Conservation Biological Control: Conservation Biological Control:

Can it Work in the Cotton System? Can it Work in the Cotton System?

Dr. Steven E. Naranjo, USDA-ARS

Conservation Biological ControlConservation Biological Control

“ Manipulation of the environment to favor “ Manipulation of the environment to favor natural enemies, either by removing or natural enemies, either by removing or mitigating adverse factors or by providing mitigating adverse factors or by providing lacking requisites.”lacking requisites.”

DeBach 1974DeBach 1974

Biological Control Biological Control -- ApproachesApproaches

*Conservation**Conservation*

ClassicalClassical AugmentationAugmentation

Conservation Biological ControlConservation Biological ControlApproachesApproaches

Reduce Direct Mortality•Selective insecticides

•Ecological•Physiological

•Cultural practices

Provide Resources•Refugia•Cover & inter-crops•Landscape pattern•Strip harvesting

AfterRabb, Stinner

& van den Bosch1976

Integration

Controlling Secondary Enemies

Manipulating Host-Plant Attributes

•Hyperparasitism•Intraguild predation

•Plant breeding•Transgenics•Cultural practices

Conservation Biological ControlConservation Biological ControlComponentsComponents

Survey & Identificationof Potentially Important

Natural Enemies

Study of Biology & Ecology;Determination of Factors

Constraining or Enhancing Biological Control

Implementation &Evaluation

Progress

SurveySurvey

Is there potential for natural Is there potential for natural biological controlbiological control?

Natural Enemy Complex Natural Enemy Complex --Western U.S.Western U.S.Parasitoids Predators

30+ species

HyposterCopidosomaMicroplitis

LysiphlebusChelonus

EretmocerusEncarsiaAnaphes

Leiophron

PathogensVarious viruses, bacteria & fungi

50+ species

GeocorisOriusNabisZelus

CollopsHippodamia

DrapetisChrysoperlaMisumenops

Natural Enemies Natural Enemies –– Pectinophora gossypiellaPectinophora gossypiella

Arizona/CaliforniaPredators

≈23 species described9 species (immunological ID)

Parasitoids4 native species described (rare)

16 exotic species introduced(0 established)

Pathogens3+ Viruses and bacteria

Natural Enemies Natural Enemies –– Bemisia tabaciBemisia tabaci

114+ Predators (various methods)

50+ Parasitoids

11+ Fungi

20 Predators (immunological ID)

3 Native parasitoidsMany exotic parasitoids introduced

2 established

2 Fungi?

Worldwide Arizona Cotton

Natural Enemies Natural Enemies –– Lygus hesperusLygus hesperusArizona/California

Predators10+ species described

5 species (immunological ID)

Parasitoids3 native species described2 exotic species introduced(both established in CA)

Pathogens2+ Fungi

Qualitative Gut AnalysesQualitative Gut Analyses

Frequency0.6 0.5 0.4 0.3 0.2 0.1 0.0

Frequency0.0 0.1 0.2 0.3 0.4 0.5 0.6

Geocoris spp.

Lygus hesperus

Nabis alternatus

Orius tristicolor

Sinea confusa

Zelus renardii

Collops vittatus

Hippodamia convergens

Whitefly Pink bollworm

Hagler & Naranjo 1994a,b; Naranjo & Hagler 1997

Natural Mortality of BemisiaNatural Mortality of Bemisia(Arizona Cotton)(Arizona Cotton)

Tota

l Mor

talit

y

0.7

0.8

0.9

1.0

N = 14

Dislodgement(29.2%)

Parasitism(7.1%)

Inviability(8.8%)

Physiological & Unknown

(21.5%)

Predation(33.4%)

Naranjo & Ellsworth (in prep)

Biological Control Potential?Biological Control Potential?(Sudan Cotton, (Sudan Cotton, Abdelrahman & Munir 1989))

Adu

lt w

hite

flies

per

leaf

048

121620

InsecticideUntreated

7 Oct 16 Nov 26 Dec 4 Feb 16 March

0

5

10

15

20

Nidiana1986/87

Nidiana 1987/88

Biological Control Potential?Biological Control Potential?(some more examples)(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 miteoutbreak: physiological stimulations or natural enemy disruption. Exp. Appl. Acarol. 17: 291

Reducing ConstraintsReducing Constraints

Controlling Secondary Enemies

• Hyperparasitism• Intraguild predation

Encarsia parasitizing Eretmocerus in Bemisia

Sorting out the PlayersSorting out the Players

Bemisia

Zelus spp.Sinea spp.

