Conservation Biological Control:
Can it Work in the Cotton System?
Dr. Steven E. Naranjo, USDA-ARS
Conservation Biological Control
“ Manipulation of the environment to favor
natural enemies, either by removing or
mitigating adverse factors or by providing
lacking requisites.”
DeBach 1974
Biological Control - Approaches
*Conservation*
Classical
Augmentation
Conservation Biological Control
After
Rabb, Stinner
& van den Bosch
1976
Approaches
Reduce Direct Mortality
Provide Resources
•Selective insecticides
•Ecological
•Physiological
•Cultural practices
•Refugia
•Cover & inter-crops
•Landscape pattern
•Strip harvesting
Integration
Controlling
Secondary Enemies
•Hyperparasitism
•Intraguild predation
Manipulating
Host-Plant Attributes
•Plant breeding
•Transgenics
•Cultural practices
Conservation Biological Control
Components
Survey & Identification
of Potentially Important
Natural Enemies
Study of Biology & Ecology;
Determination of Factors
Constraining or Enhancing
Biological Control
Implementation &
Evaluation
Progress
Survey
Is there potential for natural
biological control?
control
Natural Enemy Complex -Western U.S.
Parasitoids
Predators
30+ species
50+ species
Hyposter
Copidosoma
Microplitis
Lysiphlebus
Chelonus
Eretmocerus
Encarsia
Anaphes
Leiophron
Geocoris
Orius
Nabis
Zelus
Collops
Hippodamia
Drapetis
Chrysoperla
Misumenops
Pathogens
Various viruses, bacteria & fungi
Natural Enemies – Pectinophora gossypiella
Arizona/California
Predators
≈23 species described
9 species (immunological ID)
Parasitoids
4 native species described (rare)
16 exotic species introduced
(0 established)
Pathogens
3+ Viruses and bacteria
Natural Enemies – Bemisia tabaci
Worldwide
™
™
114+ Predators
(various methods)
50+ Parasitoids
Arizona Cotton
™
™
™
20 Predators
(immunological ID)
3 Native parasitoids
Many exotic
parasitoids introduced
™
™
11+ Fungi
™
2 established
2 Fungi?
Natural Enemies – Lygus hesperus
Arizona/California
Predators
10+ species described
5 species (immunological ID)
Parasitoids
3 native species described
2 exotic species introduced
(both established in CA)
Pathogens
2+ Fungi
Qualitative Gut Analyses
Whitefly
Pink bollworm
Hippodamia convergens
Collops vittatus
Zelus renardii
Sinea confusa
Orius tristicolor
Nabis alternatus
Lygus hesperus
Geocoris spp.
0.6 0.5 0.4 0.3 0.2 0.1 0.0
Frequency
0.0 0.1 0.2 0.3 0.4 0.5 0.6
Frequency
Hagler & Naranjo 1994a,b; Naranjo & Hagler 1997
Natural Mortality of Bemisia
(Arizona Cotton)
Total Mortality
1.0
Inviability
(8.8%)
Physiological
& Unknown
(21.5%)
Dislodgement
(29.2%)
0.9
0.8
0.7
N = 14
Parasitism
(7.1%)
Predation
(33.4%)
Naranjo & Ellsworth (in prep)
Biological Control Potential?
(Sudan Cotton, Abdelrahman & Munir 1989)
20
Adult whiteflies per leaf
16
12
Nidiana
1986/87
Insecticide
Untreated
8
4
0
20
Nidiana 1987/88
15
10
5
0
7 Oct
16 Nov
26 Dec
4 Feb
16 March
Biological Control Potential?
(some more examples)
„
Elveens et al. 1973. Secondary outbreak induction of beet
armyworms by experimental insecticide application in cotton in
California. Environ. Entomol. 2:497
„
Ehler et al. 1973. An evaluation of some natural enemies of
cabbage looper on cotton in California. Environ. Entomol. 2: 1009
„
Stoltz & Stern. 1978. Cotton arthropod food chain disruption by
pesticides in the San Joaquin Valley, California. Environ. Entomol.
