The sublethal effects of pesticides on beneficial arthropods.

Traditionally, measurement of the acute toxicity of pesticides to beneficial arthropods has relied largely on the determination of an acute median lethal dose or concentration. However, the estimated lethal dose during acute toxicity tests may only be a partial measure of the deleterious effects. In addition to direct mortality induced by pesticides, their sublethal effects on arthropod physiology and behavior must be considered for a complete analysis of their impact. An increasing number of studies and methods related to the identification and characterization of these effects have been published in the past 15 years. Review of sublethal effects reported in published literature, taking into account recent data, has revealed new insights into the sublethal effects of pesticides including effects on learning performance, behavior, and neurophysiology. We characterize the different types of sublethal effects on beneficial arthropods, focusing mainly on honey bees and natural enemies, and we describe the methods used in these studies. Finally, we discuss the potential for developing experimental approaches that take into account these sublethal effects in integrated pest management and the possibility of integrating their evaluation in pesticide registration procedures.

[1]  L. Kaiser,et al.  A multi-step bioassay to assess the effect of the deltamethrin on the parasitic wasp Aphidius ervi. , 2006, Chemosphere.

[2]  L. Kaiser,et al.  Multistep bioassay to predict recolonization potential of emerging parasitoids after a pesticide treatment , 2006, Environmental toxicology and chemistry.

[3]  S. Fahrbach Structure of the mushroom bodies of the insect brain. , 2006, Annual review of entomology.

[4]  M. Dacher,et al.  Effects of sublethal doses of fipronil on the behavior of the honeybee (Apis mellifera) , 2005, Pharmacology Biochemistry and Behavior.

[5]  C. Bardon,et al.  Increase of the Behavioral Response to Kairomones by the Parasitoid Wasp Leptopilina heterotoma Surviving Insecticides , 2005, Archives of environmental contamination and toxicology.

[6]  W. Hutchison,et al.  Effects of spinosad and indoxacarb on survival, development, and reproduction of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) , 2005 .

[7]  M. Dicke,et al.  Impact of botanical pesticides derived from Melia azedarach and Azadirachta indica on the biology of two parasitoid species of the diamondback moth , 2005 .

[8]  L. Bortolotti,et al.  Action of fenoxycarb on metamorphosis and cocoon spinning in Chrysoperla carnea (Neuroptera: Chrysopidae): identification of the JHA-sensitive period , 2005 .

[9]  J. Devillers,et al.  Comparative Sublethal Toxicity of Nine Pesticides on Olfactory Learning Performances of the Honeybee Apis mellifera , 2005, Archives of environmental contamination and toxicology.

[10]  L. Kaiser,et al.  Diaeretiella rapae limits Myzus persicae populations after applications of deltamethrin in oilseed rape. , 2005, Journal of economic entomology.

[11]  Christine Woodcock,et al.  Activity of quassinoids as antifeedants against aphids , 1989, Journal of Chemical Ecology.

[12]  M. Saber,et al.  Lethal and Sublethal Effects of Fenitrothion and Deltamethrin Residues on the Egg Parasitoid Trissolcus grandis (Hymenoptera: Scelionidae) , 2005 .

[13]  Paul Schmid-Hempel,et al.  Evolutionary ecology of insect immune defenses. , 2005, Annual review of entomology.

[14]  J. Taséi,et al.  Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae , 2005 .

[15]  P. J. Edward George,et al.  Impact of insecticides on the haemogram of Rhynocoris kumarii Ambrose and Livingstone (Hem., Reduviidae) , 2004 .

[16]  M. Campos,et al.  Populations, longevity, mortality and fecundity of Chrysoperla carnea (Neuroptera, Chrysopidae) from olive-orchards with different agricultural management systems. , 2004, Chemosphere.

[17]  J. Stark,et al.  Effects of the agricultural adjuvant Sylgard 309 and the insecticide pymetrozine on demographic parameters of the aphid parasitoid, Diaeretiella rapae , 2004 .

[18]  G. Smagghe,et al.  Action of insect growth regulator insecticides and spinosad on life history parameters and absorption in third-instar larvae of the endoparasitoid Hyposoter didymator , 2004 .

