3 15 ¸osa, (MG), Doses that Semantically, 2,14 ¸osa, Vic 16 – 2,13 ¸osa, MG 36570-000, Brazil. The common definition of 13 ¸osa, Vic 2013 Society of Chemical Industry – c 9 They suggested that the hormetic 13 – 9 b Correspondence to:mologia, Raul Universidade Narciso Federal C. de Vic Guedes, Departamento de Ento- Department of EnvironmentalUniversity, Truro, (NS), Canada Sciences, Agricultural Campus, Dalhousie E-mail: [email protected] Departamento de Entomologia, Universidade Federal de Vic Brazil ∗ a b group recognized the general nature of the phenomenoncession in a of suc- meta-analyses. 2 CONCEPTUALENTOMOLOGY CONUNDRUM AND IN ACAROLOGY The concept of hormesis is nowas widely a recognized and general accepted stress response phenomenon. however, insecticide-induced hormesis remains subject to dose–response model isthreshold more common model in (Fig. 1), toxicologydominant than which model the is in widely toxicology. viewed as the most cause hormetic responses are limited in rangethe and No typically below Observable Effects Concentrationnot always (Fig. the 1), case for although arthropods in this their response is to pesticides. hormesis as the stimulatory effect associateddoses with low of (sublethal) compoundsrefined that to are avoid toxic referringmay at to not always the higher be response doses theas as case. has a Hormesis, ‘beneficial’, therefore, been dose–response which canresponse be relationship between defined low characterized and high by dosesticide), a of thus a reversal characterizing stressor (e.g. a in an biphasic insec- relationship. 3 4 7 – 2,5 (1888) expressed and G Christopher Cutler ∗ a Twilight of the Idols In the 16th century, the monophasic 1,2 : 690–697 www.soci.org More recently, Edward J Calabrese and his 70 8 2014; biphasic concentration–response; hormoligosis; insecticidal stress; insecticide ecotoxicology; pesticide-mediated

2013 Society of Chemical Industry The term ‘hormesis’ has its beginning in the early 1940s The concept of hormesis may have been developed from c when Chester M Southam anddose–response John to Ehrlich observed red aand cedar biphasic extracts they in referred differentGreek to fungal the ‘to strains, phenomenon excite’. as ‘hormesis’, from the Pest Manag Sci This (nonlinear) biphasicreferred relationship as described the by Arndt–Schulzhomeopathic Schulz law. community as This was its law scientific was principle,led to which, co-opted its in by marginalization. part, the It wasHueppe later and re-established has by become Ferdinand known as Hueppe’s rule. meaning that toxic substances aredoses, nonpoisonous at and low enough whattoxic are at generally highlogit enough innocuous or doses. substances a The log-probit canrelationship sigmoid scale), was be or or initially also challenged linearHugo monophasic in Schulz, (on who dose–response the demonstrated stimulation a late by substances 19th log- (sublethal) at low concentrations century that by are toxic at high concentrations. 1 HORMESIS:AND ANCIENT CURRENT ADAGES, THEORY OLD LAWS Friedrich Nietzsche in his the dose–response relationship illustratedand by Latin the adages ancient Greek middle’, ‘nothing too respectively. much’ and ‘the virtue is in the the maxim that what doesAlthough not not everything destroy that you, does not makes killNietzsche’s you will make stronger. idea you stronger, is wellthe known concept in human ofphenomenon characterized society by a hormesis, and reversal of emulates the which responselow between and high describes doses of a a stressor, such dose–response as an insecticide. Abstract Ecological backlashes such as insecticide resistance, resurgence and secondarywith pest outbreaks insecticide are use frequent problems against associated arthropodphenomenon of pest insecticide-induced species. hormesis within The entomology last andrelationship acarology. two Hormesis have describes that a been biphasic is particularly dose–response Although important characterized in the by sparking concept interest a insemantic of reversal the confusion, insecticide-induced of it hormesis has responseoutbreaks been often and between reported potential does problems low in with not many and insecticideand arthropod receive acarology. resistance. high Here, The pest we sufficient study examined species doses of the attention, and hormesis conceptfitness of of remains or consequences, natural insecticide-induced largely and a hormesis enemies, has neglected its in in importance and stressor arthropods, been in entomology its has arthropod functional (e.g. subject basis been pest and management insecticides). linked to potential and to other areas. pest Keywords: homeostatic regulation; sublethal effects pest management Raul Narciso C Guedes Insecticide-induced hormesis and arthropod (wileyonlinelibrary.com) DOI 10.1002/ps.3669 Review Received: 31 August 2013 Revised: 7 October 2013 Accepted article published: 23 October 2013 Published online in Wiley Online Library: 2 December 201 dose–response concept was applied to the discipline ofby toxicology Paracelsus, who recognized that the dose makes the poison,

