UTILIZATION OF ENTOMOPATHOGENIC NEMATODES IN THE BIOLOGICAL CONTROL OF PESTIFEROUS INSECTS

Knowledge Area (KA)	Subject of Investigation (SOI)	Field of Science (FOS)	Percent
212	3130	1120	100%

Progress 10/01/02 to 09/30/07

Outputs
OUTPUTS: During the past 5 years, a number of major outputs have been accomplished. These include a series of experiments where the entomopathogenic nematode, Steinernema carpocapsae, was reared on mutant and wild-type mutualistic bacterium Xenorhabdus nematophila resulting in infective juveniles (IJs) with and without the mutualistic bacteria. IJs without their bacteria killed insect pests and can be used where no establishment of an alien S. carpocapsae is desired in the environment. In another experimental series, we demonstrated that infectivity two entomopathogenic nematode species, S. carpocapsae and Heterorhabditis indica, were not effective against worker termites. The output of this termite study is that these nematodes should not be used as a control option for the subterranean termite species, Coptotermes formosanus. In a third series of experiments, we used a Peruvian isolate of a cold-adapted Heterorhabditis species, Alcazar-1, which was effective against the Andean potato weevils, Premnotrypes spp. Although the potato weevil complex is not established in California, potatoes are produced in cold climates. Thus, the output of our research demonstrated that nematodes such as Alcazar-1 may be used against the potato weevils should they become established in California. Finally, our research has shown that mites in the genus Sancassania will consume infective juveniles of Steinernema and this predatory activity can adversely affect the biological control potential of these nematodes. During the course of this project, seminars have been given at major universities and scientific presentations have been made at international and national society meetings. Training was given to scientists in Peru and scientists from Ukraine, Peru, and Azerbaijan have been trained in my laboratory. PARTICIPANTS: My research program involves significant collaboration with international scientists in Korea and Turkey. These scientists (i.e., Dr. H. Y. Choo and Dr. D. W. Lee from Korea and Dr. S. Hazir from Turkey) were trained in my laboratory and we designed experiments in my laboratory or during visits to their laboratory resulting in publishable data. I also have collaborative projects with a USDA scientist (Dr. L. A. Lacey). TARGET AUDIENCES: The target audiences for the research are cooperative extension specialists, farm advisors, growers, pest control applicators, home owners, organic growers, and individuals who are interested in using biological control approaches to control insect pests.

Impacts
The use of the entomopathogenic nematode, Steinernema carpocapsae, without their mutualistic bacterium, Xenorhabdus nematophila, can be used to control some soil insect pests such as the beet armyworm, Spodoptera exigua. In laboratory and greenhouse, the absence of the bacterial symbiont inhibited nematodes from producing infective juvenile (IJ) progeny within the host cadavers, but resulted in excellent host mortality. Thus, IJs without their symbiotic bacterium can be used for biological control in situations where no establishmen of this nematode species is desired. In contrast, the attachment and infectivity of two entomopathogenic nematode species, S. carpocapsae and Heterorhabditis indica, against the subterranean termite species, Coptotermes formosanus, showed that a high number of nematodes are needed to kill worker termites. The mechanism to avoid nematode infection is partly due to termite grooming behavior, but inability of the nematode to recognize termites as hosts also appears to play an important role. S. carpocapsae and H. indica are not effective control agents against C. formosanus. Working with an undescribed, cold-adapted Heterorhabditis (Alcazar-1) species isolated from the Peruvian Andes, we demonstrated that this nematode was effective against the potato weevil, Premnotrypes suturicallus, a major pest of potato tubers in Peru. Laboratory bioassays conducted in Peru showed that the nematode protected potato tubers from infestations by neonate P. suturicallus larvae and killed weevil larvae within the tubers before significant damage was incurred. Median lethal concentration (LC50) for P. suturicallus pre-pupae was 5.9 IJs per host reflecting high susceptibility. Alcazar-1 was also infective to G. mellonella larvae at temperatures similar to those recorded for daily fluctuations in the Andes. Entomopathogenic nematodes are also subject to attack by natural enemies. One of the most common natural enemies is soil mites and our research showed that mites in the genus Sancassania will consume Steinernema IJs. Such predatory activity by mites and other natural enemies can adversely affect the biological control of insect species in soil. The results of our research have shown that entomopathogenic nematodes can be effective against some species of soil insect pests such as the beet armyworm and potato weevil, but other insects are nearly refractory to nematode infection requiring uneconomical concentration levels to obtain a low level of mortality. Another major factor that affects use of these nematodes is that they have their own natural enemies. Accordingly, we have demonstrated the importance of having the right species of nematodes for an insect pest, developed innovative ideas on how to use these nematodes, shown that not all insect pests are susceptible to nematode infection, and reported on a mite species that can affect the effectiveness of the nematode.

Publications

Hazir, C., Giblin-Davis, R.M., Keskin, N., Ye, W., Kanzaki, N., Center. B. J., Hazir, S., Kaya, H.K. and Thomas, W.K. 2007. Bursaphelenchus debrae n. sp. (Nematoda: Parasitaphelenchidae), an associate of the bee Halictus brunnescens in Turkey. Nematology 9: 777-789.
Karagoz, M., Gulcu, B., Cakmak, I., Kaya, H.K. and Hazir, S. 2007. Predation of entomopathogenic nematodes by Sancassania sp. (Acari: Acaridae). Exp. Appl. Acarol. 43: 85-95.
Stevens, G.N., Arimoto, H., Ruiz-Vega, J., Kaya, H.K. and Lewis, E.E. 2008. Investigating and exploiting the influence of host desiccation on the emergence and infectivity of entomopathogenic nematodes. Biol. Control. Accepted pending revision.
Stevens, G.N., Lewis, E.E. and Kaya, H.K. 2008. Potential multitrophic influences of soil heterogeneity: roots, insect root herbivores, and entomopathogenic nematodes. Biopesticides Intern. In press.
Dara, S.K., McGuire, M.R. and Kaya, H.K. 2007. Isolation and evaluation of Beauveria bassiana (Deuteromycotina: Hypomycetes) for the suppression of the glassy-winged sharpshooter, Homalodisca caogulata (Homoptera: Cicadellidae). J. Entomol. Sci. 42, 56-65.
Lee, D.W., Choo, H.Y., Smitley, D.R., Lee, S.M., Shin, H. K., Kaya, H. K., Park, C.O. and Park, J. K. 2007. Distribution and adult activity of Popillia quadriguttata (Coleoptera: Scarabaeidae) on golf courses in Korea. J. Econ. Entomol. 100: 103-109.
Hang, D.T., Choo, H.Y., Lee, D.W., Lee, S.M., Kaya, H.K. and C.G. Park, C.G. 2007. Temperature effects on Korean entomopathogenic nematodes, Steinernema glaseri and S. longicaudum, and their symbiotic bacteria. J. Microbiol. Biotechnol. 17: 420-427.
Lacey, L.A. and Kaya, H.K. 2007. Field Manual of Techniques in Invertebrate Pathology. 2nd Ed. Springer, Dordrecht, The Netherlands.

