Adaptation of indigenous
parasitoids to the invasive tomato
pest Tuta absoluta in Italy: biology
and behaviour of the braconid
wasp Bracon nigricans
L. Zappalà, A. Biondi, G. Siscaro, G. Tropea
Garzia, K. van Achterberg, N. Desneux
EPPO/IOBC/FAO/NEPPO Joint International Symposium
on management of Tuta absoluta
Agadir, Morocco, 2011/11/16-18
Establishment of exotic species
• Related to their higher competitiveness compared to
native species as well as to the reduced control by the
natural enemies
• The knowledge of the natural limiting factors is a crucial
point in the implementation of any pest management
strategy
Aims
• Define the parasitoid complex of T. absoluta in
newly invaded areas
• Identify potential biocontrol agents
– Biological and behavioural traits of Bracon nigricans
(Szépligeti) on T. absoluta
Materials and methods - survey
• From August 2009 to present
– Collection of infested material
• Protected and open field crops
– Tomato, eggplant
• Wild plants
– Datura, Solanum…
– Use of sentinel plants
Materials and methods
Sampling sites
» 6 sites with different
ecological features:
•
•
•
•
•
Urban vegetable crops
Greenhouses
Wild flora
Fruit and ornamental trees
Mediterranean flora
Results - survey
• 14 species were collected (Zappalà et al., submitted)
– Diadegma pulchripes (Kokujev) (Hym.: Ichneumonidae)
– Bracon osculator Nees
(Hym.: Braconidae)
– Bracon nigricans (Szépligeti)
Results - survey
–
–
–
–
Neochrysocharis formosa (Westwood)
Necremnus artynes (Walker)
Pnigalio cristatus (Ratzeburg)
one sp. of the P. soemius (Walker) group
(Hym.: Eulophidae)
Reared parasitoids
• Diadegma pulchripes
– larvo-pupal endoparasitoid
• Necremnus artynes
– larval ectoparasitoid
• Bracon nigricans
– larval ectoparasitoid
Bracon nigricans
• Reported on
– Lepidoptera
•
•
•
•
•
•
•
Cnephasia sedana (Constant)
Etiella zinckenella (Treitschke)
Loxostege sticticalis (L.)
Pexicopia malvella Hübner
Phthorimaea operculella (Zeller)
Ephestia terebrellum Zeller
Cydia strobilella (L.)
– Coleoptera
• Ernobius nigrinus Sturm
• distribution
– W-Palaearctic
Materials and methods – B. nigricans
• Laboratory trials to determine
– Host stage preference
• Choice test
– Longevity
– Fecundity and fertility
– Biocontrol activity
• % parasitized hosts
• % paralyzed hosts
• At different host densities
– 10, 20 and 40 L3-L4
• Under different food regimes
– With or without additional sugaryproteinic nutrient
Materials and methods – B. nigricans
• Life tables @ constant temperature
– Age-specific values
• Survival
• Viability
– Fertility
– Fecundity
– Biocontrol activity
– Gregariousness level (1/2/3 eggs of a single clutch)
• Development time
• Survival
Results – Life tables – Daily biocontrol activity
•
•
•
100
90
80
Adult life span of females [d] 41.1 ± 3.8
Duration of the killing period [d] 37.6 ± 3.2
Duration of oviposition period [d] 36.6 ± 3.2
paralyzed
parasitized
70
% host larvae
killed
60
50
40
30
20
10
0
2
4
6
8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 54 56 58 60 62
Age ( Days)
Results – Life tables – Daily fecundity/fertility
• Mean n. (±SE) of laid eggs/female/day: 1.5±0.14; 0-8 (min-max)
• Mean n. (±SE) of offspring/female/day: 0.97±0.09; 0-5 (min-max)
4.0
3.5
Fecundity
Fertility
3.0
2.5
2.0
1.5
1.0
0.5
0.0
1
3
5
7
9
11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 57 59 61
Age (days)
Results - Host stage
2.5
n. eggs/instar (mean ± SE)
preference
d
2.0
1.5
c
1.0
0.5
b
a
a
Eggs
L1
a
0.0
% parassitism (mean ± SE)
100
90
80
70
60
50
40
30
20
10
0
L2
L3
L4
Pupae
c
b
a
a
Eggs
L1
a
L2
a
L3
L4
Pupae
One-way ANOVA, Tukey’s
test (P=0.05)
Results – Longevity
• Nutrient effects
45
A
With nutrient
40
Without nutrient
Days (mean ± SE)
35
30
25
20
B
15
a
b
10
5
0
Females
Males
t-test (P=0.05)
Results – Fecundity
• Nutrient effects
8
With nutrient
Without nutrient
7
Laid eggs/day/f emale
6
5
4
3
2
1
0
3
6
9
12
15
18
21
24
27
30
33
36
Age (days)
39
42
45
48
51
54
57
60
63
Results – Fecundity
• Nutrient effects
Total fecundity
180
8
160
7
140
With nutrient
Without nutrient
With nutrient
Without nutrient
120
6
Laid eggs/day/f emale
a
100
5
80
4
60
3
40
2
20
1
0
b
0
3
6
9
12
15
18
21
24
27
30
33
36
Age (days)
39
42
45
48
51
54
57
60
63
Results – Fertility
• Nutrient effects
8
With nutrient
7
Without nutrient
Of f spring/day/female
6
5
4
3
2
1
0
3
6
9
12
15
18
21
24
27
30
33
36
Age (days)
39
42
45
48
51
54
57
60
63
Results – Fertility
• Nutrient effects
Total fertility
180
160
8
With nutrient
Without nutrient
140
7
With nutrient
Without nutrient
120
Of f spring/day/female
6
a
100
5
80
4
60
3
40
b
20
2
0
1
0
3
6
9
12
15
18
21
24
27
30
33
36
Age (days)
39
42
45
48
51
54
57
60
63
Results – Longevity
• Host density effects
Results – Fecundity and fertility
• Host density effects
180
Total progeny
10
n.s.
