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Rohrmann GF. Baculovirus Molecular Biology: Second Edition [Internet]. Bethesda (MD): National Center for Biotechnology Information (US); 2011.

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Baculovirus Molecular Biology: Second Edition [Internet].

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Chapter 9Baculoviruses as insecticides: Three examples

, PhD.

Created: .

One of the earliest references for using natural pathogens for insect control was reported by V. Audouin in 1839, who tells of a sericulturist who emptied fungus-contaminated silkworm rearing trays out a window onto trees infested with defoliating insect larvae. Within a few days all of the defoliating insects had died of the fungus. More explicit suggestions for the microbial control of insects were made by J.L. LeConti in 1874 in an address to the AAAS, in which he recommended the study of epidemic diseases of insects and advocated their use to control insects. At the same time, Louis Pasteur, who had spent considerable effort investigating a microsporidian parasite of silkworms, recommended the use of this pathogen against an insect pest of grapes (described in (1)).

In ecosystems, baculoviruses often play a major role in the suppression of a variety of different types of insects. For example, the virus of the gypsy moth, Lymantria dispar, is considered to be the major natural regulator of dense populations of this moth (2). Likewise, baculoviruses of the Douglas fir tussock moth, Orgyia pseudotsugata, are also major factors in the control of this insect (3). They also are found to naturally control pest insects of cultivated crops. For example, they were found to be major contaminants of cabbage purchased from supermarkets in the Washington, D.C. area, and it was estimated that an average serving of cole slaw would contain over 100 million occlusion bodies (4). Once the role these viruses played in controlling natural insect populations was understood, they were considered for a variety of insect control programs, particularly of forest pests (5).

There have been numerous reviews on the development of baculoviruses to control insects, e.g (6-8), and despite this widespread interest and intrinsic attractiveness of their use, the acceptance and use of viruses for insect control has been limited. This can be attributed to their slow speed of kill, their limited host range (such that one preparation can only be used on a few insects), and to a certain degree, the complexity of producing standardized viral preparations. The slow speed of kill may be of particular advantage to the virus, because it results in greatly increased viral yields. However, delays in the death of the host result in more vegetation being consumed by the infected insect. A variety of recombinant viruses have been investigated that have been designed to enhance the efficacy of the virus by reducing the time it takes to kill target insects or causing cessation of feeding. These recombinants express insect specific toxin, insect hormones or enzymes, or are deleted for the EGT gene. A contributing factor to their limited use for biocontrol is that production of viral insecticides is labor intensive; consequently, their use has been limited to high value crops, particularly those that have become resistant to chemical insecticides or to crops in countries with access to relatively inexpensive labor. An exception appears to be their use against forest insects in North America. However, relative to the size of forested areas, these applications are also limited. In addition, the use of Bacillus thuringiensis preparations is highly competitive compared to baculoviruses because of the simplicity of their growth and formulation. In this chapter, I will review three instances where viruses have been relatively extensively applied in the field.


An NPV of the velvet bean caterpillar, Anticarsia gemmatalis: Application in Brazil

The most successful program employing baculoviruses for insect control has been developed in Brazil and to a lesser extent in Paraguay and involves a virus that infects the velvet bean caterpillar (Anticarsia gemmatalis), a pest of soybeans (9-11). Virus preparations are applied at 1.5 × 1011 occlusion bodies per hectare (about 20 g or 50 larval equivalents). This program was initiated in the early 1980s, and by 2005, the area treated had expanded to over two million ha ((7) and references therein). Initially, laboratory production was not found to be economically viable, and virus production was carried out in farmers' fields. Plots of soybeans that were naturally infested with A. gemmatalis were sprayed with virus and then the dead larvae were collected. Individuals were able to collect about 1.8 kg of larvae/day at a cost in the mid 1990s of about $15. Production varied in the 1990s from enough virus to treat 650,000 to 1.7 million ha/year. Since 1999, the production of virus has not been sufficient to meet the demand. Consequently, to increase virus production under more defined conditions, a laboratory for the large-scale production of AgMNPV was opened in 2004 with the intention of being capable of infecting 600,000 larvae per day. This would have the potential to yield enough virus to treat up to 1.5 million ha/year. Another facility was opened for the improvement of virus production and for the training of individuals for virus production. It has the capacity to infect up to 30,000 larvae per day ((7) and references therein). The infected larvae are processed into a wettable powder that involves milling the infected larvae and formulating them into a mixture that contains kaolin. Kaolin is an aluminosilicate compound first discovered in Kao-lin, China that is commonly used as an inert carrier or filler.

