ANRV297-EN52-05 ARI 21 November 2006 10:17 The Sublethal Effects of Pesticides on Beneficial Arthropods Nicolas Desneux,1 Axel Decourtye,2 and Jean-Marie Delpuech3 1Department of Entomology, University of Minnesota, St. Paul, Minnesota 55108; email: [email protected] 2ACTA, Institut Claude Bourgelat—ENVL, 69280 Marcy L’etoile,´ France; email: [email protected] 3Laboratoire de Biometrie´ et Biologie Evolutive (UMR 5558); CNRS; Universite´ Lyon 1, 69622, Villeurbanne Cedex, France; email: [email protected] Annu. Rev. Entomol. 2007. 52:81–106 Key Words First published online as a Review in ecotoxicology, insecticide, behavior, honey bee, natural enemy Advance on July 14, 2006 The Annual Review of Entomology is online at Abstract ento.annualreviews.org Traditionally, measurement of the acute toxicity of pesticides to ben- This article’s doi: eficial arthropods has relied largely on the determination of an acute 10.1146/annurev.ento.52.110405.091440 median lethal dose or concentration. However, the estimated lethal Copyright c 2007 by Annual Reviews. dose during acute toxicity tests may only be a partial measure of All rights reserved the deleterious effects. In addition to direct mortality induced by 0066-4170/07/0107-0081$20.00 pesticides, their sublethal effects on arthropod physiology and be- by UNIVERSITE CLAUDE BERNARD on 12/15/06. For personal use only. havior must be considered for a complete analysis of their impact. Annu. Rev. Entomol. 2007.52:81-106. Downloaded from arjournals.annualreviews.org An increasing number of studies and methods related to the identi- fication 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 learn- ing performance, behavior, and neurophysiology. We characterize the different types of sublethal effects on beneficial arthropods, fo- cusing 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. 81 ANRV297-EN52-05 ARI 21 November 2006 10:17 INTRODUCTION AND dose/concentration can be sublethal or lethal). DEFINITIONS A sublethal dose/concentration is defined as inducing no apparent mortality in the experi- Pollinator: an For the past 20 years, the effects of pesticides mental population. organism that carries on beneficial arthropods have been the sub- We review the sublethal effects of pesti- pollen from one ject of an increasing number of studies, and flower to another cides on beneficial arthropods reported in the the potential effects have been reviewed sev- published literature and divide these effects IPM: integrated eral times (24, 62, 128). Two groups of organ- pest management into two major groups: physiology and be- isms, natural enemies and pollinators, have havior. We focus on the side effects and not LD50: lethal dose received the most attention in this regard be- 50% on the indirect effects of pesticides, such as cause of their value in integrated pest manage- habitat destruction and damage to nesting, Sublethal effect: an ment (IPM) (131) and pollination processes effect (physiological oviposition, resting, and mating sites. This re- (105), respectively. or behavioral) on view aims to ( ) provide a better understand- Methods to test the side effects of pesti- a individuals that ing of the different types of sublethal effects survive an exposure cides have been developed as a function of the associated with pesticide exposure, ( ) clarify to a pesticide (the beneficial arthropods and pesticides studied. b the range of methods used to address sub- pesticide In each country, regulatory insect risk assess- dose/concentration lethal effects and permit new insights into ment related to agrochemical use and regis- can be sublethal or the development of better experimental ap- tration follows specific guidelines (European lethal) proaches, ( ) determine if evaluation of these Council Directive 91/414 in Europe, and the c Sublethal effects could be included in the pesticides reg- dose/concentration: Federal Insecticide Fungicide and Rodenti- istration process, and (d ) elucidate the pos- a dose or a cide Act in the United States). For a long sible consequences of the sublethal effects concentration time, the classical laboratory method for esti- of pesticides on the efficiency of beneficial defined as inducing mating the side effects of chemicals on bene- no statistically arthropods (pest limitation or pollination) and ficial arthropods was to determine a median significant mortality community dynamics. in the experimental lethal dose (LD50) or lethal concentration population (LC50) estimate. In a second step, the ef- fects of pesticides