Coccinellids

SalticidsClubionids Thomisids

Lygus hesperus

Chrysoperla spp.Collops spp. Nabis spp.

Orius tristicolor

Encarsia spp. Eretmocerus spp.

Geocoris spp.

Gossypium hirsutum

Geocoris Orius Hippodamia

Pref

eren

ce (p

aras

itize

d)

0.0

0.2

0.4

0.6

0.8

1.0

P<0.0001P<0.0001

P<0.0001

Displaced mycetome stage

VS.

Early 4th stage

Naranjo (in prep)

Geocoris Orius Hippodamia

Pref

eren

ce (p

aras

itize

d)

0.0

0.2

0.4

0.6

0.8

1.0P<0.0001

P<0.0007

P<0.0001

Early 4th stagePupal stage

VS.

Naranjo (in prep)

Visual Predators?Visual Predators?

• Late 4th Stage WF (“pupa”)• Displaced mycetomes stage• Parasitoid pupa • Early 4th Stage WF

Geocoris Orius Hippodamia

Pref

eren

ce (p

aras

itize

d)

0.0

0.2

0.4

0.6

0.8

1.0

P<0.005

P<0.837P<0.945

Displaced mycetome stage

VS.

Late 4th stage (“pupa”)

Naranjo (in prep)

Reducing ConstraintsReducing Constraints

Can insecticides be managed to Can insecticides be managed to promote biological control?promote biological control?

Compatibility?Compatibility?

Conventional Insecticides Conventional Insecticides (by Threshold)(by Threshold)

Brawley, CA 1995

0

200

400

600

800

Maricopa, AZ 1994

Cum

ulat

ive

Inse

ct-d

ays

(25

swee

ps)

0

50

100

150

200

250Control20/leaf

10/leaf5/leaf

2.5/leaf

Naranjo et al. 2002. J. Econ. Entomol

Conventional Insecticides Conventional Insecticides (by Threshold)(by Threshold)

Number of sprays0 2 4 6 8 10 12

0.0

0.2

0.4

0.6

0.8

1st spray (degree-days after planting)800 900 1000 1100 1200 1300 1400

Prop

ortio

nal r

educ

tion

0.0

0.2

0.4

0.6

0.8

Naranjo et al. 2002. J. Econ. Entomol.

Insecticide Use PatternsInsecticide Use PatternsArizona CottonArizona Cotton

1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000

Mea

n ap

plic

atio

ns p

er a

cre

0

2

4

6

8

10

12

14

0

2

4

6

8

10

12

14Pink bollwormWhiteflyLygus Other

Bt cottonInsect growth regulators

Ellsworth & Jones 2000

Selective Insecticides?Selective Insecticides?

•• BtBt Transgenic CottonTransgenic Cotton

•• Applaud Applaud (Chitin Inhibitor)(Chitin Inhibitor)•• Knack Knack ((JuvenoidJuvenoid))

Science or Emotion?Science or Emotion?

