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Home , Cosmopolites sordidus, Pachnaeus, Pachnaeus litus, Sphenophorus

CONTROL OF PESTS WITH ENTOMOPATHOGENIC NEMATODES

I. Control of with Entomopathogenic Nematodes

Kirk A. Smith biosys Palo Alto, California U.S.A.

ABSTRACT

Entomopathogenic nematodes in the genus Steinernema and Heterorhabditis have been suc- cessfully commercialized as biological control agents for a variety of curculionid species. Nema- tode-based products have been introduced for: 1) root weevils, Otiorhynchus spp. 2) billbugs, spp. 3) the apopka , Diaprepes abbreviatus, and 4) the citrus root weevil, litus. Several other species and other closely related families are potential candidates for future commercial introductions.

INTRODUCTION government, universities and industry to overcome some of these technical difficulties (Smith et al. 1992). Gaugler and Kaya (1990) recently published a There are now three major biotechnology companies complete review of current knowledge of that have been successful in introducing nematode- entomopathogenic nematodes. Klein (1990) gave a based products into some commercial and consumer condensed introduction regarding nematode efficacy markets. to the order Insecta. The intent of this paper is to provide a brief overview of entomopathogenic Production nematode efficacy against weevils, and the recent technological developments which have made Since their discovery as biological control possible the commercial success of nematode-based agents, nematodes have been produced in vivo, with products. an insect host serving as the media for nematode- Entomopathogenic nematodes in the genus bacterial growth and production. This method has Steinernema and Heterorhabditis and their limitations, because it requires a constant source of associated bacteria (Xenorhabdus spp.) have been healthy . It is also sensitive to biological successfully commercialized as biological control variation, and costs of production are high in terms agents for a variety of curculionid species. They can of equipment and man-hours. More efficient methods kill hosts rapidly, are easy to apply, and are exempted of production using in vitro methods have recently from federal and local registration requirements in been developed. Steinernema spp. are now most countries because of their safety to mammals commercially produced in monoxenic liquid culture and plants (Georgis et al. 1991). Difficulties in systems that use fermentation tank technology. This production, storage, formulation, quality control, approach is the most economical of all known methods. and application technology limited their commercial Nematode production is taking place in tanks of up success in the past. Recent public pressure to limit to 80,000 liters in volume, which has lowered costs environmental contamination associated with considerably, allowing successful introductions into chemical insecticide use has resulted in a dramatic markets requiring large numbers of nematodes or increase in research conducted by scientists in markets of low cash crop value.

