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