Table 1. Entomopathogen modes of action. Biopesticide Mode of...

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Table 1. Entomopathogen modes of action.

Biopesticide Mode of action Example(s) of pest species with resistance

baculovirus Death caused by virus replications in cells of key organs including midgut and fat body.

Resistance has developed in codling moth Cydia pomonella to Cydia pomonella granulosis virus.

fungi Replication within organs and the haemolymph, mechanical damage to cuticle, loss of host nutrients, action of fungal inhibitors.

Bacillus thuringiensis Binding of δ-endotoxin toxin to midgut epithelial cells causes ion leakage and rapid death

Resistance known to microbial Bt strains and to Cr1AC in Bt GM crops.

nematodes Reproduction of nematodes within the host plus the action of toxins from nematode-associated mutualistic bacteria

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Table 2: Microbial biopesticide active substances on EU Annex I (16/02/2011) (http://ec.europa.eu/sanco_pesticides/public/index.cfm?event=activesubstance.selection)

Grey shaded rows indicate products approved in the UK

Active Substance Product Name

Target (s)

Bacteria Bacillus thuringiensis subsp aizawai ABTS-1857

XenTari WG Caterpillars - peppers

Bacillus thuringiensis subsp aizawai GC-91 Agree 50 WP

European Grape Vine Moth (Lobesia botrana) European Grape Berry Moth (Eupoecilia ambiguella)

Bacillus thuringiensis subsp israelensis AM65-52

VectoBac (Gnatrol)

Sciarid flies on ornamentals

Bacillus thuringiensis subsp kurstaki ABTS 351

Dipel DF Lepidoptera – field vegetables, soft fruit, protected crops

Bacillus thuringiensis subsp kurstaki PB54 Belthirul

Helicoverpa armigera (tomato fruit worm) on tomato crops

Bacillus thuringiensis subsp kurstaki SA11 Delfin WG*


Bacillus thuringiensis subsp kurstaki SA12 Delfin WG


Bacillus thuringiensis subsp kurstaki EG2348 Delfin WG


Bacillus thuringiensis subsp tenebrionis NB176

Novodor FC

Colorado potato beetle Foliar feeding beetle larva, Leptinotarsa decemlineata

Fungi Beauveria bassiana ATCC 740-40 Naturalis-L Whitefly, Thrips, Spidermite

Beauveria bassiana GHA BotaniGard Homopteran pests on tomato and cucumber crops

Lecanicillium muscarium ve6 Mycotal Whitefly, Thrips, Scale insects,

Metarhizium anisopliae BIPESCO5/F52 Met52 Vine weevil

Viruses Adoxophyes orana GV strain BV-0001 Summer fruit tortix moth

Cydia pomonella granulosis virus Codling moth

Helicoverpa armigera nucleopolyhedrovirus Tomato fruitworm

Spodoptera littoralis nucleopolyhedrovirus Cotton leaf worm

*Product based on a mixture of 3 strains of microbial Bt

http://ec.europa.eu/sanco_pesticides/public/index.cfm?event=activesubstance.selection

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Table 3: Combination treatments involving microbial biopesticides and chemical pesticides: number of examples published in the literature plus total number of papers

Control agents used in combination study No. Part 1: interactions between microbial biopesticides and chemical pesticides Entomopathogenic bacteria – No. of examples 10 Entomopathogenic viruses– No. of examples 2 Entomopathogenic fungi – No. of examples 54 Entomopathogenic nematodes – No. of examples 10 Total no. of examples 76 Total no. of papers 72* Part 2: interactions between microbial biopesticides Bacterium x bacterium 8 Fungus x fungus 6 Nematode x nematode 3 Bacterium x virus 6 Bacterium x fungus 10 Bacterium x nematode 9 Virus x fungus 2 Fungus x nematode 12 Total no. of examples 57 Total no. of papers 50* Part 3: interactions between microbial biopesticides & other materials

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Total papers 142

*some papers contain more than one example. The literature search was done using Web of Science and covered publications from 1980 to the present. The literature search was done iteratively: subsets of search terms were used in different combinations (e.g. “biopesticide AND insecticide AND interaction”) until no new publications were found. The search terms used were as follows: biopesticide, entomopathogen, interaction, fungus, bacterium, virus, nematode, insect, mite, chemical, pesticide, synergistic, additive, antagonistic, sub lethal, insecticide, acaricide, biological, control, Beauveria, Metarhizium, Bacillus, baculovirus, Lecanicillium, Verticillium, Isaria, Paecilomyces, Heterorhabditis, Steinernema, neonicotinoid, organophosphate, pyrethroid, carbamate, mode, action, detoxification, resistance, pest, management..

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Table 4. Insecticide Resistance Action Committee (IRAC) v.7.0, August 2010 (groups shown in grey boxes are approved for use in the UK).

Main group and primary site of action

Chemical sub-group or exemplifying active ingredient

Example(s) of UK relevant pest species with resistance1

1 – Acetylcholinesterase (AChE) inhibitors (nerve action)

1A – carbamates e.g. primicarb Peach-potato aphid (Myzus persicae)

1B – organophosphates e.g. chlorpyrifos

Peach-potato aphid (Myzus persicae)

2 – GABA-gates chloride channel antagonists (nerve action)

2A – cyclodiene organochlorines e.g. endosulfan

2B – phenylpyrazoles e.g. fipronil

3 – Sodium channel modulators (nerve action)

3A – pyrethroids/pyrethrins e.g. deltamethrin

Peach-potato aphid (Myzus persicae), Pollen beetle (Meligethes aeneus), Onion thrips (Thrips tabaci)

3B – DDT

4 – Nicotinic acetylcholine receptor (nAChR) agonists (nerve action)

4A – neonicotinoids e.g. imidacloprid

Tobacco whitefly (Bemisia tabaci)*

4B – nicotine

5 – Nicotinic acetylcholine receptor (nAChR) allosteric activators (nerve action)

5 – spinosyns e.g. spinosad Western flower thrips (Frankliniella occidentalis)

6 – Chloride channel activators (nerve & muscle action)

6 – avermectins e.g. abamectin

7 – Juvenile hormone mimics (growth regulation)

7A – juvenile hormone analogues e.g. hydroprene

7B – fenoxycarb

7C – pyriproxyfen

8 – Miscellaneous non-specific (multi-site) inhibitors

8A – alkyl halides e.g. methyl bromide

8B – chloropicrin

8C – sulfuryl fluoride

8D – borax

8E – tartar emetic

9 – Selective homopteran feeding blockers (nerve action)

9B – pymetrozine Tobacco whitefly (Bemisia tabaci), Glasshouse whitefly (Trialeurodes vaporariorum)

9C – flonicamid Tobacco whitefly (Bemisia tabaci), Glasshouse whitefly (Trialeurodes vaporariorum)

10 – Mite growth inhibitors (growth regulation)

10A – clofentezine Two-spotted spider mite (Tetranychus urticae)

10B – etoxazole Two-spotted spider mite (Tetranychus urticae)

12 – Inhibitors of mitochondrial ATP synthase (energy metabolism)

12A – diafenthiuron

12B – organotin miticides e.g. fenbutatin oxide

12C – propargite

12D – tetradifon

13 – Uncouplers of oxidative phosphorylation via disruption of the proton gradient (energy metabolism)

13 – chlorfenapyr

14 – Nicotinic acetylcholine receptor (nAChR) channel

14 – nereistoxin analogues e.g. cartap hydrochloride

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blockers (nerve action)

15 – Inhibitors of chitin biosynethesis, type 0 (growth regulation)

15 – benzoylureas e.g. diflubenzuron

Glasshouse whitefly (Trialeurodes vaporariorum)

16 – Inhibitors of chitin biosynethesis, type 1 (growth regulation)

16 – buprofezin

17 – Moulting disruptor, dipteran (growth regulation)

17 – cyromazine

18 – Ecdysone receptor agonists (growth regulation)

18 – diacylhydrazines e.g. methoxyfenozide

19 – Octopamine receptor agonists (nerve action)

19 – amitraz

20 – Mitochondrial complex III electron transport inihibitors (energy metabolism)

20A – hydramethylnon

20B – acequinocyl

20C – fluacrypyrim

21 – Mitochondrial complex I electron transport inhibitors (energy metabolism)

21A – METI acaricides and insecticides e.g. tebufenpyrad

Two-spotted spider mite (Tetranychus urticae)

21B – rotenone

22 – Voltage-dependent sodium channel blockers (nerve action)

22A – indoxacarb

22B – metaflumizone

23 – Inhibitors of acetyl CoA carboxylase (lipid synthesis, growth regulation)

23 – tetronic & tetramic acid derivatives e.g. spirotetramat

24 – Mitochondrial complex IV electron transport inihitors (energy metabolism)

24A – aluminium phosphide

24B – cyanide

25 – Mitochondrial complex II electron transport inhibitors (energy metabolism)

25 – cyenopyrafen

28 – Ryanodine receptor modulators (nerve & muscle action)

28 – diamides e.g. chlorantraniliprole

Compounds of unknown or uncertain mode of action

e.g. azadirachtin

1 Insecticide and acaricide resistance based on scientific literature and expert opinion. * Tobacco whitefly (Bemisia tabaci) is a quarantine pests in the UK, and is not established here and so any suspected infestations must be reported to the Defra Plant Health and Seeds Inspectorate (PHSI).