Keywords: billbugs, biological control, entomopathogenic nematodes, weevils,

1 Formulation Efficacy

The successful market introduction of an Steinernematids and heterorhabditids differ in entomopathogenic nematode based-product host seeking behavior, tolerance to environmental requires a reliable and stable formulation. This has parameters, behavior in the soil and pathogenicity to been a difficult task, because most larger markets are various insect species (Gaugler 1988). The success demanding a product with a minimum shelf-life of six of entomo-pathogenic nematodes is largely due to months when stored at room temperatures (20°- the extensive amount of scientific research 25°C). Nematode products contain living conducted, both in the laboratory and in the field. that have certain temperature, oxygen and moisture Probably the most studied group of weevil requirements necessary for their survival and species are the so-called root weevils such as effectiveness as control agents. While no nematode black vine weevil, Otiorhynchus sulcatus, and formulation has been completely successful in strawberry root weevil, O. ovatus. These insects are reaching these goals, some have come very close serious pests on several crops throughout western (Georgis 1992). Europe, and North America. Table 1 summarizes several field studies of black vine weevil in Application Technology containerized ornamental plants supervised by the biosys company. Our experience with this insect has Strategies must also be developed which insure shown that rates of 7.5x109 nematodes per hectare are the successful delivery of the nematode to the target necessary for consistent control. Both S. site and target insect, thereby increasing the carpocapsae and H. bacteriophora under probability of nematode-insect interaction. This has appropriate environmental conditions give control not been a simple task. Many parameters must be equal to, or better than, registered insecticides when investigated to improve performance. Determining targeted against the immature life stages. In North target insect life-stage susceptibility is critical, since America, Helix and BioSafe-N (S. carpocapsae) are different life stages of different species are not equally sold commercially for use on cranberry. BioVector is susceptible. Research by the biosys company has sold for other berry crops and also mint, while Exhibit shown that pest population levels and behavior have is sold for use on ornamental plants. Several thousand a great influence on nematode performance and must hectares have been treated to date. be considered carefully (unpublished data). Often, Table 2 shows data on the pathogenicity of larval stages of insects such as borers are not various Steinernema spp. against neonate larvae of accessible to nematodes. Selecting the most black vine weevil (Shanks, unpublished data). Other appropriate nematode species and/or strain is studies have shown that all larval and pupal stages important for efficacy and commercial development. are susceptible. Abiotic factors such as soil type, soil temperature Billbugs, Sphenophorus spp., have become and moisture, and biotic factors, including pathogens significant pests of turf in North America and Japan. and predators, can greatly influence the nematodes’ All immature stages are susceptible to ability to effectively kill the target pest. entomopathogenic nematodes. Table 3 summarizes Application strategies, including field dosage, field trial results of Exhibit (S. carpocapsae) against volume, irrigation and appropriate application bluegrass billbug, S. purvulus, in the United States. methods, are very important, especially if nematodes Although it was less effective on billbug populations are to be integrated with other control strategies. than the insecticide isazophos, the control effect is Compatibility with a wide range of agrichemicals has within acceptable limits. In Japan (Table 4), field trials been demonstrated (biosys, unpublished data). This conducted by SDS Biotech in cooperation with biosys has benefited the successful introduction with has displayed good levels of control against hunting existing Integrated Pest Management programs. Crop billbug, S. venatus, with BioSafe (S. carpocapsae). morphology and phenology must be considered in Adults of this species are also susceptible. These predicting whether nematodes are viable control results have made it possible to register BioSafe for candidates. Additional research has shown the commercial sale in Japan. potential for entomopathogenic nematodes to be Another commercial success story in the United used in other habitats (e.g. aquatic, foliar, and States has been the introduction of BioVector (S. cryptic), and in manure. carpocapsae) for control of the apopka weevil, Diaprepes abbreviatus, and the citrus root weevil, . These two insects cause extensive

2 Table 1. Field efficacy of entomopathogenic nematodes against black vine weevil, Otiorhynchus sulcatus

Table 2. Susceptibility of neonate black vine weevil larvae, Otiorhynchus sulcatus to various steinernematid species

3 Table 3. Field efficacy of entomopathogenic nematodes against bluegrass billbug, Sphenophorus purvulus, in the U.S.A.

Table 4. Field efficacy against hunting billbug, venatus, in Japan

root damage to citrus in the state of Florida. Thousands REFERENCES of hectares of citrus orchards and nurseries have been treated with BioVector. Tables 5a and 5b show Ahmad, R. 1974. Investigations on the white- the results of a seven-month study examining adult fringed weevils Naupactus durius Boh. insect emergence after a single, early-season and Pantomorus auripes Hustache application (Bullock, unpublished data). (Coleoptrea, Curculionidae) and their The sweetpotato weevil, Cylas formicarius, is natural enemies in Argentina. Technical a serious pest of sweet potato all over the world. Bulletin of the Commonwealth Institute of Research efforts have shown that there is a good Biological Control 17: 37-51. potential for controlling this pest with Bedding, R.A., and L.A. Miller. 1981. Use of entomopathogenic nematodes. Table 6 shows results a nematode, Heterorhabditis heliothidis, to from one recent study (Jansson et al. 1990). control black vine weevil, Otiorhynchus Table 7 lists various “weevil” pests that are sulcatus, in potted plants. Annals of reported in the literature to be susceptible to Applied Biology 99: 211-216. entomopathogenic nematodes. As previously Bélair, G., and G. Boivin. 1985. Susceptibility mentioned, some of these pests are now being of the carrot weevil (Coleoptera: controlled effectively with commercial Curculionidae) to Steinernema feltiae, S. entomopathogenic nematode-based products. bibionis and Heterorhabditis heliothidis. 4 Table 5a. Field efficacy of entomopathogenic nematodes against apopka weevil, Diaprepes abbreviatus

