| |
Aphid Natural Enemy Interactions:
A Laboratory Experiment RESULTS
Specimen data Specimen data are given in Tables 1 and 2.
Table 1. Example of class data set: total aphid mortality
attributed to predator (lacewing larva Chrysoperla carnea),
fungus or parasitoid and the mean percentage mortality of aphids
in
each
treatment
| 1. No natural
enemies |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
0 |
0 |
0 |
10 |
0 |
0.00 |
| 2 |
0 |
0 |
0 |
10 |
0 |
0.00 |
| 3 |
0 |
0 |
0 |
10 |
0 |
0.00 |
| 4 |
0 |
0 |
0 |
10 |
0 |
0.00 |
| 5 |
0 |
0 |
0 |
10 |
0 |
0.00 |
| 6 |
0 |
0 |
0 |
10 |
0 |
0.00 |
| 7 |
0 |
0 |
0 |
10 |
0 |
0.00 |
| 8 |
0 |
0 |
0 |
10 |
0 |
0.00 |
| 9 |
0 |
0 |
0 |
10 |
0 |
0.00 |
| 10 |
0 |
0 |
0 |
10 |
0 |
0.00 |
| |
|
|
|
|
Mean |
0.00 |
| |
|
|
|
|
St. Deviation |
0.00 |
| 2. Fungus |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
0 |
0 |
0 |
10 |
0.00 |
0.00 |
| 2 |
0 |
0 |
0 |
10 |
0.00 |
0.00 |
| 3 |
0 |
5 |
0 |
10 |
0.50 |
50.00 |
| 4 |
0 |
3 |
0 |
10 |
0.30 |
30.00 |
| 5 |
0 |
1 |
0 |
10 |
0.10 |
10.00 |
| 6 |
0 |
5 |
0 |
10 |
0.50 |
50.00 |
| 7 |
0 |
3 |
0 |
10 |
0.30 |
30.00 |
| 8 |
0 |
2 |
0 |
10 |
0.20 |
20.00 |
| 9 |
0 |
1 |
0 |
10 |
0.10 |
10.00 |
| 10 |
0 |
1 |
0 |
10 |
0.10 |
10.00 |
| |
|
|
|
|
Mean |
21.00 |
| |
|
|
|
|
St. Deviation |
18.53 |
| 3. Parasitoid |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
0 |
0 |
0 |
10 |
0.00 |
0.00 |
| 2 |
0 |
0 |
1 |
10 |
0.10 |
10.00 |
| 3 |
0 |
0 |
0 |
10 |
0.00 |
0.00 |
| 4 |
0 |
0 |
0 |
10 |
0.00 |
0.00 |
| 5 |
0 |
0 |
7 |
10 |
0.70 |
70.00 |
| 6 |
0 |
0 |
5 |
10 |
0.50 |
50.00 |
| 7 |
0 |
0 |
0 |
10 |
0.00 |
0.00 |
| 8 |
0 |
0 |
4 |
10 |
0.40 |
40.00 |
| 9 |
0 |
0 |
5 |
10 |
0.50 |
50.00 |
| 10 |
0 |
0 |
0 |
10 |
0.00 |
0.00 |
| |
|
|
|
|
Mean |
22.00 |
| |
|
|
|
|
St. Deviation |
27.41 |
| 4. Lacewing |
| |
Total aphid
mortality attributed to: |
Total number
of aphids in treatment |
Proportion
mortality |
Percentage
mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
3 |
0 |
0 |
10 |
0.30 |
30.00 |
| 2 |
7 |
0 |
0 |
10 |
0.70 |
70.00 |
| 3 |
7 |
0 |
0 |
10 |
0.70 |
70.00 |
| 4 |
10 |
0 |
0 |
10 |
1.00 |
100.00 |
| 5 |
1 |
0 |
0 |
10 |
0.10 |
10.00 |
| 6 |
3 |
0 |
0 |
10 |
0.30 |
30.00 |
| 7 |
0 |
0 |
0 |
10 |
0.00 |
0.00 |
| 8 |
3 |
0 |
0 |
10 |
0.30 |
30.00 |
| 9 |
6 |
0 |
0 |
10 |
0.60 |
60.00 |
| 10 |
6 |
0 |
0 |
10 |
0.60 |
60.00 |
| |
|
|
|
|
Mean |
46.00 |
| |
|
|
|
|
St. Deviation |
30.98 |
| 5. Fungus
and parasitoid |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
0 |
0 |
0 |
10 |
0.00 |