7: 703 (Thrips, beet armyworm, cabbage looper)
„
Trichilo & Wilson. 1993. An ecosystem analysis of spider mite
outbreak: physiological stimulations or natural enemy disruption.
Exp. Appl. Acarol. 17: 291
Reducing Constraints
Controlling Secondary Enemies
• Hyperparasitism
• Intraguild predation
Encarsia parasitizing
Eretmocerus in Bemisia
Sorting out the Players
Clubionids
Coccinellids
Sinea spp.
Zelus spp.
Salticids
Chrysoperla spp.
Collops spp.
Thomisids
Nabis spp.
Geocoris spp.
Lygus hesperus
Encarsia spp.
Orius tristicolor
Bemisia
Gossypium hirsutum
Eretmocerus spp.
VS.
Displaced mycetome stage
Early 4th stage
Preference (parasitized)
1.0
P<0.0001
0.8
P<0.0001
P<0.0001
0.6
0.4
0.2
0.0
Geocoris
Orius
Hippodamia
Naranjo (in prep)
VS.
Pupal stage
Preference (parasitized)
1.0
Early 4th stage
P<0.0001
P<0.0001
0.8
P<0.0007
0.6
0.4
0.2
0.0
Geocoris
Orius
Hippodamia
Naranjo (in prep)
Visual Predators?
• Late 4th Stage WF (“pupa”)
• Displaced mycetomes stage
• Parasitoid pupa
• Early 4th Stage WF
VS.
Displaced mycetome stage
Late 4th stage (“pupa”)
Preference (parasitized)
1.0
P<0.005
0.8
0.6
P<0.945
P<0.837
Geocoris
Orius
0.4
0.2
0.0
Hippodamia
Naranjo (in prep)
Reducing Constraints
Can insecticides be managed to
promote biological control?
Compatibility?
Conventional Insecticides (by Threshold)
250
Cumulative Insect-days (25 sweeps)
200
Maricopa, AZ 1994
Control
20/leaf
150
10/leaf
5/leaf
100
2.5/leaf
50
0
800
Brawley, CA 1995
600
400
200
0
Naranjo et al. 2002. J. Econ. Entomol
Proportional reduction
Conventional Insecticides (by Threshold)
0.8
0.8
0.6
0.6
0.4
0.4
0.2
0.2
0.0
0.0
12
800
900 1000 1100 1200 1300 1400
1st spray (degree-days after planting)
0
2
4
6
8
10
Number of sprays
Naranjo et al. 2002. J. Econ. Entomol.
Insecticide Use Patterns
Arizona Cotton
Bt cotton
Insect growth regulators
Mean applications per acre
14
14
Pink bollworm
Whitefly
Lygus
Other
12
10
12
10
8
8
6
6
4
4
2
2
0
Ellsworth & Jones 2000
0
199
1
199
2
199
3
199
4
199
5
199
6
199
7
199
8
199
9
199
0
200
0
Selective Insecticides?
• Bt Transgenic Cotton
• Applaud (Chitin Inhibitor)
• Knack (Juvenoid)
Science or Emotion?
• Resistance management
• Food safety
• Non-target effects
Non-Target Effects
¾
Natural enemy abundance
¾
Natural enemy diversity
¾
Natural enemy function
Natural Enemy Abundance
1999
2000
2001
Hymenoptera
0.76
0.53
0.47
Drapetis sp.