Progress 01/01/06 to 12/31/06

Outputs
Andean potato weevils, Premnotrypes spp., are the most important insect pests of potatoes throughout the Andean region. Although they are endemic to the Andes, no significant natural enemies of these pests have been reported until the discovery of an undescribed entomopathogenic nematode in the genus Heterorhabditis. This nematode was isolated from potato weevils that were infected at high rate in a commercial potato storage unit in Peru and was designated as strain Alcazar-1. The potential of this nematode to suppress potato weevil, Premnotrypes suturicallus, populations was evaluated. Evaluations were also made on the tolerance of this nematode to the cold Andean temperatures, its infectivity against different stages of P. suturicallus, and its recycling potential within this host. Because the potato weevil does not occur in North America, Alcazar-1 was tested on a surrogate host, Galleria mellonella, at UC Davis. Alcazar-1 was infective to G. mellonella larvae at temperatures similar to those recorded for daily fluctuations in the Andes. In laboratory bioassays conducted in Peru, the nematode protected potato tubers from infestations by neonate P. suturicallus larvae and killed weevil larvae within the tubers before significant damage was incurred. Median lethal concentration (LC50) for P. suturicallus pre-pupae was 5.9 infective juveniles per host reflecting high susceptibility. Alcazar-1 has a high reproductive potential in P. suturicallus pre-pupae, producing an average of 97,817 infective juveniles per host. These results suggest that Alcazar-1 has excellent potential for biological control of the Andean potato weevil.

Impacts
Entomopathogenic nematodes such as Heterorhabditis sp. Alcazar-1 can be effective biological control agents against potato weevil larvae. Alcazar-1 is adapted to cold temperatures where much of California potatoes are grown. Should the potato weevil become established in California, baseline data on the effectiveness of cold-adapted entomopathogenic nematodes are now available.

Publications

Kaya, H. K. and Lewis, E. E. 2006. Third International Symposium on Entomopathogenic Nematodes and Symbiotic Bacteria. Biol. Control 38:1-3.
Lewis, E. E., Campbell, J., Griffin, C., Kaya, H. and Peters, A. 2006. Behavioral ecology of entomopathogenic nematodes. Biol. Control 38: 66-79.
Kaya, H. K., Aguillera, M. M., Alumai, A., Choo, H. Y., de la Torre, M., Fodor, A., Ganguly, S., Hazır, S., Lakatos, T., Pye, A., Wilson, M., Yamanaka, S., Yang, H. and Ehlers, R.-U. 2006. Status of entomopathogenic nematodes and their symbiotic bacteria from selected countries or regions of the world. Biol. Control 38: 134-155.
Parsa, S., Alcazar, J., Salazar, J., and Kaya, H. K. 2006. An indigenous Peruvian entomopathogenic nematode for suppression of the Andean potato weevil. Biol. Control 39: 171-178.

Progress 01/01/05 to 12/31/05

Outputs
The attachment and infectivity of two entomopathogenic nematode species, Steinernema carpocapsae and Heterorhabditis indica, on soldiers and workers of a subterranean termite species, Coptotermes formosanus were investigated. With S. carpocapsae, more nematodes attached to soldiers of C. formosanus in the absence of workers compared to soldiers that were in the presence of workers. With soldiers alone, workers alone and mixture of equal numbers of workers and soldiers, soldiers in the mixed groups had lower mortality than soldiers alone after 1 and 4 days. Exposure of small groups of C. formosanus to S. carpocapsae resulted in higher mortality of soldiers after 1- and 4-days post exposure. Mortality in soldiers alone exposed to H. indica was not significant compared to mortality in mixed groups at 1-day exposure, but was significant after 4 days. Termite soldiers experienced rapid mortality when exposed to S. carpocapsae. When soldiers alone or workers alone are exposed to the nematodes, there is a differential susceptibility of soldiers and workers to nematode infection with soldiers being more susceptible than workers. Most importantly, a high number of nematodes are needed to kill worker termites and S. carpocapsae and H. indica are not effective control agents against C. formosanus. The mechanism to avoid nematode infection is partly due to termite grooming behavior, but inability of the nematode to recognize termite as a host is being investigated.

Impacts
Entomopathogenic nematodes should not be used against subterranean termites until a more virulent nematode can be isolated. In part, grooming behavior of the worker termites appears to be the mechanism to avoid nematode infection.

Publications

Godfrey, L. D., Grafton-Cardwell, E. E., Kaya, H. K. and Chaney, W. E.. 2005. Microorganisms and their byproducts, nematodes, oils and particle films have important agricultural uses. Calif. Agric. 59(1): 35-40.
Mankowski, M., Kaya, H. K., Grace, J. K. and Sipes, B. S. 2005. Differential susceptibility of subterranean termite castes to entomopathogenic nematodes. Biocontrol Sci. Technol. 15: 367-377.

Progress 01/01/04 to 12/31/04

Outputs
Steinernema carpocapsae was reared on mutant and wild-type bacterium Xenorhabdus nematophila. Nematodes reared on the mutant X. nematophila HGB151, in which an insertion of the bacterial gene, rpoS, eliminates the retention of the bacterium in the intestinal vesicle of the nematode, produced infective juveniles without their symbiotic bacterium. Nematodes reared on the wild-type bacterium (HGB007) produced infective juveniles with their symbiotic bacterium. The two bacterial strains were not significantly different in their effect on progeny production, sex ratio, or nematode morphology. Infective juveniles with or without their symbiotic bacterium were equally infectious to the beet armyworm, Spodoptera exigua, larvae in laboratory and greenhouse and across a range of soil moistures, but the absence of the bacterial symbiont inhibited nematodes from producing infective juvenile progeny within the host cadavers. Initial studies with the subterranean termite, Coptotermes formosanus, indicate that the workers are not highly susceptible to S. carpocapsae or Heterorhabditis bacteriophora.