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Figure 1. Drug combination isobologram at ED50 (from Chou, 2006)

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Appendix 1: Papers published on the effect of combinations of microbial biopesticides and chemical pesticides

MCA microbial control agent

Scale = laboratory (L), greenhouse (G) or field (F) scale experiment

Strategy: were the MCA and chemical pesticide combined simultaneously (SIM) or sequentially (SEQ)?

Result: did the combination of microbial control agent and pesticide result in an increase (I) in the level of pest control, a decrease (D) or a similar (S) level to when the agents were used individually?

Mechanism? Is the mechanism of interaction known?

Part 1: interactions between microbial biopesticides and chemical pesticides Microbial biopesticides (bacteria) with conventional pesticide

MCA chemical pest scale strategy Result Mechanism? Reference

Bacillus thuringiensis

Spinosad, pyrethrin & neem oil

Colorado potato beetle (Leptinotarsa decemlineata)

Laboratory & field

SIM I - Barcic, J. I., R. Bazok, et al. (2006). Combinations of several insecticides used for integrated control of Colorado potato beetle (Leptinotarsa decemlineata, Say., Coleoptera : Chrysomelidae). Journal of Pest Science 79: 223-232.


Methyl parathion, pyrethrin

Fall armyworm (Spodoptera frugiperda)

Laboratory SIM D - Habib, M. E. M. and M. A. Garcia (1981). Compatibility and syngergism between Bacillus thuringiensis var kurstaki and 2 chemical insecticides. Zeitschrift Fur Angewandte Entomologie-Journal of Applied Entomology 91: 7-14.

Bacterium (Bacillus thuringiensis) & fungus (Beauveria bassiana

Larvadex (cyromazine)

House fly (Musca domestica)

Field SIM I - Mwamburi, L. A., M. D. Laing, et al. (2009). Interaction between Beauveria bassiana and Bacillus thuringiensis var. israelensis for the control of house fly larvae and adults in poultry houses. Poultry Science 88: 2307-2314.

Bacillus thuringiensis toxins

Botanical insecticides

Rice leafroller (Cnaphalocrocis medinalis)

Laboratory SIM I - Nathan, S. S., P. G. Chung, et al. (2004). Effect of botanical insecticides and bacterial toxins on the gut enzyme of the rice leaf-folder Cnaphalocrocis medinalis. Phytoparasitica 32: 433-443.

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Nematode (Heterorhabditis bacteriophora), fungi (Beauveria bassiana & Metarhizium anisopliae) & bacterium (Bacillus thuringiensis)

Imidacloprid & clothianidin

Amphimallon majale & Japanese beetle (Popillia japonica)

Laboratory, glasshouse & field

- I & D - Morales-Rodriguez, A. and D. C. Peck (2009). Synergies between biological and neonicotinoid insecticides for the curative control of the white grubs Amphimallon majale and Popillia japonica. Biological Control 51: 169-180.

Bacterium (Bacillus thuringiensis) & fungal mycotoxin (Metarhizium anisopliae)

Tea saponin Beet armyworm (Spodoptera exigua)

Laboratory SIM I Changes in antioxidant enzymes, superoxidase dismutase & catalases

Rizwan-Ul-Haq, M., Q. B. Hu, et al. (2009). Study of destruxin B and tea saponin, their interaction and synergism activities with Bacillus thuringiensis kurstaki against Spodoptera exigua (Hubner) (Lepidoptera: Noctuidae). Applied Entomology and Zoology 44: 419-428.


Deltamethrin Diamondback moth (Plutella xylostella)

Laboratory - D Cross resistance

Sayyed, A. H., G. Moores, et al. (2008). Cross-resistance between a Bacillus thuringiensis Cry toxin and non-Bt insecticides in the diamondback moth. Pest Management Science 64: 813-819.


Azadirachtin (neem oil)

Cotton bollworm (Helicoverpa armigera)

Laboratory SIM I - Singh, G., P. J. Rup, et al. (2007). Acute, sublethal and combination effects of azadirachtin and Bacillus thuringiensis toxins on Helicoverpa armigera (Lepidoptera : Noctuidae) larvae. Bulletin of Entomological Research 97: 351-357.


Neem oil Cotton bollworm (Helicoverpa armigera)

Laboratory SIM I - Trisyono, A. and M. E. Whalon (1999). Toxicity of neem applied alone and in combinations with Bacillus thuringiensis to Colorado potato beetle (Coleoptera : Chrysomelidae). Journal of Economic Entomology 92: 1281-1288.

Microbial biopesticides (virus) with conventional pesticide


Nucleopolyhedrovirus Spinosad Fall Laboratory SIM I, S & - Mendez, W. A., J. Valle, et al. (2002). Spinosad and

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armyworm (Spodoptera frugiperda)

& field D nucleopolyhedrovirus mixtures for control of Spodoptera frugiperda (Lepidoptera : Noctuidae) in maize. Biological Control 25: 195-206.

Nucleopolyhedrovirus (SpltNPV)

Azadirachtin (neem)

Oriental leafworm (Spodoptera litura)

Laboratory SIM I - Nathan, S. S. and K. Kalaivani (2006). Combined effects of azadirachtin and nucleopolyhedrovirus (SpltNPV) on Spodoptera litura Fabricius (Lepidoptera : Noctuidae) larvae. Biological Control 39: 96-104.

Microbial biopesticides (fungus) with conventional pesticide


Beauveria bassiana & Metarhizium anisopliae

Imidacloprid Guava weevil (Conotrachelus psidii)

Laboratory SIM I - Brito, E. S., A. R. de Paula, et al. (2008). Combining vegetable oil and sub-lethal concentrations of Imidacloprid with Beauveria bassiana and Metarhizium anisopliae against adult guava weevil Conotrachelus psidii (Coleoptera : Curculionidae). Biocontrol Science and Technology 18: 665-673.

Lecanicillium muscarium

Savona, spraying oil & Agri-50E

Tobacco whitefly (Bemisia tabaci)

Glasshouse SEQ - - Cuthbertson, A. G. S., L. F. Blackburn, et al. (2010). Chemical compatibility testing of the entomopathogenic fungus Lecanicillium muscarium to control Bemisia tabaci in glasshouse environment. International Journal of Environmental Science and Technology 7: 405-409.


Majestik, Spray Oil, Agri-50E, Savona & Oberon


Laboratory SEQ - - Cuthbertson, A. G. S., L. F. Blackburn, et al. (2008). Further compatibility tests of the entomopathogenic fungus Lecanicillium muscarium with conventional insecticide products for control of sweetpotato whitefly, Bemisia tabaci on poinsettia plants. Insect Science 15: 355-360.


Imidacloprid, buprofezin, teflubenzuron and nicotine


Laboratory - - - Cuthbertson, A. G. S., K. F. A. Walters, et al. (2005). Compatibility of the entomopathogenic fungus Lecanicillium muscarium and insecticides for eradication of sweetpotato whitefly, Bemisia tabaci. Mycopathologia 160: 35-41.

Metarhizium Neem oil Turnip aphid Laboratory SIM - - de Araujo, J. M., E. J. Marques, et al. (2009).

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anisopliae & Beauveria bassiana

(Lipaphis erysimi) Potential of Metarhizium anisopliae and Beauveria bassiana Isolates and Neem Oil to control the aphid Lipaphis erysimi (Kalt.) (Hemiptera: Aphididae). Neotropical Entomology 38: 520-525.

Beauveria bassiana

Diflubenzuron Savanna grasshopper complex

Field SIM I - Delgado, F. X., J. H. Britton, et al. (1999). Field assessment of Beauveria bassiana (Balsamo) vuillemin and potential synergism with diflubenzuron for control of savanna grasshopper complex (Orthoptera) in Mali. Journal of Invertebrate Pathology 73: 34-39.

Beauveria bassiana

Monocroptophos - Laboratory - - - Devi, K. U., N. N. R. Reddy, et al. (2004). Esterase-mediated tolerance to a formulation of the organophosphate insecticide monocrotophos in the entomopathogenic fungus, Beauveria bassiana (Balsamo) Vuill: a promising biopesticide. Pest Management Science 60: 408-412.