0.19
0.95
0.34
Chrysoperla carnea
0.21
0.28
0.71
Pseudatomoscelis seriatus
0.11
0.25
0.33
Lygus hesperus
0.20
0.42
0.81
Nabis alternatus
0.14
0.69
0.40
Zelus renardii
0.22
0.11
0.12
Orius tristicolor
0.45
0.54
0.49
Goecoris pallens
0.42
0.12
0.73
Geocoris punctipes
0.25
0.72
0.86
Hippodamia convergens
0.16
0.57
0.56
Collops vittatus
0.39
0.13
0.75
Misumenops celer
0.63
0.92
0.59
Lepidoptera
0.04
0.01
0.01
Naranjo 2002, in prep
Principal Response Curves Analysis
z
z
z
Time-dependent multivariate analysis
Derived from redundancy analysis
(constrained form of principal
component analysis)
Provides a simple means of
visualizing and testing the overall
response of a biological community to
an environmental disturbance
Hymenoptera
Coccinellidae
L. hesperus
1999
0.4
P. seriatus
C. carnea
S. albofasc.
O. tristicolor
Canonical coefficient
0.2
M. celer
Non-Bt
N. alternatus
Drapetis sp.
0.0
Araneida
Z. renardii
Thomisidae
-0.2
P = 0.13
Thanatus sp.
Bt cotton
Anthicus spp.
G. pallens
G. punctipes
-0.4
Metaphid. spp.
H. convergens
C. vittatus
-0.6
-0.8
Naranjo (in prep)
Habronatus spp.
exp(cdtbk)
9 Jun
Jul
8 Aug
1.34 x19 control
29 Jun
O. abdominalis
Salticidae
Scymnus sp.
28 Aug
17 Sep
Formicidae
S. confusa
Trachelus sp.
R. forticornis
N. calcaratus
D. reticulata
3.18
2.04
1.79
1.43
1.3
1.29
1.12
1.1
1.04
0.91
0.88
0.8
0.57
0.56
0.54
0.5
0.41
0.32
0.24
0.19
0.08
0.06
0.04
-0.02
-0.05
-0.07
-0.09
-0.23
-0.24
-0.79
Species weight
Selectivity of Bt cotton
C. carnea
O. tristicolor
C. vittatus
2000
0.4
H. convergens
Hymenoptera
D. reticulata
N. alternatus
Canonical coefficient
0.2
M. celer
Non-Bt
0.0
Drapetis sp.
G. punctipes
S. albofasc.
L. hesperus
P = 0.52
-0.2
Thanatus sp.
Habronatus spp.
S. confusa
Bt cotton
Formicidae
R. forticornis
-0.4
Metaph. spp.
Scymnus sp.
Coccinellidae
-0.6
Labridura spp.
P. seriatus
Thomisidae
-0.8
Naranjo (in prep)
Salticidae
9 Jun
29 Jun
19 Jul
8 Aug
28 Aug
17 Sep
O. abdominalis
Z. renardii
Anthicus spp.
G. pallens
N. calcaratus
Araneida
2.62
2.57
2.12
1.45
1.37
1.28
1.2
1.08
0.93
0.64
0.55
0.48
0.26
0.16
0.13
0.12
0.08
0.06
0
-0.01
-0.08
-0.15
-0.17
-0.24
-0.33
-0.53
-0.54
-0.57
-0.58
-1.12
Species weight
Selectivity of Bt cotton
Drapetis sp.
M. celer
0.4
Bt cotton
Hymenop
2001
C. carnea
O. tristicolor
L. hesperus
Canonical coefficient
0.2
Anthicus spp.
H. convergens
Non-Bt
P. seriatus
S. albofacs.
0.0
D. reticulata
Nysius sp.
-0.2
N. calcaratus
P = 0.005
Scymnus sp.
G. punctipes
Bt cotton spray
-0.4
G. pallens
Habronatus sp
Z. renardii
Non-Bt spray
Coccinellidae
-0.6
R. forticornis
Araneida
Labridura
-0.8
Naranjo (in prep)
Salticidae
9 Jun
29 Jun
19 Jul
8 Aug
28 Aug
17 Sep
Thomisidae
Metaph. spp.
N. alternatus
Thanatus sp.