Impacts
In some situations where no establishment of an alien entomopathogenic nematode is desired in the environment, the use of Steinernema carpocapsae without their symbiotic bacterium may be used to control some soil insect pests. The use of entomopathogenic nematodes should not be used against termites until a more virulent nematode can be isolated.

Publications

Mitani, D. K., Kaya, H. K. and Goodrich-Blair, H. 2004. Comparative study of the entomopathogenic nematode, Steinernema carpocapsae, reared on mutant and wild-type Xenorhabdus nematophila. Biol. Control 29: 382-391.
Kaya, H. K. and Koppenhofer, A. M. 2004. Biological control of insects and other invertebrates with nematodes. In: Nematology--Advances and Perspectives, Vol II, Z. X. Chen, S. Y. Chen, and D. W. Dickson, eds. Tsinghua University Press, Beijing, P. R. China. Pp. 447-496.

Progress 01/01/03 to 12/31/03

Outputs
The neonicotinoid insecticide, imidacloprid, interacted synergistically with five entomopathogenic nematode species against five white grub species. Tank mixing this insecticide had no negative effect on nematode survival and infectivity at the recommended field rate of application. Combined application of imidacloprid and nematodes had no negative effect on white grubs producing nematode progeny. Moreover, synergistic activity with this insecticide and nematode combination was observed. In a survey conducted for entomopathogenic nematodes in Oaxaca State, Mexico, three isolates identified as Steinernema feltiae, Steinernema species and Heterorhabditis bacteriophora were found. These nematode species are being evaluated against white grubs.

Impacts
The application of combination of imidacloprid and entomopathogenic nematodes has shown that this combination provides consistent synergistic results against white grub pests in turfgrass. This combination needs less chemical pesticide and nematodes, provides excellent control of the white grubs and will benefit turfgrass managers where grubs are a problem, especially in high value turfgrass. The isolation of nematode species in Mexico provides new of genetic and biological control material for use against soil insect pests.

Publications

Campbell, J. F., Lewis, E. E., Stock, S. P., Nadler, S. and Kaya, H. K. 2003. Evolution of host search strategies in entomopathogenic nematodes. J. Nematol. 35:142-145.
Koppenhofer, A. M., Cowles, R. S., Cowles, E. A., Fuzy, E. M. and Kaya, H. K. 2003. Effect of neonicotinoid synergists on entomopathogenic nematode fitness. Entomol. Exp. Appl. 106: 7-18.
Ruiz Vega, J., Aquino Bolanos, T., Kaya, H. K. and Stock, P. 2003. Colecta y evaluacion de nematodos entomopathagenos para el control de gallinas ciegas Phyllophaga vetula (Horn) en Oaxaca, Mexico. Folia Entomol. Mex. 42: 169-175.

Progress 01/01/02 to 12/31/02

Outputs
An ant deterrent factor(s) (ADF) produced by Xenorhabdus nematophila and Photorhabdus luminescens, the symbiotic bacteria of the nematodes, Steinernema carpocapsae and Heterorhabditis bacteriophora, respectively, was investigated in vitro and in vivo. In vitro studies showed that ADF activity was present in the supernatants of bacterial cultures. The compound(s) was filterable, heat stable, and acid sensitive, and passed through a 10-kDa pore-sized membrane. Thus, ADF appeared to be a small, extra-cellular, and possibly non-proteinaceous compound(s). The degree of ADF repellency detected depended on the ant species being tested, the sucrose concentration, and the strain, form, and age of the ADF-producing bacteria. In vivo studies showed that the ants touched the bacteria-killed insect with their antennae, but often left the cadaver without feeding on it. This was in contrast to a freeze-killed control insect which was readily consumed. These findings demonstrate that the symbiotic bacteria of some species of entomopathogenic nematodes produce a compound(s) that deters scavengers such as ants and thus could protect nematodes from being eaten during reproduction within insect cadavers.

Impacts
The ant deterrent factor(s) (ADF) protects the nematode-killed insects from being consumed by scavengers and allows for the nematodes to reproduce and recycle in the soil environment. The nematodes are then able to exert natural biological control of soil insect pests. In addition, isolation of the ADF compound(s) may eventually serve as a means to deter or repel insect pests from crops or domestic animals.

Publications

Lacey, L. A., Rosa, J. S., Simoes, N. O., Amaral, J. J. and Kaya H. K. 2001. Comparative dispersal and larvicidal activity of exotic and Azorean isolates of entomopathogenic nematodes against Popillia japonica (Coleoptera: Scarabaeidae). Euro. J. Entomol. 98: 439-444.
Kaya, H. K. 2002. Natural enemies and other antagonists, in: Entomopathogenic Nematology, R. Gaugler, ed. CAB International, Wallingford, UK, pp. 189-203.
Zhou, X., Kaya, H. K., Heungens, K. and Goodrich-Blair, H.. 2002. Response of ants to a deterrent factor(s) produced by the symbiotic bacteria of entomopathogenic nematodes. Appl. Environ. Microbiol. 68: 6202-6209.

Progress 01/01/01 to 12/31/01

Outputs
The development of five geographic isolates of the entomopathogenic nematode, Steinernema feltiae, was examined in an insect host at 5, 8, 10, 15, 20, 25, and 28 C. Three nematode isolates were from Mediterranean region, two were from the subtropical region, and one was from tropical region. All isolates killed 100 percent of the insect hosts and developed and produced progeny between 8 and 25 C. At 28 C, mortality was 100 percent, but no nematode progeny was observed. The highest infective nematode production was observed at 15 C for all isolates. The tropical isolate had the lowest production of infective nematodes. At 25 C, the infective nematodes emerged from the host cadavers from 5 to 7 days. At 25 C, four out of the five isolates had shorter times to host death. Longer infective nematodes were observed at 8 C than at 15 and 23 C. The data suggest that the developmental time influences the body length of the infective nematode.

Impacts
Developmental temperatures of entomopathogenic nematodes can predict whether the nematodes will successfully reproduce and continue to infect pest species in the field. Geographical isolates showed very little differences in temperature tolerance in infectivity and reproduction. All else being equal, these isolates could be used in biological control programs within the tolerant temperature ranges.

