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Applied and Environmental Microbiology, November 2001, p. 5166-5170, Vol. 67, No. 11
0099-2240/01/$04.00+0 DOI: 10.1128/AEM.67.11.5166-5170.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Quantification of Soil-to-Plant Transport of
Recombinant Nucleopolyhedrovirus: Effects of Soil Type and
Moisture, Air Currents, and Precipitation
James R.
Fuxa* and
Arthur R.
Richter
Department of Entomology, Louisiana
Agricultural Experiment Station, Louisiana State University
Agricultural Center, Baton Rouge, Louisiana 70803
Received 25 June 2001/Accepted 31 August 2001
 |
ABSTRACT |
Significantly more occlusion bodies (OB) of DuPont viral construct
HzSNPV-LqhIT2, expressing a scorpion toxin, were transported by
artificial rainfall to cotton plants from sandy soil (70:15:15 sand-silt-clay) than from silt (15:70:15) and significantly more from
silt than from clay (15:15:70). The amounts transported by 5 versus 50 mm of precipitation were the same, and transport was zero when there
was no precipitation. In treatments that included precipitation, the
mean number of viable OB transported to entire, 25- to 35-cm-tall
cotton plants ranged from 56 (clay soil, 5 mm of rain) to 226 (sandy
soil, 50 mm of rain) OB/plant. In a second experiment, viral transport
increased with increasing wind velocity (0, 16, and 31 km/h) and was
greater in dry (
1.0 bar of matric potential) than in moist (0.5
bar) soil. Wind transport was greater for virus in a clay soil than in
silt or sand. Only 3.3 × 10
7 (clay soil, 5 mm rain)
to 1.3 × 106 (sandy soil, 50 mm rain) of the OB in
surrounding soil in experiment 1 or 1.1 × 107
(0.5 bar sandy soil, 16-km/h wind) to 1.3 × 106
(1.0 bar clay soil, 31-km/h wind) in experiment 2 were transported by
rainfall or wind to cotton plants. This reduces the risk of environmental release of a recombinant nucleopolyhedrovirus (NPV), because only a very small proportion of recombinant virus in the soil
reservoir is transported to vegetation, where it can be ingested by and
replicate in new host insects.
| |
INTRODUCTION |
Nucleopolyhedroviruses (NPV) are
important agents of natural mortality for certain insects and
crustaceans (5). In addition to their very specific host
ranges, these viruses are characterized by their capability for causing
epizootics with high prevalence and case-fatality rates in host insects
(8). For these reasons, NPV have been researched
extensively as environmentally safe, viral insecticides
(24). To this end, epizootiology has contributed to
improvements in their efficacy and methods of utilization
(7).
NPV have succeeded in pest management in certain cases, but certain
weaknesses, such as the slow death of the infected insect, have
hindered their development as insecticides (8). Genetic modification has been pursued as a means to improve their lethal time
(3). For example, survival times of the tobacco budworm, Heliothis virescens, and the bollworm, Helicoverpa
zea, were reduced when infected with Heliothis NPV
expressing highly specific toxin from the scorpion Leiurus
quinquestriatus hebraeus (DuPont construct HzSNPV.LqhIT2)
(16).
Epizootiology of DNA-recombinant NPV has assisted in their risk
assessment for pesticide regulatory agencies. Knowledge of viral
persistence, population growth, and spread can reduce their risk of
environmental release, even when the possibility of harmfulness to
nontarget organisms is difficult or impossible to ascertain (9). For example, Autographa californica NPV
expressing toxin from the scorpion Androctonus australis
produced smaller populations on leaves and in soil and was dispersed
less by biotic agents than the wild-type, parental NPV (6, 20,
21). Similarly, the population density of HzSNPV.LqhIT2 in soil
was less than that of wild-type Heliothis NPV
(11). The reduced population density and dispersal of the
recombinant NPVs reduce the likelihood that they will contact nontarget
organisms in the environment.