Formicidae
C. vittatus
3.92
1.37
1.36
1.33
1.32
1.24
1.15
1.14
0.93
0.65
0.5
0.47
0.35
0.25
0.24
0.18
0.17
0.14
0.1
0.05
0.03
0.02
0.01
0
-0.01
-0.05
-0.07
-0.16
-0.2
Species weight
Selectivity of Bt cotton
G. punctipes
G. pallens
L. hesperus
2002
0.4
N. alternatus
P. seriatus
C. vittatus
Canonical coefficient
0.2
M. celer
D. reticulata
Non-Bt
C. carnea
Coccinellidae
0.0
H. convergens
Hymenop
Bt cotton
-0.2
Z. renardii
Salticidae
Anthicus spp.
P = 0.008
Scymnus sp.
-0.4
Bt-spray
N. calcaratus
Formicidae
Non Bt-spray
-0.6
S. albofacs.
Metaph. spp.
Habronatus sp
Thomisidae
-0.8
Naranjo (in prep)
Nysius sp.
9 Jun
29 Jun
19 Jul
8 Aug
28 Aug
17 Sep
Araneida
Thanatus sp.
O. abdominalis
R. forticornis
O. tristicolor
Drapetis sp.
3.48
2.3
2.26
1.81
1.41
0.57
0.54
0.5
0.29
0.24
0.21
0.17
0.13
0.11
0.07
0.06
0.05
0.04
0.03
0.02
0.01
8e-3
2e-3
0
-2e-3
-0.02
-0.04
-0.13
-0.35
Species weight
Selectivity of Bt cotton
G. punctipes
Araneida
N. alternatus
2003
0.4
Z. renardii
M. celer
O. tristicolor
Canonical coefficient
0.2
L. hesperus
Bt/RR
Thanatus sp.
C. carnea
Drapetis sp.
0.0
Habronatus sp
Non-Bt/RR
Salticidae
RR
P = 0.21
-0.2
Bt
Coccinellidae
Formicidae
R. forticornis
Sinea spp.
-0.4
P. seriatus
Metaph. spp.
Nysius sp.
-0.6
H. convergens
Scymnus sp.
S. albofacs.
-0.8
Naranjo (in prep)
Thomisidae
9 Jun
29 Jun
19 Jul
8 Aug
28 Aug
D. reticulata
N. calcaratus
C. vittatus
Hymenop
Anthicus spp.
G. pallens
2.5
1.88
1.72
1.37
1.28
0.73
0.56
0.51
0.46
0.41
0.3
0.27
0.23
0.13
0.1
0.08
-0.07
-0.19
-0.35
-0.41
-0.43
-0.49
-0.63
-0.75
-0.97
-1.05
-1.39
-1.4
-1.83
Species weight
Selectivity of Bt/RR cotton
Natural Enemy Function
Predation on Pink Bollworm Eggs
2001
Proportion eaten
0.6
2002
Bt
Non-Bt
2003
0.6
0.5
0.5
0.4
0.4
0.3
0.3
0.2
0.2
0.1
0.1
0.0
0.0
Naranjo 2002, in prep
Natural Enemy Function
Predation on Pink Bollworm Pupae
0.8
2002
2003
0.8
Proportion eaten
Bt
Non-Bt
Naranjo (in prep)
0.6
0.6
0.4
0.4
0.2
0.2
0.0
0.0
Natural Enemy Function
Mortality of Whitefly Nymphs
2001
Marginal rate of mortality
0.8
2002
2003
0.8
Bt
Non-Bt
0.6
0.6
0.4
0.4
0.2
0.2
0.0
0.0
Predation
Naranjo 2002, in prep
Parasitism
Predation
Parasitism
Predation
Parasitism
Selective Insecticides?
• Bt Transgenic Cotton
• Applaud (Chitin Inhibitor)
• Knack (Juvenoid)
Selectivity of IGRs
1997
0.2
B
P
C
P
C
C
C
C
B
C
C
C
C
Control
0.0
-0.1
-0.2
P = 0.002
-0.3
-0.4
Bup
-0.5
Pyr
-0.6
Conven
-0.7
-0.8
29 Jul
5 Aug
12 Aug
19 Aug
26 Aug
3.027
2.019
1.296
1.23
0.963
0.962
0.775
0.625
0.597
0.459
0.247
0.171
0.165
0.138
0.108
0.104
0.034
0.024
-0.01
-0.011
Species weight
Canonical coefficient
0.1
L. hesperus
O. tristicolor
G. punctipes
C. carnea s.l.
P. seriatus
D. nr. divergens
M. celer
Z. renardii
Other Araneida
N. alternatus
S. albofasciatus
Sinea spp.