Publications

Hazir, S., Stock, S. P., Kaya, H. K., Koppenhofer, A. M. and Keskin, N. 2001. Developmental temperature effects on five geographic isolates of the entomopathogenic nematode Steinernema feltiae (Nematoda: Steinernematidae). J. Invertebr. Pathol. 77:243-250.
Lacey, L. A., Frutos, R., Kaya, H. K. and Vail, P. 2001. Insect pathogens as biological control agents: do they have a future? Biol. Contr. 21:230-248.

Progress 01/01/00 to 12/31/00

Outputs
Infective juveniles of the entomopathogenic nematodes, Steinernema carpocapsae, S. siamkayai, and S. scapterisci, are classified as ambush foragers. They attach to passing insects by standing on their tails and contacting an insect directly when standing or jumping. They responded to small air movements by increased waving and jumping behavior, and jumps were directionally biased towards the source of the movement. Mechanical contact, air movement, and host associated volatile cues were important triggers of jumping behavior for S. Carpocapsae and S. scapterisci, but host cues did not increase the proportion of jumping for S. siamkayai. Jumping by the nematodes is accomplished using a two-step process of forming and contracting a loop. The nematode bends the anterior half of its body until the head region makes contact with the side of the body. The body becomes contorted, the cuticle kinks, and sufficient energy is generated to propel the nematode through the air.

Impacts
By understanding the behavior of the infective juveniles of entomopathogenic nematodes, we can predict their biological control potential against insect pest species. For example, the steinernematid juveniles with an ambush strategy can be used against mobile insect pests.

Publications

Campbell, J. F, and Kaya, H. K. 1999. Mechanism, kinematic performance, and fitness consequences of jumping behavior in entomopathogenic nematodes (Steinernema spp.). Can. J. Zool. 77:11947-1955.
Campbell, J. F., and Kaya, H. K. 2000. Influence of insect associated cues on the jumping behavior of entomopathogenic nematodes (Steinernema spp.). Behaviour 137:591-609.
Lacey, L. A., and Kaya, H. K. (eds.). 2000. Manual of Field Techniques in Invertebrate Pathology. Kluwer Academic Publishers, Dordrecht, The Netherlands.

Progress 01/01/99 to 12/31/99

Outputs
The phased infectivity hypothesis has been invoked to explain low infection rates by infective juveniles of steinernematid and heterorhabditid nematodes. This hypothesis proposes that any given point in time not all individuals are infectious. We tested this hypothesis experimentally and showed that phased infectivity does not occur in three species of steinernematids (Steinernema carpocapsae, S. glaseri, and S. feltiae). The infective juveniles of these three species were recovered within their insect hosts. That is, when sufficient insect hosts were present, the steinernematids infected them. However, infective juveniles of one heterorhaditid species Heterorhabditis bacteriophora) frequently did not infect all available hosts suggesting that phased infectivity did occur with this species. In another study, jumping behavior by a steinernematid species (S. carpocapsae) was shown to be important in host finding. When the infective juvenile stood on its tail, it was triggered to jump by the presence of host-associated volatile cues. The direction of the jump tended to be towards the source of the host cues. This directional jumping towards the host could be an adaptation for host attack by this parasite.

Impacts
Understanding the behavior of the infective juveniles of these nematodes has implications for their successful use as biological control agents. For example, the steinernematid juveniles were all infectious, and if they found a host, they would infect it. The heterorhabditid juveniles would require a higher application rate to infect the available host. The phased infectivity of the heterorhabditid would be an advantage if hosts migrated into the treated area.

Publications

Campbell, J. F. and Kaya, H. K. 1999. How and why insect parasitic nematodes jump. Nature 397:485-486.
Campbell, J. F., Koppenhofer, A. M.Kaya, H. K. and B. Chinnasri, B. 1999. Are there temporarily non-infectious dauer stages in entomopathogenic nematode populations: a test of the phased infectivity hypothesis. Parasitology 118:499-508.
Kaya, H. K., Koppenhofer, A. M. and Johnson, M. 1998. Natural enemies of entomopathogenic nematodes. Jpn. J. Nematol. 28:13-21.
Kondo, E. and Kaya, H. K. 1998. Recent development of biological control by beneficial nematodes: synopsis and discussion. Jpn. J. Nematol. 28:75-78.
Stock, S. P., Pryor, B. M. and Kaya, H. K. 1999. Distribution of entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) in natural habitats in California, USA. Biodiver. Conserv. 8:535-549.

Progress 01/01/98 to 12/01/98

Outputs
In greenhouse tests, combinations of the insecticide imidacloprid and an entomopathogenic nematode, HETERORHABDITIS BACTERIOPHORA, against field-collected third instar CYCLOCEPHALA HIRTA and C. PASADENAE showed strong synergistic effects. The synergism between imidacloprid and the entomopathogenic nematode occurred at concentrations of imidacloprid ranging from 50 to 200 g (AI)/ha and H. BACTERIOPHORA at 400,000,000 infective juveniles/ha. When the infective juveniles of H. BACTERIOPHORA were agitated in solutions of imidacloprid for 24 hours, no negative effect on their survival and infectivity was observed. In a field study, the entomopathogenic nematode, STEINERNEMA CARPOCAPSAE, provided 41 percent control of larvae of the diamondback moth whereas BACILLUS THURINGIENSIS gave 44 percent control. The combination of S. CARPOCAPSAE and B. THURINGIENSIS provided 58 percent control of diamondback moth larvae.

Impacts
(N/A)

Publications

KOPPENHOFER, A. M., and KAYA, H. K. Synergism of imidacloprid and an entomopathogenic nematode: a novel approach to white grub (Coleoptera: Scarabaeidae) control in turfgrass. J. Econ. Entomol.
BAUR, M. E., KAYA, H. K., TABASHNIK, B. E., and CHILCUTT, C. F. Suppression of diamondback moth (Lepidoptera: Plutellidae) with an entomopathogenic nematode (Rhabditida: Steinernematidae) and BACILLUS THURINGIENSIS Berliner. J. Econ. Ent.
GEORGIS, R., and KAYA, H. K. Advances in entomopathogenic nematode formulation, pp. 289-308 in: Formulation of Microbial Biopesticides, Beneficial Microorganisms Nematodes and Seed Treatments, H. D. Burges, ed. Kluwer Academic Publishers,.