Ecology of NPV in soil is essential for their long-term insect control
and risk assessment (7, 9). Soil is a major reservoir for
NPV between hosts, particularly for long-term survival. These viruses,
embedded in their proteinaceous occlusion bodies (OB), can persist in
soil more than 5 years after release in a row crop (17)
and up to 41 years after a natural epizootic in a forest ecosystem
(30). These OB in soil then can be transported onto insect
host plants, where they are ingested by their hosts to replicate and
initiate new epizootics (12, 33, 34). Like its wild-type
counterpart, the HzSNPV.LqhIT2 construct can persist in soil from one
crop-growing season to the next, when it may have the opportunity to
replicate in a new generation of host insects (11). A
major gap in our knowledge of NPV ecology in soil is the transport of
OB from soil to the insect's host plant. Rainfall (10, 13, 23,
29, 34) and air currents (13, 25, 31) have been
implicated in soil-to-plant transport in a limited number of
observational studies, but there has been little controlled
experimentation with this phenomenon (9). The proportion
of the soil population of NPV reaching foliage by these methods and the
influence of environmental variables have not been quantified. In fact,
there is little quantitative information on transport of any type of
microorganism from soil to leaves, although wind speed and amount and
intensity of rain are considered to be important factors
(19).
The purpose of the present study was to quantify, under carefully
controlled conditions, the effects of soil type, soil moisture, precipitation, and air currents on soil-to-plant transport of a
recombinant NPV. We also determined the proportion of the soil population of NPV that was transported onto plants under these variables.
| |
MATERIALS AND METHODS |
Virus and insect.
The virus, provided by DuPont Agricultural
Products (Wilmington, Del.), was a variant of the Heliothis
or Helicoverpa NPV genetically modified to express an
insect-specific neurotoxin from the scorpion L. quinquestriatus
hebraeus (HzSNPV.LqhIT2). The insects used in bioassays were
neonatal H. virescens shipped as eggs from DuPont.
Soil type-precipitation experiment.
The experiments were
conducted in a greenhouse in order to control the necessary variables.
This experiment tested the effects of soil type, precipitation, and
soil-precipitation interactions on viral transport. There were nine
treatments (three soil types × three precipitation rates) with
virus in the soil plus a control for each soil type with no virus, and
there were four replications per treatment.
Ingredient soils were mixed by weight to provide experimental soil
types with clay-silt-sand ratios of 70:15:15, 15:70:15, and 15:15:70,
respectively. The following ingredient soils were analyzed for content
at the Louisiana State University Agricultural Center Soil Laboratory:
(i) Quickrete Play Sand (Quickrete Co., Atlanta, Ga.), 4.8% silt,
1.0% clay, and 94.2% sand; (ii) white clay (Southern Pottery, Baton
Rouge, La.), 9.2% silt, 90.0% clay, and 0.8% sand; and (iii) silt
from a field near Baton Rouge, 81.0% silt, 15.2% clay, and 3.8%
sand. Samples of the final soil mixtures then were analyzed again at
the Soil Laboratory with the following results: the clay mixture was
70.3% clay, 15.3% silt, and 14.4% sand, with 1.22% organic matter
and a pH of 6.8. The silt mixture was 15.8% clay, 69.5% silt, and
14.7% sand, with 1.66% organic matter and a pH of 7.5. The sand
mixture was 14.6% clay, 14.5% silt, and 70.9% sand, with 1.14%
organic matter and a pH of 7.2. After the three soil types were
prepared, the moisture of each was determined with a Jet-Filled
Tensiometer (model 2725 ARL; Soil Moisture Equipment Corp., Santa
Barbara, Calif.) embedded in the soil for 24 h. Distilled water
was added to soil to result in a water potential of 0.5 bar in every
treatment, which was confirmed with another 24-h tensiometer reading.
For each replication of each treatment, HzSNPVLqhIT2 was mixed into 68 kg of the appropriate soil type at 2,500 viral OB/g
of soil. This
amount of soil was spread out on a 1.5-m by 1.5-m
area, and the OB were
suspended in 200 ml of distilled water and
then sprayed evenly over the
entire soil surface with a CO
2 sprayer.
The soil
was then mixed thoroughly by hand to evenly distribute
the
virus.
For each treatment or replication, a cotton plant was grown in a
3.8-liter pot, which in turn was placed in the center of
a 1.2-m by
1.2-m flat. All plants in the experiment were 25 to
35 cm high,
assigned in a manner such that all treatments within
a replication
included plants of a similar height. Untreated soil
was added to the
flat to a height of 3.8 cm below the top edge
of the pot. This soil
layer was covered with plastic, and the
virus-treated soil then was
layered onto the untreated soil so
that the entire flat contained
virus-treated soil to a depth of
2.5 cm, up to the top edge of the pot
with the cotton plant. A
control for each soil type was set up in an
identical manner,
except that no virus was added to the
soil.