• Resistance management• Food safety• Non-target effects

Non-Target Effects

Natural enemy abundanceNatural enemy diversity

Natural enemy function

Natural Enemy AbundanceNatural Enemy Abundance

LepidopteraMisumenops celer

Collops vittatusHippodamia convergens

Geocoris punctipesGoecoris pallens

Orius tristicolorZelus renardii

Nabis alternatusLygus hesperus

Pseudatomoscelis seriatusChrysoperla carnea

Drapetis sp.Hymenoptera

0.040.630.390.160.250.420.450.220.140.200.110.210.190.76

0.010.920.130.570.720.120.540.110.690.420.250.280.950.53

0.010.590.750.560.860.730.490.120.400.810.330.710.340.47

1999 2000 2001

Naranjo 2002, in prep

Principal Response Curves AnalysisPrincipal Response Curves Analysis

Time-dependent multivariate analysisDerived 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

Spec

ies

wei

ght

3.182.041.791.431.31.291.121.11.040.910.880.80.570.560.540.50.410.320.240.190.080.060.04-0.02-0.05-0.07-0.09-0.23-0.24-0.79

HymenopteraCoccinellidaeL. hesperusP. seriatusC. carnea

S. albofasc.O. tristicolor

M. celerN. alternatusDrapetis sp.

AraneidaZ. renardii

ThomisidaeThanatus sp.Anthicus spp.

G. pallensG. punctipes

Metaphid. spp.H. convergens

C. vittatusHabronatus spp.O. abdominalis

SalticidaeScymnus sp.FormicidaeS. confusa

Trachelus sp.R. forticornisN. calcaratusD. reticulata

1999

9 Jun 29 Jun 19 Jul 8 Aug 28 Aug 17 Sep

Can

onic

al c

oeffi

cien

t

-0.8

-0.6

-0.4

-0.2

0.0

0.2

0.4

P = 0.13

Selectivity of Bt cottonSelectivity of Bt cotton

Bt cotton

Non-Bt

exp(cdtbk)1.34 x control

Naranjo (in prep)

Selectivity of Bt cottonSelectivity of Bt cotton2.622.572.121.451.371.281.21.080.930.640.550.480.260.160.130.120.080.060-0.01-0.08-0.15-0.17-0.24-0.33-0.53-0.54-0.57-0.58-1.12

C. carneaO. tristicolor

C. vittatusH. convergensHymenopteraD. reticulataN. alternatus

M. celerDrapetis sp.G. punctipesS. albofasc.L. hesperus

Thanatus sp.Habronatus spp.

S. confusaFormicidae

R. forticornisMetaph. spp.Scymnus sp.CoccinellidaeLabridura spp.

P. seriatusThomisidaeSalticidae

O. abdominalisZ. renardii

Anthicus spp.G. pallens

N. calcaratusAraneida

2000

9 Jun 29 Jun 19 Jul 8 Aug 28 Aug 17 Sep

Can

onic

al c

oeffi

cien

t

-0.8

-0.6

-0.4

-0.2

0.0

0.2

0.4

P = 0.52

Bt cotton

Non-Bt

Naranjo (in prep)

Spec

ies

wei

ght

Spec

ies

wei

ght

3.921.371.361.331.321.241.151.140.930.650.50.470.350.250.240.180.170.140.10.050.030.020.010-0.01-0.05-0.07-0.16-0.2

Drapetis sp.M. celer

HymenopC. carnea

O. tristicolorL. hesperus

Anthicus spp.H. convergens

P. seriatusS. albofacs.D. reticulataNysius sp.

N. calcaratusScymnus sp.G. punctipes

G. pallensHabronatus sp

Z. renardiiCoccinellidaeR. forticornis

AraneidaLabriduraSalticidae

ThomisidaeMetaph. spp.N. alternatusThanatus sp.FormicidaeC. vittatus

2001

9 Jun 29 Jun 19 Jul 8 Aug 28 Aug 17 Sep

Can

onic

al c

oeffi

cien

t

-0.8

-0.6

-0.4

-0.2

0.0

0.2

0.4

P = 0.005

Selectivity of Bt cottonSelectivity of Bt cottonBt cotton

Non-Bt

Bt cotton spray

Non-Bt spray

Naranjo (in prep)

Spec

ies

wei

ght

3.482.32.261.811.410.570.540.50.290.240.210.170.130.110.070.060.050.040.030.020.018e-32e-30-2e-3-0.02-0.04-0.13-0.35

G. punctipesG. pallens

L. hesperusN. alternatusP. seriatusC. vittatus

M. celerD. reticulata

C. carneaCoccinellidaeH. convergens

HymenopZ. renardiiSalticidae

Anthicus spp.Scymnus sp.S. albofacs.