Progress 01/01/97 to 12/01/97

Outputs
The interactions between entomopathogenic nematodes and the bacterium, BACILLUS THURINGIENSIS subspecies JAPONENSIS (Buibui strain), on the white grub, CYCLOCEPHALA HIRTA and C. PASADENAE, caused additive grub mortalities or greater than additive mortalities including synergism. To achieve this additive or synergistic effects, the grubs had to be exposed to the bacterium at least 7 days before they were treated with the nematodes, STEINERNEMA GLASERI or HETERORHABDITIS BACTERIOPHORA. However, S. KUSHIDAI showed no additive or synergistic effect with the bacterium. Comparing the ability of in vitro-produced, commercially formulated with in vivo-produced, nonformulated STEINERNEMA CARPOCAPSAE showed that in vivo- produced nematodes were more efficacious against black cutworm and diamondback moth larvae than in-vitro produced nematodes. The in vitro-produced, formulated nematodes were desiccated and required 24 to 72 h to rehydrate. Nematodes that had rehydrated for 72 h were more efficacious than those that had rehydrated for a shorter period of time.

Impacts
(N/A)

Publications

KOPPENHOFER, A. M., and KAYA, H. K. 1997. Additive and synergistic interaction between entomopathogenic nematodes and BACILLUS THURINGIENSIS for scarab grub control. Biol. Contr. 8:131-137.
BAUR, M. E., KAYA, H. K., and TABASHNIK, B. E. 1997. Efficacy of a dehydrated steinernematid nematode against black cutworm (Lepidoptera:Noctuidae) and diamondback moth (Lepidoptera:
BAUR, M. E., KAYA, H. K., GAUGLER, R., and TABASHNIK, B. 1997. Effects of adjuvants on entomopathogenic nematode persistence and efficacy against PLUTELLA XYLOSTELLA. Biocontr. Sci. Technol. In

Progress 01/01/96 to 12/30/96

Outputs
The interactions between two entomopathogenic nematode species, STEINERNEMA CARPOCAPSAE, an ambush forager, and S. GLASERI, a cruise forager, were studied. Both nematode species were provided wax moth larvae as hosts at 0, 2, or 10 cm soil depth. Populations of infective juveniles in soil were monitored at 30-day intervals over 120 days using wax moth larvae as baits. With hosts at 2 or 10 cm depth, the presence of S. GLASERI had a strong negative effect on S. CARPOCAPSAE, but S. GLASERI was not affected by the presence of S. CARPOCAPSAE. S. CARPOCAPSAE dominated over S. GLASERI at 0 cm depth. If two nematode species with different foraging strategies are present in soil, they can coexist providing that hosts are present through the soil habitat. In a morphometric study of HETERORHABDITIS species, male characters such as testis reflexion and total length and infective juvenile characters such as tail length and total length are useful and reliable for identification to the species level.

Impacts
(N/A)

Publications

STOCK, S. P., and KAYA, H. K. 1996. A multivariate analysis of morphometric characters of HETERORHABDITIS species (Nemata: Heterorhabditidae) and the role of morphometrics in the taxonomy of species of the genus. J. Parasitol. 8:806-8.
KOPPENHOFER, A. M., BAUR, M. E., and KAYA, H. K. 1996. Competition between two steinemematid nematode species for an insect host at different soil depths. J. Parasitol. 82:34-40.
KOPPENHOFER, A. M., and KAYA, H. K. 1996. Coexistence of entomopathogenic nematode species (Steinernematidae, Heterorhabditidae) with different foraging behavior. Fund. Appl. Nematol. 19:175-183.
TACHIBANA, M., HORI, H., SUZUKI, N., UECHI, T., KOBAYASHI, D., IWAHANA, H., and KAYA, H. K. 1996. Larvicidal activity of the symbiotic bacterium XENORHABDUS JAPONICUS from the entomopathogenic nematode STEINERNEMA KUSHIDAI against cupreous.
KOPPENHOFER, A. M., JAFFEE, B. A., MULDOON, A. E., STRONG, D. R., and KAYA, H. K. 1996. Effect of nematode-trapping fungi on an entomopathogenic nematode originating from the same field site in California. J. Invertebr. Pathol. 68:246-252.
STRONG, D. R., KAYA, H. K., WHIPPLE, A., CHILD, A., KRAIG, S. BONDONNO, M., DYER, K. and MARON, J. L. 1996. Entomopathogenic nematodes: natural enemies of root-feeding caterpillars on bush lupine. Oecologia 108:167-173.

Progress 01/01/95 to 12/30/95

Outputs
The presence of hosts at different depths of soil and the influence of differentsoil moistures on the infectivities of two insect parasitic nematode species, STEINERNEMA CARPOCAPSAE (SC) and S. GLASERI (SG), were investigated. At -0.006 MegaPascal (Mpa) water potential in a sandy loam soil, SC tended to be equally infective at depths between 0 and 10 cm whereas SG showed consistent infectivity from 2 to 10 cm but was inconsistently less infective at 0 cm. SC started infecting hosts at -5 MPa (dry soil) and had the highest infectivity between -0.1 MPa and -0.01 MPa. In very wet soils, SC was not as infective as compared to the intermediate moisture levels. SG was more restricted at the low soil moistures. It started infecting hosts at -0.3 MPa. Its infectivity increased constantly at higher soil moistures but dropped in water saturated soil (-O.003 MPa). In soil competition studies, we demonstrated that SC, an ambush forager, was superior to SG, a cruiser forager when competing for a host on the soil surface, but below the soil surface SG was superior to SC. Within an insect host, SG outcompeted SC. The intrinsic superiority of SG was ascribed to its faster development that deprives its slower SC competitor of food resources.

Impacts
(N/A)

Publications

Progress 01/01/94 to 12/30/94

Outputs
Exposure to NaCl, KCl, and CaCl2 affected HETERORHABDITIS BACTERIOPHORA and STEINERNEMA GLASERI differently. Survival, virulence and penetration efficiency of S. GLASERI were not affected by these salts except at high concentrations. KCl and CaCl2 had no effect on H. BACTERIOPHORA survival, virulence and penetration efficiency, but NaCl adversely affected this nematode at each of these parameters at high salinity NaCl appeared to be toxic to H. BACTERIOPHORA and affected its host-finding behavior. S. CARPOCAPSAE was attracted to roots of marigold and tomato. Aqueous root extracts of marigold and tomato did not adversely affect infectivity of S. GLASERI compared with the control, but alpha-terthienyl, a root exudate of marigolds, at concentrations of 10, 20, and 40 ppm reduced the proportion that infected insects by 28, 55, and 64%, respectively. Very little is known about the biology of the nematode, AGAMERMIS UNKA, an important parasite of the brown planthopper. The sex ratio showed that the there was a heavy bias towards female. Temperature influenced egg hatch with 25 C being optimal.