Immediately after the soil was added to each flat, one of three rates
of precipitation (0, 5, or 50 mm) was applied in 1 min
by an overhead
sprinkler system designed to water evenly over
the entire flat. The low
rate of 5 mm/min has successfully contributed
to artificial epizootics
in a similar greenhouse microcosm in
previous research
(
21). The leaves were allowed to dry, and
then they all
were excised from the plant. The entire procedure
was repeated for each
replication or treatment. The experimental
area was decontaminated with
0.525% NaClO after all treatments
were run in one
replication.
All of the leaves from each plant were weighed and then homogenized for
2 min in a Sorvall Omni-Mixer (DuPont Instruments,
Newtown, Conn.) in
distilled water at a ratio of 3 g of plant
tissue to 10 ml of
water. Aliquots were fed to neonatal
H. virescens larvae by
droplet-feeding bioassay (
14). The larvae then were
transferred to 30-ml individual cups containing tobacco budworm
artificial diet (Southland Products, Lake Village, Ark.) and kept
at
26.7°C until they died or pupated. Death due to nuclear polyhedrosis
was confirmed by detection of OB under phase-contrast
microscopy.
A standard bioassay curve was determined in order to convert vegetation
bioassay percentages of mortality to concentrations
of viral OB in the
leaf samples. Known amounts of leaf tissue
were homogenized as
described above, and known amounts of the
virus were added to the
homogenate, which then was homogenized
for an additional 2 min. The
homogenate was then bioassayed as
described above. The bioassay
standard curve had two replications,
with eight doses and 50 insects
per dose per
replication.
Soil type-air current-soil moisture experiment.
The soil
type-air current-soil moisture experiment tested the effects of soil
type, wind velocity, soil moisture, and soil-wind-moisture interactions
on viral transport. There were 18 treatments (three soil types × three wind velocities × 2 soil moisture levels) with virus in the
soil plus a control with no virus for each soil type at the low
moisture level, and there were four replications per treatment.
The same three soil types were used as in the soil type-precipitation
experiment. Distilled water was added to each batch
of soil to
establish soil water potentials at either
0.5 (moist)
or
1.0 (dry)
bar, as described above. A floor model, 41-cm-diameter
electric fan
provided the wind or air current at velocities of
16.1 and 30.6 km/h,
as determined with a model 05-005 anemometer
(Science First, Buffalo,
N.Y.) at 100 cm from the
fan.
For each treatment or replication, a potted cotton plant was set in a
flat, and soil was added as described above, except
that the plant was
set at the middle of one edge of the flat instead
of the center. The
fan faced the flat at 30 cm outside the far
edge of the flat and was
run at the appropriate velocity for 2
min. The remainder of the
experiment (collection of leaves, bioassay,
data analysis, and
decontamination) was the same as in the soil
type-precipitation
experiment.
Statistical analysis.
The main experimental data were tested
by the general linear models (GLM) analysis of variance, with the Tukey
Studentized range honestly significant difference (HSD) test for
comparison among means (SAS/STAT user's guide, vol. 2, GLM-VARCOMP,
version 6, 4th ed. SAS Institute, Cary, N.C., 1990). Two analyses were run for each experiment, one each with bioassay percentage of mortality
or number of OB per plant as the dependent variable. The virus-plant
standard curve data were subjected to probit analysis with MicroProbit
3.0 (T. C. Sparks and A. Sparks, Lily Research Laboratories,
Greenfield, Ind.).
| |
RESULTS |
Soil type-precipitation experiment.
Precipitation clearly
transported the NPV from soil onto cotton plants (Tables
1 to 3). The percentages of mortality due to and the amounts of HzSNPV.LqhIT2 transported from soil to cotton plants did not differ significantly between 5 versus 50 mm of precipitation (Tables 1 and 3). However, both amounts of artificial rainfall transported significantly more OB than zero precipitation, in
which there was no viral contamination of plants. There was no viral
contamination of control plants, which were subjected to 50 mm of
precipitation.
Soil type clearly affected viral transport due to precipitation (Tables
1 to
3). Significantly greater percentages of mortality
and OB
transport resulted from artificial rainfall applied to
cotton plants in
sandy soil than in silt, and significantly more
occurred in silt than
in clay (Tables
1 and
3). The interaction
between soil type and
precipitation also was significant for the
percentage of infection and
the number of OB transported (Table
2),
probably because there was less difference in plant contamination
between amounts of rainfall in sandy soil than in silt or clay
(Tables
1 and
3).