Tagetes extract Sugar beet root maggot (Tetanops myopaeformis)

Laboratory SIM S - Dunkel, F. V., S. T. Jaronski, et al. (2010). Effects of Steam-Distilled Shoot Extract of Tagetes minuta (Asterales: Asteraceae) and Entomopathogenic Fungi on Larval Tetanops myopaeformis. Environmental Entomology 39: 979-988.

Paecilomyces fumosoroseus

Malathion, carbaryl, primicarb, pymetrozine, cypermethrin, and deltamethrin

Glasshouse whitefly (Trialeurodes vaporariorum)

Glasshouse - - - Er, M. K. and A. Gokce (2004). Effects of selected pesticides used against glasshouse tomato pests on colony growth and conidial germination of Paecilomyces fumosoroseus. Biological Control 31: 398-404.

Metarhizium anisopliae

Spinosad Wireworm species - Agriotes lineatus & Agriotes obscurus

Laboratory SIM I - Ericsson, J. D., J. T. Kabaluk, et al. (2007). Spinosad interacts synergistically with the insect pathogen Metarhizium anisopliae against the exotic wireworms Agriotes lineatus and Agriotes obscurus (Coleoptera : Elateridae). Journal of Economic Entomology 100: 31-38.

Beauveria bassiana & Metarhizium

Permethrin Mosquito (Anopheles gambiae)

Laboratory SIM I - Farenhorst, M., B. G. J. Knols, et al. (2010). Synergy in efficacy of fungal entomopathogens and permethrin against West African insecticide-

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anisopliae resistant Anopheles gambiae mosquitoes. Plos One 5(8).

Beauveria bassiana

Imidacloprid Brown planthopper (Nilaparvata lugens)

Laboratory SIM I - Feng, M. G. and X. Y. Pu (2005). Time-concentration-mortality modeling of the synergistic interaction of Beauveria bassiana and imidacloprid against Nilaparvata lugens. Pest Management Science 61: 363-370.

Beauveria bassiana

Imidacloprid & cyromazine


Laboratory SIM & SEQ

I - Furlong, M. J. and E. Groden (2001). Evaluation of synergistic interactions between the Colorado potato beetle (Coleoptera : Chrysomelidae) pathogen Beauveria bassiana and the insecticides, imidacloprid, and cyromazine. Journal of Economic Entomology 94: 344-356.

- - Mosquito Computer simulation

SIM I - Hancock, P. A. (2009). Combining Fungal Biopesticides and Insecticide-Treated Bednets to Enhance Malaria Control. Plos Computational Biology 5.


teflubenzuron Cupreous chafer (Anomala cuprea)

Laboratory & field

SIM I & S - Hiromori, H. and J. Nishigaki (1998). Joint action of an entomopathogenic fungus (Metarhizium anisopliae) with synthetic insecticides against the scarab beetle, Anomala cuprea (Coleoptera : Scarabaeidae) larvae. Applied Entomology and Zoology 33: 77-84.


Fenitrothion or Cupreous chafer (Anomala cuprea)

Laboratory SIM I Weakened immune system

Hiromori, H. and J. Nishigaki (2001). Factor analysis of synergistic effect between the entomopathogenic fungus Metarhizium anisopliae and synthetic insecticides. Applied Entomology and Zoology 36: 231-236.


Permethrin Deer tick (Ixodes scapularis)

Laboratory & field

SIM S - Hornbostel, V. L., E. Zhioua, et al. (2005). Pathogenicity of Metarhizium anisopliae (Deuteromycetes) and permethrin to Ixodes scapularis (Acari : Ixodidae) nymphs. Experimental and Applied Acarology 35: 301-316.

Metarhizium anisopliae & Beauveria bassiana

Permethrin Mosquito (Culex quinquefasciatus)

Laboratory SEQ (in space)

S - Howard, A. F. V., R. N'Guessan, et al. (2010). The entomopathogenic fungus Beauveria bassiana reduces instantaneous blood feeding in wild multi-insecticide-resistant Culex quinquefasciatus mosquitoes in Benin, West

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Africa. Parasites & Vectors 3.

Beauveria bassiana

Triflumuron Two-spotted spider mite (Tetranychus urticae)

Laboratory SIM I - Irigaray, F., V. Marco-Mancebon, et al. (2003). The entomopathogenic fungus Beauveria bassiana and its compatibility with triflumuron: effects on the twospotted spider mite Tetranychus urticae. Biological Control 26: 168-173.

Beauveria bassiana

Neem Tobacco whitefly (Bemisia tabaci)

- SIM I - Islam, M. T., S. J. Castle, et al. (2010). Compatibility of the insect pathogenic fungus Beauveria bassiana with neem against sweetpotato whitefly, Bemisia tabaci, on eggplant. Entomologia Experimentalis et Applicata 134: 28-34.

Paecilomyces fumosoroseus

Azadirachtin (neem)

Silverleaf whitefly (Bemisia argentifolii)


S/D - James, R. R. (2003). Combining azadirachtin and Paecilomyces fumosoroseus (Deuteromycotina : Hyphomycetes) to control Bemisia argentifolii (Homoptera : Aleyrodidae). Journal of Economic Entomology 96: 25-30.

Beauveria bassiana

Imidacloprid Silverleaf whitefly (Bemisia argentifolii)

- SIM D - James, R. R. and G. W. Elzen (2001). Antagonism between Beauveria bassiana and imidacloprid when combined for Bemisia argentifolii (Homoptera : Aleyrodidae) control. Journal of Economic Entomology 94: 357-361.


Imidacloprid Cassava burrower bug (Cyrtomenus bergi)

Laboratory & Glasshouse

SIM I - Jaramillo, J., C. Borgemeister, et al. (2005). Effect of combined applications of Metarhizium anisopliae (Metsch.) Sorokin (Deuteromycotina : Hyphomycetes) strain CIAT 224 and different dosages of imidacloprid on the subterranean burrower bug Cyrtomenus bergi Froeschner (Hemiptera : Cydnidae). Biological Control 34: 12-20.


Hydramethylnon German cockroach (Blattella germanica)

Laboratory - - - Kaakeh, W., B. L. Reid, et al. (1996). Horizontal transmission of the entomopathogenic fungus Metarhizium anisopliae (Imperfect fungi: Hyphomycetes) and hydramethylnon among German cockroaches (Dictyoptera: Blattellidae). Journal of Entomological Science 31: 378-390.


Imidacloprid German cockroach

Laboratory SIM I - Kaakeh, W., B. L. Reid, et al. (1997). Toxicity of imidacloprid in the German cockroach

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(Blattella germanica)

(Dictyoptera: Blattellidae), and the synergism between imidacloprid and Metarhizium anisopliae (Imperfect Fungi: Hyphomycetes). Journal of Economic Entomology 90: 473-482.

Beauveria bassiana

Dimethoate Tarnished plant bug (Lygus lineolaris)

Laboratory & field

- S - Kouassi, M., D. Coderre, et al. (2003). Compatibility of Zineb, Dimethoate and Beauveria bassiana (Balsamo) Vuillemin against tarnished plant bug (Hemiptera: Miridae). Journal of Entomological Science 38: 359-367.


Lambda-cyhalothrin

Sahelian grasshoppers

Field SIM S - Kpindou, O. K. D., C. J. Lomer, et al. (2001). Effect of a mixture of lambda-cyhalothrin and spores of Metarhizium anisopliae (flavoviride) var. acridum Driver and Milner (biopesticide) applied to grasshopper larvae in Mali. Journal of Applied Entomology-Zeitschrift Fur Angewandte Entomologie 125: 249-253.


Fenitrothion Sahelian grasshoppers

Field - - - Langewald, J., Z. Ouambama, et al. (1999). Comparison of an organophosphate insecticide with a mycoinsecticide for the control of Oedaleus senegalensis (Orthoptera : Acrididae) and other Sahelian grasshoppers at an operational scale. Biocontrol Science and Technology 9: 199-214.

Bacterium (Bacillus thuringiensis) & fungus (Beauveria bassiana)

Carbofuran European corn borer (Ostrinia nubilalis)

Field SIM (but not tank mixed)

I - Lewis, L. C., E. D. Berry, et al. (1996). Aptness of insecticides (Bacillus thuringiensis and carbofuran) with endophytic Beauveria bassiana, in suppressing larval populations of the European corn borer. Agriculture Ecosystems & Environment 57: 27-34.


Fipronil, teflubenzuron & fenitrothion

- Laboratory SIM - - Luke, B. M. and R. P. Bateman (2006). Effects of chemical and botanical insecticides used for locust control on Metarhizium anisopliae var. acridum conidia after short- to medium-term storage at 30 degrees C. Biocontrol Science and Technology 16: 761-766.


Abamectin & fenbutatin oxide

- Laboratory - - - Mochi, D. A., A. C. Monteiro, et al. (2005). Action of pesticides to Metarhizium anisopliae in soil. Neotropical Entomology 34(6): 961-971.