690 691 18 34 – 30,32 14,16,30,31 Furthermore, the 15 and have received some which should reduce the 18 Nonetheless, most entomological wileyonlinelibrary.com/journal/ps 18,19,22 likely contributing to the semantic In a general sense, different hormetic 20,21 Cohen readily recognizes the conceptual 15,18,19 23 ). 14,25,26 Recognition of the mechanisms underlying ultimately affecting fitness-related traits. et al 29 – 14,31,35,36 14,23,24 23,27 The distinction between hormesis and hormoligosis has been therefore, insecticide hormoligosis ishormesis basically in a which a specialcompound biphasic is case observed dose–response when of the organism fordue is an to already another under insecticidal environmental stress factor or agent. previously recognized. confusion. However, aof shift the favoringseems hormesis the to phenomenon proper be within recognition taking insecticide place, toxicology misuse of thehormoligosis, term if ‘hormoligosis’ used, should (Fig. be 2).induced restricted The hormesis to where cases term the of biphasic insecticide insecticide- dose–responsewhen takes the place organismenvironmental factor. in already under stress due2.2 to another Pesticide-mediated homeostaticThe modulation concepts of hormesisrelated and to insecticide hormoligosiswere arthropods as recently they questioned and by insecticides Cohen, in certain situations Two main overallproviding a alternative mechanistic hypotheseshormesis explanation theory currently for of prevail Stebbing hormesis: (alsothe the in referred to growth Maia as growth hypothesisand control, the and principle of ‘overcompensation’to physiological hormesis. resource theory), allocation as applied However, the hormesis conceptand is the not homeostatic species- modulation(i.e. or determined notion target-driven by is the management-based fieldrather use than of the registered toxicological recommendations) dose–response. 3 FUNCTIONALFITNESS BASIS CONSEQUENCES AND POTENTIAL The mechanismsarthropods underlying insecticide-induced remainadvances. hormesis largely in unknown, despite a few recent hormesis is crucial toand understand consequences. the process and its relevance distinction between hormesis and hormoligosis,misuse and of the general the latterstudies when with referring insects tohowever, the and former challenged mites. in by The insecticide homeostatic Cohen concept modulation’ in in of arthropods favor in hormesishormesis of two is not was, circumstances: applicable ‘pesticide-mediated to (1) situations in which stimulatoryare effects observed in apesticide nontarget under consideration; pest and (2) species onemeasure can not only controlled quantitatively lethal by doses the of a given pesticide in target pests. support (e.g. Yu and acarological studiesterms, neglect particularly the regardingwhich distinction the between insecticide suboptimal the Indeed, hormoligosis environment hormesis in redefined is and and referred hormoligosisand are acaricide to have treated literature, been take synonymously equivocally in place. the insecticide suggestion that the quantification of dose–response relationships and determination of lethal dosesonly as possible in toxicological target endpoints species are is incorrect. agents, chemicals,gene radiation, expression in temperature, components ofways, etc. physiological including response likely hormones, path- heat change shockenzymes, proteins and antioxidant to excite) = 2013 Society of Chemical Industry c : 690–697 70 2014; small quantities) and defined it as a phenomenon in subharmful quantities of many stress agents may be = Depiction of the linear, threshold and hormesis dose–response ... This original definition emphasizes situations in which stim- 17 ’. and oligo ( which ‘ helpful when presented to organisms in suboptimal environments ... ulation under sublethal exposure of awhen given the compound organism will is occur already underconditions stress or (i.e. a due second to stress suboptimal agent).that This concept of is hormesis, distinct from although the later