[19]  R. Schmuck Effects of a Chronic Dietary Exposure of the Honeybee Apis mellifera (Hymenoptera: Apidae) to Imidacloprid , 2004, Archives of environmental contamination and toxicology.

[20]  C. Gaimon,et al.  A Method to Quantify and Analyze the Foraging Activity of Honey Bees: Relevance to the Sublethal Effects Induced by Systemic Insecticides , 2004, Archives of environmental contamination and toxicology.

[21]  L. Kaiser,et al.  Oviposition behaviour and patch‐time allocation in two aphid parasitoids exposed to deltamethrin residues , 2004 .

[22]  K. Takasu,et al.  Effects of selective insecticides on host searching and oviposition behavior of Neochrysocharis formosa(Westwood)(Hymenoptera: Eulophidae), a larval parasitoid of the American serpentine leafminer , 2004 .

[23]  Tong‐Xian Liu,et al.  Lethal and sublethal effects of two insect growth regulators on adult Delphastus catalinae (Coleoptera: Coccinellidae), a predator of whiteflies (Homoptera: Aleyrodidae) , 2004 .

[24]  K. Walters,et al.  Consumption rates and predatory activity of adult and fourth instar larvae of the seven spot ladybird, Coccinella septempunctata (L.), following contact with dimethoate residue and contaminated prey in laboratory arenas , 2004 .

[25]  J. Stark,et al.  Toxicity of Spinosad in Protein Bait to Three Economically Important Tephritid Fruit Fly Species (Diptera: Tephritidae) and Their Parasitoids (Hymenoptera: Braconidae) , 2004, Journal of economic entomology.

[26]  The Effect of Insecticides Considered Harmless to Honey Bees (Apis mellifera): Proboscis Conditioning Studies by Using the Insect Growth Regulators Tebufenozide and Diflubenzuron , 2004 .

[27]  Nicolas Desneux,et al.  Effects of sub-lethal and lethal doses of lambda-cyhalothrin on oviposition experience and host-searching behaviour of a parasitic wasp, Aphidius ervi. , 2004, Pest management science.

[28]  James Devillers,et al.  Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. , 2004, Ecotoxicology and environmental safety.

[29]  P. D. del Estal,et al.  Influence of Azadirachtin, a Botanical Insecticide, on Chrysoperla carnea (Stephens) Reproduction: Toxicity and Ultrastructural Approach , 2004, Journal of economic entomology.

[30]  N. Desneux,et al.  Dose-response relationship in lethal and behavioural effects of different insecticides on the parasitic wasp Aphidius ervi. , 2004, Chemosphere.

[31]  J. Devillers,et al.  Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.) , 2004 .

[32]  W. Jones Sex ratio and host size in a parasitoid wasp , 1982, Behavioral Ecology and Sociobiology.

[33]  Axel Decourtye,et al.  Statistical analysis of honeybee survival after chronic exposure to insecticides , 2003, Environmental toxicology and chemistry.

[34]  John E Banks,et al.  Population-level effects of pesticides and other toxicants on arthropods. , 2003, Annual review of entomology.

[35]  M. Ahmad,et al.  Effects of neem‐treated aphids as food/hosts on their predators and parasitoids , 2003 .

[36]  G. Smagghe,et al.  Toxicity and Pharmacokinetics of Insect Growth Regulators and Other Novel Insecticides on Pupae of Hyposoter didymator (Hymenoptera: Ichneumonidae), a Parasitoid of Early Larval Instars of Lepidopteran Pests , 2003 .

[37]  R. Guedes,et al.  Permethrin-induced hormesis on the predator Supputius cincticeps (Stål, 1860) (Heteroptera: Pentatomidae) , 2003 .

[38]  J. Delpuech,et al.  Reduction in the Sex Ratio of the Progeny of a Parasitoid Wasp (Trichogramma brassicae) Surviving the Insecticide Chlorpyrifos , 2003, Archives of environmental contamination and toxicology.