0.00 |
| 2 |
0 |
1 |
0 |
10 |
0.10 |
10.00 |
| 3 |
0 |
0 |
0 |
10 |
0.00 |
0.00 |
| 4 |
0 |
0 |
0 |
10 |
0.00 |
0.00 |
| 5 |
0 |
2 |
3 |
10 |
0.50 |
50.00 |
| 6 |
0 |
1 |
0 |
10 |
0.10 |
10.00 |
| 7 |
0 |
1 |
0 |
10 |
0.10 |
10.00 |
| 8 |
0 |
1 |
2 |
10 |
0.30 |
30.00 |
| 9 |
0 |
1 |
0 |
10 |
0.10 |
10.00 |
| 10 |
0 |
1 |
0 |
10 |
0.10 |
10.00 |
| |
|
|
|
|
Mean |
13.00 |
| |
|
|
|
|
St. Deviation |
15.67 |
| 6. Lacewing
and fungus |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
6 |
0 |
0 |
10 |
0.60 |
60.00 |
| 2 |
4 |
6 |
0 |
10 |
1.00 |
100.00 |
| 3 |
0 |
2 |
0 |
10 |
0.20 |
20.00 |
| 4 |
0 |
0 |
0 |
10 |
0.00 |
0.00 |
| 5 |
2 |
0 |
0 |
10 |
0.20 |
20.00 |
| 6 |
3 |
1 |
0 |
10 |
0.40 |
40.00 |
| 7 |
0 |
3 |
0 |
10 |
0.30 |
30.00 |
| 8 |
4 |
3 |
0 |
10 |
0.70 |
70.00 |
| 9 |
5 |
0 |
0 |
10 |
0.50 |
50.00 |
| 10 |
0 |
1 |
0 |
10 |
0.10 |
10.00 |
| |
|
|
|
|
Mean |
40.00 |
| |
|
|
|
|
St. Deviation |
30.55 |
| 7. Lacewing
and parasitoid |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
0 |
0 |
10 |
10 |
1.00 |
100.00 |
| 2 |
4 |
0 |
1 |
10 |
0.50 |
50.00 |
| 3 |
5 |
0 |
0 |
10 |
0.50 |
50.00 |
| 4 |
2 |
0 |
1 |
10 |
0.30 |
30.00 |
| 5 |
5 |
0 |
0 |
10 |
0.50 |
50.00 |
| 6 |
1 |
0 |
2 |
10 |
0.30 |
30.00 |
| 7 |
7 |
0 |
1 |
10 |
0.80 |
80.00 |
| 8 |
2 |
0 |
2 |
10 |
0.40 |
40.00 |
| 9 |
5 |
0 |
0 |
10 |
0.50 |
50.00 |
| 10 |
0 |
0 |
1 |
10 |
0.10 |
10.00 |
| |
|
|
|
|
Mean |
49.00 |
| |
|
|
|
|
St. Deviation |
25.58 |
| 8. Lacewing,
fungus and parasitoid |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
0 |
0 |
10 |
10 |
1.00 |
100.00 |
| 2 |
1 |
5 |
1 |
10 |
0.70 |
70.00 |
| 3 |
0 |
0 |
0 |
10 |
0.00 |
0.00 |
| 4 |
0 |
4 |
1 |
10 |
0.50 |
50.00 |
| 5 |
2 |
0 |
0 |
10 |
0.20 |
20.00 |
| 6 |
0 |
0 |
0 |
10 |
0.00 |
0.00 |
| 7 |
8 |
1 |
0 |
10 |
0.90 |
90.00 |
| 8 |
1 |
0 |
1 |
10 |
0.20 |
20.00 |
| 9 |
3 |
0 |
0 |
10 |
0.30 |
30.00 |
| 10 |
0 |
7 |
0 |
10 |
0.70 |
70.00 |
| |
|
|
|
|
Mean |
45.00 |
| |
|
|
|
|
St. Deviation |
36.29 |
| |
|
|
|
|
|
|
Table 2. Example of class data set: total
aphid mortality attributed to predator (ladybird adult Adalia
bipunctata), fungus or parasitoid and the mean percentage
mortality of aphids in each treatment
| 1. No natural
enemies |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
0 |
0 |
0 |
10 |
0 |
0.00 |
| 2 |
0 |
0 |
0 |
10 |
0 |
0.00 |
| 3 |
0 |
0 |
0 |
10 |
0 |
0.00 |
| |
|
|
|
|
Mean |
0.00 |
| |
|
|
|
|
St. Deviation |
0.00 |
| 2. Fungus |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
0 |
1 |
0 |
10 |
0.10 |
10.00 |
| 2 |
0 |
5 |