encompasses the former; Pest Manag Sci 2.1 Insecticide hormoligosis The term ‘hormoligosis’, or more preciselysis’, ‘insecticide was hormoligo- coined by Thomas DLuckey Luckey developed in his the influential term 1968 paper. from the Greek hormo ( models (solid line) generallyscale used was in assumed toxicology allowing (a forNo a log-logit Observable linear or Effects relationship). Concentration. log-probit Arrows The(control) indicate black expected the dashed response line without insecticide indicates exposure. the confusion in entomology and acarology. Intional these fields, terms, two addi- ‘insecticidehomeostatic hormoligosis’ and ‘pesticide-mediated modulation’,analogously or have complementary tohistorical the been precedence concept of of used hormesis. theof The term this ‘hormesis’ synonymously, concept and makedifficult the this to generality semantic justify. confusion Inmisconceptions) unnecessary addition, about and there the areand original pesticide-mediated misunderstandings homeostatic definitions modulation. (or of hormoligosis Figure 1. Insecticide-induced hormesis www.soci.org 45 14 54 By – Based et al 19,45 14,51 : 690–697 Although 31,35 70 48 14 34,38 45 – – 2014; 30,32 35,39 In both situations, improved Pest Manag Sci 46,47 Cadmium-exposed springtails and 14,25,26 14,31 In other cases, there may be no evidence of 14 This increased energy uptake favors growth These recent findings suggest that insecticide- 14 31,45,47,49,50 Hormesis by resource allocation is a more traditional and widely The fitness consequences of hormesis likely depend on the Hormesis by acquisition reflects the increased performance of a overcorrection (or overcompensation) bylow the levels of control inhibition by the system toxic compound. to accepted notion inthe which balance between the potentially energy-conflicting stress-exposed physiological trade-offs, individual favoring shifts oneanother (e.g. (e.g. reproduction) longevity). at the expense of underlying mechanism involved. The initial suspicionsis that horme- in individualhas traits been may challenged not offitness late translate by into due reports improved ofmites. to enhanced fitness population insecticide-induced hormesis in insects and stress-exposedindividualandisexplainedbyanunlimitedincrease in energy uptake fromis the not environment, when limited. such a resource trade-offs within a generation ofinsecticide, insects but exposed trade-offs to across low generations dosesany may of evidence occur, of without overall biological fitness being compromised. azadirachtin-exposed bean beetlestrade-off shifts, (bruchids) the bothgrowth first and exhibited favoring reproduction, longevity andat the at the latter the expense favoring expense of reproduction of longevity. with potential consequences for arthropod pest management. 4 HORMESISHormesis IN ARTHROPODS hasthe been scientific a literature with subject over of 1700 growing published attention papers in Similarly, evolution of insecticidelow resistance doses during of exposure insectchanges to growth in regulators metabolism may or signaling induceof a that evolutionary longer may life mediate span without evolution trade-offs with fecundity. 3.2 Principle ofThe resource allocation principle ofphysiological energetic models resource that predict trade-offs allocationallocation in resource among is different the physiological general processes. basissuggest of three broadunderlying hormesis: categories acquisition, medication of andview allocation. energy/mass This holds management twobetween physiology fundamental and fitness, and assumptions: the existence of physiological thecosts associated functional with a link toxicto challenge. support There these assumptions is and ample this theory. evidence rate, and possibly maximizesand size, population which increase growthwith reproduction insecticide-exposed rate. spined soldier This bugs and is aphids. exemplified by findings induced hormesis in arthropods may indeedpected and be reported with adaptive, other stress as agents for sus- other taxa, interesting, this hypothesismainly remains focused on highly growth asmechanistic speculative a underpinning. life-history and trait lacking is a general performance of one trait impairs the performance of themay other. have This either positive or negativeindividual fitness depending consequences on for the the traits involved andgenerational may effects. exhibit trans- on this principle and energy conservation laws, Jager contrast, hormesis by medicationis, may or occur contains, when thedeficient. an This toxicant