Metarhizium Abamectin & Mediterranean Laboratory SEQ S - Mochi, D. A., A. C. Monteiro, et al. (2006).

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anisopliae trichlorfon fruit fly (Ceratitis capitata)

Pathogenicity of Metarhizium anisopliae for Ceratitis capitata (Wied.) (Diptera: Tephritidae) in soil with different pesticides. Neotropical Entomology 35: 382-389.

Beauveria bassiana

Neem oil Oriental leafworm (Spodoptera litura)

Laboratory SIM I - Mohan, M. C., N. P. Reddy, et al. (2007). Growth and insect assays of Beauveria bassiana with neem to test their compatibility and synergism. Biocontrol Science and Technology 17: 1059-1069.


Larvadex House fly (Musca domestica)

Field SIM I - Mwamburi, L. A., M. D. Laing, et al. (2009). Interaction between Beauveria bassiana and Bacillus thuringiensis var. israelensis for the control of house fly larvae and adults in poultry houses. Poultry Science 88: 2307-2314.



European chafer (Amphimallon majale) & Japanese beetle (Popillia japonica)




Chlorpyrifos, propetamphos, & cyfluthrin

German cockroach (Blattella germanica)

Laboratory SIM I - Pachamuthu, P. and S. T. Kamble (2000). In vivo study on combined toxicity of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) strain ESC-1 with sublethal doses of chlorpyrifos, propetamphos, and cyfluthrin against German cockroach (Dictyoptera : Blattellidae). Journal of Economic Entomology 93: 60-70.


Chlorpyrifos, propetamphos, & cyfluthrin

German cockroach (Blattella germanica)

Laboratory - - - Pachamuthu, P., S. T. Kamble, et al. (1999). Virulence of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) strain ESC-1 to the German cockroach (Dictyoptera : Blattellidae) and its compatibility with insecticides.

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Journal of Economic Entomology 92: 340-346.


Imidacloprid Sugarcane rootstalk borer (Diaprepes abbreviatus)

Laboratory SIM I - Quintela, E. D. and C. W. McCoy (1997). Pathogenicity enhancement of Metarhizium anisopliae and Beauveria bassiana to first instars of Diaprepes abbreviatus (Coleoptera: Curculionidae) with sublethal doses of imidacloprid. Environmental Entomology 26: 1173-1182.



Laboratory SEQ D - Quintela, E. D. and C. W. McCoy (1998). Conidial attachment of Metarhizium anisopliae and Beauveria bassiana to the larval cuticle of Diaprepes abbreviatus (Coleoptera Curculionidae) treated with imidacloprid. Journal of Invertebrate Pathology 72: 220-230.



Laboratory SIM I - Quintela, E. D. and C. W. McCoy (1998). Synergistic effect of imidacloprid and two entomopathogenic fungi on the behavior and survival of larvae of Diaprepes abbreviatus (Coleoptera : Curculionidae) in soil. Journal of Economic Entomology 91: 110-122.


Tea saponin Beet armyworm (Spodoptera exigua)



Lecanicllium longisporum

Imidacloprid Aphids Laboratory SEQ I Increased insect movement

Roditakis, E., I. D. Couzin, et al. (2000). Improving secondary pick up of insect fungal pathogen conidia by manipulating host behaviour. Annals of Applied Biology 137: 329-335.


Imidacloprid Leaf-cutting ant (Atta sexdens rubropilosa)

Laboratory SEQ I - Santos, A. V., B. L. de Oliveira, et al. (2007). Selection of entomopathogenic fungi for use in combination with sub-lethal doses of imidacloprid: perspectives for the control of the leaf-cutting ant Atta sexdens rubropilosa Forel (Hymenoptera : Formicidae). Mycopathologia 163: 233-240.

Metarhizium Lambda- Locust and Laboratory - - - Sanyang, S., H. F. Van Emden, et al. (2000).

16

flavoviridae cyhalothrin grasshopper Laboratory shelf-life of oil-formulated conidia of the locust and grasshopper fungal pathogen Metarhizium flavoviridae Gams & Rozsypal, in mixtures with the pyrethroid insecticide lambda-cyhalothrin. International Journal of Pest Management 46: 165-168.

Metarhizium flavoviride

Cypermethrin African migratory locust (Locusta migratoria migratorioides)

Laboratory SIM I - Sanyang, S. and H. F. van Emden (1996). The combined effects of the fungus Metarhizium flavoviride Gams & Rozsypal and the insecticide cypermethrin on Locusta migratoria migratorioides

(Reiche & Fairmaire) in the laboratory. International Journal of Pest Management 42: 183-187.

Beauveria bassiana

e.g. imidacloprid, thiamethoxam, dinotefuran, spinosad, spinetoram, beta-cyfluthrin, esfenvalerate, zeta-cypermethrin, lambda-cyhalothrin, borax mixed with orange oil and detergents

Chilli thrips (Scirtothrips dorsalis)

Field - - - Seal, D. R. and V. Kumar (2010). Biological response of chilli thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae), to various regimes of chemical and biorational insecticides. Crop Protection 29: 1241-1247.

Beauveria bassiana

Imidacloprid & diatomaceous earth

Mole cricket (Scapteriscus borellii)

Laboratory SEQ I & S Damage to insect cuticle

Thompson, S. R. and R. L. Brandenburg (2006). Effect of combining imidacloprid and diatomaceous earth with Beauveria bassiana on mole cricket (Orthoptera : Gryllotalpidae) mortality. Journal of Economic Entomology 99: 1948-1954.

Beauveria bassiana

Nereistoxin Diamondback moth (Plutella xylostella)

Laboratory SIM I - Tian, L. and M. G. Feng (2006). Evaluation of the time-concentration-mortality responses of Plutella xylostella larvae to the interaction of Beauveria bassiana with a nereistoxin analogue insecticide.

17

Pest Management Science 62: 69-76.

Beauveria bassiana

Imidacloprid Chrysanthemum aphid (Macrosiphoniella sanborni) & peach-potato aphid (Myzus persicae)

Laboratory SIM I - Ye, S. D., Y. H. Dun, et al. (2005). Time and concentration dependent interactions of Beauveria bassiana with sublethal rates of imidacloprid against the aphid pests Macrosiphoniella sanborni and Myzus persicae. Annals of Applied Biology 146: 459-468.

Beauveria bassiana

Fenitrothion Sunn pest (Eurygaster integriceps)

Laboratory SEQ D - Zibaee, A., A. R. Bandani, et al. (2009). Effect of the entomopathogenic fungus, Beauveria bassiana, and its secondary metabolite on detoxifying enzyme activities and acetylcholinesterase (AChE) of the Sunn pest, Eurygaster integriceps (Heteroptera: Scutellaridae). Biocontrol Science and Technology 19: 485-498.


Fipronil & imidacloprid

Western flower thrips (Frankliniella occidentalis)

Laboratory SIM S - Ansari, M.A., M. Brownbridge et al. (2008) Efficacy of entomopathogenic fungi against soil-dwelling life stages of western flower thrips, Frankliniella occidentalis, in plant-growing media. Entomologia Experimentalis et Applicata 127: 80-87.


? Western flower thrips (Frankliniella occidentalis)

Laboratory SIM I - Ansari, M.A., F. A. Shah et al. (2007) Control of western flower thrips (Frankliniella occidentalis) pupae with Metarhizium anisopliae in peat and peat alternative growing media. Biological Control 40: 293-297.


Neem seed cake

Black vine weevil (Otiorhynchus sulcatus)

Field SIM I - Shah, F.A., M. Gaffney et al. (2008). Neem seed cake enhances the efficacy of the insect pathogenic fungus Metarhizium anisopliae for the control of black vine weevil, Otiorhynchus sulcatus (Coleoptera: Curculionidae). Biological Control 44, 111-115.


Fipronil & imidacloprid


Laboratory SIM I - Shah, F.A., A. Ansari et al. (2008). Evaluation of black vine weevil (Otiorhynchus sulcatus) control strategies using Metarhizium anisopliae with sublethal doses of insecticides in disparate horticultural growing media. Biological Control 40 :

18

246-252.

Microbial biopesticides (nematode) with conventional pesticide


Steinernema carpocapsae

spiromesifen, thiacloprid, imidacloprid and pymetrozine


Laboratory - I - Cuthbertson, A. G. S., J. J. Mathers, et al. (2008). The integrated use of chemical insecticides and the entomopathogenic nematode, Steinernema carpocapsae (Nematoda : Steinernematidae), for the control of sweetpotato whitefly, Bemisia tabaci (Hemiptera : Aleyrodidae). Insect Science 15: 447-453.

