The Influence of
Aphid Natural Enemies on the
Spread of Barley
Yellow Dwarf Virus
Douglas W. Johnson*, Richard Harrington, Mark S. Taylor and Adam J. Burgess
*Department of Entomology, University of Kentucky, Research and Education
Center, P.O. Box 469, Princeton, KY 42445 USA
and
Department of
Entomology and Nematology, IACR-Rothamsted, Harpenden,
Hertfordshire, AL5 2JQ.
IOBC Bulletin 21(8):63-68, 1998
Results are reported of a field and
laboratory study on the influence of adult, coccinellid predators Coccinella septempunctata (L.) and braconid parasitoids Aphidius rhopalosiphi deStefani-Perez
on the spread of barley yellow dwarf virus by bird cherry-oat aphid (Rhopalosiphum padi (L.)) and
English grain aphid (Sitobion avenae (F.)).
Introduction:
Barley yellow dwarf (BYD) is the
most widespread and economically important disease of cereals world wide (Plumb
1983). Though BYD virus produces a disease in cereals, the disease epidemiology
is obligatorily dependent upon aphids for all movement and spatial development
(Irwin and Thresh 1990). Among the most important of these aphid vectors are the
bird cherry-oat aphid (Rhopalosiphum padi (L)) and grain aphid (Sitobion avenae
(F.)) (Mann et al. 1996).
In the UK a 'Decision Support System'
is being developed to assist rationalization of spraying of autumn sown crops
for control of the main aphid vectors (Harrington et. al. 1994; Mann
et al. 1996) It has been suggested that natural enemies of the aphid
vectors may affect aphid movement (Sopp et al.
1987; Knaust 1996) thereby influencing disease
development and thus would need to be accounted for in the Decision Support
System. Two common natural enemies of cereal aphids, the adult, coccinellid predator (Coccinella septempunctata (L.)) and the braconid parasitoid (Aphidius rhopalosiphi deStefani-Perez)
were chosen for examination. In this communication the authors outline the
experiment and present a preliminary view of a portion of the resulting
data.
Methods and Materials:
All experiments were conducted at
IACR-Rothamsted, Harpenden,
All insects were reared in controlled
environment (CE) rooms under a 16 hours : 8 hours
(light : dark) cycle at ca. 60% RH. Aphids and coccinellids were held at a constant 18oC, while
parasitoids were held at a constant 15oC. Six aphid colonies were
maintained. Each of the two aphid species was maintained separately on
BYDV-infected wheat and barley and non-BYDV infected barley. Two parasitoid
colonies were maintained one for each aphid species. Seven spot ladybirds (C.
septempunctata) were collected during September
1996 at Rothamsted Experimental Station and nearby.
They were fed for one week by allowing them free choice
in an aphid colony of appropriate species. They were then held in 9 cm
disposable petri dishes at 4oC until
needed. New aphids of the appropriate species were supplied to predator and
parasitoid colonies from the aphid colonies reared on non-BYDV infected plants.
In all predator and parasitoid colonies the aphid host was barley.
Forty eight, three-meter square plots
of wheat and barley (24 plots each) were planted on 3 September 1996 utilizing
standard agricultural practices with the exception that no insecticides were
applied to either seed or plots. In each plot areas were identified for
placement of cages. Ideally each area was two adjacent rows of 12 plants. Plants
were checked for natural aphid infestation and any aphids were removed and the
species, numbers and position of infested plants were recorded. Test plants were
then covered with a 25 cm x 25 cm x 50 cm (length x width x height) mesh cage to
prevent further colonization from wild aphid populations.
CE rooms were held at 10 hours : 14 hours (light : dark) and corresponding
14oC : 9oC temperature. Wheat and barley were sown in
square, 25 plant grids at ca. 3 cm spacings in 53 cm x
53 cm x 5 cm (length x width x depth) trays. Each tray held 4 grids. At GS 12,
20 individual grids were covered using the same cages utilized in the field
study.
On 18 September (GS
12, 20) the first field experiment was begun. Two plants, one each nearest the
center of the two rows within a cage, were infested with 5 viruliferous fourth instar winged
individuals of appropriate species. The aphids were confined to the plants using
clip cages (Mann et al. 1995) and were held on the plants for five days.