second essential view is element more in limited in which scope. the individual is The 30,33 2013 Society of Chemical Industry www.soci.org RNC Guedes and GC Cutler c This idea has proven popular 33,34 The control mechanisms that regulate growth Citations of insecticide-induced hormesis (A), insecticide 33,37 wileyonlinelibrary.com/journal/ps 3.1 Growth hormesisAccording theory to thehomeostasis overcompensation. growth theory, hormesis is a byproduct of Figure 2. hormoligosis (B)registered and over pesticide-mediated 10-yearhormesis periods homeostatic was since initially regulation theScience proposed. database 1940s, (C) (accessed Data when 20 August were the 2013). obtained concept from of the Web of and is based on control systems and growth analysis. counteract the perturbing orHormesis inhibitory is effects the of alleged toxic result agents. of both transient and sustained assumption is that self-regulated processes (e.g. growth)organism and thus self-regulation require controlresponses. systems with feedback

692 693 This 79,80 56,84,85,89,90 56,84,85 and because of suggest potential 72 Although no direct 74,75 . 22,77,78 Insecticide-induced hormesis 93 and neither factor seems to play – wileyonlinelibrary.com/journal/ps 76 91 Frequent or improper insecticide use – 73 88 – 81,82 L.) led to higher egg-laying activity by 84,86 Eurytetranychus buxi Since then, these outbreaks have been relatively 56,83 , insecticides remain a major component of insect suggests that there is less potential for hormesis in natural 20 ıve about potential stimulatory effects of chemicals on these ¨ Insecticide applications leading to outbreaks of pest species Buxus sempervirens the boxwood mite were recognized as early asof the the large-scale early use of 1950s, organochlorine insecticides followingpest for control. the arthropod onset decades, no such observationsthe literature. with It is natural also enemies likelyexperimental that appear bias the long-standing in toward emphasis and theon deleterious natural effects enemies have of meantna insecticides that researchers have remained taxa. Although naturalMorse enemies may be subject to hormesis, frequent, particularly for broad-spectrum insecticides. Insecticide-induced hormesis iscases. potentially important in both 5.1 Insecticide-inducedpopulations hormesis in insecticide-resistant Sincethe1950s,theevolutionofinsecticideresistanceinarthropod pests has beenarthropod a pest management. major concern in agricultural and medical 5 PESTINSECTICIDE-INDUCED MANAGEMENT, HORMESIS AND ECOLOGICAL BACKLASHES More than 50Silent years Spring afterpest the management publication and are ofHowever, changes in still attitudes Rachel and surrounded policy over the by Carson‘s useagainst of pesticides controversy. pest speciesinsecticides have with led improved safety to profilesand the towards the human environment. development health and use of enemies in the field becauseto they are insecticides generally more compared susceptible with pest species, a direct role in the expression of hormesis in natural enemies. 4.3 Plant-mediated hormesis? The possibility that insecticide applicationsin may induce arthropods hormesis indirectlyintriguing via concept. changes For example, in imidacloprid-treated( plant boxwoods physiology, is an is often associated withto two pest ecological control failures: backlashes insecticide that resistanceor and can pest outbreaks, lead resurgence both of whichecological have some consequences common of causes and insecticide are applications. is potentially a complicating factor for arthropod pesticide evidence ofno hormesis concentration–response waswere relationship provided changes wasand in in established the plant reported nor these herbicide-inducedof physiology performance studies improvement plant assessed), (i.e. species their of findings, economic value, the density-dependence of natural enemiesspecies. on their Both prey may or have host anbility effect, of but natural the enemies overall to lowermore current suscepti- modern insecticides insecticides, is disputable for form of ecological backlash was frequently dealt with byinsecticide increasing use, which often‘pesticide leads syndrome’. to the ‘pesticide treadmill’ or indirect impacts of insecticidemanagement, hormesis possibility that in have arthropods been largely and neglected. their , , Bra- 15 14,15,18,50,56 2013 Society of Chemical Industry c spp. and the Oligonychus ilicis Sitophilus granarius , and the two-spotted , the ladybird beetle Geocoris Here, we focus on trends Drosophila melanogaster More recently, pyrethroid- 15 were early subjects of study, Hormesis studies on natural 71 – 18,63,64 . 