5 Table 5b. Field efficacy of entomopathogenic nematodes against citrus root weevil, Pachnaeus litus

6 Table 6. Field efficacy of entomopathogenic nematodes against sweetpotato weevil, Cylas formicarius elegantulus

7 Table 7. Weevils that are susceptible to entomopathogenic nematodes

Journal of Nematology 17: 363-366. 1991. Monitoring of sugar-beet weevil Bluel, S., and H. Kaserer. 1989. (Temnorrhinus mendicus Gyll.) (Coleoptera Investigations on the control of Curculionidae) and preliminary biological Otiorrhynchus sulcatus F. on vines and control trials by entomogenous nematodes. ornamental plants. Mitteilungen Informatore Fitopatologico 41: 55-59. Klosterneuburg, Rebe und Wein, Obstbau Burlando, T.M., H.K. Kaya, and P. Timper. und Fruchteverwertung 39: 124-129. (in 1993. Insect-parasitic nematodes are German, English summary) effective against black vine weevil. Boivin, G., and G. Bélair. 1989. Infectivity of California Agriculture 47: 16-18. two strains of Steinernema feltiae Burman, M. 1981. The pathogenicity of (Rhabditida: Steinernematidae) in relation to Neoaplectana carpocapsae Weiser temperature, age, and sex of carrot weevil (Nematoda) toward Hylobius abietis L. (Coleoptera: Curculionidae) adults. Journal (Insecta). Ph.D. Thesis. University of of Economic Entomology 82: 762-765. Umea, Sweden. Boselli, M., G.M. Curto, and G.L. Lazzari. Burman, M., A. E. Pye, and N.O. Nodd. 1979.

8 Preliminary field trial of the nematode nematodes (Steinernematidae: Nematoda). Neoaplectana carpocapsae against larvae Journal of Invertebrate Pathology 43: of the lage pine weevil, Hylobius abietis 130-131. (Coleoptera: Curculionidae). Annales Hanula, J.L. 1993. Vertical distribution of Entomologici Fennici 45: 88. black vine weevil (Coleoptera: Deseö, K.V., and M. Costanzi. 1987. Control Curculionidae) immatures and infection by of curculionides in flowers and entomogenous nematodes in soil columns ornamentals with entomoparasitic and field soil. Journal of Economic nematodes. La Difesa delle Piante 10: Entomology 86: 340-347. 127-132. (in Italian, English summary). Harlan, D.P., S.R. Dutky, G.R. Padgett, J.A. Diaz, M.M., and E.A. Hernandez. 1978. Mitchell, Z.A. Shaw, and F.J. Bartlett. Comprobacion del caracter 1971. Parasitism of Neoaplectana dutkyi entomopathogenico del nematodo del in white-fringed larvae. Journal of genero Neoaplectana aislado del picudo Nematology 3: 280-283. verde azul Pachnaeus litus. Germar. Arteaga-Hernandez, E.M., and Z. Mrácek. Cienc. Tec. Agric. 1: 5-10. 1984. Heterorhabditis heliothidis, a Dorschner, K.W., F. Agudelo-Silva, and C.R. parasite of insect pests in Cuba. Folia Baird. 1989. Use of heterorhabditid and Parasitologica 31: 11-17. steinernematid nematodes to control black Jackson, T.A., J.F. Pearson, and T.H. Barrow. vine weevils in hop. Florida Entomologist 1985. Control of the black vine weevil in 72: 544-556. strawberries with the nematode Figueroa, W. 1990. Biocontrol of the banana Steinernema glaseri. Proceedings of the root borer weevil, sordidus New Zealand Weed and Pest Control (Germar), with steinernematid nematodes. Conference 38: 158-161. Journal of Agriculture of the University of Jansson, R.K., S.H. Lecrone, R. Gaugler, and Puerto Rico 74: 15-19. G.c. Smart Jr. 1990. Potential of Figueroa, W., and J. Roman. 1990. Biocontrol entomopathogenic nematodes as biological of the sugarcane rootstalk borer, control agents of sweet potato weevil Diaprepes abbreviatus (L.) (Coleoptera: (Coleoptera: Curculionidae). Journal of Curculionidae), with entomophilic Economic Entomology 83: 1818-1826. nematodes. Journal of Agriculture of the Jaworska, M., and K. Wiech. 1988. University of Puerto Rico 74: 395-404. Susceptibility of the clover root weevil, Gaugler, R. 1988. Ecological considerations in Sitona hispidulus F. (Col., Curculionidae) the biological control of soil-inhabiting to Steinernema feltiae, S. bibionis, and insects with entomopathogenic nematodes. Heterorhabditis bacteriophora. Journal Agriculture Ecosystems & Environment 24: of Applied Entomology 106: 372-376. 351-360. Kisimoto, R., Y. Yamada, and K. Suzuki. 1987. Gaugler, R., and H.K. Kaya, editors. 1990. The entomogenous nematode Steinernema Entomopathogenic Nematodes in feltiae as a biological control agent of the Biological Control. CRC Press, Boca rice water weevil, the brown rice Raton, FL. planthopper, and the diamondback moth. Georgis, R. 1992. Present and future In: Recent Advances in Biological Control prospects for entomopathogenic nematode of Insect Pests by Entomogenous products. Biocontrol Science and Nematodes in Japan, N. Ishibashi (ed.). Technology 2: 83-99. Ministry of Education, Culture and Georgis, R., H.K. Kaya, and R. Gaugler. 1991. Science, Japan, Saga University, Japan, pp. Effect of steinernematid and 111-115. (Japanese with English summary). heterorhabditid nematodes (Rhabditida: Klein, M.G. 1990. Efficacy against soil- Steinernematidae and Heterorhabditidae) on inhabiting insect pests. In: Entomopatho- nontarget . Environmental genic Nematodes in Biological Control, Entomology 20: 815-822. R. Gaugler and H.K. Kaya. (eds.). CRC Georgis, R., and G.O. Poinar Jr. 1984. Field Press, Boca Raton, Florida, USA., pp. 195- control of the strawberry root weevil, 214. Nemocestes incomptus, by neoaplectanid Klingler, J. 1990. Entomophagous nematodes

