Eugene M. Fuzy

Comparison of neonicotinoid insecticides as synergists for entomopathogenic nematodes

Abstract In previous greenhouse and field studies, the neonicotinoid insecticide imidacloprid and the entomopathogenic nematodes Heterorhabditis bacteriophora and Steinernema glaseri interacted synergistically against third-instars of the Japanese beetle, Popillia japonica , the oriental beetle, Exomala (= Anomala ) orientalis , and three masked chafer species, Cyclocephala hirta , C . pasadenae , and C . borealis (Coleoptera: Scarabaeidae). We tested whether this interaction would also occur with other neonicotinoids, primarily thiamethoxam. In laboratory, greenhouse and field experiments, imidacloprid provided stronger and more consistent synergism with nematodes than thiamethoxam. White grub mortality resulting from nematode–neonicotinoid combinations was synergistic/additive/antagonistic in 75/25/0% of our observations with imidacloprid and 37/42/21% of our observations with thiamethoxam. Neonicotinoid–nematode interactions varied with white grub species. Imidacloprid always interacted synergistically with nematodes against E . orientalis and P . japonica , whereas no enhancement occurred against Rhizotrogus majalis and Maladera castanea . Against E . orientalis , imidacloprid interacted synergistically with five nematode species, H . bacteriophora , H . megidis , H . marelatus , S . glaseri , and S . feltiae . Synergistic combinations of nematodes and a neonicotinoid insecticide could be used for curative treatments of white grub infestations, especially against E . orientalis and P . japonica . This combination may allow spot-treatment of turf areas that exceed damage thresholds, thereby limiting the environmental impact of the insecticide application.

Steinernema scarabaei for the control of white grubs.

Abstract The efficacy of the new entomopathogenic nematode species, Steinernema scarabaei , isolated from white grubs in New Jersey for the control of economically important white grub species (Coleoptera: Scarabaeidae) was compared to that of two strains of Steinernema glaseri , four strains/isolates of Heterorhabditis bacteriophora (including two fresh isolates from scarab larvae), and an undescribed Heterorhabditis species from Korea. The efficacy was tested against the oriental beetle, Exomala (= Anomala ) orientalis , the Japanese beetle, Popillia japonica , and the northern masked chafer, Cyclocephala borealis , under laboratory, greenhouse, and field conditions, and against the European chafer, Rhizotrogus majalis , in the laboratory. Under laboratory and greenhouse conditions, S. scarabaei was highly pathogenic to P. japonica , E. orientalis , and R. majalis , but was less effective against C. borealis . However, S. scarabaei provided excellent control of P. japonica , E. orientalis , and C. borealis under field conditions. P. japonica was the most nematode-susceptible white grub species. Against this species the superiority of S. scarabaei over the other nematodes tested became only apparent under field conditions and with very low nematode rates in the laboratory. C. borealis was less susceptible to all nematodes tested and only in a field experiment did S. scarabaei clearly outperform H. bacteriophora . Both E. orientalis and R. majalis were highly susceptible to S. scarabaei but showed moderate to low susceptibility to all other nematodes tested. In a field experiment, S. scarabaei also controlled P. japonica and E. orientalis larvae more quickly than H. bacteriophora . There was weak synergism between S. scarabaei and the neonicotinoid insecticide imidacloprid against E. orientalis larvae but not against P. japonica and C. borealis larvae. Overall, S. scarabaei shows exceptional potential for the biological control of white grubs.

Pathogenicity of Heterorhabditis bacteriophora, Steinernema glaseri, and S. scarabaei (Rhabditida: Heterorhabditidae, Steinernematidae) Against 12 White Grub Species (Coleoptera: Scarabaeidae)

We compared the pathogenicity of the entomopathogenic nematodes Heterorhabditis bacteriophora, Steinernema glaseri, and S. scarabaei against third instars of 12 white grub species. The Japanese beetle (Popillia japonica) was highly susceptible to all nematode species. Oriental beetle [Exomala (=Anomala) orientalis], European chafer (Rhizotrogus majalis), Asiatic garden beetle (Maladera castanea), and the May/June beetles Phyllophaga crinita, Ph. congrua, and Ph. (Subgenus Phytalus) georgiana were highly susceptible to S. scarabaei but had mediocre to low susceptibility to H. bacteriophora and S. glaseri. The black turfgrass ataenius (Ataenius spretulus) was very susceptible to H. bacteriophora but had mediocre susceptibility to S. glaseri and S. scarabaei. Northern (Cyclocephala borealis) and southern masked chafer (C. lurida) had mediocre and southwestern masked chafer (C. pasadenae) and green June beetle (Cotinis nitida) had low susceptibility to all nematode species.