N. calcaratusFormicidae

Metaph. spp.Habronatus sp

ThomisidaeNysius sp.Araneida

Thanatus sp.O. abdominalisR. forticornisO. tristicolorDrapetis sp.

2002

9 Jun 29 Jun 19 Jul 8 Aug 28 Aug 17 Sep

Can

onic

al c

oeffi

cien

t

-0.8

-0.6

-0.4

-0.2

0.0

0.2

0.4

P = 0.008

Selectivity of Bt cottonSelectivity of Bt cotton

Bt cotton

Non-Bt

Non Bt-spray

Bt-spray

Naranjo (in prep)

Spec

ies

wei

ght

2.51.881.721.371.280.730.560.510.460.410.30.270.230.130.10.08-0.07-0.19-0.35-0.41-0.43-0.49-0.63-0.75-0.97-1.05-1.39-1.4-1.83

G. punctipesAraneida

N. alternatusZ. renardii

M. celerO. tristicolorL. hesperusThanatus sp.

C. carneaDrapetis sp.

Habronatus spSalticidae

CoccinellidaeFormicidae

R. forticornisSinea spp.P. seriatus

Metaph. spp.Nysius sp.

H. convergensScymnus sp.S. albofacs.ThomisidaeD. reticulataN. calcaratus

C. vittatusHymenop

Anthicus spp.G. pallens

2003

9 Jun 29 Jun 19 Jul 8 Aug 28 Aug

Can

onic

al c

oeffi

cien

t

-0.8

-0.6

-0.4

-0.2

0.0

0.2

0.4

P = 0.21

Selectivity of Bt/RR cottonSelectivity of Bt/RR cotton

BtNon-Bt/RR

Bt/RR

RR

Naranjo (in prep)

Natural Enemy FunctionNatural Enemy FunctionPredation on Pink Bollworm EggsPredation on Pink Bollworm Eggs

2001

Prop

ortio

n ea

ten

0.0

0.1

0.2

0.3

0.4

0.5

0.6 BtNon-Bt

2002 2003

0.0

0.1

0.2

0.3

0.4

0.5

0.6

Naranjo 2002, in prep

Natural Enemy FunctionNatural Enemy FunctionPredation on Pink Bollworm PupaePredation on Pink Bollworm Pupae

2002

Prop

ortio

n ea

ten

0.0

0.2

0.4

0.6

0.8BtNon-Bt

2003

0.0

0.2

0.4

0.6

0.8

Naranjo (in prep)

Natural Enemy FunctionNatural Enemy FunctionMortality of Whitefly NymphsMortality of Whitefly Nymphs

2001

Predation Parasitism

Mar

gina

l rat

e of

mor

talit

y

0.0

0.2

0.4

0.6

0.8BtNon-Bt

2002

Predation Parasitism

2003

Predation Parasitism0.0

0.2

0.4

0.6

0.8

Naranjo 2002, in prep

Selective Insecticides?Selective Insecticides?

•• BtBt Transgenic CottonTransgenic Cotton

•• Applaud Applaud (Chitin Inhibitor)(Chitin Inhibitor)

•• Knack Knack ((JuvenoidJuvenoid))

Selectivity of Selectivity of IGRsIGRs

Control

BupPyr

Conven

1997

29 Jul 5 Aug 12 Aug 19 Aug 26 Aug 2 Sep

Can

onic

al c

oeffi

cien

t

-0.8

-0.7

-0.6

-0.5

-0.4

-0.3

-0.2

-0.1

0.0

0.1

0.2

Species weight

3.0272.0191.2961.230.9630.9620.7750.6250.5970.4590.2470.1710.1650.1380.1080.1040.0340.024-0.01-0.011