9 against the black vine weevil Pathology 60: 104-106. Otiorrhynchus sulcatus, in Switzerland. Peña, J. E., and R. Duncan. 1991. Preliminary Mitteilungen der Schweizerischen results on biological control of Entomologischen Gesellschaft 63: 375-380. Cosmopolites sordus. Tropical Fruit (German with English summary) News: 8-10. Liu, N.X., Z.Y. Zhang, J.T. Cheng, and L.S. Pye, A.E., and M. Burman. 1977. Zheng. 1989. Study on the entomo- Pathogenicity of the nematode pathogenic nematodes for biological Neoaplectana carpocapsae (Rhabditida, control of bamboo weevils Cyrtotrechalus Steinernematidae) and certain longimanus Fabricius (Coleop.: Curcu- microorganisms towards the large pine lionidae). Natural Enemies of Insects 11: weevil, Hylobius abietis (Coleoptera, 44-50. (In Chinese) Curculionidae). Annales Entomologici Mannion, C.M., and R.K. Jansson. 1992. Fennici 43: 115-119. Movement and postinfection emergence of Roman, J., and W. Figueroa. 1985. Control of entomopathogenic nematodes from the larvae of the sugarcane borer, sweetpotato weevil, Cylas formicarius (F.) Diaprepes abbreviatus (L.) with the (Coleoptera: Apionidae). Biological entomogenous nematode, Neoaplectana Control 2: 297-305. carpocapsae Weiser. Journal of Mesneses-Carbonell, R. 1983. Pathogens and Agriculture of the University of Puerto nematodes for control of rice water weevil Rico 69: 153-158. in Cuba. International Rice Research Rutherford, T.A., D. Trotter, and J.M. Webster. Newsletter 8: 16-17. 1987. The potential of heterorhabditid Montes, M., and R. Montejo. 1991. Lucha nematodes as control agents of root biologica contra Pachnaeus litus Germar weevils. Canadian Entomologist 119: 67- con la utilizacion de Heterorhabditis 73. heliothidis (Khan, Brooks and Hirsch- Schmitt, A.T., S.R. Gowen, and N.G.M. Hague. mann) Poinar. In: Les Colloques 58: 1992. Baiting techniques for the control Rencontres Caraïbes en lutte biologique. of Germar C. Pavis and A. Kermarrec (eds.). (Coleoptera: Curculionidae) by Steinernema Institut National de la Recherche carpocapsae (Nematoda: Steinernematidae). Agronomique, Paris, France, pp. 157-160 Nematropica 22: 159-163. (In Spanish with English summary) Schroeder, W.J. 1987. Laboratory bioassays Nagata, T. 1987a. Infectivity of Steinernema and field trials of entomogenous feltiae on the rice water weevil, nematodes for control of Diaprepes Lissorhoptrus oryzophilus Kuschel. In: abbreviatus (Coleoptera: Curculionidae) in Recent Advances in Biological Control of citrus. Environmental Entomology 16: Insect Pests by Entomogenous Nematodes 987-989. in Japan, N. Ishibashi (ed.). Ministry of Schroeder, W.J. 1990. Suppression of Education, Culture and Science, Japan, Diaprepes abbreviatus (Coleoptera: Saga University, Japan, pp. 65-70. (In Curculionidae) adult emergence with soil Japanese with English summary) application of entomopathogenic Nagata, T. 1987b. Infectivity of Steinernema nematodes (Nematoda: Rhabditida). feltiae to the chestnut curculio, Curculio Florida Entomologist 73: 680-683. dentipes Roelofs. In: Recent Advances in (Scientific Notes) Biological Control of Insect Pests by Shanks, C.H., JR, and F. Agudelo-Silva. 1990. Entomogenous Nematodes in Japan. N. Field pathogenicity and persistence of Ishibashi (ed.). Ministry of Education, heterorhabditid and steinernematid Culture and science, Japan, Saga nematodes (Nematoda) infecting black vine University, Japan, pp. 60-64. (In Japanese weevil larvae (Coleoptera: Curculionidae) in with English summary) cranberry bogs. Journal of Economic Nyczepir, A.P., J.A. Payne, and J.J. Hamm. Entomology 83: 107-110. 1992. Heterorhabditis bacteriophora: A Shetlar, D.J. 1989. Entomogenous nematodes new parasite of pecan weevil, Curculio for control of turfgrass insects with notes caryae. Journal of Invertebrate on other biological control agents. In:

