely addressed. In the present study, we evaluated the potential of Phytoseius finitimus to feed and reproduce on three major greenhouse pests, the two-spotted spider mite, the greenhouse whitefly and the western flower thrips. Additionally, we estimated the effect of cattail pollen when provided to the predator alone or in mixed diets with prey. Contrary to thrips larvae, both spider mite larvae and whitefly crawlers sustained the development of P. finitimus. In addition, females consumed more spider mite eggs and larvae, as well as whitefly crawlers than thrips larvae, but laid eggs when feeding on all prey. When provided alone, cattail pollen sustained the development and reproduction of the predator. The addition of pollen in mixed diets with prey reduced prey consumption, though it increased the predator’s egg production. We discuss the implications of our findings for biological pest control.     

Synergism of imidacloprid and entomopathogenic nematodes against white grubs: the mechanism

Entomopathogenic nematodes and the chloronicotinyl insecticide, imidacloprid, interact synergistically on the mortality of third-instar white grubs (Coleoptera: Scarabaeidae). The degree of interaction, however, varies with nematode species, being synergistic for Steinernema glaseri (Steiner) and Heterorhabditis bacteriophora Poinar, but only additive for Steinernema kushidai Mamiya. The mechanism of the interaction between imidacloprid and these three entomopathogenic nematodes was studied in the laboratory. In vials with soil and grass, mortality, speed of kill, and nematode establishment were negatively affected by imidacloprid with S. kushidai but positively affected with S. glaseri and H. bacteriophora. In all other experiments, imidacloprid had a similar effect for all three nematode species on various factors important for the successful nematode infection in white grubs. Nematode attraction to grubs was not affected by imidacloprid treatment of the grubs. Establishment of intra-hemocoelically injected nematodes was always higher in imidacloprid-treated grubs but the differences were small and in most cases not significant. The major factor responsible for synergistic interactions between imidacloprid and entomopathogenic nematodes appears to be the general disruption of normal nerve function due to imidacloprid resulting in drastically reduced activity of the grubs. This sluggishness facilitates host attachment of infective juvenile nematodes. Grooming and evasive behavior in response to nematode attack was also reduced in imidacloprid-treated grubs. The degree to which different white grub species responded to entomopathogenic nematode attack varied considerably. Untreated Popillia japonica Newman (Coleoptera: Scarabaeidae) grubs were the most responsive to nematode attack among the species tested. Untreated Cyclocephala borealis Arrow (Coleoptera: Scarabaeidae) grubs showed a weaker grooming and no evasion response, and untreated C. hirta LeConte (Coleoptera: Scarabaeidae) grubs showed no significant response. Chewing/biting behavior was significantly increased in the presence of nematodes in untreated P. japonica and C. borealis but not in C. hirta and imidacloprid-treated P. japonica and C. borealis. Our observations, however, did not provide an explanation for the lack of synergism between imidacloprid and S. kushidai.