On 14 October (GS 12, 22-23) the second field experiment was begun. Aphid
infestation was the same as the first experiment except that fourth instar non-winged individuals were used and confined on the
plants in clip cages for only 24 hours. In the CE rooms caged plants (GS 12, 20)
were infested with fourth instar apterae, using the same procedure as was utilized in the
field trials except that all 10 aphids were in a single clip cage and only the
center plant in each grid was infested. After 48 hours the clip cages were
carefully removed.
One week before delivery into test
cages ladybird beetles were removed from the cold storage and allowed "free
choice" feeding on appropriate aphid species for 4 days, followed by 3 days of
starvation. Three days prior to introduction into the test cages parasitoids
were removed from the colony with an aspirator. They were held in 3 cm x 7.5 cm
(diameter x length) glass bottles with net tops and fed a 50:50 mixture of honey : water on saturated Kimwipe®. On the day of introduction they were individually
sexed and females were placed into small aspirators (Tamaki et al. 1970).
On the day of clip cage removal,
predators and parasitoids were released into the cages during the afternoon.
Predators were introduced into the cages by placing a 1.3 cm x 5 cm (diameter x
length) uncapped glass vial containing one beetle in the center of the caged
area. Parasitoids were delivered near the volumetric center of the cage via an
aspirator.
In all experiments the predator /
parasitoid treatments were maintained for two weeks. At the end of this period
the aphids were counted and recorded by plant location, the cages were removed,
and the plants sprayed with an insecticide to prevent further aphid movement. In
the field trials test areas were sprayed every two weeks until plant leaf
samples were taken for BYDV assay. In the CE room trial plants were sprayed
immediately after cage removal and moved to a room that did not contain aphids
and thereafter inspected to ensure that no aphids survived.
After the predator / parasitoid
treatments were removed plants were allowed to grow for a further 5 weeks, after
which a portion of the youngest completely unrolled leaf on the main stem was
taken for analysis. The presence of BYDV MAV and PAV was confirmed by positive
reaction with BYDV antiserum in enzyme-linked immunosorbent assay (ELISA).
Data were analyzed to test for
differences in mean percent aphid infestation and mean percent virus infection
resulting from the main effects 'Experiment' , 'Crop', 'Aphid Sp.' and 'Predator
/ Parasitoid Treatment'. Analysis was carried out using Statistical Analysis
System (SAS Institute 1995). Percentages were analyzed by applying an analysis
of variance (ANOVA) to square-root arcsin transformed
data at the p= .05 level of significance. Results are reported as
percentages.
Results &
Discussion:
Tables
1, 2 and 3 summarize the mean percent aphid infestations for field experiment 1,
2 and CE room respectively. Preliminary statistical analysis indicated
significant differences for all main effects as follows; Experiment P = 0.0004,
Crop P = 0.0001, Aphid Sp. P = 0.0108, and Predator / Parasitoid Treatment P =
0.0017. However, several significant interactions were also indicated. They are;
Experiment * Aphid Sp. P = 0.0001, Crop * Predator / Parasitoid Treatment P =
0.0179 and Aphid Sp. * Predator / Parasitoid Treatment P = 0.0328.
The first field experiment has greater
overall values for infestation followed by the controlled environment experiment
and then the second field experiment. This outcome might be expected solely on
the basis of temperature. Temperatures in the first field experiment were warmer
than in the second field experiment while the controlled environment room
experiment was conducted at intermediate temperatures. It is also possible that
plant size had an effect. The first field experiment and the controlled
environment experiment were both started with "two leaf" stage plants while the
second field experiment was at the "one to two tiller"
stage. This later stage would have provided more leaf area per plant on which
the aphids might settle and thus resulting in less need to move.
Barley plants tended to have higher
infestation levels than wheat plants. This effect is constant across all three
experiments, and both aphid species. Additionally, with one exception (See Table
2, second field experiment x R. padi x
parasitoid), it is consistent within all predator / parasitoid
treatments.