10 Integrated Pest Management for Turfgrass Wiech, K., and M. Jaworska. 1990. and Ornamentals. A.R. Leslie and R.L. Susceptibility of Sitona weevils (Col., Metcalf (eds.). U.S. Environmental Curculionidae) to entomogenous Protection Agency, Washington, D.C., pp. nematodes. Journal of Applied 223-253. Entomology 110: 214-216. Simanton, W.A., and R.C. Bullock. 1973. Evaluation of dip treatments to destroy Diaprepes abbreviatus on citrus nursery DISCUSSION trees. Florida Entomologist 56: 305-310. Simons, W.R. 1981. Biological control of In the Discussion, after the first session on Otiorhynchus sulcatus with heterorhabditid entomopathogenic nematodes, one participant was nematodes in the glasshouse. The interested in the fact that some nematodes are effective Netherlands Journal of Plant Pathology against Lepidoptera, while other nematode species 87: 149-158. are not. He wondered whether this might be related Smith, K.A., R.W. Miller, and D.H. Simser. to some internal defence mechanism and/or external 1992. Southern Cooperative Series morphology which might determine whether the Bulletin, 370: Entomopathogenic Nematode nematode can penetrate the membrane of the insect. Bibliography: Heterorhabditid and Dr. Kaya pointed out that the dense hairs on the body Steinernematide Nematodes. University of of some species of larvae protect them against Arkansas, Arkansas Agriculture Experiment nematodes. Furthermore, Steinernema carpocapsae Station, Fayetteville, Arkansas, A is one of the few nematode species which goes publication of the Nematode Subcommittee through nictating behavior standing on its tail, and of the Southern Project S-240 Development can actually jump onto an insect host. Dr. Smith was of Entomopathogens as Control Agents asked about the cost of nematode applications to for Insect Pests. 81 pp. control e.g. turf billbugs. He replied that the cost Smith, M.T., R. Georgis, A.P. Nyczepir, and varies according to the species of nematode, but at R.W. Miller. 1993. Biological control of application rates of half a billion to three billion the pecan weevil, Curculio caryae nematode nematodes per acre (1 to 7 billion per (Coleoptera: Curculionidae), with hectare), the cost would range from US$20 to US$200 entomopathogenic nematodes. Journal of per acre (approximately US50 to 500 per hectare). Nematology 25: 78-82. Swain, R.B. 1943. Nematode parasites of the Participants were also interested in formulation white-fringed . Journal of techniques. Dr. Smith explained that an infective Economic Entomology 36: 671-673. juvenile has no mouth and cannot absorb food directly Tedders, W.L., D.J. Weaver, E.J. Hunt, and from a nutrient source. One formulation had extended C.R. Gentry. 1982. Bioassay of the shelf-life to a commercially viable period by Metarrhizium anisopliae, Beauveria reducing the nematodes’ metabolic rate. He pointed bassiana and Neoaplectana carpocapsae out that farmers do not like radically new products, against larvae of the plum curculio, and prefer those which resemble the conventional Conotrachelus nenuphar (Herbst) formulations they are used to. For this reason, (Coleoptera: Curculionidae). Environ- commercial firms are now exploring the possibility of mental Entomology 11: 901-904. granule applications, and also of aerial spraying. Thomas, H.A. 1970. Neoaplectanid nematodes as parasites of the pales weevil larvae, The important question was raised whether Hylobius pales. Entomological News 81: entomopathogenic nematodes have an effect on 91. beneficial insects such as natural enemies of pests. Treverrow, N., R.A. Bedding, E.B. Dettmann, Dr. Kaya replied that in general, if the natural enemies and C. Maddox. 1991. Evaluation of of an insect pest live above the ground, they are not entomopathogenic nematodes for control affected by nematodes. If they are living in the soil of Cosmopolites sordidus Germar there may be a possibility of infection, although in (Coleoptera: Curcilionidae), a pest of practice this did not seem to happen. He suggested bananas in Australia. Annals of Applied that more work needs to be carried out on natural Biology 119: 139-146. enemies which live in the soil, particularly predators.

