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I: Biological Control (12 Articles) |
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I.6 Grasshopper Pathogens and Integrated Pest ManagementDonald L. Hostetter and Douglas A. Streett Introduction IntroductionSome 97 percent of all animals on Earth are invertebrates, and between 75 and 80 percent of these are insects. One of the most serious gaps in our knowledge of invertebrates in general, and insects specifically, is a thorough understanding of their diseases. As would be expected, mankind’s knowledge of insect parasites and predators preceded that of the disease-causing agents of insects. Although the early interests in insect pathology were primarily concerned with beneficial insects, such as the honeybee and the silkworm, many investigators recognized that harmful insects were subject to disease. Almost from the time of their discovery, insect diseases have been proposed as possible tools for controlling insect pests. It was not until 1836 that Agostino Bassi, for whom the insect-infecting fungus Beauveria bassiana is named, suggested that microorganisms could be used to control destructive insects. Another 43 years would pass before Elie Metchnikoff published his account of a natural infection of the wheat cockchafer (Anisoplia austriaca) by the green-muscardine fungus (Metarhizium anisopliae [Metchnikoff]) and provided experimental methods for testing the possibility of controlling insects with fungi (Steinhaus 1956). Micro-organisms with the ability to cause acute and chronic disease in grasshoppers and locusts currently are found among the bacteria, fungi, protozoa, rickettsia, and viruses (Bidochka and Khachatourians 1991). BacteriaOne of the first attempts to use bacteria as a control agent of insects was against grasshoppers in Mexico (d’Herelle 1911). The bacterium Coccobacillus acridorum d’Herelle was isolated from large numbers of dying grasshoppers that had migrated to Mexico from Guatemala. D’Herelle claimed to have begun epidemics among grasshopper populations in Mexico, Colombia, and Argentina, along with some success in Algeria and Tunisia. His results were not reproducible by others and soon viewed with doubt. This bacteria was later determined to be Aerobacter aerogenes (Kruse), a member of the coliform group capable of invading warmblooded animals (Steinhaus 1949). Another bacterium, Serratia marcescens Bozio, was isolated from desert locusts (Schistocerca gregaria [Forskäl]) raised in a laboratory. S. marcescens was cultured, formulated on a bran bait, and used in field tests against the desert locust in Kenya. The results were uncertain (Stevenson 1959). This gram-negative bacterium is found worldwide and is well known as a pathogen of laboratory insects. The most promising bacteria currently being used for insect control belong to the spore-forming group Bacillus thuringiensis Berliner, often referred to as “Bt.” A diamond-shaped crystalline toxin is produced within the bacteria as they mature and form spores. The toxin is the active ingredient that kills insect larvae. After it is consumed, the toxin is dissolved in the insects’ alkaline gut juices and becomes activated. The gut is unable to process food, the larvae stop eating, and the gut ruptures, causing the larvae to die. Grasshoppers have a built-in barrier against Bt because their gut juices are acidic, and the absence of an alkaline environment prevents the toxin from dissolving and becoming activated (Prior and Greathead 1989). Two isolates of Bt from the Dulmage Collection originally isolated from grasshoppers were inactive against M. sanguinipes, as were 26 other prospective isolates (Streett and Woods 1992 unpubl). Continued examination of the Bt group, along with advances in formulation chemistry and genetic manipulation, may produce future successes with these bacteria against grasshoppers. FungiMore than 750 species of insect-infecting fungi have been documented (National Academy of Sciences 1979, Roberts and Humber 1984). Although fungi are among the best known and most often reported pathogens associated with grasshoppers and locusts, only a few different fungi have been recorded. The most common are Beauveria bassiana (Balsamo) Vuillemin, Metarhizium anisopliae (Metchnikoff) Sorokin, and Entomophaga grylli (Fresenius) Batko. Fungi are “contact” pathogens. They do not infect when they are eaten by the insect, as do other pathogens. Fungal infection may occur during the feeding process when conidia contact the mouthparts (Foster et al. 1991 unpubl.). The infection process begins after a spore comes in contact with a suitable host and germinates in the form of a “tube.” The tube penetrates the body