C. vittatus
Salticidae
H. convergens
D. reticulata
G. pallens
Other Coccinellidae
R. forticornis
Anthicidae
2 Sep
Naranjo et al. 2003 Biological Control (in press)
Selectivity of IGRs
1999
0.2
C
C
Control
0.0
-0.1
Pyr
-0.2
-0.3
P = 0.002
Bup
-0.4
-0.5
-0.6
Conven
-0.7
-0.8
5 Aug
12 Aug
19 Aug
26 Aug
M. celer
G. punctipes
L. hesperus
O. tristicolor
D. nr. divergens
C. carnea s.l.
Other Coccinellidae
Other Araneida
C. vittatus
R. forticornis
D. reticulata
P. seriatus
N. alternatus
Salticidae
Z. renardii
Sinea sspp.
G. pallens
H. convergens
S. albofasciatus
Anthicidae
2.037
1.975
1.932
1.715
1.635
1.394
0.957
0.624
0.554
0.412
0.404
0.393
0.292
0.27
0.269
0.17
0.157
0.033
0.01
-0.084
Species weight
Canonical coefficient
0.1
B
P
C
2 Sep
Naranjo et al. 2003 Biological Control (in press)
Implementation & Evaluation
Can conservation contribute to pest
control?
Whitefly Pest Management
1997
Adults per leaf
25
20
IGR
Conventional
Untreated
15
10
5
0
29 June
19 July
8 Aug
28 Aug
17 Sept
Life Table Analyses
1997
Predation
Parasitism
Other
1-14 days post-spray
14-27 days post spray
Untreated A
A
Conventional B
B
Pyriproxyfen B
A
Buprofezin AB
0
Naranjo & Ellsworth (in prep)
Insecticide
A
1
2
3
4
5
6
7
0
1
K-values (marginal)
2
3
4
5
Impact of Conservation
Adults per leaf
25
IGR
Conventional
Untreated
20
15
“Bio-residual”
10
5
ET
0
29 June
19 July
8 Aug
28 Aug
17 Sept
Naranjo & Ellsworth (in prep)
Ef
Ch fec
em tive
Us ica
e
l
Pest
Management
Av
o
id
an
ce
Sa
m
pl
in
g
Thresholds
Insecticides
Resistance Manage.
Detection, Pest and Stickiness
Sampling & Monitoring
Cultural
control
Crosscommodity
Areawide
Pest Biology
& Ecology
Host plant
resistance
Biological
control
Foundation of
IPM
Cultural
control
Crosscommodity
Areawide
Pest Biology
& Ecology
Host plant
resistance
Biological
control
Some mitigating factors
Selective Insecticide Use
Arizona Cotton
Bt cotton
Pyriproxyfen
Buprofezin
80
% Acreage treated
70
60
50
40
30
20
10
0
1996
1997
1998
1999
2000
Lygus Control - no selective options!
1997
1999
0.1
0.1
No Lygus control
Canonical coefficient
C
C
0.0
0.0
-0.1
-0.1
P = 0.003
-0.2
C
C
-0.2
Lygus control
-0.3
-0.3
-0.4
-0.4
-0.5
29 Jul
5 Aug
12 Aug
19 Aug
26 Aug
2 Sep
-0.5
P = 0.002
22 Jul
29 Jul
5 Aug
12 Aug
19 Aug
26 Aug
2 Sep
Naranjo et al. 2003 Biological Control (in press)
Thanks to
Peter Ellsworth
Virginia Barkley
Becci Burke
Kim Beimfohr
Luis Cañas
Jonathan Diehl
Jeanette Martin
Donna Meade
Greg Owens