11 He also pointed out that insects such as scarab beetles are exposed to infection for only a short period of time during the larval stage, since the adults have a hard carapace which is resistant to nematode attack. One participant was interested in what would happen if a scarab beetle were to eat a nematode. Dr. Kaya answered that eating the nematode would probably not lead to infection of the beetle unless infective juveniles were very abundant. However, if a natural enemy were a parasitoid developing inside a larva, it would be exposed to entomopathogenic nematodes and would be killed by them. Dr. Smith pointed out that if a cockroach eats a nematode, the structure of the cockroach’s stomach is such that the nematode is torn apart and there is no infection. There is considerable concern in Europe on the effect of nematodes on non-target species, and many studies are under way, but as yet no effect has been found. He pointed out that many different crops in the United States receive nematode applications every year. There is no information on whether there has been any change in the microbial populations of the soil as a result, but suggested that this would be an interesting topic of study. Dr. Smith felt that soil microorganisms seem to have little influence on nematode effectiveness, compared to abiotic factors such as soil moisture. He was asked whether any nematodes are known to eat insect eggs, and replied that in general, insect eggs do not seem to be susceptible. However the nematode Deladenus siricidicola in Australia invades the ovary of Sirex noctilio, which then lays eggs which contain nematodes. The eggs of bark beetles can also be infected with nematodes.

It was pointed out that not all infective juveniles are infectious, and that at most only 10-20% are infectious at any one time. An increase in this rate to e.g. 90% would greatly increase the effectiveness of nematode applications. Dr. Smith was asked whether the efficiency of infective juveniles in terms of their behavior had been considered. Dr. Smith replied that nictating behavior is dominant in young juvenile nematodes. As they age, their lipid content falls and they change from ambushing to hunting behavior. When S. carpocapsae was applied to insects such as weevils which are difficult to kill, there was a population reduction of 20%. Four weeks later, there was a population reduction of 60%. He was interested in the reason for this change in mortality rate, which might reflect a change in nematode behavior, and pointed out that it may not be advantageous for all nematodes to behave in the same way. Dr. Kaya supported this view, and pointed out that nematodes are part of an evolutionary process adapted to survival of the species. From the point of view of efficient use of available resources, it would be disadvantageous for all nematodes to become infective at the same time, however desirable this might be from the commercial point of view.

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