[39]  D. Goulson,et al.  Impact of a Nucleopolyhedrovirus Bioinsecticide and Selected Synthetic Insecticides on the Abundance of Insect Natural Enemies on Maize in Southern Mexico , 2003, Journal of economic entomology.

[40]  A. Decourtye,et al.  Learning performances of honeybees (Apis mellifera L) are differentially affected by imidacloprid according to the season. , 2003, Pest management science.

[41]  G. Amdam,et al.  Social exploitation of vitellogenin , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[42]  D. Ambrose,et al.  Impact of cypermethrin on the functional response, predatory and mating behaviour of a non‐target potential biological control agent Acanthaspis pedestris (Stål) (Het., Reduviidae) , 2003 .

[43]  H. Thompson Behavioural Effects of Pesticides in Bees–Their Potential for Use in Risk Assessment , 2003, Ecotoxicology.

[44]  François-Xavier Dechaume-Moncharmont Butinage collectif chez l'abeille Apis mellifera L. : étude théorique et expérimentale , 2003 .

[45]  J. Tautz,et al.  Automatic life-long monitoring of individual insect behaviour now possible. , 2003, Zoology.

[46]  J. Todd,et al.  Effects of ingestion of a biotin-binding protein on adult and larval honey bees , 2002 .

[47]  Don R. Reynolds,et al.  Remote-sensing, telemetric and computer-based technologies for investigating insect movement: a survey of existing and potential techniques , 2002 .

[48]  G. Salerno,et al.  Sub-lethal effects of deltamethrin on walking behaviour and response to host kairomone of the egg parasitoid Trissolcus basalis. , 2002, Pest management science.

[49]  R. S. Thorn,et al.  Effects of Acute Sublethal Exposure to Coumaphos or Diazinon on Acquisition and Discrimination of Odor Stimuli in the Honey Bee (Hymenoptera: Apidae) , 2002, Journal of economic entomology.

[50]  L. Kaiser,et al.  Stimulating effects of the insecticide chlorpyrifos on host searching and infestation efficacy of a parasitoid wasp. , 2002, Pest management science.

[51]  H. Amano,et al.  Effects of contact, oral and persistent toxicity of selected pesticides on Cotesia plutellae (Hym., Braconidae), a potential parasitoid of Plutella xylostella (Lep., Plutellidae) , 2002 .

[52]  J. Devillers,et al.  Effects of imidacloprid on the neural processes of memory in honey bees. , 2002 .

[53]  J. Devillers,et al.  The proboscis extension response: assessing the sublethal effects of pesticides on the honey bee. , 2002 .

[54]  R. Gooneratne,et al.  Sublethal responses of wolf spiders (Lycosidae) to organophosphorous insecticides , 2002, Environmental toxicology.

[55]  M. A. Al-Deeb,et al.  Effect of Insecticides Used in Corn, Sorghum, and Alfalfa on the Predator Orius insidiosus (Hemiptera: Anthocoridae) , 2001, Journal of economic entomology.

[56]  Tong‐Xian Liu,et al.  EFFECTS OF THE INSECT GROWTH REGULATOR FENOXYCARB ON IMMATURE CHRYSOPERLA RUFILABRIS (NEUROPTERA: CHRYSOPIDAE) , 2001 .

[57]  P. Fouillet,et al.  Modification, by the Insecticide Chlorpyrifos, of the Behavioral Response to Kairomones of a Parasitoid Wasp, Leptopilina boulardi , 2001, Archives of environmental contamination and toxicology.

[58]  M. Lambin,et al.  Imidacloprid-induced facilitation of the proboscis extension reflex habituation in the honeybee. , 2001, Archives of insect biochemistry and physiology.

[59]  A. Cortesero,et al.  Selectivity assessment of chlorfenvinphos reevaluated by including physiological and behavioral effects on an important beneficial insect , 2001, Environmental toxicology and chemistry.

[60]  L. Belzunces,et al.  Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera , 2001, Environmental toxicology and chemistry.

[61]  B. Qi,et al.  Effects of Neem-Fed Prey on the Predacious Insects Harmonia conformis (Boisduval) (Coleoptera: Coccinellidae) and Mallada signatus (Schneider) (Neuroptera: Chrysopidae) , 2001 .