As of this writing all experimental
plants have been subject to ELISA for detection of BYDV. However, analysis of
the complete experiment is not yet available. The infection data reported here
are from all three experiments, and include both barley and wheat but, only the
aphid S. avenae, and the two natural enemies
treatments: 'no predator or parasitoid', and 'single predator'. Initial ANOVA
indicated significant differences between the three experiments. However, there
was no significant difference between barley and wheat or between; 'no predator
or parasitoid', and 'single predator'.
Percent virus infection for field
experiments 1, 2 and CE room respectively were (mean ± standard error) 46.8 ±
4.1, 23.3 ± 3.7 and 30.3 ± 4.5 (n=12, F=8.92, P = 0.0013 ). Percent infection by
crop was 37.0 ± 3.9 for barley and 29.9 ± 4.1 for wheat (n=18, P = 0.1250).
Percent infections by treatments was; 'no predator or parasitoid' 31.1 ± 3.7 and
'single predator' at 35.9 ± 4.4 (n=18, P =0.3248). There were no significant
three way interactions or two way interactions involving the factor
'Experiment'. However, there may be a two way interaction involving the factors
'Crop' and 'Treatment' (P = 0.0512).
Summary:
There was a significant different
between the overall mean percent virus infection in the three experiments. The
virus infection levels follow the same pattern as the aphid infestation levels
with the first field experiment having the greatest percent virus infection,
followed by the CE room experiment then the second field experiment. There was
no significant difference between crop type, however
the barley plots did produce a greater mean infection. The
was no difference between the two predator / parasitoid
treatments.
Currently, the available percent aphid
infestation and percent virus infection data do not provide evidence to indicate
that natural enemies either reduce or enhance the level of BYDV. However, the
reader is reminded that this is a very preliminary analysis. We suggest for
example that the number of aphids present at the time of cage removal may prove
to be a significant co-variate. Though two cages might
have quite similar percent infestations they may be infested with very different
numbers of aphids. Additionally this communication does not report any analysis
of the spatial distribution of either aphid infestation or virus infections,
which will be examined later.
References:
Harrington, R., Mann, J.A., Plumb,
R.T., Smith, A.J., Taylor, M.S., Foster, G.N., Holmes, S.J., Masterman, A.J., Tones, S.J., Knight, J.D., Oakley, J.N.,
Barker, I., & Walters, K.F.A., 1994. Monitoring and forecasting for BYDV
control - the way forward? Aspects Applied Biology. 37:197-206.
Irwin, M. & Thresh, J. M., 1990.
Epidemiology of barley yellow dwarf: A study in ecological complexity. Annual
Review Phytopathology 28:393-424.
Knaust, H.J., 1996.Untersuchungen zur sekundaren ausbreitung von getreideblattlausen und deren
bedeutung fur die epidemiologie des BYD-virus. Hannover Univ. Ph. D. Diss. Cuvilier Verlag,
Mann, J.A., Tatchell, G.M., Dupuch, M.J.,
Harrington, R.,
Mann, J.A.,
Harrington, R., Morgan, D., Walters, K.F.A., Barker,
Plumb, R.T., 1983. Barley yellow dwarf virus - a global problem. In Plant Virus Epidemiology. ed. R.T. Plumb, J.M Thresh, pp. 185-98.
SAS Institute. 1995. SAS procedure
guide for personal computers Ver. 6, ed. SAS
Institute,
Sopp, P.I.,
Tamaki, G., Halfhill, J.M. & Hathaway, D.O.,
1970. Dispersal and
Reduction of Colonies of Pea Aphids by Aphidius smithi
(Hymenoptera: Aphidiidae). Annals Entomological
Society
Tottman, D.R. & Broad,
H., 1987. Decimal
code for the growth stages of cereals. Annals Applied Biology
110:683-687.