Some of the reasons for the feasibility of this viral control program are caused by specific features of AgMNPV. First, the virus is highly virulent for A. gemmatalis and usually only needs to be applied one time. In contrast, chemical insecticides often need to be applied twice. Furthermore, AgMNPV lacks the chitinase and cathepsin genes, so the insects die without 'melting,' and the dead insects can be more readily collected and processed than if they had disintegrated (12) (see Chapter 3). Another factor contributing to the success of the program is that soybean plants can endure significant defoliation without a reduction in yield. The virus can also be spread by insect predators and can survive passage through the digestive tract of beetles and hemiptera (11). Overall, the use of the viruses is 20-30% less expensive than chemical insecticides, and it has been estimated that the use of up to 17 million liters of chemical insecticides has been eliminated since the beginning of the program. Limitations have included the reluctance of farmers to monitor their fields to determine the optimal timing for virus application and its use in regions that have low mean temperatures, which lengthens the time required to kill the insects. Extended periods of drought also adversely affect the efficacy of the virus preparation ((7) and references therein).

A granulovirus of the codling moth, Cydia pomonella: Application in North America and Europe

Whereas the use of AgMNPV has been limited predominantly to one major area in Brazil, a granulovirus of the codling moth Cydia pomonella (CpGV) has been used in a number of countries in North America and Europe for the control of the insect on pear and apple crops. CpGV was originally isolated from C. pomonella in Mexico in 1963 (13). Because of the development of resistance of codling moth to several chemical insecticides and for a variety of other safety and environmental reasons, the use of CpGV has increased in Europe and North America since 2000. The virus is used on a hundred thousand or more hectares on these continents. Currently, commercial preparations of the virus are available from several different companies and include preparations called Cyd-X and VirosoftCP4 in North America and in Europe include Carpovirusine™ (France), Madex™ and Granupom™ (Switzerland), Granusal™ (Germany), and Virin-CyAP (Russia). The virus is highly virulent for codling moth with LD50's as low as 1.2-5 occlusion bodies per insect. The codling moth lays eggs on fruit trees, and after hatching, the larvae browse on leaves before entering fruit. They need to feed inside fruit for normal development, which can result in severe damage. Depending on the climate, there can be from one to three generations per season, and to ensure exposure during the brief window from hatching to entry into fruit requires the application of CpGV at least at weekly intervals up to six times in a season.

Recently, resistance to the virus has been described in Europe, with these insects able to tolerate CpGV over 1,000 times higher than previously observed. In laboratory experiments, it was determined that a gene conferring resistance is located on the male (Z) chromosome, and it was found that females with a single Z chromosome could be selected that were almost 100,000 times less susceptible to the CpGV infection (14). Because of the complexity of baculovirus replication it was often assumed that it would be challenging for an insect to develop resistance. However, these results clearly indicate that the alteration of a single or limited number of linked genes can severely compromise the infectivity of these viruses. Although the mechanism of CpGV resistance is not clear, its evolution emphasizes how dependent baculoviruses are on their hosts for carrying out their replication cycle and how a change in a single receptor or other protein, such as would be required for DNA replication, can interfere with virus infectivity.

An NPV of the cotton bollworm, Helicoverpa armigera: Application in China

The cotton bollworm, Helicoverpa armigera, is a major pest of cotton, and with the intensive use of chemical insecticides it has developed resistance in many parts of the world. One approach to counteract this resistance has been the use of baculoviruses for control of this insect. In China, HearNPV has been produced for use against the cotton bollworm. In the most recent available data (from 2005), about 1,600 tons of infected insects were processed by 12 different producers (15). The insects were grown on an artificial diet composed of mainly corn and wheat, and the infected larvae were processed after removal of lipids into wettable powders or emulsions. Treatment involves spraying fields 3 to 5 times per growing season to control two generations of the cotton bollworm. It was estimated that the virus preparation was used on 200,000 to 300,000 hectares of cotton in 2005. In India, it has been reported that insects are collected by shaking larvae off pea plants onto blankets. HearNPV is then produced by feeding the larvae virus-contaminated chickpea seeds (7).

