Chapter 22
Natural and Engineered Viral Agents
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James L. Vaughn Insect Biocontrol Laboratory, Plant Sciences Institute, Agricultural Research Service, U.S. Department of Agriculture, BARC-West, Beltsville, MD 20705-2350
Of the many viruses infecting insects, the nuclear polyhedrosis viruses and the granulosis viruses, both members of the family Baculoviridae, are the most promising candidates for use in insect pest management because they have many of the desired characteristics of the ideal microbial agent. They are found only in Arthropods; infecting the immature, feeding stage of the insect and causing devastating epizootics in natural populations. The range of susceptible insects is limited to closely related species, often only within the same genera. In addition, the infectious virion is embedded in a protein body that protects it from inactivation in storage and in the field. Increased levels of resistance to chemical insecticides, the public's concern with environmental contamination and the possible health effects of chemicals in their food, have focused attention on the use of alternative methods for pest management. The papers in this session review the current research on these viruses, including altering the viruses with recombinant DNA techniques to develop more effective pest management tools.
More than 460 years ago an Italian poet, Vida, in a poem about silkworms, described a disease that was probably caused by a virus. Presumably the same disease, called "grasserie" in French, was described in the scientific literature by Nysten in 1908 (1). In 1890-1892 a disease was described that killed enormous numbers of the nun moth, Lymantria monacha, in the spruce forests of central Europe (2). Wahl in 1909 (3) identified the causative agent of the disease as a virus. In 1921 Allen reported an outbreak of a polyhedrosis disease in the fall armyworm, Spodopterafrugiperda,that left dead larvae hanging from the tips of blades of grass in considerable numbers (4). These
This chapter not subject to U.S. copyright Published 1994 American Chemical Society Hedin et al.; Natural and Engineered Pest Management Agents ACS Symposium Series; American Chemical Society: Washington, DC, 1993.
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and other similar outbreaks of virus diseases in a number of insect pests often were quite spectacular and they attracted the attention of entomologists working on pest management, who sought to use them to control pest insects. The first recorded attempt to use a virus in insect control was by German foresters who tried to use the pathogen of the nun moth to control later infestations of this pest. However, since viruses had not been described at that time, the foresters did not know how to produce the pathogen and the results were not consistently favorable. In 1938 a heavy infestation of the European spruce sawfly, Gilpinia hercyniae, caused extensive damage in Quebec, Canada. By 1940 the insect population had declined to the point where no great damage was caused. A virus of unknown origin was eventually credited with causing the decline and viral epizootics followed the spreading insect population into Northeastern United States where the virus continued to suppress the population (7). These and many subsequent epizootics have resulted in a continuing interest in the viruses as control agents. More than 1600 virus isolates from about 1100 species of insects and mites have been recorded (5). These viruses are classified into seven families (6). Members of three families, Poxviridae, Reoviridae, and Baculoviridae, have shown the most potential as biocontrol agents. Viruses belonging to the family Poxviridae cause disease in grasshoppers, forest lepidoptera, and turf beetles (As examples see ref. 7-9). However, because of their similarity to the pox viruses from vertebrates they were not considered good candidates for insect control until detailed study of the viral genome by restriction enzyme nucleotide fragment patterns demonstrated that they were quite different. There is no record of the entomopox viruses causing disease in vertebrates (10). Therefore it is likely that these viruses will become useful control agents in the future. Reoviruses from insects, called "cytoplasmic polyhedrosis viruses," are unique among the members of this family in that they are the only ones in the family that have the infectious virions enclosed in a protein crystal. Only the cytoplasmic polyhedrosis virus from the pine caterpillar, Dendrolimus spectabilis, has been widely used as a control agent (77). These viruses are not highly lethal, but rather persist in the infected population causing lethargy in infected larvae and lower fecundity in adults. They are most suitable for use in situations, such as the forest, where some insect damage can be tolerated. Most of the viruses thus far considered for biocontrol of insects belong to the family Baculoviridae. This family contains three genera: Nuclear polyhedrosis viruses, Granulosis viruses, and Non-occluded viruses. This session will deal primarily with the Nuclear Polyhedrosis viruses and the Granulosis viruses. Members of these genera occur exclusively in arthropods, primarily in insects. This provides a basis for the presumed safety of these viruses. All the viruses in these two genera have the infectious virion enclosed in a protein matrix that provides protection and stability during storage, shipping and following application. The viruses infect the larval stage of the insects and cause an acute disease most often resulting in death of the infected insect. Thus, they have most of the characteristics desired of a microbial pest management agent; lethality, safety, and stability.
Hedin et al.; Natural and Engineered Pest Management Agents ACS Symposium Series; American Chemical Society: Washington, DC, 1993.