Steinernema feltiae

Including – spinosad, Bacillus thuringiensis, diflubenzuron, acephate & fenoxycarb

- Laboratory - - - De Nardo, E. A. B. and P. S. Grewal (2003). Compatibility of Steinernema feltiae (Nematoda : Steinernematidae) with pesticides and plant growth regulators used in glasshouse plant production. Biocontrol Science and Technology 13: 441-448.

Heterorhabditis bacteriophora & Steinernema glaseri

Imidacloprid Japanese beetle (Popillia japonica), Oriental beetle (Exomala orientalis), masked chafers (Cyclocephala borealis, C. pasadenae & C. hirta)

Glasshouse & field

SEQ I - Koppenhofer, A. M., I. M. Brown, et al. (2000). Synergism of entomopathogenic nematodes and imidacloprid against white grubs: Greenhouse and field evaluation. Biological Control 19: 245-251.

H. bacteriophora, H. megidis, H. marclatus, S. glaseri & S.feltiae

Imidacloprid & thiamethoxam

European chafer (Rhizotrogus majalis), Garden beetle (Maladera

Glasshouse & field

SEQ I & S - Koppenhofer, A. M., R. S. Cowles, et al. (2002). Comparison of neonicotinoid insecticides as synergists for entomopathogenic nematodes. Biological Control 24: 90-97.

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castanea), Oriental beetle (Exomala orientalis) & Japanese beetle (Popillia japonica)

Steinernema glaseri, S. carpocapsae, S. feltiae, Heterorhabditis bacteriophor, H. megidis

Acetamiprid, imidacloprid & thiamethoxam

Scarab species


- - Koppenhofer, A. M., R. S. Cowles, et al. (2003). Effect of neonicotinoid synergists on entomopathogenic nematode fitness. Entomologia Experimentalis et Applicata 106: 7-18.

Heterorhabditis bacteriophora

Chlorantraniliprole

Japanese beetle (Popillia japonica) & masked chafers (Cyclocephala borealis)

Glasshouse SEQ I - Koppenhofer, A. M. and E. M. Fuzy (2008). Effect of the anthranilic diamide insecticide, chlorantraniliprole, on Heterorhabditis bacteriophora (Rhabditida : Heterorhabditidae) efficacy against white grubs (Coleoptera: Scarabaeldae). Biological Control 45: 93-102.

Steinernema glaseri, Heterorhabditis bacteriophora & Steinernema kushidai

Imidacloprid Masked chafers ((Cyclocephala pasadenae & C. hirta)

Laboratory - I Reduce activity of larvae

Koppenhofer, A. M., P. S. Grewal, et al. (2000). Synergism of imidacloprid and entomopathogenic nematodes against white grubs: the mechanism. Entomologia Experimentalis et Applicata 94: 283-293.

Heterorhabditis bacteriophora

Imidacloprid Masked chafers ((Cyclocephala pasadenae & C. hirta)

Glasshouse & field

SIM & SEQ

I - Koppenhofer, A. M. and H. K. Kaya (1998). Synergism of imidacloprid and an entomopathogenic nematode: A novel approach to white grub (Coleoptera : Scarabaeidae) control in turfgrass. Journal of Economic Entomology 91: 618-623.

Heterorhabditis marelatus

Halofenozide Japanese beetle (Popillia japonica)

- SIM S - Mannion, C. M., H. E. Winkler, et al. (2000). Interaction between halofenozide and the entomopathogenic nematode Heterorhabditis marelatus for control of Japanese beetle (Coleoptera Scarabaeidae) larvae. Journal of

20

Economic Entomology 93: 48-53.



European chafer Amphimallon majale & Popillia japonica (Popillia japonica)



Part 2: interactions between microbial biopesticides Microbial biopesticide (bacteria) with microbial biopesticide (bacteria)

MCA pest scale strategy Result Mechanism? Reference

Bacillus thuringiensis kurstaki & israelensis

- Laboratory SIM D - Del Rincon-Castro, M. C., J. Barajas-Huerta, et al. (1999). Antagonism between Cry1Ac1 and Cyt1A1 toxins of Bacillus thuringiensis. Applied and Environmental Microbiology 65: 2049-2053.

Bacillus thuringiensis israelensis toxins Cyt1Aa, Cry4Ba and Cry11Aa.

Mosquito (Anopheles albimanus)

Laboratory SIM I - Fernandez-Luna, M. T., B. E. Tabashnik, et al. (2010). Single concentration tests show synergism among Bacillus thuringiensis subsp israelensis toxins against the malaria vector mosquito Anopheles albimanus. Journal of Invertebrate Pathology 104: 231-233.

Xenorhabdus nematophila & Bacillus thuringiensis

Beet armyworm (Spodoptera exigua)

Laboratory SIM I Improved passage of Xenorhabdus nematophila through gut wall

Jung, S. and Y. Kim (2006). Synergistic effect of Xenorhabdus nematophila K1 and Bacillus thuringiensis subsp aizawai against Spodoptera exigua (Lepidoptera Noctuidae). Biological Control 39: 201-209.

Xenorhabdus nematophila, Photorhabdus

Beet armyworm Spodoptera

Laboratory SIM I Improved passage of Xenorhabdus

Jung, S. C. and Y. Kim (2006). Synergistic effect of entomopathogenic bacteria (Xenorhabdus sp. and Photorhabdus temperata ssp. temperata) on the pathogenicity

21

temperata & Bacillus thuringiensis

exigua nematophila & Photorhabdus temperata through gut wall

of Bacillus thuringiensis ssp. aizawai against Spodoptera exigua (Lepidoptera Noctuidae). Environmental Entomology 35: 1584-1589.

Xenorhabdus nematophila & Bacillus thuringiensis

Diamondback moth (Plutella xylostella)

Laboratory SIM I Improved passage of Xenorhabdus nematophila

through gut wall

Jung, S. C. and Y. G. Kim (2007). Potentiating effect of Bacillus thuringiensis subsp kurstaki on pathogenicity of entomopathogenic bacterium Xenorhabdus nematophila K1 against diamondback moth (Lepidoptera : Plutellidae). Journal of Economic Entomology 100: 246-250.

Bacillus thuringiensis toxins Cry1Ab and Cry1Ac

Maize stem borer (Chilo partellus)

Laboratory SIM I Increased toxin binding

Sharma, P., V. Nain, et al. (2010). Synergistic activity between Bacillus thuringiensis Cry1Ab and Cry1Ac toxins against maize stem borer (Chilo partellus Swinhoe). Letters in Applied Microbiology 51: 42-47.

Bacillus thuringiensis toxins CryA & CryIV

Trichoplusia ni

Laboratory SIM I - Tabashnik, B. E. (1992). Evaluation of synergism among Bacillus thuringiensis toxins. Applied and Environmental Microbiology 58: 3343-3346.

Bacillus thuringiensis israelensis & Bacillus sphaericus toxins

Mosquito (Culex spp.)

Laboratory SIM I - Wirth, M. C., J. A. Jiannino, et al. (2004). Synergy between toxins of Bacillus thuringiensis subsp israelensis and Bacillus sphaericus. Journal of Medical Entomology 41: 935-941.

Microbial biopesticide (fungus) with microbial biopesticide (fungus)


Beauveria bassiana

Coffee berry borer (Hypothenemus hampei)

Laboratory SIM I & D - Cruz, L. P., A. L. Gaitan, et al. (2006). Exploiting the genetic diversity of Beauveria bassiana for improving the biological control of the coffee berry borer through the use of strain mixtures. Applied Microbiology and Biotechnology 71: 918-926.

- Mosquito Computer simulation

- - - Hancock, P. A., M. B. Thomas, et al. (2009). An age-structured model to evaluate the potential of novel malaria-control

22

interventions: a case study of fungal biopesticide sprays. Proceedings of the Royal Society B-Biological Sciences 276: 71-80.


Tropical bont tick (Amblyomma variegatum)

Laboratory & Field

SIM I & S - Maranga, R. O., G. P. Kaaya, et al. (2005). Effects of combining the fungi Beauveria bassiana and Metarhizium anisopliae on the mortality of the tick Amblyomma variegatum (Ixodidae) in relation to seasonal changes. Mycopathologia 159: 527-532.


Mosquito (Anopheles gambiae)

Laboratory SIM S - Mnyone, L. L., M. J. Kirby, et al. (2009). Infection of the malaria mosquito, Anopheles gambiae, with two species of entomopathogenic fungi: effects of concentration, co-formulation, exposure time and persistence. Malaria Journal 8.

Beauveria bassiana & Nomuraea rileyi

Oriental leafworm (Spodoptera litura)


S - Rao, C. U. M., K. U. Devi, et al. (2006). Effect of combination treatment with entomopathogenic fungi Beauveria bassiana and Nomuraea rileyi (Hypocreales) on Spodoptera litura (Lepidoptera : Noctuidaeae). Biocontrol Science and Technology 16: 221-232.