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TABLE 2.
General linear models procedure analysis of variance
indicating sources of variation in the soil type-precipitation
experiment
|
|
Only a small proportion of HzSNPV.LqhIT2 in soil was transported by
precipitation onto cotton plants. The 1.44 m
2 of
soil surrounding each plant to a depth of 3.8 cm weighed 68
kg with
2,500 viral OB/g, for a total viral population of 1.7
× 10
8 OB/flat. Thus, the proportion of OB
transported by precipitation
from soil to a 25- to 35-cm-high plant
ranged from 3.3 × 10
7 (clay soil, 5 mm of
precipitation) to 1.3 × 10
6 (sandy soil,
50 mm of precipitation) (Table
3). If one
assumes
that viral OB in only the top 0.2 cm of soil are subject to
possible
transport by precipitation, then the proportion of OB
transported
to foliage of cotton plants still ranged only from 6.2 × 10
6 to 2.5 × 10
5. In spite of the small proportion of soil
NPV transported, this
was still sufficient to initiate infection rates
of 4.5 to 38.0%
in first-instar
H. virescens.
Soil type-air current-soil moisture experiment.
Air currents
also transported the NPV from soil onto cotton plants (Tables
4 to 6). The percentage of mortality due
to and amounts of HzSNPV.LqhIT2 transported from soil to cotton plants were significantly greater in a 30.6-km/h wind than at 16.1 km/h (Tables 4 and 6); there was no viral contamination of plants without
air currents. There was no viral contamination of control plants, which
were subjected to a wind velocity of 30.6 km/h.
Soil type and moisture clearly affected viral transport due to air
currents (Tables
4,
5, and
6). Significantly greater
mortality and OB
transport resulted in artificial wind applied
to cotton plants in clay
than in silt or in sandy soil (Tables
4 and
6), the opposite of soil
effects in the precipitation
experiment (Tables
1 and
3). Furthermore,
the percentage of
mortality and the number of OB on plants were
significantly greater
in dry (
1.0 bar) than in moist (
0.5 bar) soil
(Tables
4 and
6). All two-way interactions (soil type × moisture;
soil type
× wind; moisture × wind) were significant (Table
5). The three-way
interaction (soil
type × moisture × wind) was significant when
the number of
OB per plant was the dependent variable, but not
when the percentage of
mortality was the dependent variable.
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TABLE 5.
GLM procedure analysis of variance indicating sources of
variation in the soil type, soil-moisture-wind experiment
|
|
As in the precipitation experiment, only a small proportion of
HzSNPV.LqhIT2 in soil was transported by wind onto cotton plants.
The
1.44 m
2 of soil in the flat to a depth of 3.8 cm
again contained a total
of 1.7 × 10
8 OB.
Thus, the proportion of OB transported by wind from soil
to a 25- to
35-cm-high plant ranged from 1.1 × 10
7
(
0.5 bar sandy soil, 16.1-km/h wind) to 1.3 × 10
6 (
1.0 bar clay, 30.6-km/h wind) (Table
6). If one assumes that
viral OB in only
the top 0.2 cm of soil are subject to possible
transport by wind, then
the proportion of OB transported to foliage
of cotton plants still
ranged only from 2.1 × 10
6 to 2.6 × 10
5. Thus, the greatest proportion of OB
transported by artificial
wind was almost identical to the greatest
proportion transported
by artificial precipitation. In spite of the
small proportion
of soil NPV transported, this was still sufficient to
initiate
infection rates of 0.5 to 31.0% in first-instar
H. virescens.
| |
DISCUSSION |
The results showed conclusively that some physical force is
required to transport NPV onto cotton plants, because no virus was
detected on plants in any of the controls in the precipitation or wind
experiments. NPV transport increased with increasing wind velocity, but
there was no difference in transport between different amounts of rain,
although rain intensity has been positively correlated with splash
transport of fungal phytopathogens (22). It is possible that a less intense rainfall than 5 mm in 2 min would have resulted in
significantly less viral transport. Once OB were splashed onto the
plant, additional precipitation probably did not wash them away,
because several studies have indicated that rain does not remove viral
OB from leaf surfaces (18).