Ecological characterization of Steinernema scarabaei, a scarab-adapted entomopathogenic nematode from New Jersey

This study describes the basic ecological characteristics of the entomopathogenic nematode Steinernema scarabaei (Rhabditida: Steinernematidae) that was originally isolated from epizootics in scarab populations in New Jersey turfgrass areas. Under laboratory conditions, S. scarabaei infected a limited range of insect species and appeared best adapted to scarab larvae as hosts. It uses a widely ranging foraging strategy with a low attachment rate to mobile hosts on the soil surface but with excellent infection of sedentary host placed at >or=2 cm soil depth. It has a wide thermal activity range with optimum infectivity from 17.5 to 25 degrees C. Because of its foraging strategy and adaptation to scarab larvae as hosts, S. scarabaei has outstanding potential for the control of scarab pests.

Early timing and new combinations to increase the efficacy of neonicotinoid–entomopathogenic nematode (Rhabditida: Heterorhabditidae) combinations against white grubs (Coleoptera: Scarabaeidae)

BACKGROUND An investigation was carried out to determine whether new neonicotinoid-nematode combinations and earlier applications against younger larval stages could increase the efficacy of synergistic neonicotinoid-entomopathogenic nematode combinations against white grubs. RESULTS In the laboratory, combinations of the neonicotinoids imidacloprid and clothianidin and the nematodes Heterorhabditis bacteriophora Poinar and H. zealandica Poinar against third instars were compared. In Anomala orientalis (Waterhouse) and Popillia japonica Newman, H. bacteriophora-imidacloprid combinations showed the most consistent synergism but did not cause significantly higher mortality than H. zealandica-imidacloprid combinations. In Cyclocephala borealis Arrow, there was no clear trend as to which combinations caused the most consistent synergism, but H. zealandica-imidacloprid combinations tended to cause the highest mortalities. In the laboratory, imidacloprid-H. bacteriophora combinations provided more consistent synergism against third-instar than against second-instar A. orientalis, but mortality was higher in second instars. In field experiments, imidacloprid-H. bacteriophora combinations against A. orientalis and P. japonica provided more consistent synergism when applied in mid-September but more consistent control when applied in late August. CONCLUSIONS Imidacloprid is a better synergist for entomopathogenic nematodes than clothianidin. Imidacloprid-nematode combinations are more effective against second instars than against third instars, allowing rate reductions of both agents to make this approach more competitive with full-rate applications of neonicotinoid alone.

Biological and chemical control of the Asiatic garden beetle, Maladera castanea (Coleoptera: Scarabaeidae).

The efficacy of chemical and biological control agents against larvae of the Asiatic garden beetle, Maladera castanea (Arrow), in turfgrass under laboratory, greenhouse, and field conditions were determined. In field trials where insecticides were applied preventively against eggs and young larvae, the molt-accelerating compound halofenozide and the neonicotinoids imidacloprid and thiamethoxam were ineffective, whereas another neonicotinoid, clothianidin, provided 62-93% control. In greenhouse experiments against third instars in pots, the carbamate insecticide carbaryl was ineffective, whereas the organophosphate trichlorfon provided 71-83% control. In laboratory, greenhouse, and field experiments, the entomopathogenic nematode Heterorhabditis bacteriophora Poinar and Steinernema glaseri Steiner (not tested in the field) were ineffective against third instars, whereas S. scarabaei Stock & Koppenhöfer provided excellent control. In microplot field experiments at a rate of 2.5 x 10(9) infective juveniles per ha, H. bacteriophora provided 12-33% control and S. scarabaei 71-86% control. Combinations of S. scarabaei and imidacloprid did not provide more control of third instars compared with S. scarabaei alone.

Effect of neonicotinoid synergists on entomopathogenic nematode fitness

In previous greenhouse and field studies, the neonicotinoid insecticide imidacloprid interacted synergistically with five entomopathogenic nematode species against five scarab species. Two other neonicotinoids, thiamethoxam and acetamiprid, showed a weaker interaction with nematodes in scarab larvae. Entomopathogenic nematodes have the potential to recycle in hosts after inundative applications, thereby increasing the persistence of nematodes and insect control. Thus we investigated the effect of neonicotinoids on nematode fitness after tank mixing and after combined applications. Tank mixing only had a negative effect on nematode survival and infectivity in a few nematode–insecticide combinations and only if both insecticide concentration and exposure time were several times higher than typical for field applications. Combined application of nematodes with imidacloprid generally had no negative effect on the percentage of scarab cadavers producing progeny or the number of nematode progeny emerging per cadaver. In experiments with a synergistic increase in scarab mortality, the total number of progeny in combination treatments was up to four times higher than in nematodes only treatments. Similarly, nematode populations in soil from combination treatments were 13.2 times greater than for nematodes only treatments at 28 days after treatment. Combined imidacloprid–nematode applications did not affect the pathogenicity or infectivity of the nematode progeny. Combining thiamethoxam with nematodes had no negative effects on nematode reproduction in the majority of treatments. However, due to the weaker interaction of thiamethoxam and nematodes on scarab mortality, the total number of nematode progeny per treatment generally did not increase compared with nematodes only treatments. The demonstrated tank mix compatibility of imidacloprid and nematodes improves the feasibility of combining these agents for curative white grub control. The positive effect of imidacloprid on nematode reproduction after combined application may increase the likelihood of infection of white grubs by subsequent generations of nematodes, thereby improving their field persistence and biological control potential.