wall, enters the body cavity, and releases a protoplast that begins asexual reproduction. Rapid growth of the fungus overwhelms the insect host and it dies. After death of the host, the fungus grows back through the body wall and forms vegetative stalks that produce primary spores (conidia) that are forcibly discharged into the atmosphere. These spores are capable of continuing the infection cycle. Toward the end of the season, or if environmental conditions are unfavorable for conidia production, “resting spores” are produced. Resting spores are the environmentally resistant or protective stage that overwinters in the soil litter or in dead grasshoppers. Beauveria bassiana has been successfully developed and used as a microbial control agent of various insects in the Soviet Union and China (Goettel 1992). Interest in B. bassiana as a control agent for rangeland grasshoppers has been renewed with the recent isolation of a strain— virulent to some species of grasshoppers—from a grasshopper in Montana (Johnson et al. 1988 unpubl., Foster et al. 1992 unpubl.). Extensive laboratory and field testing of this strain has indicated good potential for control of grasshoppers and resulted in the first aerially applied field tests of B. bassiana against grasshoppers on rangeland in the United States (Foster et al. 1991–93 unpubl.). Technology for mass production has been developed by Mycotech Corporation (Butte, MT), and a commercial product was registered for use against rangeland grasshoppers by the Environmental Protection Agency in 1995. B. bassiana is expected to be competitive with current chemical insecticides and could be a very useful microbial control agent in future grasshopper integrated pest management (IPM) programs. Metarhizium anisopliae is another fungus that has been isolated from grasshoppers and is known to have a worldwide distribution. It also can be mass produced and formulated as a microbial insecticide. One isolate has been used successfully as a control agent against the sugarcane spittlebug in Brazil (Roberts et al. 1991). It has not been tested in the field as a grasshopper control agent but should be considered as a potential tool that merits further tests. Entomophaga grylli, formerly referred to as a complex of fungi composed of “pathotypes,” is now known to consist of at least four species: E. calopteni(Bessey) Humber, E. macleodii, E. praxibuli, and E. asiatica. E. calopteni is the only species that has been formally described to date (Humber 1989). E. asiatica, isolated from one grasshopper in Japan, was screened for activity and placed into the pathogenic insect fungus collection at the U.S. Department of Agriculture’s Agricultural Research Service laboratory in Ithaca, NY (Carruthers et al. 1989 unpubl.). All Entomophaga spp. isolated from grasshoppers and locusts are infective only for members of this group. This fungus also has a worldwide distribution. Entomophaga spp., unlike B. bassiana and M. anisopliae, cannot be produced in large quantities on or in artificial media at the present time. Entomophaga spp. cannot be used as microbial insecticides in large-scale spray applications now. A classical introduction method uses individually infected grasshoppers, each injected with an amount of the infective stage (protoplasts) of Entomophaga sp. that will cause their death within 7 to 10 days. Before dying of the fungus disease, the infected grasshoppers are released into a susceptible population in the field. Distribution of the disease occurs and is dependent upon dispersal of spores from dead, infected grasshoppers to noninfected ones within the population. A series of biological and environmental factors must occur in sequence before such epidemics develop. One of the native North American fungi, Entomophaga macleodii (pathotype I) infects grasshoppers from several genera and produces infective conidia as well as resting spores. The primary host of this fungus is the clearwinged grasshopper (Camnula pellucida [Scudder]), which belongs to the bandwinged group of grasshoppers. The other North American species is E. calopteni (pathotype II). It occurs only in a Melanoplus species (a member of the spurthroated group) and produces only resting spores upon death of the host. The Australian fungus, E. praxibuli, was isolated from Praxibulus sp. grasshoppers in Australia in 1985 during a fungus epidemic. This fungus is similar to E. macleodii in producing both infective conidia and resting spores. Laboratory tests and field observations indicate that E. praxibuli has a greater host range than E. macleodii and is infective for at least 14 species of grasshoppers from the three major subfamilies: the spurthroated, slantfaced, and bandwinged