0 |
10 |
0.50 |
50.00 |
| 3 |
0 |
3 |
0 |
10 |
0.30 |
30.00 |
| |
|
|
|
|
Mean |
30.00 |
| |
|
|
|
|
St. Deviation |
20.00 |
| 3. Parasitoid |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
0 |
0 |
0 |
10 |
0.00 |
00.00 |
| 2 |
0 |
0 |
1 |
10 |
0.10 |
10.00 |
| 3 |
0 |
0 |
2 |
10 |
0.20 |
20.00 |
| |
|
|
|
|
Mean |
10.00 |
| |
|
|
|
|
St. Deviation |
10.00 |
| 4. Ladybird |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
1 |
0 |
0 |
10 |
0.10 |
10.00 |
| 2 |
3 |
0 |
0 |
10 |
0.30 |
30.00 |
| 3 |
3 |
0 |
0 |
10 |
0.30 |
30.00 |
| |
|
|
|
|
Mean |
23.33 |
| |
|
|
|
|
St. Deviation |
11.55 |
| 5. Fungus
and parasitoid |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
0 |
5 |
0 |
10 |
0.50 |
50.00 |
| 2 |
0 |
3 |
0 |
10 |
0.30 |
30.00 |
| 3 |
0 |
5 |
0 |
10 |
0.50 |
50.00 |
| |
|
|
|
|
Mean |
43.33 |
| |
|
|
|
|
St. Deviation |
11.55 |
| 6. Ladybird
and fungus |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
5 |
2 |
0 |
10 |
0.70 |
70.00 |
| 2 |
3 |
3 |
0 |
10 |
0.60 |
60.00 |
| 3 |
3 |
1 |
0 |
10 |
0.40 |
40.00 |
| |
|
|
|
|
Mean |
56.67 |
| |
|
|
|
|
St. Deviation |
15.28 |
| 7. Ladybird
and parasitoid |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
6 |
0 |
0 |
10 |
0.60 |
60.00 |
| 2 |
5 |
0 |
2 |
10 |
0.50 |
50.00 |
| 3 |
4 |
0 |
3 |
10 |
0.40 |
40.00 |
| |
|
|
|
|
Mean |
66.67 |
| |
|
|
|
|
St. Deviation |
5.77 |
| 8. Ladybird,
fungus and parasitoid |
| |
Total aphid
mortality attributed to: |
Total number of aphids
in treatment |
Proportion mortality
|
Percentage mortality |
| Group |
Predator |
Fungus |
Parasitoid |
| 1 |
5 |
4 |
1 |
10 |
1.00 |
100.00 |
| 2 |
4 |
3 |
0 |
10 |
0.70 |
70.00 |
| 3 |
6 |
4 |
0 |
10 |
1.00 |
100.00 |
| |
|
|
|
|
Mean |
90.00 |
| |
|
|
|
|
St. Deviation |
17.32 |
| |
|
|
|
|
|
|
Data analysis Examples of data analysis are shown in Figures 1 and 2 and
Tables 3 and 4. Figure 1. Mean percentage mortality of
aphids in treatments with different natural enemy combinations
(Predator = lacewing, parasitoid and entomopathogenic fungus)
Error bars indicate standard error of overall
mean mortality (n=10) 
Figure 2. Mean percentage mortality of
aphids in treatments with different natural enemy combinations
(Predator = ladybird, parasitoid and entomopathogenic fungus)
Error bars indicate standard error of overall
mean mortality (n=3) 
Table 3. SPSS output (non-parametric one-way ANOVA)
for sample data set in Table 1 (Predator = lacewing larva Chrysoperla
carnea)
The treatment No natural enemies
is excluded from the analysis because of the zero mean.