Previous research quantifying soil-to-plant transport of microorganisms
generally has not incorporated the control of abiotic factors as
independent variables. An observational study implicated road dust in
dispersal of Neodiprion sertifer NPV up to 30 m or more
in a forest ecosystem (25), and a Pseudoplusia
includens NPV exhibited a dose response in terms of viral
epizootics in the insects infesting soybean after one-time application
of the virus to soil (33). Other research has dealt
primarily with phytopathogens, especially fungi. For example, dust
dispersed by wind was a primary source of inoculum for
Colletotrichum truncatum (4), and rain splash
and wind interacted in the transport of Colletotrichum
gloeosporioides, a commercial mycoherbicide (32). Soil surface microtopography (i.e., roughness) greatly influenced splash transport of fungal phytopathogens, with splash distance increasing as roughness declined (22).
It was interesting that the type of soil in the current research
affected efficiency of soil-to-plant transport differently in wind than
in rain. Rain splash transported more virus from sand than silt and
more from silt than clay. In a wind, the order was the opposite: clay
was best for transport, then silt, then sand. Dry soil was better than
moist soil, probably because the former is more conducive to formation
of airborne dust. The reasons for these opposite effects may relate to
NPV adhesion to soil particles and to the size of those particles.
Inorganic soil particulates include coarse sand (0.2 to 2.0 mm in
diameter), fine sand (0.02 to 0.2 mm), silt (0.002 to 0.02 mm), and
clay (<0.002 mm) (2, 26). If NPV in our research was
adhering to clay particles, which have a dominant role in the ecology
of soil microorganisms (2), this may explain the efficient
transport of NPV from dry clay soil by wind. Soil compaction probably
did not affect transport in our research, because the experiments were
run immediately after treated soil was added loosely to the flats.
Previous research of NPV surface characteristics and soil interactions
is sparse. Surface characteristics of NPV polyhedra are largely unknown
and complex, though they may behave as hydrophobic entities
(27). Polyhedra of cypovirus (cytoplasmic polyhedrosis virus), which have an amino acid composition similar to polyhedra of
NPV (28), may adsorb to soil particles mainly by coulomb force, depending on pH and the inorganic fractions of soil
(15). Negative as well as positive adsorption of OB to
soil particles is possible; it cannot be assumed that adhesion explains
all microbial responses in soil (26).
The current results should be useful in epizootiology and risk
assessment of baculoviruses. For example, in previous research, the
percentage of silt in soil was negatively correlated with naturally
occurring epizootics of nuclear polyhedrosis in populations of
Spodoptera frugiperda infesting pastures over a 2-year
period (10). This finding is consistent with results of
the current research, under the safe assumption that the S. frugiperda NPV in pasture soils was subject to both wind and rain
during the 2 years. Our results also are pertinent to environmental
risk assessment of recombinant NPV. The proportion of HzSNPV.LqhIT2 in
soil that was transported to cotton plants was so small
less than
0.003% from the top 0.2 cm of soil under the best conditions, and far
less under more stringent conditionsthat this reduces the probability
of the recombinant virus replicating in host insects, which, in turn,
reduces the probability that it will come into contact with nontarget
organisms. Of course, the small proportion of HzSNPV.LqhIT2
transported still was sufficient to infect up to 38% of H. zea larvae under the best conditions (Table 1). However, we used
larvae that were <1 day old for our bioassays, the most susceptible
stage of the insect. The susceptibility of H. zea to HzSNPV
decreases by 250× in larvae between the ages of 3 and 8 days
(1). Furthermore, HzSNPV.LqhIT2 does not accumulate in
soil from season to season in the cotton agroecosystem
(11). Although HzSNPV.LqhIT2 is unlikely to be used in
pest management in cotton, the current results are relevant to
epizootiology and risk assessment of NPV in general, because the
insertion of a scorpion toxin gene does not alter the polyhedrin
protein comprising the OB (3).
Further research is necessary to further elucidate abiotic
soil-to-plant transport of NPV, particularly the effect of plant height
and the thresholds of soil inocula necessary to initiate epizootics. It
also would be helpful to learn the dimensions of the soil
"universe"the distance from the plant and soil depthfrom which
transport to a particular plant is likely.
| |
ACKNOWLEDGMENT |
This work was supported by USDA Risk Assessment grant
98-33120-6435.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Entomology, 402 Life Sciences Bldg., Louisiana State University, Baton Rouge, LA 70803. Phone: (225) 578-1836. Fax: (225) 578-1643. E-mail: jfuxa{at}lsu.edu.