20
160
40
140
120
100
80
60
40
20
0
Fecundity
One-way ANOVA
Tukey’s test (P=0.05)
Fertility
Results – Biocontrol activity
• Nutrient effects
*
140
n. of larvae (mean±SE)
parasitized
paralyzed
120
killed
100
80
60
A
a
**
40
B
b
20
0
t-test (P=0.05)
With nutrient
Without nutrient
Results - Biocontrol activity
n. of larvae (mean±SE)
• Host density effects
350
parasitized
300
paralyzed
250
***
killed
b
**
200
*
150
100
A
A
ab
A
a
50
0
One-way ANOVA
Tukey’s test (P=0.05)
10
20
40
Results – Gregariousness level
• No significant effects
70
– on young instars tot mortality
– cannibalism events positively
correlated with the
gregariousness rate
60
50
40
30
20
50
45
40
35
30
25
20
15
10
5
0
A
10
0
1 Egg
eggs mortality
A
b
b
2 Eggs
larval cannibalism
3 Eggs
larval mortality
pupal mortality
300
A
250
b
200
Hours
Days
– on young instars development
time (270 hrs on average)
– on the progeny adult longevity
150
100
50
1 Egg
2 Eggs
females
males
3 Eggs
0
1 Egg
eggs
2 Eggs
larvae
3 Eggs
pupae
Results – Gregariousness level
• No significant effects
70
– on young instars tot mortality
– cannibalism events positively
correlated with the
gregariousness rate
60
50
40
30
20
50
45
40
35
30
25
20
15
10
5
0
A
10
0
1 Egg
eggs mortality
A
b
b
2 Eggs
larval cannibalism
3 Eggs
larval mortality
pupal mortality
300
A
250
b
200
Hours
Days
– on young instars development
time (270 hrs on average)
– on the progeny adult longevity
150
100
50
1 Egg
2 Eggs
females
males
3 Eggs
0
1 Egg
eggs
2 Eggs
larvae
3 Eggs
pupae
Results – Gregariousness level
• No significant effects
70
– on young instars tot mortality
– cannibalism events positively
correlated with the
gregariousness rate
60
50
40
30
20
50
45
40
35
30
25
20
15
10
5
0
A
10
0
1 Egg
eggs mortality
A
b
b
2 Eggs
larval cannibalism
3 Eggs
larval mortality
pupal mortality
300
A
250
b
200
Hours
Days
– on young instars development
time (270 hrs on average)
– on the progeny adult longevity
150
100
50
1 Egg
2 Eggs
females
males
3 Eggs
0
1 Egg
eggs
2 Eggs
larvae
3 Eggs
pupae
Results – Gregariousness level
• No significant effects
70
– on young instars tot mortality
– cannibalism events positively
correlated with the
gregariousness rate
60
50
40
30
20
50
45
40
35
30
25
20
15
10
5
0
A
10
0
1 Egg
eggs mortality
A
b
b
2 Eggs
larval cannibalism
3 Eggs
larval mortality
pupal mortality
300
A
250
b
200
Hours
Days
– on young instars development
time (270 hrs on average)
– on the progeny adult longevity
150
100
50
1 Egg
2 Eggs
females
males
3 Eggs
0
1 Egg
eggs
2 Eggs
larvae
3 Eggs
pupae
Results – Gregariousness level
• Significant effects
1.2
Emerged adults/host
– on the parasitoid fitness
(emerged adults/host)
c
1.4
b
1.0
0.8
0.6
a
0.4
0.2
0.0
1 Egg
3 Eggs
c
80
Mean n. emerged progeny
– on the parasitoid offspring
– No significant effects on
the progeny sex-ratio
2 Eggs
70
60
b
50
40
40
30
20
10
0
a
26
12
29
17
9
1 Egg
2 Eggs
females
males
3 Eggs
Discussion – Indigenous parasitoids
• Several Eulophid and Ichneumonid wasps got adapted to
the exotic pest
• Very few egg parasitoids
• Presence in all the investigated sites
• No parasitoids inside greenhouses
• Interesting data obtained by means of sentinel plants
• Relatively low total parasitism rate
Discussion - B. nigricans
• Adaptation process
– positive correlation between gregariousness level and
fitness
• Progeny increase and time development decrease
– T. absoluta not suitable as host feeding substrate
– young instars high mortality
Discussion - B. nigricans
• Biocontrol potential
– positive correlation between host density and the wasp
• biocontrol activity
– n. of killed larvae
• fitness
– Increasing progeny
– Increasing male longevity
» More matings  more female progeny
• Importance of alternative food sources availability in the
field for the wasp activity
– Ecological infrastructures
• flowering
• honeydew
• alternative hosts
Discussion - Perspectives
• Searching for other natural enemies
–
–
–
–
Other larval parasitoids
Egg parasitoids
Predators
Pathogens
• Introduction of exotic parasitoids
?
• Improving knowledge on B. nigricans
– Behavioural studies
• Host location capacity
– Intraguild predation and other interactions
– Efficacy in semi-field and field conditions
• Banker plants
– Side effects of pesticides used on tomato crops
Potential demographic effects of
various bioinsecticides on Bracon
nigricans (Hym.: Braconidae a new
parasitoid of Tuta absoluta (Lep.:
Gelechiidae) (Biondi et al., IN THE
POSTER AREA)

Tuta absoluta: the tomato leafminer - OIRED