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NATURAL AND ENGINEERED PEST MANAGEMENT AGENTS
Most of the pest management agents discussed during this Conference were similar to synthetic chemicals in the form in which they are applied in the field and the way in which they affect the pest. Viruses are different in significant ways: They are applied as living organisms, and as such, can multiply in the field after application. They are obligate pathogens, meaning that they can multiply only in the tissues and cells of a susceptible host. The effect on the insect is the result of a series of physiological processes - a disease, not a poison. These differences give the viruses some of their advantages over the other control agents and at the same time result in some restraints on their use and effectiveness as pest management agents. The specificity of the viruses can be either an advantage or a disadvantage. Because the viruses are host specific, they will not kill beneficial insects such as honey bees or parasitic insects. Therefore, using viruses does not remove the natural pressures on the target insect or on other potential pests controlled by parasites or predators and lead to increased need for chemical control. They will not harm plants or vertebrates; nor will they accumulate in other organisms in the food chain as do some chemicals. Because of their specificity and the fact that they can multiply in the field after application, no tolerance levels are established for viruses; thus, there is no residue problem. Specificity is also a disadvantage in some situations. If a crop is attacked by more than one pest, a single virus may not prevent economic loss. From the commercial viewpoint, the specificity limits the potential market size for a product and the earnings from sales in that market may not be sufficient to recover the costs of development. If independent applications of different viruses are required to control several pests, the cost to the grower may also be a disadvantage. Since no effect on the pest is obtained until there has been some replication of the applied virus, there is a time lag between the application and the appearance of signs of the disease. During this incubation period the insect continues to feed and may cause economic losses even though the pest population is eventually reduced. This must be considered when a decision whether or not to use viruses is being made. Developing a virus for pest management is influenced greatly by the production methods available. Because viruses must be produced in the tissues of their hosts, the only means of producing them generally is to rear and infect large numbers of the host insect. In developed countries this has discouraged companies from producing viruses for a commercial market. This is particularly true if there is no artificial diet for the insect and it must be grown on foliage. The recent developments in large-volume cell culture indicate that this will soon be a more attractive alternative production system for some viruses. Until recently patent protection for viral pest management products was not considered possible. Thus, companies that did make the considerable investment required to develop a viral product had no protection from competitors while they recovered this cost. However, recently patents have
Hedin et al.; Natural and Engineered Pest Management Agents ACS Symposium Series; American Chemical Society: Washington, DC, 1993.
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been issued for two virus strains obtained from nature. Certainly patent protection will be available for genetically altered viruses such as will be described in following chapters. This should serve as encouragement for further development by commercial firms. In this brief introduction I have attempted to provide a broad overview of the reasons why certain viral pathogens of pest insects have held the attention of entomologists for at least a century. I have also introduced some of the problems that have prevented or delayed the fulfillment of the promise that these organisms showed 100 years ago in Germany. In the first three chapters prepared by the speakers in this session the details of this history will be presented. In the final chapter one of the exciting new areas in the field of insect virology, the genetic manipulation of the nuclear polyhedrosis viruses, will be discussed. This new technology holds great promise for overcoming some of the restraints to the use of viruses in pest management. These recent advances and the increased pressure to reduce the use of chemical insecticides have provided a new opportunity for the incorporation of viruses into pest management and are the reasons for including this topic in the Conference. Literature Cited 1. 2. 3. 4. 5.
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7. 8. 9. 10. 11.
Steinhaus, Ε. Α.; Principles of Insect Pathology; McGraw-Hill: New York NY, 1949; pp 417-545. Hofmann, O.; Die Schlaffsucht (Flacherie) derNonne (Liparis monacha) nebst einem Anhang. Insektentotende Pilze mit besonderlr. Berucksichtigung der Nonne. P. Weber: Frankfurt a. M., 1891. Wahl, B.; Zentr. Gesell Forstw. 1909; 35, 164. Allen, H. W.; J. Econ. Entomol; 1921; 14, 510-511. A Catalog of Viral Diseases of Insects, Mites, and Ticks; Martignoni, M. E.; Iwai, P. J. Eds.; General Technical Report PNW-195; Pacific Northwest Research Station, United States Department of Agriculture: Washington, D. C., 1986; 4th Edition Revised. Classification and Nomenclature of Viruses, Fifth Report of the International Committee on Taxonomy of Viruses; Francki, R. I. B.; Fauquet, C. M.; Knudson, D. L.; Brown, F. Eds.; Archives of Virology Suppl. 2; Springer - Verlag: Wein, Austria, 1991. Bird, F. T.; Sanders, C. J.; Burke, J. M. J. Invertebr. Pathol. 1971, 18, 159-161. Milner, R. J.; Lutton, G. G. Entomophaga 1975, 20, 213-220. Henry, J. E.; Nelson, B. P.; Jutila, J. W. J. Virol. 1969. 3, 605-610. Langridge, W. H. R.; Orna, E.; Henry, J. E. J. Invertebr. Pathol. 1983, 42, 327-333. Katagiri, K.; In Microbial Control of Pests and Plant Diseases 1970-1980; Burges, H. D. Ed.; Academic Press: New York, NY, 1981, pp 433-440.
RECEIVED April 30, 1993
Hedin et al.; Natural and Engineered Pest Management Agents ACS Symposium Series; American Chemical Society: Washington, DC, 1993.