Impacts
(N/A)

Publications

Progress 01/01/93 to 12/30/93

Outputs
The entomopathogenic nematodes, HETERORHABDITIS BACTERIOPHORA and STEINERNEMA GLASERI, were exposed to different concentrations of various salt solutions (sodium chloride, potassium chloride, and calcium chloride). The nematodes' survival, virulence and penetration efficiency were not affected by these salts normally found in soils with high salinity. We conclude that these two nematode species should be efficacious against insect pests in agricultural soils with high salinity. In other studies, combining two entomopathogenic nematodes with different search strategies suppressed two pest species of soil insects when they occurred in the same habitat. STEINERNEMA CARPOCAPSAE which has a sit and wait strategy and tends to be near the surface was effective against the caterpillars of the black cutworm which feeds near the soil surface. HETERORHABDITIS BACTERIOPHORA which has an active foraging strategy and occurs deeper in the soil profile was effective against larvae of the black vine weevil which feeds on roots of ornamental plants.

Impacts
(N/A)

Publications

Progress 01/01/92 to 12/30/92

Outputs
A field test was conducted against third instar CYCLOCEPHALA HIRTA that includedthe following treatments: untreated control; chemical insecticide, bendiocarb; milky disease bacterium, BACILLUS POPILLIAE; and entomopathogenic nematodes, STEINERNEMA FELTIAE and HETERORHABDITIS BACTERIOPHORA. There were no significant differences in population reduction among the treatments, but the larval population in all plots showed a dramatic decline. The C. HIRTA population had a natural occurrence of milky disease and blue disease caused by RICKETTSIELLA POPILLIAE. The prevalence of blue disease during the course of the study averaged less than 10% but that of milky disease averaged about 20%. More significantly, the soil from all treatment plots when bioassayed for B. POPILLIAE showed that 67 to 90% of the larvae became infected with the bacterium. None of the larvae became infected with the blue disease organism. Thus, we conclude that B. POPILLIAE was occurring in epizootic proportions in our field tests and was a significant mortality factor in causing the decline of the C. HIRTA population.

Impacts
(N/A)

Publications

Progress 01/01/91 to 12/30/91

Outputs
The impact of the nematode-parasitic fungus HIRSUTELLA RHOSSILIENSIS on the effectiveness of three entomopathogenic nematode species was assessed against a susceptible insect host in soil. The presence of fungal conidia on the third-stage cuticle of STEINERNEMA CARPOCAPSAE and HETERORHABDITIS BACTERIOPHORA interfered with infection of insect larvae. Conidia on the third-stage cuticle of STEINERNEMA GLASERI and on the ensheathing second-stage cuticle of H. BACTERIOPHORA did not reduce the nematodes' ability to infect the insect larvae. The LD50 values for S. CARPOCAPSAE, S. GLASERI, and H. BACTERIOPHORA in sand containing the insect-parasitic fungus were not different from those from sterilized sand when susceptible insect hosts were added at the same time as the nematodes. However, when the insects were added 3 days after the nematodes, the LD50 of S. GLASERI was higher in fungal-infested sand than sterilized sand, whereas the LD50 of H. BACTERIOPHORA was the same in infested and sterilized sand. The LD50 value for S. CARPOCAPSAE could not be calculated because the data were too variable to detect significant differences. In other studies, H. BACTERIOPHORA and S. GLASERI can survive in sea water suggesting that soil used in ship ballasts was one means through which these nematodes have become distributed throughout the world. H. BACTERIOPHORA can survive and infect insects in sand at salt (NaC1 or KC1) concentrations up to electrical conductivity of 18.

Impacts
(N/A)

Publications

Progress 01/01/90 to 12/30/90

Outputs
The nematode-parasitic fungus, HIRSUTELLA RHOSSILIENSIS, affects the survival ofentomopathogenic nematodes in soil. Nematode survival was lower in nonsterilized soil than in sterilized soil containing the fungus. Differential survival among nematode species was observed. Survival of STEINERNEMA GLASERI, a motile species which does not retain the second stage cuticle, was significantly less than HETERORHABDITIS BACTERIOPHORA, a motile species which loses its second stage cuticle, or S. CARPOCAPSAE, a less motile species which loses its second stage cuticle. In other studies, entomopathogenic nematodes outcompeted the entomopathogenic fungus, BEAUVERIA BASSIANA. In the soil, the nematodes were found more frequently near healthy hosts than fungal-infected hosts. These data suggest that the antagonistic relationship between B. BASSIANA and the nematodes are minimized in the soil. Entomopathogenic nematodes have been isolated from five of the six major Hawaiian islands. Of 351 sites representing diverse ecological habitats, 22 sites were positive for a HETERORHABDITIS s. (probably a new species) and two sites were positive for STEINERNEMA s. (near FELTIAE). The heterorhabditids were isolated primarily from the coastal areas in sandy soils suggesting that they may have been introduced on soil used as ship ballasts. Research on the effect on salinity on nematode survival is being pursued.

Impacts
(N/A)

Publications

Progress 01/01/89 to 12/30/89

Outputs
The persistence of Heterorhabditis bacteriophora was evaluated in agricultural soil in Davis, and the nematode was recvered for more than a year after application. The persistence of this nematode was attributed to the presence of insect hosts which allowed the nematode to recycle. Slow-release of Steinernema carpocapsae and H. bacteriophora encapsulated in 1.5% alginate gels at 20, 25, and 30C showed that H. bacteriophora was released faster than S. carpocapsae at all three temperatures. More nematodes were released at 25 and 30C than at 20C. The second-stage cuticle ensheathing the third-stage infective juveniles of S. carpocapsae and H. bacteriophora showed differences in retention. S. carpocapsae's second-stage cuticle was easily lost by movement through soil, wheareas H. bacteriophora retains its cuticle. The presence of the second-stage cuticle conferred resistance to infection by the insect-parasitic fungus, Hirsutella rhossiliensis. Loss of this second-stage cuticle resulted in fungal infection in both nematode species. The interaction of the fungus, Beauveria bassiana, and H. bacteriophora and S. carpocapsae indicate that the fungus and the nematode are not compatible when both occur in the same insect. Generally, the nematodes outcompete the fungus when both are placed in the presence of an insect host at the same time.