grasshoppers. Following a review of the known literature and a series of laboratory evaluations, the Australian isolate E. praxibuli was selected as a candidate for a classical biological control program for grasshopper populations in western North Dakota (Carruthers et al. 1989–91 unpubl.). ProtozoaThe microsporidia comprise the most important group of the protozoan pathogens of insects with over 250 species currently documented (Maddox 1987). The most probable route of infection occurs when insects’ food is contaminated with spores. Upon ingestion into the midgut of a host, the spores forcibly extrude a hollow filament that penetrates or is placed near the epithelial cells lining the gut. The infective sporoplasm travels through the tube and into the cell, where asexual reproduction of spores begins. Spores can be released prior to death of the infected host through regurgitation or in feces. Microsporidia also can be passed on to the next generation of host insects on the surface of eggs, or within eggs laid by infected females. Some microsporidia may also be mechanically transmitted by the feeding or ovipositing activities of insect parasites of the infected host. Micro-sporidial infections can range from acute, leading to death in several days, to chronic, with little evidence of infection and prolonged life stages. Microsporidia can be serious pathogens in laboratory colonies of insects. Within the family Microsporida, the genera Nosema and Vairimorpha have proven to contain the most promising candidates for grasshopper and locust control. Nosema locustae (Canning) was first isolated from infected migratory locusts in a laboratory colony in Great Britain (Canning 1953). It has received the most attention as a biological control agent for grasshoppers. Nosema was thoroughly investigated in a series of laboratory and field evaluations, registered, and developed as the first commercial microbial product for grasshopper control (Henry 1978 and 1982, Henry and Oma 1981). Applications were difficult to evaluate and did not meet expectations. N. locustae was widely acclaimed but unfortunately is not extensively used in grasshopper control programs. For grasshopper control in environmentally sensitive areas, N. locustae is still worthy of consideration. In many cases, in sensitive areas, no action is chosen over N. locustae for economic reasons and because results with Nosema have been irregular ( See I.4 ). Nosema acridophagus Henry and N. cuneatum Henry are two other grasshopper-isolated species of microsporidia that have potential as microbial control agents (Henry 1967, Henry and Oma 1974). Both have demonstrated variable virulence and have been adapted to production in surrogate hosts (certain species of caterpillars). These agents may have a place in future IPM programs (Streett 1987). A Vairimorpha sp. was isolated from Mormon crickets (Anabrus simplex Haldeman) in Utah and Colorado during an epidemic in 1989. The crickets are very susceptible to this Vairimorpha and it may be considered as a control agent for Mormon crickets. Field observations indicate that infection causes increased mortality among crickets while decreasing development of nymphs and adult reproduction (Henry and Onsager 1989 unpubl.). VirusesThe only viruses isolated from grasshoppers and cricket species to date are members of the entomopoxvirus and crystalline array virus groups. The entomopoxviruses are the best known of the viruses reported from grasshoppers and crickets. The entomopoxviruses isolated from M. sanguinipes have received the closest examination and evaluation (Henry and Jutila 1966). Fewer than 10 entomopoxviruses have been isolated from grasshoppers (Streett et al. 1986). Two other poxviruses, one from Arphia conspersa Scudder and one from the African grasshopper Oedaleus senegalensis (Krauss), are potential microbial control agents (Streett 1987). These viruses were originally viewed with caution because of their resemblance to vertebrate orthopoxviruses (Bidochka and Khachatourians 1991). Examination of this group has revealed no biochemical similarity or infectivity of vertebrates, however (Arif 1984, Streett and McGuire 1990). The crystalline array viruses do closely resemble the picornaviruses of vertebrates and are not currently considered to be exploitable as a microbial agent for grasshoppers (Greathead 1992). Nuclear polyhedrosis viruses (NPV’s), probably the most common of insect viruses, have not been isolated from grasshoppers or crickets. One report has documented transmission (by feeding) of an NPV from Spodoptera littoralis (a caterpillar) to both Schistocerca gregaria and Locusta migratoria, resulting in a phenomenon known as “dark cheeks” (Bensimon