Kruskall Wallis Test
Table 4. SPSS output (non-parametric one-way
ANOVA) for sample data set in Table 2 (Predator = ladybird adult
Adalia bipunctata)
The treatment No natural enemies
is excluded from the analysis because of the zero mean.
Kruskall Wallis Test
DATA INTERPRETATION Is
there higher mortality (synergism) in the treatments with multiple
natural enemies?
- Previous research (Roy et al.,
1998) has shown that the mortality attributed to entomopathogenic
fungi can be enhanced in the presence of foraging natural enemies.
This could be because of increased movement of the host aphid
in response to the predator or parasitoid. Alternatively, the
predator or parasitoid may passively vector the fungus.
- From the specimen data
(Tables 1 and 2) provided it is apparent that overall aphid mortality
varies
with different natural enemies and, as with class data, the
results are quite variable and not always consistent. Despite
this, some
general trends are apparent.
- When aphids are exposed to a ladybird
adult in combination with a parasitoid and entomopathogenic
fungus the aphid mortality is greater than that attributed
to the single
natural enemies (synergistic effect).
- However, when lacewing
larvae are used as the predator in the system the effect
of the multiple
natural enemies is not synergistic. The differences in
foraging behaviour of lacewing larvae and ladybird adults may account
for
this. Students could be encourage to assess these differences
both by searching the literature or design of experiments.
(Do ladybird adults search more extensively than lacewing
larvae?
Do aphids exhibit a greater alarm response in the presence
of
ladybird adults compared to lacewing larvae?)
Are any of the natural enemy combinations antagonistic?
- Overall parasitism may be decreased when both the parasitoid and entomopathogenic fungus are present because
of competition for host resources.
DISCUSSION
Success in achieving learning objectives
- Students rapidly gain the necessary skills for handling
and sexing insects.
- The data set can be analysed at various
levels of complexity (summary statistics or more
complex analysis)
- Potential interactions between natural enemies are demonstrated
- Students can access published literature to discuss the data
either from an applied aspect (biological control) or more theoretically
(predator prey interactions, intraguild predation)
- Students gain practice in handling insects
(including sexing parasitoids)
Other potential applications
- The practical could be scaled down to assess just two natural
enemies.
- Specimen data for two predators (Chrysoperla carnea larvae
and Adalia bipunctata adults) are given here, but
other natural enemies could be used (e.g. adults or larvae
of the ladybird Coccinella
septempunctata, larvae of the hoverfly Episyrphus balteatus).
Possible further developments
- Experiments could be designed to look at the interactions
between natural enemies and their prey from a behavioural perspective,
- do predators avoid parasitised aphids?
- how does parasitism affect aphid behaviour?
BIBLIOGRAPHY
Ferguson, K.I. & Stiling, P. (1996) Non-additive effects
of multiple natural enemies on aphid populations. Oecologia,
108, 375-379
Polis, G.A. & Holt, R.D. (1992) Intra-guild predation: the
dynamics of complex trophic interactions. Trends Ecology and
Evolution, 7, 151-154
Rosenheim, J.A. (1995) Intra-guild predation among biological-control
agents: theory and evidence. Biological Control,
5, 303-335
Roy, H.E., Pell, J.K., S.J.Clark & P.G.Alderson (1998) Implications
of predator foraging on aphid pathogen dynamics. Journal of
Invertebrate Pathology, 71, 236-247
Roy, H.E., Pell, J.K., S.J.Clark & P.G.Alderson (1999) Effects
of fungal infection on the alarm response of pea aphids. Journal
of Invertebrate Pathology, 74, 69-75
Roy, H. E., Pell, J. K.,& Alderson, P. G. (2001) Targeted
dispersal of the aphid pathogenic fungus Erynia neoaphidis
by the aphid predator Coccinella septempunctata. Biocontrol
Science and Technology, 11, 101-112
Roy, H. E., Pell, J. K. & Alderson, P.G. (2003) Effect of
Erynia neoaphidis infection and coccinellid foraging on
the spatial distribution of aphids on plants. Journal
of Invertebrate Pathology, 81, 127-129
|
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