Impacts
(N/A)

Publications

Progress 01/01/88 to 12/30/88

Outputs
Laboratory studies were conducted to determine the effectiveness of Steinernema feltiae, 11 strain, Heterorhabditis heliothidis, NC strain, and Heterorhabditis sp. HP88 strain against the western spotted cucumber beetle, Diabrotica undecimpunctata. The LC(subscript 50) against 3rd instar beetles for S. feltiae, H. heliothidis, and Heterorhabditis HP 88 was 37, 12, and 14 infective nematodes, respectively. Field studies were conducted in San Luis Obispo, California, where natural beetle populations occurred. Zucchini (dark green var. 16815) plants were treated with S. feltiae and Heterorhabditis HP 88 because these two nematodes are available from commercial sources. Treatments were water, Diazinon, and three concentrations of each nematode species. The treatments were applied as a drench every two weeks. Fruit yield, root ratings and dry plant weight showed no significant differences among treatments. This was attributed to the patchy distribution of the larval infestation. Continued studies on the use of H. heliothidis to control black vine weevil in containerized plantings at a professional building complex in San Francisco have shown that the nematode recycled and persisted in the soil for one year. Soil which had been in the container for more than 1 year had poor nematode persistence compared with soil which had been recently obtained from the nursery. The difference in persistence is believed to be associated with greater numbers of microorganisms in older soil.

Impacts
(N/A)

Publications

Progress 01/01/87 to 12/30/87

Outputs
The slow release of the entomogenous nematodes, Steinernema feltiae, and Heterorhabditis heliothidis from 1.0, 1.5, and 2.0% alginate capsules was studied. For S. feltiae the percentage of nematodes released ranged between 59 and 67% from the 1% capsules, between 40 and 78% from the 1.5% capsules and between 15 and 66% from the 2% capsules. The majority of nematodes emerged from the 1% capsules between the 2nd and 15th day, from the 1.5% capsules between the 13th and 22nd day, and from the 2.0 capsules between the 15th and 25th day. However, considerable variations were observed as once a given capsule had nematodes emerging, the nematodes within tended to emerge about the same time. For H. heliothidis, similar emergence patterns were observed, although the emergence times tended to be 5 to 7 days earlier from the 1.5 and 2.0% capsules compared to those with S. feltiae. H. heliothidis is being used to control black vine weevil larvae in containerized plantings at a professional building complex in San Francisco. The nematodes were applied at the rate of 132 infectives/cm, and alternate hosts were placed in one treatment and not in another. By using an insect bioassay, nematodes have been recovered from the alternate host treatment plots for over 5 months but in the plots with no alternate hosts, persistence of the nematode has been for no more than 6 weeks.

Impacts
(N/A)

Publications

Progress 01/01/86 to 12/30/86

Outputs
The entomogenous nematode, Steinernema feltiae, and a tomato seed were successfully encapsulated in an alginate capsule. When these capsules were placed on 0.8% agar for 7 days, the seed germination and ca. 20% of the nematodes escaped from the capsules, whereas only 0.1% escaped from capsules without seed. When capsules containing nematodes and a seed were planted in sterilized and nonsterilized soil, nematodes escaped to infect Galleria mellonella larvae. When seed in capsules containing ca. 274 nematodes per capsule were planted in nonsterilized soil, Galleria mortality was 90% one week later. In sterilized soil, Galleria mortality was 96%. Galleria mortality declined to 27%, 23%, and 0% in weeks 2, 4, and 8 postplanting in nonsterilized soil and Galleria mortality was 81%, 51%, and 0% in weeks 2, 4, and 8 in sterilized soil. Nematode parasites in Ips paraconfusus from ponderosa pine in California and I. pini from ponderosa pine in Idaho and from Jeffery pine in California were studied. Four and five species of nematode parasites were isolated from the hemocoel of I. paraconfusus and I. pini, respectively. The parasites from I. paraconfusus were Parasitaphelenchus sp., Contortylenchus elongatus, C. reversus, and C. brevicomi, and from I. pini were Parasitaphelenchus, sp., Contortylenchus sp. 1., Contortylenchus sp. 2, C. reversus, and Parasitylenchus ovarius. Nematode parasitism was studied in relation to elevation soruce of bole and time of collection.

Impacts
(N/A)

Publications

Progress 01/01/85 to 12/30/85

Outputs
The entomogenous nematodes, Heterorhabditis and Steinernema, have been successfully encapsulated in an alginate matrix. This matrix can be utilized as a delivery system for entomogenous nematodes such as baits or slow-release of nematodes for insect control. When Heterorhabditis and Steinernema were injected into the same host, Steinernema was dominant over Heterorhabditis. However, when Heterorhabditis and Steinernema were placed into the soil with one host present, Heterorhabditis was dominant. This study showed that Steinernema was instrinsically superior within a host but extrinsically inferior when it had to compete for the same host in the soil. The opposite was true for Heterorhabditis. Studies on the nematodes in the bark beetles, Ips paraconfusus and I. pini have been initiated. Initial indications show that Parasitaphelencus, Parasitorhabditis, Contortylenchus and Parasitylenchus are present in bark beetle populations.

Impacts
(N/A)

Publications

Progress 01/01/84 to 12/30/84

Outputs
The application of the entomogenous nematode, Steinernema feltiae, was successful against the seslid borer, Synanthedon culiciformis in alder trees but not against S. resplendens in sycamore trees. The reason for the difference is that S. culiciformis occurs in moist galleries in the heartwood while S. culiciformis occurs in the bark. The dry habitat of the bark is not favorable for the nematode. Attempts to control the gypsy moth, Lymatria dispar, in Pennsylvania oak forests with S. feltiae and S. bibionis were not successful. Although 50-70% mortalities of larvae under nematode-treated nylon pack cloth lined with Terri cloth occurred, the treated trees were defoliated.

Impacts
(N/A)

Publications

Progress 01/01/83 to 12/30/83

Outputs
Mutualistically associated bacteria were isolated from two genera of nematodes; Xenorhabdus nematophilus from four species of Steinernema and X. luminescens from two species of Heterorhabditis. The soluble proteins obtained from the primary and secondary forms of these bacteria were subjected to electrophoretic examination on acrylamide gels. General protein and several isoenzyme electrophoregrams were compared. The results showed distinct subspecific differences in profiles of X. nematophilus and suggested new subspecific groupings in X. luminescens. The entomogenous nematode, Steinernema feltiae, was applied to overwintering codling moth prepupae that occurred in corrugated paper bands placed around apple tree trunks. Nematode applications made in October resulted in 80% mortality while July applications resulted in 32% mortality. February applications provided the best results with 95% mortality. The bands remained moist from rainfall during February which enhanced nematode survival. Insufficient moisture in July and October caused nematodes to desiccate and die before most could infect the codling moth.