P = 0.002

L. hesperusO. tristicolorG. punctipesC. carnea s.l.

P. seriatusD. nr. divergens

M. celerZ. renardii

Other AraneidaN. alternatus

S. albofasciatusSinea spp.C. vittatusSalticidae

H. convergensD. reticulata

G. pallensOther Coccinellidae

R. forticornisAnthicidae

B P C CP B C CC C C C C

Naranjo et al. 2003 Biological Control (in press)

Selectivity of Selectivity of IGRsIGRs1999

5 Aug 12 Aug 19 Aug 26 Aug 2 Sep

Can

onic

al c

oeffi

cien

t

-0.8

-0.7

-0.6

-0.5

-0.4

-0.3

-0.2

-0.1

0.0

0.1

0.2 BPC C C

Species weight

2.0371.9751.9321.7151.6351.3940.9570.6240.5540.4120.4040.3930.2920.270.2690.170.1570.0330.01-0.084

P = 0.002

M. celerG. punctipesL. hesperus

O. tristicolorD. nr. divergens

C. carnea s.l.Other Coccinellidae

Other AraneidaC. vittatus

R. forticornisD. reticulata

P. seriatusN. alternatus

SalticidaeZ. renardii

Sinea sspp.G. pallens

H. convergensS. albofasciatus

Anthicidae

Control

Bup

Pyr

Conven

Naranjo et al. 2003 Biological Control (in press)

Implementation & EvaluationImplementation & Evaluation

Can conservation contribute to pest Can conservation contribute to pest control?control?

29 June 19 July 8 Aug 28 Aug 17 Sept

Adu

lts p

er le

af

0

5

10

15

20

25 IGRConventionalUntreated

Whitefly Pest ManagementWhitefly Pest Management1997

Life Table AnalysesLife Table Analyses

K-values (marginal)0 1 2 3 4 5 6 7

Buprofezin

Pyriproxyfen

Conventional

Untreated A

B

AB

1-14 days post-spray 14-27 days post spray

0 1 2 3 4 5

A

A

B

A

Predation Parasitism Other Insecticide

B

1997

Naranjo & Ellsworth (in prep)

Impact of ConservationImpact of Conservation

29 June 19 July 8 Aug 28 Aug 17 Sept

Adu

lts p

er le

af

0

5

10

15

20

25 IGRConventionalUntreated

ET

“Bio-residual”

Naranjo & Ellsworth (in prep)

Biological control

Pest Biology& Ecology

Culturalcontrol

Cross-commodityAreawide

Host plantresistance

Detection, Pest and StickinessSampling & Monitoring

ThresholdsInsecticides

Resistance Manage.

Avoid

ance

Effe

ctive

Che

mica

lUse

PestManagement

Sam

plin

g

Biological control

Pest Biology& Ecology

Culturalcontrol

Cross-commodityAreawide

Host plantresistance

Foundation of IPM

Some mitigating factorsSome mitigating factors

Selective Insecticide UseSelective Insecticide UseArizona CottonArizona Cotton

1996 1997 1998 1999 2000

% A

crea

ge tr

eate

d

0

10

20

30

40

50

60

70

80Bt cotton Pyriproxyfen Buprofezin

Lygus Control Lygus Control -- no selective options!no selective options!

29 Jul 5 Aug 12 Aug 19 Aug 26 Aug 2 Sep

Can

onic

al c

oeffi

cien

t

-0.5

-0.4

-0.3

-0.2

-0.1

0.0

0.1

C

P = 0.003

22 Jul 29 Jul 5 Aug 12 Aug 19 Aug 26 Aug 2 Sep-0.5

-0.4

-0.3

-0.2

-0.1

0.0

0.1

C C C

P = 0.002

1997 1999

No Lygus control

Lygus control

Naranjo et al. 2003 Biological Control (in press)

Thanks toThanks to

Peter Ellsworth

Virginia BarkleyBecci BurkeKim BeimfohrLuis CañasJonathan DiehlJeanette MartinDonna MeadeGreg Owens