[62]  E. Beers,et al.  Effect of Pesticides on Colpoclypeus florus (Hymenoptera: Eulophidae) and Trichogramma platneri (Hymenoptera: Trichogrammatidae), Parasitoids of Leafrollers in Washington , 2001, Journal of economic entomology.

[63]  R. Maleszka,et al.  Contrasting Effects of Imidacloprid on Habituation in 7- and 8-Day-Old Honeybees (Apis mellifera) , 2001, Neurobiology of Learning and Memory.

[64]  P. Fouillet,et al.  Partial compensation of the sublethal effect of deltamethrin on the sex pheromonal communication of Trichogramma brassicae. , 2001, Chemosphere.

[65]  G. Theophilidis,et al.  The cardiotoxic action of the pyrethroid insecticide deltamethrin, the azole fungicide prochloraz, and their synergy on the semi-isolated heart of the bee Apis mellifera macedonica , 2001 .

[66]  D. Potter,et al.  Lethal and Sublethal Effects of Bendiocarb, Halofenozide, and Imidacloprid on Harpalus pennsylvanicus (Coleoptera: Carabidae) Following Different Modes of Exposure in Turfgrass , 2001, Journal of economic entomology.

[67]  J. Taséi,et al.  Sub‐lethal effects of imidacloprid on bumblebees, Bombus terrestris (Hymenoptera: Apidae), during a laboratory feeding test , 2000 .

[68]  M. Vighi,et al.  Risk Assessment for Honeybees from Pesticide-Exposed Pollen , 2000 .

[69]  T. P. Hutchinson Graphing the survivorship of bees , 2000, Insectes Sociaux.

[70]  Functional cytochrome oxidase histochemistry in the honeybee brain , 2000, Brain Research.

[71]  W. J. Lewis,et al.  Disruptive Sublethal Effects of Insecticides on Biological Control: Altered Foraging Ability and Life Span of a Parasitoid after Feeding on Extrafloral Nectar of Cotton Treated with Systemic Insecticides , 2000 .

[72]  Z. Simões,et al.  Inhibition of vitellogenin synthesis in Apis mellifera workers by a juvenile hormone analogue, pyriproxyfen. , 2000, Journal of insect physiology.

[73]  M. V. Srinivasan,et al.  Honeybee Memory: Navigation by Associative Grouping and Recall of Visual Stimuli , 1999, Neurobiology of Learning and Memory.

[74]  R. Menzel Memory dynamics in the honeybee , 1999, Journal of Comparative Physiology A.

[75]  E. Pilling,et al.  Sensitivity of non-target arthropods to plant protection products: Could Typhlodromus pyri and Aphidius spp. be used as indicator species? , 1999 .

[76]  C. Fléché,et al.  Toxicity of cypermethrin and fenitrothion on the hemolymph carbohydrates, head acetylcholinesterase, and thoracic muscle Na+, K+-ATPase of emerging honeybees (Apis mellifera mellifera. L). , 1999, Ecotoxicology and environmental safety.

[77]  P. E. George,et al.  Insecticidal impact on the post‐embryonic development of Rhynocoris kumarii Ambrose and Livingstone (Het., Reduviidae) , 1999 .

[78]  P. Calow,et al.  Is the per capita rate of increase a good measure of population‐level effects in ecotoxicology? , 1999 .

[79]  Peter G. Kevan,et al.  Pollinators as bioindicators of the state of the environment: species, activity and diversity , 1999 .

[80]  W. J. Lewis,et al.  A comparison of color-, shape- and pattern-learning by the hymenopteran parasitoid Microplitis croceipes , 1999, Journal of Comparative Physiology A.

[81]  J. Stark,et al.  Importance of population structure at the time of toxicant exposure. , 1999, Ecotoxicology and environmental safety.

[82]  Terrier,et al.  Modifications of the sex pheromonal communication of trichogramma brassicae by a sublethal dose of deltamethrin , 1999, Chemosphere.

[83]  D. Mayer,et al.  Field and laboratory tests of the effects of fipronil on adult female bees of Apis mellifera, Megachile rotundata and Nomia melanderi , 1999 .