19,68 Panonychus citri , granary weevil The fruit fly and the braconid parasitoid wasp 16,56 Chrysopa californica Podisus distinctus and Supputius cinceticeps : 690–697 Insecticide-induced population stimulation in Thus, there is awareness of the hormesis 70 The big-eyed bug Acheta domesticus 62 50 – 67 This provides support for the perception that – 2014; Tetranychus urticae This is important because exposure to low insecticide 17,57 65 . Musca domestica 55 and more recently by Cutler. 15,18 18 Insecticide-induced hormesis in arthropod pests has been There are few reports of insecticide-induced hormesis in natural studiedfordifferentbiologicaltraits,butitsimpactonreproductive traits and potentialreported. fitness consequences are most commonly Pest Manag Sci Coleomegilla maculata con hebetor 4.2 Hormesis inInterest natural enemies in insecticide-inducedpods, hormesis particularly in predators,with nontarget started the in arthro- lacewing the 1950s and 1960s More long-term laboratoryconfirm this and perception. field studies are necessary to Insecticide-induced hormesisaccording to the(http://thomsonreuters.com/web-of-science/). Thomson However, Reuters only 82 (4.82%) database of Web those of(including hormoligosis) and papers Science only 50 (2.94%) explore are devoted to insects and insecticide-induced mites. Comprehensive hormesis lists of theseCohen, studies were reported by www.soci.org 4.1 Hormesis inInsecticide-induced arthropod pest species hormesisreceived in only modest arthropod attention comparedin with pest other hormesis studies disciplines species (e.g.because biomedical has the phenomenon sciences). and This itsnized is importance since surprising have the been 1950s. recog- doses often occurs in the fieldthe due lower to exposure insecticide of nontargeted degradation arthropods and (i.e.nontargeted beneficials and pests) that are usually lessto exposed the or compound more than the tolerant target species. induced outbreaks of the southern red mite, were examined. house fly and house cricket particularly with exposure to sublethalinsecticides. doses of organochlorine spider mite, mites has been observed since the 1970s and hasof sparked concerns insecticide-induced pest outbreaksspecies: the among citrus at red mite, least two mite phenomenon in insects and mites,modest, but despite interest the remains increase relatively in attention in the last decade. and deficiencies in howin the insect subject has and beentoxicological mite endpoint explored in studies. thus insecticide far The studieslikely with been past arthropods one of has focus the barriers onand to recognizing lethality both importance the occurrence as ofsublethal the phenomenon. hormesis In the in past decade, the insectssublethal significance of effects and the of insecticides mites, onaccepted. arthropods which has is become more a insecticide-inducedhormesisinarthropodpestspeciesisadaptive, with potential consequences for pest management. enemies compared with arthropod pests, which may belack due of to the preliminary evidence ofinduced occurrence. Although insecticide- pest population outbreaks have been reported for enemies are more common with insect predators thanWe parasitoids. are awareentomopathogens. of no study to date dealing with hormesis in spined soldier bugs were subsequently studied. , . In 50 100 50 56 : 690–697 70 Other envi- planthoppers, 13,15 2014; Olygonychus ilicis ) and its phytoseid – 64 9 ; Leucopetera coffeella ). 50 Insecticide-induced hormesis Pest Manag Sci et al Both phenomena have common 50,85 ) exposed to the pyrethroid insecticide Oligonychus ilicis 84.85 ; The southern red mite, In addition, insecticide-induced hormesis 102 By contrast, secondary pest outbreaks – also 56,85 Observed concentration–response values and curve 74,75,103,104 and thrips. Amblyseius herbicolus 101 ) of the southern red mite ( The reduction of natural enemies is commonly thought to be the The hormesis phenomenon is not, however, restricted to m r deltamethrin (modified from Cordeiro causeofthephenomenon,althoughithasseldombeentested,par- ticularly at the population level. may lead tomanagement arthropod of pest insecticide-resistantresistance outbreaks, development populations in and insects, or illustratingthis may phenomenon the augment to importance pest impair of management. the insecticides (or pesticides) as stress agents. predator ( Figure 4. (Brain–Cousen model) based( on the intrinsic rate of population growth 