A recombinant HearNPV is being evaluated in China that expresses a gene encoding an insect-specific toxin (AaIT) from a scorpion found in the Middle East and Africa called Androctonus australis. The use of this recombinant baculovirus is limited to experimental plots of about 2 hectares. In this construct, the AaIT gene is inserted at the EGT locus. This causes problems with the production of the recombinant virus in infected insect larvae. Since the toxin is active against larvae, and deletion of the EGT gene reduces the time it takes the virus to kill the insect, the levels of production are significantly affected; under optimal conditions virus yield is less than 50% of wt. However, the yield from cotton plants treated with this virus is about 25% higher than from plants treated with wt virus. Consequently, this recombinant has significant advantages over the wt virus (15).

A variety of other viruses that are being produced in China range from 120 tons of AcMNPV to less than 50 tons of several other viruses in 2005. These were used to control a variety of insects mostly on vegetables and tea. The data described above is from (15) and Xiu-lian Sun (pers. Comm.).

References

1.
Steinhaus, E.A., Disease in a minor chord1975, Columbus, Ohio: Ohio State University Press. 488.
2.
Podgwaite, J.D., Natural disease within dense gypsy moth populations, in The Gypsy Moth: Research Towards Integrated Pest Management, C.C. Doane and M.L. McManus, Editors. 1981, U.S. Dept. of Agriculture: Washington, D.C.
3.
Thompson, C.G., Nuclear polyhedrosis epizootiology, in The Douglas-fir tussock moth: a synthesis, M.H. Brookes, R.W. Stark, and R.W. Campbell, Editors. 1978, U.S. Department of Agriculture: Washington, D.C.
4.
Heimpel A.M. et al. The presence of nuclear polyhedrosis virus of Trichoplusia ni on cabbage from the market shelf. Environ. Entomol. 1973;2:72–75.
5.
Huber, J., Use of baculoviruses in pest management programs, in The biology of baculoviruses, R.R. Granados and B.A. Federici, Editors. 1986, CRC: Boca Raton. p. 181-202.
6.
Black, B.C., et al., Commercialization of baculoviral insecticides, in The Baculoviruses, L.K. Miller, Editor. 1997, Plenum Press: New York. p. 341-387.
7.
Szewczyk B. et al. Baculoviruses — re-emerging biopesticides. Biotechnol. Adv. 2006;24:143–160. [PubMed: 16257169]
8.
Inceoglu A.B., Kamita S.G., Hammock B.D. Genetically modified baculoviruses: a historical overview and future outlook. Adv Virus Res. 2006;68:323–60. [PubMed: 16997016]
9.
Moscardi F. Use of viruses for pest control in brazil: The case of the nuclear polyhedrosis virus of the soybean caterpillar, Anticarsia gemmatalis. Memorias do Instituto Oswaldo Cruz. Rio de. 1989;84:51–56.
10.
Moscardi F. Assessment of the application of baculovirus for control of lepidoptera. Ann. Rev. Entomol. 1999;44:257–289. [PubMed: 15012374]
11.
Moscardi, F. and D.R. Sosa-Gomez, A case study in Biological control: soybean defoliating caterpillars in Brazil, in 1st International Crop Science Congress1993, Crop Science Society of America, Inc.: Madison, WI.
12.
Oliveira J.V. et al. Genome of the most widely used viral biopesticide: Anticarsia gemmatalis multiple nucleopolyhedrovirus. J Gen Virol. 2006;87(Pt 11):3233–50. [PubMed: 17030857]
13.
Tanada Y. A granulosis virus of the codling moth, Carpocapsae pomonella (Linnaeus) (Olethreutidae, Lepidoptera) J. Insect Pathol. 1964;6:78–80.
14.
Asser-Kaiser S. et al. Rapid emergence of baculovirus resistance in codling moth due to dominant, sex-linked inheritance. Science. 2007;317(5846):1916–8. [PubMed: 17901332]
15.
Sun X., Peng H. Recent advances in biological control of pest insects by using viruses in China. Virolog. Sinica. 2007;22:158–162.
Copyright © 2011, George Rohrmann.
Bookshelf ID: NBK49501
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