Fungus (Metarhizium anisopliae) & nematode (Steinernema feltiae)

Wax moth (Galleria mellonella)

Laboratory - - - Staves, P. A. and R. J. Knell (2010). Virulence and competitiveness: testing the relationship during inter- and intraspecific mixed infections. Evolution 64: 2643-2652.

Microbial biopesticide (nematode) with microbial biopesticide (nematode)


Nematodes (Steinernema carpocapsae, Steinernema glaseri & Heterorhabditis bacteriophora) & fungus (Beauveria

Ectinohoplia rufipes & Oriental beetle (Exomala orientalis)

Field SIM S - Choo, H. Y., H. K. Kaya, et al. (2002). Entomopathogenic nematodes (Steinernema spp. and Heterorhabditis bacteriophora) and a fungus Beauveria brongniartii for biological control of the white grubs, Ectinohoplia rufipes and Exomala orientalis, in Korean golf courses. Biocontrol 47: 177-192.

23

brongniartii)

Nematodes (Heterorhabditis bacteriophora & Steinernema carpocapsae) & bacterium (Bacillus thuringiensis)

Masked chafer (Cyclocephala hirta), black vine weevil (Otiorhynchus sulcatus) & cabbage looper (Trichoplusia ni)

- SIM I - Kaya, H. K., T. M. Burlando, et al. (1995). Intergration of entomopathogenic nematodes with Bacillus thuringiensis or pesticidal soap for control insect pests. Biological Control 5( 432-441.

Heterorhabditis bacteriophora & Steinernema glaseri

Japanese beetle (Popillia japonica), oriental beetle (Exomala orientalis), masked chafers (Cyclocephala borealis, C. pasadenae & C. hirta)

Glasshouse & field

SIM I - Koppenhofer, A. M., I. M. Brown, et al. (2000). Synergism of entomopathogenic nematodes and imidacloprid against white grubs: Greenhouse and field evaluation. Biological Control 19: 245-251.

Microbial biopesticide (bacteria) with microbial biopesticide (virus)


Bacterium (Bt sweetcorn) & nucleopolyhedroviruses

Fall armyworm (Spodoptera frugiperda)

Field SEQ (plant already has Bt toxins)

I - Farrar, R. R., B. M. Shepard, et al. (2009). Supplemental control of lepidopterous pests on Bt transgenic sweet corn with biologically-based spray treatments. Journal of Insect Science 9.

Virus (granulovirus (TnGV)) & bacterium (Bacillus thuringiensis)

Cabbage looper (Trichoplusia

- - I Virus destroys structural

Granados, R. R., Y. Fu, et al. (2001). Enhancement of Bacillus thuringiensis toxicity to lepidopterous species with the enhancin from Trichoplusia ni granulovirus.

24

ni) integrity of peritrophic membrane

Biological Control 20: 153-159.

Bacterium (Bacillus thuringiensis Cry1 Ac toxin) & nuclear polyhedrosis virus

Cotton bollworm (Helicoverpa armigera)


I, S & D

- Liu, X. X., Q. W. Zhang, et al. (2006). Effects of Cry1 Ac toxin of Bacillus thuringiensis and nuclear polyhedrosis virus of Helicoverpa armigera (Hubner) (Lepidoptera : Noctuidae) on larval mortality and pupation. Pest Management Science 62: 729-737.

Bacterium (Bacillus thuringiensis) & virus (Anagrapha falcifera multiple nucleopolyhedrovirus)

European corn-borer (Ostrinia nubilalis), corn earworm (Helicoverpa tea) & fall armyworm (Spodoptera frugiperda)

Laboratory SIM S & D - Pingel, R. L. and L. C. Lewis (1999). Effect of Bacillus thuringiensis, Anagrapha falcifera multiple nucleopolyhedrovirus, and their mixture on three lepidopteran corn ear pests. Journal of Economic Entomology 92: 91-96.

Bacterium (Bacillus thuringiensis) & virus


Laboratory SIM - - Raymond, B., A. H. Sayyed, et al. (2007). Exploiting pathogens and their impact on fitness costs to manage the evolution of resistance to Bacillus thuringiensis. Journal of Applied Ecology 44: 768-780.

Bacterium (Bacillus thuringiensis) & nucleopolyhedrosis virus


Laboratory SIM D - Raymond, B., A. H. Sayyed, et al. (2006). The compatibility of a nucleopolyhedrosis virus control with resistance management for Bacillus thuringiensis: Co-infection and cross-resistance studies with the diamondback moth, Plutella xylostella. Journal of Invertebrate Pathology 93: 114-120.

Microbial biopesticide (bacteria) with microbial biopesticide (fungus)


Nematode symbiotic bacteria (Photorhabdus luminescens &

- Laboratory SIM D - Ansari, M. A., L. Tirry, et al. (2005). Antagonism between entomopathogenic fungi and bacterial symbionts of entomopathogenic nematodes. Biocontrol 50: 465-475.

25

Xenorhabdus poinarii) & fungi (Metarhizium anisopliae, Beauveria bassiana, B. brongniartii and Paecilomyces fumosoroseus)

Bacterium (Bacillus thuringiensis) & fungus destruxins (Metarhizium anisopliae)

Spruce budworm (Choristoneura fumiferana)

Laboratory SIM I - Brousseau, C., G. Charpentier, et al. (1998). Effects of Bacillus thuringiensis and destruxins (Metarhizium anisopliae mycotoxins) combinations on spruce budworm (Lepidoptera : Tortricidae). Journal of Invertebrate Pathology 72: 262-268.

Bacterium (Bacillus thuringiensis CryIIIA delta-endotoxin) & fungus (Beauveria bassiana)


Laboratory SIM S - Costa, S. D., M. E. Barbercheck, et al. (2001). Mortality of Colorado potato beetle (Leptinotarsa decemlineata) after sublethal stress with the CryIIIA delta-endotoxin of Bacillus thuringiensis and subsequent exposure to Beauveria bassiana. Journal of Invertebrate Pathology 77: 173-179.

Bacterium (Serratia entomophila) & fungus (Metarhizium anisopliae)

New Zealand grass grub (Costelytra zealandica)

Laboratory SIM I - Glare, T. R. (1994). Stage-dependent synergism using Metarhizium anisopliae and Serratia entomophila against Costelytra zealandica. Biocontrol Science and Technology 4: 321-329.

Bacterium (Bacillus thuringiensis) & fungi (Metarhizium anisopliae &


Laboratory SIM I - Kryukov, V. Y., V. P. Khodyrev, et al. (2009). Synergistic Action of entomopathogenic hyphomycetes and the bacteria Bacillus thuringiensis ssp. morrisoni in the infection of Colorado potato beetle Leptinotarsa decemlineata. Applied Biochemistry and Microbiology 45: 511-516.

26

Beauveria bassiana)


European corn borer (Ostrinia nubilalis)

Field SIM (but not tank mixed)

I - Lewis, L. C., E. D. Berry, et al. (1996). Aptness of insecticides (Bacillus thuringiensis and carbofuran) with endophytic Beauveria bassiana, in suppressing larval populations of the European corn borer. Agriculture Ecosystems & Environment 57: 27-34.


House fly (Musca domestica)

Field SIM I - Mwamburi, L. A., M. D. Laing, et al. (2009). "Interaction between Beauveria bassiana and Bacillus thuringiensis var. israelensis for the control of house fly larvae and adults in poultry houses. Poultry Science 88: 2307-2314.

Bacterium (Bacillus thuringiensis) & fungus (Leptolegnia chapmanii)

Mosquito (Aedes aegypti)

Field (simulated)

SIM I - Pelizza, S. A., A. C. Scorsetti, et al. (2010). Individual and combined effects of Bacillus thuringiensis var. israelensis, temephos and Leptolegnia chapmanii on the larval mortality of Aedes aegypti. Biocontrol 55: 647-656.





Bacterium (Bacillus thuringiensis) & fungus (Beauveria bassiana)


Field SIM I Wraight, S. P. and M. E. Ramos (2005). Synergistic interaction between Beauveria bassiana- and Bacillus thuringiensis tenebrionis-based biopesticides applied against field populations of Colorado potato beetle larvae. Journal of Invertebrate Pathology 90: 139-150.

Microbial biopesticide (bacteria) with microbial biopesticide (nematode)


27

Nematodes (Steinernema carpocapsae & Heterorhabditis bacteriophora) & bacteria (Photorhabdus luminescens & Xenorhabdu nematophilus)

African cotton leafworm (Spodoptera littoralis)

Laboratory - - - Abdel-Razek, A. (2006). Infectivity prospects of both nematodes and bacterial symbionts against cotton leafworm, Spodoptera littoralis (Biosduval) (Lepidoptera : Noctuidae). Journal of Pest Science 79: 11-15.