et al. 1987). SummaryGrasshoppers and locusts, like all other animals, are subject to pathogenic micro-organisms. Representatives from all of the major groups of known pathogens have been isolated from grasshoppers and crickets. The fungi Entomophaga spp. and Beauveria spp. are the most frequently reported and observed pathogens. Spectacular mortality due to Entomophaga sp. is often observed within grasshopper populations throughout the world. Fungi, at the current time and state of technology, probably have the greatest potential as microbial control agents. Bacterial pathogens do not exhibit much promise as tools for grasshopper control now. Technological advances in molecular biology may lead to development of strains of Bacillus thuringiensis that will be active against grasshoppers. Efforts to isolate bacteria, particularly spore-formers, from grasshoppers and crickets on a worldwide scale should be supported. Protozoans, particularly Nosema spp. and Vairimorpha spp., are also promising candidates for reducing grasshopper populations in environmentally sensitive areas. Although Nosema locustae, the first registered and commercially produced microbial control agent for grasshopper suppression, has not met expectations, it still remains a viable alternative to chemical control in long-term management programs. Continued research with grasshopper and cricket viruses undoubtedly will result in new isolates that may be considered as management tools. Viruses have the potential to be “tailored” to fit specialized control requirements in localized areas and may become a tool of choice—with substantial research and development—for long-term population reduction in grasshoppers in the future. Insect pathogens will play a larger role in future grasshopper management strategies as requirements for control are redefined and evolve in the decades ahead. Previous Article
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• Section I Contents References CitedArif, B. M. 1984. The entomopoxviruses. Advances in Virus Research 29: 195–213. Bensimon, A. S.; Zinger, E.; Gerasi, A.; Hauschner, I.; Sela, I. 1987. “Dark cheeks,” a lethal disease of locusts provoked by a lepidopterous baculovirus. Journal of Invertebrate Pathology 50: 254–260. Bidochka, M. J.; Khachatourians, G. G. 1991. Microbial and protozoan pathogens of grasshoppers and locusts as potential biocontrol agents. Biocontrol Science and Technology 1: 243–259. Canning, E. U. 1953. A new microsporidian, Nosema locustae n. sp., from the fat body of the African migratory locust, Locusta migratoria migratorioides Reiche and Fairmaire. Parasitology 43: 287–290. d’Herelle, F. 1911. Sur une épizootie de natur bactérienne sévissant sur les sauterelles au Mexique. Compt. rend. acad. sci. Paris: 152: 1413–1415. Goettel, M. S. 1992. Fungal agents for biocontrol. In: Lomer, C. J.; Prior, C., eds. Biological control of locusts and grasshoppers. Wallingford, UK: C.A.B. International: 122–132. Greathead, D. J. 1992. Natural enemies of tropical locusts and grasshoppers: their impact and potential as biological control agents. In: Lomer, C. J.; Prior, C., eds. Biological control of locusts and grasshoppers. Wallingford, UK: C.A.B. International: 105–121. Henry, J. E. 1967. Nosema acridophagus sp. n., a microsporidian isolated from grasshoppers. Journal of Invertebrate Pathology 9: 331–341. Henry, J. E. 1978. Microbial control of grasshoppers with Nosema locustae Canning. Miscellaneous Publications Entomological Society America 11: 85–95. Henry, J. E. 1982. Production and commercialization of microbials: Nosema locustae and other protozoa. In: Invertebrate pathology and microbial control, Proceedings 3rd. international colloquium on invertebrate pathology; [dates of meeting unknown]; Brighton, UK. [Place of publication and publisher unknown]: 103–106. Henry, J. E.; Jutila, J. W. 1966. The isolation of a polyhedrosis virus from a grasshopper. Journal of Invertebrate Pathology 8: 417–418. Henry, J. E.; Oma, E. A. 1974. Effects of infections by Nosema locustae Canning, Nosema acridophagus Henry, and Nosema cuneatum Henry (Microsporida: Nosematidae) in Melanoplus bivittatus (Say) (Orthoptera: Acrididae). Acrida 3: 223–231. Henry, J. E.; Oma, E. A. 1981. Pest control by Nosema locustae, a pathogen of grasshoppers and crickets. In: Burges, H. D., ed. Microbial control of pests and plant diseases 1970–1980. New York: Academic Press: 573–586. Humber, R. A. 1989. Synopsis of a revised classification for the Entomophthorales: (Zygomycotina). Mycotaxon 34: 441–460. Maddox, J. V. 1987. Protozoan diseases. In: Fuxa, J. R.; Tanada, Y., eds. Epizootiology of insect diseases. New York: John Wiley & Sons: 417–452. National Academy of Sciences. 