Mating Disruption of Oriental Beetle (Coleoptera: Scarabaeidae) in Turfgrass Using Microencapsulated Formulations of Sex Pheromone Components

Abstract The feasibility of mating disruption in the oriental beetle, Anomala orientalis Waterhouse, with microencapsulated sprayable formulations of (Z)-7-tetradecen-2-one, the major sex pheromone component, was evaluated in turfgrass areas. The effect of the applications was measured by monitoring male A. orientalis captures in pheromone-baited traps throughout the flight period and estimating A. orientalis larval densities in September in soil/sod samples. Trap captures were 90–100% lower in the treated areas during the first 7–10 d after treatment, but started to increase thereafter. Therefore, applications were repeated after 14 d in most treatments. The formulation tested in 2002 and 2003 reduced trap captures by 87–88% with two applications of each 12.5 or 50 g pheromone/ha but only by 74% by a single application of 75 g pheromone/ha. Reductions of A. orientalis larval populations by 68–74% were not significant because of very high variability of larval densities in the nontreated areas. Two different formulations tested in 2004 were less effective. Significant amounts of the pheromone remained on grass foliage after application, but 51 and 73% of this residue were washed off the foliage with 3.2- and 6.4-mm post-treatment irrigation, respectively. Shoes walked at 1 day after treatment through pheromone-treated areas were sufficiently contaminated with pheromone to attract high numbers of A. orientalis males in nontreated areas. Mating disruption is a promising strategy for A. orientalis management in turfgrass. However, more persistent formulations need to be developed that have a lower potential to contaminate shoes and other clothing articles with pheromone.

Attraction of four entomopathogenic nematodes to four white grub species

To better understand the differences in the efficacy of entomopathogenic nematode species against white grub species, we are studying the various steps of the infection process of entomopathogenic nematodes into different white grub species using nematode species/strains with particular promise as white grub control agents. In this study we compared the attraction of the entomopathogenic nematodes Steinernema scarabaei (AMK001 strain), Steinernema glaseri (NC1 strain), Heterorhabditis zealandica (X1 strain), and Heterorhabditis bacteriophora (GPS11 strain) to third-instars of the scarabs Popillia japonica, Anomala orientalis, Cyclocephala borealis, and Rhizotrogus majalis, and late-instar greater wax moth, Galleria mellonella, larvae. Individual larvae were confined at the bottom of 5.5 cm vertical sand columns, nematodes added to the sand surface after 24 h, and nematodes extracted after another 24 h. Nematode attraction to hosts was strongly affected by nematode species but the effect of insect species varied with nematode species. S. glaseri had a high innate dispersal rate (i.e., in absence of insects) and was strongly attracted to insects without significant differences among insect species. S. scarabaei had a very low innate dispersal rate so that even a strong relative response to insects resulted in low absolute dispersal rates toward insects. S. scarabaei tended to be most attracted to G. mellonella and least attracted to C. borealis. H. zealandica had a high innate dispersal rate but only responded weakly to insects without significant differences among species. H. bacteriophora had limited innate dispersal and only weakly responded to insects with G. mellonella tending to be the most attractive and C. borealis the least attractive insect. It has to be noted that we cannot exclude that the use of different rearing hosts (A. orientalis and P. japonica larvae for S. scarabaei, G. mellonella larvae for the other nematodes) might have had an impact on the nematodes dispersal and relative attraction behavior. This study indicates that host attractiveness and nematode dispersal rates may contribute but do not play a major role in the variability in white grub susceptibility and/or nematode virulence.

Effects of Turfgrass Endophytes (Clavicipitaceae: Ascomycetes) on White Grub (Coleoptera: Scarabaeidae) Control by the Entomopathogenic Nematode Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae)

Abstract We evaluated the effect of endophyte infection in the two turfgrasses tall fescue (Festuca arundinacea Schreber) and strong creeping red fescue (F. rubra L. ssp. rubra) on the susceptibility of three white grub species to the entomopathogenic nematode Heterorhabditis bacteriophora Poinar. Endophyte infection in strong creeping red fescue (only tested under greenhouse conditions) had no effect on nematode-susceptibility of third-instar oriental beetle (Exomala (=Anomala) orientalis Waterhouse) and northern masked chafer (Cyclocephala borealis Arrow). In tall fescue under greenhouse conditions, endophyte infection had a weak and variable enhancing effect on nematode-susceptibility of second- and third-instar E. orientalis and no effect on nematode susceptibility of third-instar C. borealis and Popillia japonica. However, under field conditions with natural white grub populations, endophyte infection in tall fescue had no significant effects on nematode efficacy against E. orientalis, P. japonica, and C. borealis. While it is possible that stronger interactions between endophytes and nematodes may occur with different grass species, cultivars, and endophyte strains, nematode-endophyte interactions appear to be too variable to allow predictions on nematode efficacy based on turfgrass endophyte status.