[84]  L. Belzunces,et al.  Joint actions of deltamethrin and azole fungicides on honey bee thermoregulation , 1998, Neuroscience Letters.

[85]  F. Pompanon,et al.  Inhibition of sex pheromone communications of Trichogramma brassicae (Hymenoptera) by the insecticide chlorpyrifos , 1998 .

[86]  P. Fouillet,et al.  Sublethal effects of the insecticide chlorpyrifos on the sex pheromonal communication of Trichogramma brassicae , 1998 .

[87]  J. Stark,et al.  Multiple routes of pesticide exposure and the risk of pesticides to biological controls : A study of neem and the sevenspotted lady beetle (Coleoptera: Coccinellidae) , 1998 .

[88]  D. Dietrich,et al.  Effects of Conventional Insecticides and Insect Growth Regulators on Fecundity and Other Life-Table Parameters of Micromus tasmaniae (Neuroptera: Hemerobiidae) , 1998 .

[89]  S. A. Hassan,et al.  Side‐effects of insecticides used in tomato fields on the egg parasitoid Trichogramma pretiosum Riley (Hym., Trichogrammatidae), a natural enemy of Tuta absoluta (Meyrick) (Lep., Gelechiidae) , 1998 .

[90]  T S Dhadialla,et al.  New insecticides with ecdysteroidal and juvenile hormone activity. , 1998, Annual review of entomology.

[91]  J. Stark,et al.  Comparison of two population‐level ecotoxicological endpoints: The intrinsic (rm) and instantaneous (ri) rates of increase , 1997 .

[92]  G. Hamilton,et al.  Effect of Insecticides on Two Predators of the Colorado Potato Beetle (Coleoptera: Chrysomelidae) , 1997 .

[93]  P. Visscher,et al.  Survivorship of foraging honey bees , 1997, Insectes Sociaux.

[94]  C. Frampton,et al.  Lacewings (Neuroptera: Hemerobiidae and Chrysopidae) and Integrated Pest Management: Enzyme Activity as Biomarker of Sublethal Insecticide Exposure , 1997 .

[95]  C. Abramson,et al.  Task-Dependent Effects of Dicofol (Kelthane) on Learning in the Honey Bee (Apis mellifera) , 1997, Bulletin of environmental contamination and toxicology.

[96]  F. Frey,et al.  Action of insecticides on the cellular immune reaction of Drosophila melanogaster against the parasitoid Leptopilina boulardi , 1996 .

[97]  P. Jepson,et al.  The influence of insecticide residues on primary parasitoid and hyperparasitoid foraging behaviour in the laboratory , 1996 .

[98]  P. Jepson,et al.  Effects of honeydew and insecticide residues on the distribution of foraging aphid parasitoids under glasshouse and field conditions , 1996 .

[99]  S. Clark,et al.  Effect of pirimicarb on the foraging behaviour of Diaeretiella rapae (Hymenoptera: Braconidae) on host-free and infested oilseed rape plants , 1996 .

[100]  Mark A. Jervis,et al.  The Life-cycle , 1996 .

[101]  R. Menzel,et al.  Learning and memory in honeybees: from behavior to neural substrates. , 1996, Annual review of neuroscience.

[102]  P. Jepson,et al.  The toxic effects of direct pesticide exposure for a nontarget weed-dwelling chrysomelid beetle (Gastrophysa polygoni) in cereals , 1995 .

[103]  L. Belzunces,et al.  Alteration of the homing‐flight in the honey bee Apis mellifera L. Exposed to sublethal dose of deltamethrin , 1995 .

[104]  A. Dinter,et al.  Side‐effects of insecticides on two erigonid spider species , 1995 .

[105]  C. Walker,et al.  Mechanism of synergism between the pyrethroid insecticide λ-cyhalothrin and the imidazole fungicide prochloraz, in the honeybee (Apis mellifera L.) , 1995 .

[106]  R. S. Chandel,et al.  Effects of diflubenzuron and penfluron on workers of Apis cerana indica F and Apis mellifera L , 1995 .