Impacts
(N/A)

Publications

Progress 01/01/82 to 12/30/82

Outputs
No significant difference in the infectivity of Neoaplectana carpocapsae produced in vivo and in vitro to Spodoptera exigua pupae were observed. However, S. exigua pupating without pupal cells were more susceptible to N. carpocapsae than S. exigua pupating within cells. This difference was attributed to the abnormal situation of pupating without pupal cells which affected the physiology and morphology of the pupae. Field tests with N. carpocapsae against the artichoke plume moth showed that the larvae were highly susceptible and the control obtained was equal to the standard insecticide (methidathion). The associated nematode, Bursaphelenchus seani, from the reproductive tract of the solitary bee, Anthophora bomboides, grew on various fungal hosts including two insect pathogenic ones, Beauveria bassiana and Ascosphaera apis. Field observations on the association of the nematode with the bee showed that dauer juvenile formation was coincident with the occurrence of the prepupal bee stage in July.

Impacts
(N/A)

Publications

Progress 01/01/81 to 12/30/81

Outputs
The susceptibility of newly-hatched larvae of the armyworm, Pseudaletia unipuncta, to the entomogenous nematode, Neoaplectana carpocapsae, was compared with 2- and 4-day-old larvae. The newly-hatched larvae was less susceptible to nematode infection because of their migratory behavior. However, the nematode did not infect the pupae of beneficial ichneumonid and braconid parasites. The pupae were protected by a pore-free inner layer of silk within the cocoon. Furthermore, the nematode did not adversely affect the honey bee. Nematodes sprayed directly into a hive did not infect the brood due to high temperatures which are detrimental to the nematodes. A few adult workers were infected, but the overall strength of the colony was not affected. A nematode, Bursaphelenchus seani, was isolated from the reproductive tract of the solitary bee, Anthophora bomboides. This nematode does not appear to harm its host. The relationship between the nematode and bee is being investigated.

Impacts
(N/A)

Publications

Progress 01/01/80 to 12/30/80

Outputs
The suceptibility of pupae of different lepidopterous species to the entomogenous nematode Neoaplectana carpocapsae was examined. In general, soil-pupating species were less susceptible to the nematode than those that pupate above ground. However, not all above-ground-pupating insects were very susceptible to this nematode. The utilization of N. carpocapsae against the soil-pupating insect, Spodoptera exigua, was investigated further. Prepupae in soil were highly (100% infection) and pupae moderately susceptible (10-83% depending on nematode concentration). Moreover, adults which emerged from nematode-treated soil were killed by the nematode within 2 days, especially at the higher concentrations (25 and 50 nematodes/cm 2 of soil surface). The combined mortalities of pupae and adults at these concentration levels equaled 93%. The utilization of N. carpocapsae against soil-pupating insects appears to be feasible and tests to substantiate this will be conducted under simulated field conditions.

Impacts
(N/A)

Publications

Progress 01/01/79 to 01/30/80

Outputs
The nematode Neoplectana carpocapsae, which had developed and reproduced in armyworm hosts infected with agranulosis virus, contained sufficient virus to infect first and second instar armyworm larvae. Treatment of the nematode containing virus with the antiviral agent, 0.04% formaldehyde or high pH (10.0) did not inactivate the virus. Virus not in the intestinalumen of the nematode (i.e., suspended in water) was inactivated within a short time by the antiviral agents. A paper reporting these results have been accepted for publication. The behavior of nematode-infected face fly, Musca autumnalis was investigated. Female flies infected with the nematode, Heterotylenchus autumnalis, behaved differently from healthy flies. These nematode-infected flies visited faces of cattle when they were young to obtain protein. However, once the nematodes invaded the flies' ovaries, the flies tended to visit cattle dung. In contrast, healthy female flies showed a cyclical behavioral pattern of face visitation (to obtain protein) followed by dung visitation (to deposit eggs).

Impacts
(N/A)

Publications

Progress 01/01/78 to 12/30/78

Outputs
The nematode, Neoaplectana carpocapsae, developed and reproduced in armyworm hosts infected with a granulosis virus. Macerated tissues of the infective stage nematodes (dauer juveniles) from granulosis-virus-infected hosts had sufficient virus to infect 1st and 2nd instar army-worms. Examination of the dauer juveniles confirmed the presence of the virus in the intestinal lumen. No virus was observed in the tissues of the nematode. The possibility of utilizing the virus and nematode in an integrated pest management system is being pursued. Various strains of Neoaplectana carpocapsae are being tested to determine their response to high temperatures. Preliminary studies indicate that some strains are able to reproduce at 30 degrees C while other can develop to adulthood but not reproduce. The nematode, Heterotylenchus autumnalis, is an obligate parasite of the face fly, Musca autumnalis. Intensive studies at a cattle ranch in Yuba County, California showed that population densities of the host and nematode infections were highest in flies from cow pats receiving full sun. Average host population densities was 13.5 puparia per pat and nematode infection averaged 38.6%. Pats in partial sun averaged 13.5 puparia and 13.1% nematode infection. No face fly was recovered from shaded pats. When data from pats exposed during the day or night were compared, no significant differences in host population density or nematode infection rates were apparent.

Impacts
(N/A)

Publications

Progress 01/01/77 to 12/30/77

Outputs
The DD-136 strain of Neoaplectana carpocapsae can develop to adults at 30 degrees C, but cannot reproduce. At temperature above 33 degrees C, the nematode cannot survive. Therefore, the likelihood of this nematode developing in warm-blooded animals is remote. N. carpocapsae adversely affects the development of immature stages of Apanteles militaris, a gregarious internal parasitoid of the armyworm, Pseudaletia unipuncta. The infection by the nematode kills the host before A. militaris can complete its development. The nematode cannot invade and infect pupae of A. militaris encased in cocoons. However, if cocoons are cut open, pupae become infected. N. carpocapsae develops and reproduces in unparasitized armyworms, in armyworms containing 9-day-old A. militaris, and in those from which A. militaris had emerged. Significantly less nematodes reproduced in the host from which A. militaris emerged than in unparasitized or parasitized armyworms. The nematode, Heterotylenchus autumnalis, was found in face fly populations in 6 counties in northern California. Seasonal trends showed that the highest incidence of infection in face flies occurred in the spring of the year.

Impacts
(N/A)

Publications