This paper was approved for publication by the Director of the
Louisiana Agricultural Experiment Station as manuscript no. 01-17-0404.
| |
REFERENCES |
| 1.
|
Allen, G. E., and C. M. Ignoffo.
1969.
The nucleopolyhedrosis virus of Heliothis: quantitative in vivo estimates of virulence.
J. Invertebr. Pathol.
13:378-381[CrossRef].
|
| 2.
|
Bitton, G., and K. C. Marshall.
1980.
Adsorption of microorganisms to surfaces.
Wiley & Sons, New York, N.Y.
|
| 3.
|
Bonning, B. C., and B. D. Hammock.
1996.
Development of recombinant baculoviruses for insect control.
Annu. Rev. Entomol.
41:191-210[CrossRef][Medline].
|
| 4.
|
Buchwaldt, L.,
R. A. A. Morrall,
G. Chongo, and C. C. Bernier.
1996.
Windborne dispersal of Colletotrichum truncatum and survival in infested lentil debris.
Phytopathology
86:1193-1198.
|
| 5.
|
Federici, B. A.
1997.
Baculovirus pathogenesis, p. 33-59.
In
L. K. Miller (ed.), The baculoviruses. Plenum Press, New York, N.Y.
|
| 6.
|
Fuxa, J. A.,
J. R. Fuxa, and A. R. Richter.
1998.
Host-insect survival time and disintegration in relation to population density and dispersion of recombinant and wild-type nucleopolyhedroviruses.
Biol. Control
12:143-150[CrossRef].
|
| 7.
|
Fuxa, J. R.
1990.
New directions for insect control with baculoviruses, p. 97-113.
In
R. R. Baker, and P. E. Dunn (ed.), New directions in biological control Alan R. Liss, Inc., New York, N.Y.
|
| 8.
|
Fuxa, J. R.
1991.
Insect control with baculoviruses.
Biotechnol. Adv.
9:425-442.
|
| 9.
|
Fuxa, J. R.
1991.
Release and transport of entomopathogenic microorganisms, p. 83-113.
In
M. Levin, and H. Strauss (ed.), Risk assessment in genetic engineering McGraw-Hill, New York, N.Y.
|
| 10.
|
Fuxa, J. R., and J. P. Geaghan.
1983.
Multiple-regression analysis of factors affecting prevalence of nuclear polyhedrosis virus in Spodoptera frugiperda (Lepidoptera: Noctuidae) populations.
Environ. Entomol.
12:311-316.
|
| 11.
|
Fuxa, J. R.,
M. M. Matter,
A. Abdel-Rahman,
S. Micinski,
A. R. Richter, and J. L. Flexner.
2001.
Persistence and distribution of wild-type and recombinant nucleopolyhedroviruses in soil.
Microb. Ecol.
41:222-232[Medline].
|
| 12.
|
Fuxa, J. R., and A. R. Richter.
1999.
Classical biological control in an ephemeral crop habitat with Anticarsia gemmatalis nucleopolyhedrovirus.
BioControl
44:403-419.
|
| 13.
|
Hostetter, D. L., and M. R. Bell.
1985.
Natural dispersal of baculoviruses in the environment, p. 249-284.
In
K. Maramorosch, and K. E. Sherman (ed.), Viral insecticides for biological control Academic Press, Orlando, Fla.
|
| 14.
|
Hughes, P. R., and H. A. Wood.
1981.
A synchronous peroral technique for the bioassay of insect viruses.
J. Invertebr. Pathol.
37:154-159[CrossRef].
|
| 15.
|
Hukuhara, T., and H. Wada.
1972.
Adsorption of polyhedra of a cytoplasmic-polyhedrosis virus by soil particles.
J. Invertebr. Pathol.
20:309-316[CrossRef].
|
| 16.
|
Ignoffo, C. M.,
J. F. H. Wong, and S. G. Saathoff.
1999.
Mortality and feeding of mid-stadium larvae of Helicoverpa zea and Heliothis virescens fed a wild strain or a recombinant strain of Baculovirus heliothis expressing an insect-specific toxin of the scorpion Leiurus quinquestriatus hebraeus.
Appl. Entomol. Zool.