[107]  P. Jepson,et al.  Sub‐lethal effects of deltamethrin residues on the within‐crop behaviour and distribution of Coccinella septempunctata , 1994 .

[108]  R. Currie,et al.  EVALUATION OF THE REPELLENT EFFECTS OF A NEEM INSECTICIDE ON FORAGING HONEY BEES AND OTHER POLLINATORS , 1994, The Canadian Entomologist.

[109]  J. Taséi,et al.  Effects of sublethal doses of deltamethrin (Decis Ce) on Bombus terrestris , 1994 .

[110]  E. Grafius,et al.  Pesticides Affect Immature Stages of Diadegma insulare(Hymenoptera: Ichneumonidae) and Its Host, the Diamondback Moth (Lepidoptera: Plutellidae) , 1993 .

[111]  M. Hammer,et al.  Functional Organization of Appetitive Learning and Memory in a Generalist Pollinator, the Honey Bee , 1993 .

[112]  K. Richards Non-Apis bees as crop pollinators , 1993 .

[113]  P. Jepson,et al.  The dietary toxicity of deltamethrin to the carabid, Nebria brevicollis (F.) , 1993 .

[114]  A. Ruijter,et al.  Method for honeybee brood feeding tests with insect growth‐regulating insecticides , 1992 .

[115]  M. Dicke,et al.  Ecology of infochemical use by natural enemies in a tritrophic context. , 1992 .

[116]  R. S. Chandel,et al.  Toxicity of diflubenzuron and penfluron to immature stages of Apis cerana indica F and Apis mellifera L , 1992 .

[117]  C. Dedryver,et al.  Effect of three insecticides on the life cycle of Aphidius uzbekistanicus Luz. (Hym., Aphidiidae) , 1991 .

[118]  P. Kevan POLLINATION: KEYSTONE PROCESS IN SUSTAINABLE GLOBAL PRODUCTIVITY , 1991 .

[119]  G. D. Waller,et al.  Recovery of learning responses by honeybees following a sublethal exposure to permethrin , 1990 .

[120]  E. Little Behavioral toxicology: Stimulating challenges for a growing discipline , 1990 .

[121]  Brian A. Croft,et al.  Arthropod biological control agents and pesticides , 1990 .

[122]  G. Bicker,et al.  Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor‐like antigen in the brain of the honeybee , 1989, The Journal of comparative neurology.

[123]  M. Wong-Riley Cytochrome oxidase: an endogenous metabolic marker for neuronal activity , 1989, Trends in Neurosciences.

[124]  J. P. Rieth,et al.  The repellent effect of two pyrethroid insecticides on the honey bee * , 1988 .

[125]  M. Hoy,et al.  Sublethal effects of pesticides on the parasitoid Aphytis melinus (Hymenoptera: Aphelinidae) , 1988 .

[126]  K. Haynes Sublethal effects of neurotoxic insecticides on insect behavior. , 1988, Annual review of entomology.

[127]  W. Wilson,et al.  The Behavior of Insecticide-Exposed Honey Bees , 1987 .

[128]  Hilvarenbeek Beekeeping,et al.  A field study on the effect on honey bee brood of Insegar (fenoxycarb) applied on blooming apple orchards , 1987 .

[129]  C. Fonta,et al.  Toxic and repellent effects of cypermethrin on the honeybee: Laboratory, glasshouse and field experiments† , 1985 .

[130]  G. Viggiani Bionomics of the Aphelinidae , 1984 .

[131]  C. Masson,et al.  Analyse des effets, en particulier de la répulsivité, d'un pyréthrinoïde de synthèse, la deltaméthrine, sur les abeilles , 1983 .

[132]  Abdominal grooming in the cockroach: Development of an adult behavior , 1978 .

[133]  E. R. Jaycox,et al.  Behavioral Changes in Worker Honey Bees (Apis mellifera) Induced by Injections of a Juvenile Hormone Mimic , 1974 .

[134]  A. Mansingh,et al.  The cholinergic system in insect development. , 1969, Annual review of entomology.

[135]  K. Frisch The dance language and orientation of bees , 1967 .

[136]  K. Takeda Classical conditioned response in the honey bee , 1961 .