Nematode (Steinernema carpocapsae) & bacterium (Bacillus thuringiensis)


Laboratory & field

SIM D & S - Baur, M. E., H. K. Kaya, et al. (1998). Suppression of diamondback moth (Lepidoptera : Plutellidae) with an entomopathogenic nematode (Rhabditida : Steinernematidae) and Bacillus thuringiensis Berliner." Journal of Economic Entomology 91: 1089-1095.

Bacterium (Bacillus thuringiensis toxin) & nematode (Steinernema riobrave)

Pink bollworm (Pectinophora gossypiella)

Laboratory - I - Gassmann, A. J., S. P. Stock, et al. (2006). Effect of entomopathogenic nematodes on the fitness cost of resistance to Bt toxin Cry1Ac in pink bollworm (Lepidoptera : Gelechiidae). Journal of Economic Entomology 99: 920-926.

Bt crop (Bacillus thuringiensis) & nematodes (Steinernema riobrave & Heterorhabditis bacteriophora)

- - - - - Gassmann, A. J., S. P. Stock, et al. (2008). Synergism between entomopathogenic nematodes and Bacillus thuringiensis crops: integrating biological control and resistance management. Journal of Applied Ecology 45: 957-966.

Bacterium (Bacillus thuringiensis) & nematode (species ?)

Masked chafers (Cyclocephala hirta & C. pasadenae) & Anomala orientalis

Laboratory SEQ I - Koppenhofer, A. M., H. Y. Choo, et al. (1999). Increased field and greenhouse efficacy against scarab grubs with a combination of an entomopathogenic nematode and Bacillus thuringiensis. Biological Control 14: 37-44.

28

Bacterium (Bacillus thuringiensis) & nematodes (Heterorhabditis bacteriophora, Steinernema glaseri & S. kushidai)

Masked chafers (Cyclocephala hirta & C. pasadenae)


I & S - Koppenhofer, A. M. and H. K. Kaya (1997). Additive and synergistic interaction between entomopathogenic nematodes and Bacillus thuringiensis for scarab grub control. Biological Control 8: 131-137.

Nematodes (Steinernema carpocapsae & S. feltiae) & bacterium (Bacillus thuringiensis)

Crane fly (Tipula paludosa)

Laboratory & field

SIM I & S - Oestergaard, J., C. Belau, et al. (2006). Biological control of Tipula paludosa (Diptera: Nematocera) using entomopathogenic nematodes (Steinernema spp.) and Bacillus thuringiensis subsp israelensis. Biological Control 39: 525-531.

Nematodes (Steinernema carpocapsae) & bacterium (Bacillus thuringiensis)


Field SIM & SEQ

S - Schroer, S., D. Sulistyanto, et al. (2005). Control of Plutella xylostella using polymer-formulated Steinernema carpocapsae and Bacillus thuringiensis in cabbage fields. Journal of Applied Entomology 129: 198-204.

Nematodes (Heterorhabditis indica & Steinernema carpocapsae), fungi (Beauveria bassiana & Metarhizium anisopliae) & bacterium (Serratia marcescens)

Pecan weevil (Curculio caryae)

Laboratory SIM I (only one combination) & D

- Shapiro-Ilan, D. I., M. Jackson, et al. (2004). Effects of combining an entomopathogenic fungi or bacterium with entomopathogenic nematodes on mortality of Curculio caryae (Coleoptera: Curculionidae). Biological Control 30: 119-126.

Microbial biopesticide (virus) with microbial biopesticide (fungus)

29


Nucleopolyhedrovirus & fungus (Entomophaga maimaiga)

Gypsy moth (Lymantria dispar)

Field - S Different life-stage

Malakar, R., J. S. Elkinton, et al. (1999). Interactions between two gypsy moth (Lepidoptera : Lymantriidae) pathogens: Nucleopolyhedrovirus and Entomophaga maimaiga (Zygomycetes : Entomophthorales): Field studies and a simulation model. Biological Control 16: 189-198.

Nucleopolyhedrovirus & fungus (Entomophaga maimaiga)

Gypsy moth (Lymantria dispar)


- - Malakar, R., J. S. Elkinton, et al. (1999). Within-host interactions of Lymantria dispar (Lepidoptera: Lymantriidae) nucleopolyhedrosis virus and Entomophaga maimaiga (Zygomycetes: Entomophthorales). Journal of Invertebrate Pathology 73: 91-100.

Microbial biopesticide (fungus) with microbial biopesticide (nematode)


Nematode (Hetrorhabditis bacteriophora) & fungus (Metarhizium anisopliae)

Sugar cane borer (Diatraea saccharalis)

Laboratory SIM I (faster time of death but reduced number of infective juveniles)

- Acevedo, J. P. M., R. I. Samuels, et al. (2007). Interactions between isolates of the entomopathogenic fungus Metarhizium anisopliae and the entomopathogenic nematode Heterorhabditis bacteriophora JPM4 during infection of the sugar cane borer Diatraea saccharalis (Lepidoptera : Pyralidae). Journal of Invertebrate Pathology 96: 187-192.

Nematode (Hetrorhabditis bacteriophora & Steinernema yirgalemense) & fungus (Metarhizium anisopliae & Beauveria bassiana)

Barley chafer (Coptognathus curtipennis)

Laboratory SIM & SEQ for Hetrorhabditis bacteriophora & Metarhizium anisopliae

I - Anbesse, S. A., B. J. Adge, et al. (2008). Laboratory screening for virulent entomopathogenic nematodes (Heterorhabditis bacteriophora and Steinernema yirgalemense) and fungi (Metarhizium anisopliae and Beauveria bassiana) and assessment of possible synergistic effects of combined use against grubs of the barley chafer Coptognathus curtipennis. Nematology 10: 701-709.

Nematodes (Heterorhabditis

Black vine weevil

Laboratory &

SIM & SEQ I - Ansari, M. A., F. A. Shah, et al. (2008). Combined use of entomopathogenic nematodes and

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bacteriophora, Steinernema feltiae & Steinernema kraussei ) & fungus (Metarhizium anisopliae)

(Otiorhynchus sulcatus)

glasshouse Metarhizium anisopliae as a new approach for black vine weevil, Otiorhynchus sulcatus, control. Entomologia Experimentalis et Applicata 129: 340-347.

Nematodes (Steinernema kraussei ) & fungus (Metarhizium anisopliae)


Glasshouse SIM I - Ansari, M. A., F. A. Shah, et al. (2010). The entomopathogenic nematode Steinernema kraussei and Metarhizium anisopliae work synergistically in controlling overwintering larvae of the black vine weevil, Otiorhynchus sulcatus, in strawberry growbags. Biocontrol Science and Technology 20: 99-105.

Nematodes (Heterorhabditis bacteriophora) & fungus (Metarhizium anisopliae)

Welsh chafer (Hoplia philanthus)

Field SIM I - Ansari, M. A., F. A. Shah, et al. (2006). Field trials against Hoplia philanthus (Coleoptera: Scarabaeidae) with a combination of an entomopathogenic nematode and the fungus Metarhizium anisopliae CLO 53. Biological Control 39: 453-459.

Nematodes (Heterorhabditis megidis & Steinernema glaseri) & fungus (Metarhizium anisopliae)

Welsh chafer (Hoplia philanthus)

Laboratory & glasshouse

SIM & SEQ I (but some negative effects on nematode reproduction)

- Ansari, M. A., L. Tirry, et al. (2004). Interaction between Metarhizium anisopliae CLO 53 and entomopathogenic nematodes for the control of Hoplia philanthus. Biological Control 31: 172-180.

Nematodes (Steinernema carpocapsae & Heterorhabditis bacteriophora)


Laboratory SIM I - Barbercheck, M. E. and H. K. Kaya (1991). Competitive interactions between entomopathogenic nematodes and Beauveria bassiana (Deuteromycotina, hyphomycetes) in soilborne larvae of Spodoptera exigua (Lepidioptera, Noctuidae). Environmental Entomology 20: 707-712.

Nematodes (Steinernema

Ectinohoplia rufipes &

Field SIM I - Choo, H. Y., H. K. Kaya, et al. (2002). Entomopathogenic nematodes (Steinernema spp.

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carpocapsae, Steinernema glaseri & Heterorhabditis bacteriophora) & fungus (Beauveria brongniartii)

Oriental beetle (Exomala orientalis)

and Heterorhabditis bacteriophora) and a fungus Beauveria brongniartii for biological control of the white grubs, Ectinohoplia rufipes and Exomala orientalis, in Korean golf courses. Biocontrol 47: 177-192.