1979. Microbial processes: promising technologies for developing countries. Washington, DC: National Academy of Sciences. Prior, C.; Greathead, D. J. 1989. Biological control of locusts: the potential for the exploitation of pathogens. Plant Protec. Bull. 37. Rome: United Nations Food and Agriculture Organization: 37–48. Roberts, D. W.; Humber, R. A. 1984. Entomopathogenic fungi. In: Roberts, D. W.; Aist, J. R., eds. Infection process of fungi, a conference report of the Rockefeller Foundation. New York: Rockefeller Foundation. 201 p. Roberts, D. W.; Fuxa, J. R.; Gaugler, R.; Goettel, M.; Jaques, R.; Maddox, J. 1991. Use of pathogens in insect control. In: Pimentel, D., ed. CRC handbook of pest management in agriculture. Boca Raton, FL: CRC Press: 243–278. Steinhaus, E. A. 1949. Principles of insect pathology. New York: McGraw–Hill. 757 p. Steinhaus, E. A. 1956. Microbial control—the emergence of an idea, a brief history of insect pathology through the nineteenth century. Hilgardia 26: 107–160. Stevenson, J. P. 1959. Epizootology of a disease of the desert locust, Schistocerca gregaria (Forskäl), caused by nonchromogenic strains of Serratia marcescens Bizio. Journal of Insect Pathology 1: 232–244. Streett, D. A. 1987. Future prospects for microbial control of grasshoppers. In: Capinera, J. L., ed. Integrated pest management on rangeland: a shortgrass prairie perspective. Boulder, CO: Westview Press: 205–218. Streett, D. A.; McGuire, M. R. 1990. Pathogenic diseases of grasshoppers. In: Chapman, R. F.; Joern, A., eds. Biology of grasshoppers. New York: John Wiley & Sons: 484–516. Streett, D. A.; Oma, E. A.; Henry, J. E. 1986. Characterization of the DNA from Orthopteran entomopoxviruses. In: Samson, R.; Vlak, J.; Peters, D., eds. Fundamental and applied aspects of invertebrate pathology. Wageningen, The Netherlands: Grafisch Bedrijf Ponson and Looijen: 408. References Cited—Unpublished
Availability note: Copies of the annual reports from the Grasshopper Integrated Pest Management Project are available from USDA, APHIS, PPQ, 4700 River Road, Riverdale, MD 20737.
Carruthers, R. I.; Humber, R. A. 1989. Entomophaga grylli as a biological control agent for grasshoppers. In: Cooperative Grasshopper Integrated Pest Management Project, 1988 annual report. Boise, ID: U.S. Department of Agriculture, Animal and Plant Health Inspection Service: 330–335. Carruthers, R. I.; Humber, R. A.; Ramos, M. E. 1989–91. Development of Entomophaga grylli as a biological control agent for grasshoppers. In: Cooperative Grasshopper Integrated Pest Management Project, 1988–90 annual reports. Boise, ID: U.S. Department of Agriculture, Animal and Plant Health Inspection Service. Foster, R. N.; Reuter, K. C.; Bradley, C. A.; Wood, P. P. 1991. Preliminary investigations on the effect of Beauveria bassiana on several species of rangeland grasshoppers. In: Cooperative Grasshopper Integrated Pest Management Project, 1991 annual report. Boise, ID: U.S. Department of Agriculture, Animal and Plant Health Inspection Service: 203–208. Foster, R. N.; Reuter, K. C.; Bradley, C.; Britton, J.; Black, L.; Drake, S.; Leisner, L.; Tompkins, M.; Fuller, B.; Hildreth, M.; Kahler, E.; Radsick, B. 1992. Development of the fungus Beauveria bassiana as a bio-insecticide for grasshoppers on rangeland. In: Cooperative Grasshopper Integrated Pest Management Project, 1992 annual report. Boise, ID: U.S. Department of Agriculture, Animal and Plant Health Inspection Service: 207–213. Foster, R. N.; Reuter, K. C.; Tompkins, M. T.; Bradley, C.; Britton, J.; Underwood, N.; Black, L. R.; Vigil, E.; Daye, G.; Radsick, B.; Fuller, B.; Brinkman, M.; Kahler, E. 1993. Development of the fungus Beauveria bassiana as a bio-insecticide for grasshoppers on rangeland. In: Cooperative Grasshopper Integrated Pest Management Project, 1993 annual report. Boise, ID: U.S. Department of Agriculture, Animal and Plant Health Inspection Service: 233–238. Henry, J. E.; Onsager, J. A. 1989. Efficacy of Nosema locustae and Vairimorpha sp. against young nymphs of the Mormon cricket, Anabrus simplex. In: Cooperative Grasshopper Integrated Pest Management Project, 1989 annual report. Boise, ID: U.S. Department of Agriculture, Animal and Plant Health Inspection Service: 241–48. Johnson, D. L.; Pavlov, E.; Bradley, C. 1988. Activity of Beauveria bassiana sprayed onto wheat against grasshoppers. Pesticide Res. Rep. Ottawa, ON: Agriculture Canada, Expert Committee on Pesticide Use in Agriculture. Streett, D. A.; Woods. S. A. 1992. Grasshopper pathogen evaluation. In: Cooperative Grasshopper Integrated Pest Management Project, 1992 annual report. Boise, ID: U.S. Department of Agriculture, Animal and Plant Health Inspection Service: 179–185. |