on beneficial arthropods were examined further by running selectivity PHYSIOLOGICAL EFFECTS tests (pest/beneficial arthropods) to identify products with the lowest nontarget activity General Biochemistry and (24). However, estimation of selectivity was Neurophysiology based on LD50 values, and side effects of pes- Studies on effects of pesticides on insect bio- ticides on beneficial arthropods still occurred chemistry have been conducted with both because of the lack of attention to sublethal pollinator and natural enemy models. More by UNIVERSITE CLAUDE BERNARD on 12/15/06. For personal use only. effects. Because of the increasing economic in-depth studies have been performed us- Annu. Rev. Entomol. 2007.52:81-106. Downloaded from arjournals.annualreviews.org importance of beneficial arthropods in agri- ing honey bees primarily because more is culture and the recognition of limitations as- known about their biochemical systems. Ex- sociated with traditional methods for study- periments on bee physiology have been done ing sublethal effects of pesticides (80), a mainly by measuring the activity of enzymes growing body of literature is aimed at ad- after or during exposure to pesticides. Af- dressing this issue. Now, it is important ter injection of emerging honey bees in to step back and review what these studies the laboratory, fenitrothion (organophospho- have documented to determine the directions rus) and cypermethrin (pyrethroid) led to of future studies and applications. Sublethal decreases in Na+/K+ ATPase and acetyl- effects are defined as effects (either physio- cholinesterase (AChE) activities (12). Re- logical or behavioral) on individuals that sur- lated glycemic disorders were also linked vive exposure to a pesticide (the pesticide to enzyme inhibition. Na+/K+ ATPase is a 82 Desneux · Decourtye · Delpuech ANRV297-EN52-05 ARI 21 November 2006 10:17 transmembrane enzyme that releases energy tested) was toxin specific as well as species necessary for cell metabolism and establishes specific. The inhibition of AChE could lead the ionic concentration balance that main- to general perturbation in all systems because CO: cytochrome tains the cell potential. Thus, the inhibition it is a major component in all synaptic oxidase of Na+/K+ exchange provoked by pyrethroids transmission (74), especially when inhibition might affect a wide range of cellular functions. continues for a long time after exposure. For For example, the pyrethroid deltamethrin example, eight days were required after a 24- causes marked dysfunctions in myocardial or 48-h exposure to the organophosphorus cells. Indeed, Papaefthimiou & Theophilidis diazinon and chlorpyrifos for AChE inhibi- (97) have demonstrated the cardiotoxicity of tion in wolf spiders (Lycosidae) to disappear deltamethrin using intracellular recordings (132). Thus, pesticide effects on important from the myocardial cells of the semi-isolated enzyme systems cannot be extrapolated or hearts of honey bee. The frequency and the deduced from LD50 values. force of spontaneously generated cardiac con- Effects on neurophysiology have also been tractions were modified by deltamethrin. The described. The metabolic activity in the honey imidazole fungicide prochloraz had a simi- bee brain was investigated using cytochrome lar impact, but its effects were more intense. oxidase (CO) histochemistry. Because CO is When prochloraz and deltamethrin are com- the terminal enzyme in the electron transport bined there is a synergistic interaction. The chain of the mitochondrial respiratory pro- joint effects of both compounds were also in- cesses, histochemistry is used as an endoge- vestigated on honey bee thermoregulation by nous metabolic marker for neuronal activity infrared thermography. When associated with (145). Using CO histochemistry to carry out prochloraz, deltamethrin elicited a joint hy- metabolic mapping of discrete brain regions, pothermia at doses that did not induce a sig- Armengaud et al. (7) showed that CO histo- nificant effect on thermoregulation when used chemistry could be used to identify the tar- alone (133). One hypothesis was that imida- get structures of cholinergic ligands in the zoles delayed the metabolism, detoxification, honey bee brain, particularly in the case of and excretion of pyrethroids by inhibition of the neonicotinoid imidacloprid. In a behav- microsomal oxidation and thus enhanced the ioral and histochemical analysis of the effect toxicity of the pyrethroid to the honey bees of imidacloprid on olfactory learning