34:279-283.
|
| 17.
|
Jaques, R. P.
1967.
The persistence of a nuclear polyhedrosis virus in the habitat of the host insect. Trichoplusia ni. I. Polyhedra deposited on foliage.
Can. Entomol.
99:785-794.
|
| 18.
|
Jaques, R. P.
1985.
Stability of insect viruses in the environment, p. 285-360.
In
K. Maramorosch, and K. E. Sherman (ed.), Viral insecticides for biological control Academic Press, San Diego, Calif.
|
| 19.
|
Kinkel, L. L.
1997.
Microbial population dynamics on leaves.
Annu. Rev. Phytopathol.
35:327-347[CrossRef][Medline].
|
| 20.
|
Lee, Y., and J. R. Fuxa.
2000.
Transport of wild-type and recombinant nucleopolyhedroviruses by scavenging and predatory arthropods.
Microb. Ecol.
39:301-313[Medline].
|
| 21.
|
Lee, Y., and J. R. Fuxa.
2001.
Competition between wild-type and recombinant nucleopolyhedroviruses in a greenhouse microcosm.
Biol. Control
20:84-93[CrossRef].
|
| 22.
|
Madden, L. V.
1997.
Effects of rain on splash dispersal of fungal pathogens.
Can. J. Plant Pathol.
19:225-230.
|
| 23.
|
Mitchell, F. L., and J. R. Fuxa.
1990.
Multiple regression analysis of factors influencing a nuclear polyhedrosis virus in populations of fall armyworm (Lepidoptera: Noctuidae) in corn.
Environ. Entomol.
19:260-267.
|
| 24.
|
Moscardi, F.
1999.
Assessment of the application of baculoviruses for control of Lepidoptera.
Annu. Rev. Entomol.
44:257-289[CrossRef][Medline].
|
| 25.
|
Olofsson, E.
1988.
Dispersal of the nuclear polyhedrosis virus of Neodiprion sertifer from soil to pine foliage with dust.
Entomol. Exp. Appl.
46:181-186[CrossRef].
|
| 26.
|
Savage, D. C., and M. Fletcher.
1985.
Bacterial adhesion. Mechanisms and physiological significance.
Plenum Press, New York, N.Y.
|
| 27.
|
Small, D. A.,
N. F. Moore, and P. F. Entwistle.
1986.
Hydrophobic interactions involved in attachment of a baculovirus to hydrophobic surfaces.
Appl. Environ. Microbiol.
52:220-223[Abstract/Free Full Text].
|
| 28.
|
Tanada, Y., and H. K. Kaya.
1993.
Insect pathology.
Academic Press, San Diego, Calif.
|
| 29.
|
Thompson, C. G.
1978.
Nuclear polyhedrosis epizootiology. The Douglas-fir tussock moth: a synthesis.
USDA For. Serv. Sci. Edu. Agency Tech. Bull.
1585:136.
|
| 30.
|
Thompson, C. G.,
D. W. Scott, and B. E. Wickman.
1981.
Long-term persistence of the nuclear polyhedrosis virus of the Douglas-fir tussock moth, Orgyia pseudotsugata (Lepidoptera: Lymantriidae), in forest soil.
Environ. Entomol.
10:254-255.
|
| 31.
|
Thompson, C. G., and E. A. Steinhaus.
1950.
Further tests using a polyhedrosis virus to control the alfalfa caterpillar.
Hilgardia
19:411-415.
|
| 32.
|
Yang, X. B., and D. O. Tebeest.
1992.
Rain dispersal of Colletotrichum gloeosporioides in simulated rice field conditions.
Phytopathology
82:1219-1222.
|
| 33.
|
Young, S. Y., and W. C. Yearian.
1979.
Soil application of Pseudoplusia NPV: persistence and incidence of infection in soybean looper caged on soybean.
Environ. Entomol.
8:860-864.
|
| 34.
|
Young, S. Y., and W. C. Yearian.
1986.
Movement of a nuclear polyhedrosis virus from soil to soybean and transmission in Anticarsia gemmatalis (Hübner) (Lepidoptera: Noctuidae) populations on soybean.
Environ. Entomol.
15:573-580.
|
Applied and Environmental Microbiology, November 2001, p. 5166-5170, Vol. 67, No. 11
0099-2240/01/$04.00+0 DOI: 10.1128/AEM.67.11.5166-5170.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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