Nematodes (Heterorhabditis indica & Steinernema carpocapsae), fungi (Beauveria bassiana & Metarhizium anisopliae) & bacterium (Serratia marcescens)

Pecan weevil (Curculio caryae)

Laboratory SIM I (only one combination) & D

- Shapiro-Ilan, D. I., M. Jackson, et al. (2004). Effects of combining an entomopathogenic fungi or bacterium with entomopathogenic nematodes on mortality of Curculio caryae (Coleoptera : Curculionidae). Biological Control 30: 119-126.

Fungus (Metarhizium anisopliae) & nematode (Steinernema feltiae)


Laboratory - - - Staves, P. A. and R. J. Knell (2010). Virulence and competitiveness: testing the relationship during inter- and intraspecific mixed infections." Evolution 64: 2643-2652.

Fungi (Lecanicillium muscarium, Paecilomyces fumosoroseus & Beauveria bassiana) & nematodes (Steinernema feltiae & Heterorhabditis bacteriophora)

Onion thrips (Thrips tabaci)

Field SIM I - Jung, K. (2008) Biological control of Thrips tabaci in the field – possibilities and practical limits. Insect Pathogens and Insect Parasitic Nematodes. IOBC/wprs Bulletin Vol. 31: 344-348.

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Bacterium (Beauveria bassiana) & nematode (Heterorhabditis indica)


Laboratory SEQ D - Dar-Issa, O. M., N. M. Iraki et al. (2003) Effect of Beauveria bassiana on the invasion and proliferation of the entomopathogenic nematode Heterorhabditis indica inside Galleria mellonella larvae. Insect Pathogens and Insect Parasitic Nematodes. IOBC/wprs Bulletin Vol. 26: 169-172.

Part 3: interactions between microbial biopesticides & other materials

MCA Chemical/material pest scale strategy Result Mechanism? Reference

Beauveria bassiana Diatomaceous earth

Flour beetle (Tribolium castaneum)

Laboratory SIM I Diatomaceous earth damages insect cuticle

Akbar, W., J. C. Lord, et al. (2004). Diatomaceous earth increases the efficacy of Beauveria bassiana against Tribolium castaneum larvae and increases conidia attachment. Journal of Economic Entomology 97: 273-280.

Beauveria bassiana Neem tree extract Onion thrips (Thrips tabaci)

Glasshouse SIM I & D Method of application and dose important

Al-mazra'awi, M. S., A. Al-Abbadi, et al. (2009). Effect of application method on the interaction between Beauveria bassiana and neem tree extract when combined for Thrips tabaci (Thysanoptera: Thripidae) control. Journal of Food Agriculture & Environment 7: 869-873.

Bacillus thuringiensis Zwittermicin A Gypsy moth (Lymantria dispar)

Glasshouse SIM I - Broderick, N. A., R. M. Goodman, et al. (2000). Synergy between zwittermicin A and Bacillus thuringiensis subsp kurstaki against gypsy moth (Lepidoptera : Lymantriidae)." Environmental Entomology 29: 101-107.

Nucleopolyhedrovirus (SfMNPV)

Phagostimulant Fall armyworm (Spodoptera frugiperda)

Glasshouse & field

SIM I - Castillejos, V., J. Trujillo, et al. (2002). Granular phagostimulant nucleopolyhedrovirus formulations for control of Spodoptera frugiperda in maize. Biological Control 24: 300-310.

Nucleopolyhedrovirus (SfMNPV)

Phagostimulants & viral synergists

Fall armyworm Spodoptera

Laboratory & field

SIM I - Cisneros, J., J. A. Perez, et al. (2002). Formulation of a nucleopolyhedrovirus with boric acid for control of Spodoptera frugiperda

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frugiperda (Lepidoptera: Noctuidae) in maize. Biological Control 23: 87-95.

Beauveria bassiana Potassium silicate Two-spotted spider mite (Tetranychus urticae)

Glasshouse SEQ I - Gatarayiha, M. C., M. D. Laing, et al. (2010). Combining applications of potassium silicate and Beauveria bassiana to four crops to control two spotted spider mite, Tetranychus urticae Koch. International Journal of Pest Management 56: 291-297.

- - - - - - - Gentz, M. C., G. Murdoch, et al. (2010). Tandem use of selective insecticides and natural enemies for effective, reduced-risk pest management. Biological Control 52: 208-215.

Bacillus thuringiensis Optical brightners Cotton bollworm (Helicoverpa armigera)

Laboratory SIM I, S & D

- Ibargutxi, M. A., D. Munoz, et al. (2008). Effects of stilbene optical brighteners on the insecticidal activity of Bacillus thuringiensis and a single nucleopolyhedrovirus on Helicoverpa armigera. Biological Control 47: 322-327.

Beauveria bassiana Diatomaceous earth

Stored grain beetles (Rhyzopertha dominica & Oryzaephilus surinamensis)

Laboratory SIM I - Lord, J. C. (2001). Desiccant dusts synergize the effect of Beauveria bassiana (Hyphomycetes: Moniliales) on stored-grain beetles. Journal of Economic Entomology 94: 367-372.


Oils Glasshouse whitefly (Trialeurodes vaporariorum) & tobacco whitefly (Bemisia tabaci)

- SIM I - Malsam, O., M. Kilian, et al. (2002). Oils for increased efficacy of Metarhizium anisopliae to control whiteflies. Biocontrol Science and Technology 12: 337-348.


Diatomaceous earth

Flour beetle (Tribolium confusum)

Laboratory SIM I & S - Michalaki, M. P., C. G. Athanassiou, et al. (2006). Effectiveness of Metarhizium anisopliae (Metschinkoff) Sorokin applied alone or in combination with diatomaceous earth against Tribolium confusum Du Val

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larvae: Influence of temperature, relative humidity and type of commodity. Crop Protection 25: 418-425.

Bacillus thuringiensis Plant cysteine protease

Corn earworm (Helicoverpa tea) & fall armyworm (Spodoptera frugiperda), tobacco budworm (Heliothis viriscens), southwestern corn borer (Diatraea grandiosella)

Laboratory SIM I Disruption of midgut

Mohan, S., P. W. K. Ma, et al. (2008). A naturally occurring plant cysteine protease possesses remarkable toxicity against insect pests and synergizes Bacillus thuringiensis toxin." Plos One 3(3).

Biopesticide Insecticide Mosquito - - - - Read, A. F., P. A. Lynch, et al. (2009). How to make evolution-proof insecticides for malaria control. Plos Biology 7(4).

Entomopathogenic fungi

- Mosquito - - - - Scholte, E. J., B. G. J. Knols, et al. (2004). Entomopathogenic fungi for mosquito control: A review. Journal of Insect Science 4.

Steinernema carpocapsae

Adjuvants Diamondback moth (Plutella xylostella)

Laboratory SIM I - Schroer, S., X. L. Yi, et al. (2005). Evaluation of adjuvants for foliar application of Steinernema carpocapsae against larvae of the diamondback moth (Plutella xylostella). Nematology 7: 37-44.

Nucleopolyhedrovirus Optical brightners Corn earworm (Helicoverpa tea)

Laboratory SIM I & S - Shapiro, M. and R. R. Farrar (2003). Fluorescent brighteners affect feeding rates of the corn earworm (Lepidoptera : Noctuidae) and act as enhancers and sunlight protectants for its nucleopolyhedrovirus. Journal of Entomological Science 38: 286-299.

Nucleopolyhedrovirus Optical brightners Gypsy moth (Lymantria dispar)

Field & laboratory

SIM I - Thorpe, K. W., S. P. Cook, et al. (1999). Aerial application of the viral enhancer Blankophor BBH with reduced rates of gypsy

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moth (Lepidoptera : Lymantriidae) nucleopolyhedrovirus. Biological Control 16: 209-216.


Microsporidian (Paranosema locustae)

Desert locust (Schistocerca gregaria)

Laboratory SIM I - Tounou, A. K., C. Kooyman, et al. (2008). Interaction between Paranosema locustae and Metarhizium anisopliae var. acridum, two pathogens of the desert locust, Schistocerca gregaria under laboratory conditions. Journal of Invertebrate Pathology 97: 203-210.

Bacillus thuringiensis Avidin Corn earworm (Helicoverpa zea), beet armyworm (Spodoptera exigua) & velvetbean caterpillar (Anticarsia gemmatalis)

Laboratory SIM I - Zhu, Y. C., J. J. Adamczyk, et al. (2005). Avidin, a potential biopesticide and synergist to Bacillus thuringiensis toxins against field crop insects. Journal of Economic Entomology 98: 1566-1571.


Boric acid German cockroach (Blattella germanica)

Laboratory SIM I - Zurek, L., D. W. Watson, et al. (2002). Synergism between Metarhizium anisopliae (Deuteromycota : Hyphomycetes) and boric acid against the German cockroach (Dictyoptera : Blattellidae). Biological Control 23: 296-302.

Table 1. Entomopathogen modes of action. Biopesticide Mode of...

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