Acknowledgements:
We thank all colleagues in the
Rothamsted Insect Survey who braved the foul weather
conditions while they lay prostrate counting aphids. IACR receives grant-aided
support from the Biotechnology and Biological Sciences Research Council of the
Table
1. Mean ± SE
percent plants infested with S. avenae or R.
padi from
plots planted with wheat or
barley, and subjected to various levels of predators and/or parasitoids in the
first field experiment.
|
Crop |
Barley |
Wheat | ||
|
Aphid |
R. padi. |
S. avenae |
R. padi |
S. avenae |
|
Treatment* |
|
|
|
|
|
None |
35.0 ±12.0 |
51.0 ±12.0 |
31.6 ± 10 |
44.0 ± 9.0 |
|
Predator |
17.0 ± 0.0 |
60.0 ±16.0 |
12.5 ± 3.0 |
16.0 ± 9.0 |
|
Parasitoid |
38.0 ± 16.0 |
56.0 ± 17.0 |
33.0 ± 17.0 |
57.0 ± 14.0 |
|
Both |
25.0 ± 5.0 |
73.0 ± 2.0 |
6 .4 ± 5.0 |
39.0 ± 9.0 |
|
Aphid Sp. |
30.3 ± 6.0 |
59.3 ± 6.5 |
18.6 ± 5.0 |
39.6 ± 6.3 |
|
Crop |
45.5 ± 5.4 |
30.1 ± 4.6 | ||
|
Experiment |
37.6 ± 3.7 | |||
*None =
no predator or parasitoid, Predator = one predator,
Parasitoid = one
parasitoid, Both = one predator plus one
parasitoid.
Table
2. Mean ± SE
percent plans infested with S. avenae or R.
padi from
plots planted with wheat or
barley, and subjected to various levels of predators and/or parasitoids in the
second field experiment.
|
Crop |
Barley |
Wheat | ||
|
Aphid |
R. padi. |
S. avenae |
R. padi |
S. avenae |
|
Treatment* |
|
|
|
|
|
None |
39.8 ± 11.8 |
34.2 ± 4.4 |
38.4 ± 8.2 |
18.3 ± 2.5 |
|
Predator |
48.6 ± 6.4 |
31.0 ± 8.0 |
9.1 ± 6.9 |
2.8 ±1.3 |
|
Parasitoid |
36.0 ± 4.2 |
31.3 ± 6.3 |
38.1 ± 10.6 |
22.5 ± 4.5 |
|
Both |
35.8 ± 16.7 |
25.5 ± 3.9 |
17.3 ± 9.1 |
15.6 ± 4.2 |
|
Aphid Sp. |
40.1 ± 4.9 |
30.5 ± 2.7 |
25.7 ± 5.4 |
14.5 ± 2.8 |
|
Crop |
35.1 ± 2.9 |
20.3 ± 3.3 | ||
|
Experiment |
27.9 ± 2.4 | |||
*None =
no predator or parasitoid, Predator = one predator,
Parasitoid = one
parasitoid, Both = one predator plus one
parasitoid.
Table
3. Mean ± SE
percent plants infested with S. avenae or R.
padi from
plots planted with wheat or
barley, and subjected to various levels of predators and/or parasitoids in the
controlled environment experiment.
|
Crop |
Barley |
Wheat | ||
|
Aphid |
R. padi. |
S. avenae |
R. padi |
S. avenae |
|
Treatment* |
|
|
|
|
|
None |
40.0 ± 4.6 |
37.3 ± 2.7 |
28.0 ± 8.3 |
30.7 ± 10.9 |
|
Predator |
47.0 ± 4.4 |
40.5 ± 3.8 |
46.7 ± 4.8 |
36.0 ± 10.1 |
|
Parasitoid |
48.0 ± 6.1 |
51.9 ± 11.6 |
39.7 ± 13.9 |
61.3 ± 1.3 |
|
Both |
28.7 ± 13.4 |
44.0 ± 10.0 |
17.8 ± 3.4 |
4.8 ± 8.4 |
|
Aphid Sp. |
41.0 ± 4.1 |
43.4 ± 3.8 |
33.0 ± 5.9 |
43.2 ± 5.1 |
|
Crop |
42.2 ± 2.7 |
38.1 ± 3.6 | ||
|
Experiment |
40.1 ± 2.5 | |||
*None =
no predator or parasitoid, Predator = one predator,
Parasitoid = one
parasitoid, Both = one predator plus one parasitoid
.