6 BEYONDHORMESIS INSECTICIDE-INDUCED Hormesis is ahormesis may general occur in phenomenonenemies. arthropod pest Pesticide-induced and species hormesis and insecticide-induced to their in natural yield crop plantsoutbreaks. increase, may but lead it may also mediate arthropod pest thaninsecticideresistance.Resurgenceisanincreaseinabundance of theapplication arthropod to pest levelspopulations. species higher targeted than by those the of the insecticide uncontrolled aphids called pest replacement orin type II the resurgence abundance –after insecticide are application. of an increase a nontargeted arthropod pest species causes, including reduction inincrease of the the pest number population, and of removal of natural competitors. enemies, is a possible causeof of insecticide outbreaks applications in directly somelations pest stimulating outbreaks has species. arthropod been Evidence popu- reported in mites, addition, deltamethrin did not lead to behavioral avoidancepredatory by mites the but did induce hormesis in the red mite (Fig. 4). often exhibits outbreaksapplications in against coffee the plantations coffee after leafminer, pyrethroid Mite predators ofpyrethroid the deltamethrin, which red is more mite toxic to are the red not mite. compromised by the ronmental stress factors such as temperature, diet and UV , ) ), 25 Maize 49 2013 Society of Chemical Industry www.soci.org RNC Guedes and GC Cutler c and induction Sitophilus zeamais Sitophilus zeamais SEM) of a susceptible 96,97 ± m r with added data from the susceptible 49 , one could reasonably predict that 95 et al This finding suggests a potential problem 16,45,99 49 , selected for resistance to each respective However, the stimulatory effect was observed at a 94 If the propensity to express such detoxification enzymes Intrinsic rate of population growth ( 98 3) (modified from Guedes Mechanistically, there are reasons to suspect that adaptive Evidence of a hormesis-like stimulatory egg-laying response = n strain). hormetic responses to lowthe doses development of of insecticide resistancecompounds. might Exposure or augment of increased insects to toleranceor sublethal plant to doses allelochemicals of these can pesticides are induce production important of enzymes in that detoxification processes, during the hormetic response waswithout a heritable fitness epigenetic process costs, 5.2 Insecticide-inducedoutbreaks hormesis and arthropod pest Pest resurgenceimportant and frequently and reported, have received far less attention secondary pest outbreaks, although the coupling of theinduction hormetic could response assist with in insecticide detoxification resistancehypothesis gene should development. be This explored further. wileyonlinelibrary.com/journal/ps Figure 3. to the pyrethroidwas detected fenvalerate in andPlutella a xylostella the Japanese strain carbamate of methomyl the diamondback moth, resistance management becauseresistant of insects the to sublethal prevailing doses ofsubject exposure insecticides has in of been the largely field. neglected The andhave there explored are this few scenario. studies that insecticide. and may have been an artifact of selection,individuals which allowed to the fitter survive and reproduce. Insecticide-inducedsis was horme- also reported in a strainresistant of maize weevil, to the pyrethroid insecticide deltamethrin. for managingdoses insecticide-resistant of the populations insecticideactually because may boost their population not growth field (Fig. control 3). There theseevidence is preliminary insects of and higher may most insecticide-induced resistant populations. hormetic effect on the weevil fitness was significantly affected with increasedgrowth population of theinsecticide exposure. insecticide-resistant strain following sublethal and a pyrethroid-resistant strainexposed of to the maize sublethal weevil( doses ( of the pyrethroid insecticide deltamethrin relatively high dose range exhibiting significant mortality (LD of esterasesmetabolism, (hydrolases), as observed which during insecticide-inducedinsects. hormesis are in important in pesticide

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Pest Dr were The comments greatly S.The and appreciated Duke financial and andScientific support acknowledged three and provided here. Technological anonymous Foundation by Development (Brazilian the (CNPq), MinistryState the of National Foundation Education), CAPES Council of theSciences Research of Minas and Aid Gerais Engineering (FAPEMIG)acknowledged. 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