Pesticide-Induced Stress in Arthropod Pests for Optimized Integrated Pest Management Programs

TLDR: The present review mitigates this shortcoming by hierarchically exploring within an ecotoxicology framework applied to integrated pest management the myriad effects of insecticide use on arthropod pest species.

Abstract: More than six decades after the onset of wide-scale commercial use of synthetic pesticides and more than fifty years after Rachel Carson's Silent Spring, pesticides, particularly insecticides, arguably remain the most influential pest management tool around the globe. Nevertheless, pesticide use is still a controversial issue and is at the regulatory forefront in most countries. The older generation of insecticide groups has been largely replaced by a plethora of novel molecules that exhibit improved human and environmental safety profiles. However, the use of such compounds is guided by their short-term efficacy; the indirect and subtler effects on their target species, namely arthropod pest species, have been neglected. Curiously, comprehensive risk assessments have increasingly explored effects on nontarget species, contrasting with the majority of efforts focused on the target arthropod pest species. The present review mitigates this shortcoming by hierarchically exploring within an ecotoxicology fram...

Figures

Figure 3

Full text

EN61CH03-Guedes ARI 13 February 2016 7:45
Pesticide-Induced Stress
in Arthropod Pests for
Optimized Integrated Pest
Management Programs
R.N.C. Guedes,
1, ∗
G. Smagghe,
2
J.D. Stark,
3
and N. Desneux
4
1
Departamento de Entomologia, Universidade Federal de Vic¸osa, Vic¸osa, Minas Gerais
36570-900, Brazil; email: guedes@ufv.br
2
Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University,
B-9000 Ghent, Belgium; email: guy.smagghe@ugent.be
3
Puyallup Research and Extension Center, Washington State University, Puyallup,
Washington 98371-4900; email: starkj@wsu.edu
4
French National Institute for Agricultural Research (INRA), Universit
´
e Nice Sophia Antipolis,
CNRS, UMR 1355-7254, Institut Sophia Agrobiotech, 06903 Sophia Antipolis, France; email:
nicolas.desneux@sophia.inra.fr
Annu. Rev. Entomol. 2016. 61:43–62
First published online as a Review in Advance on
October 16, 2015
The Annual Review of Entomology is online at
ento.annualreviews.org
This article’s doi:
10.1146/annurev-ento-010715-023646
Copyright
c
 2016 by Annual Reviews.
All rights reserved
∗
Corresponding author
Keywords
behavioral avoidance, ecological backlashes, pest outbreaks, pest
resurgence, pesticide-induced hormesis, dominance shift
Abstract
More than six decades after the onset of wide-scale commercial use of syn-
thetic pesticides and more than fifty years after Rachel Carson’s Silent Spring,
pesticides, particularly insecticides, arguably remain the most influential pest
management tool around the globe. Nevertheless, pesticide use is still a con-
troversial issue and is at the regulatory forefront in most countries. The older
generation of insecticide groups has been largely replaced by a plethora of
novel molecules that exhibit improved human and environmental safety pro-
files. However, the use of such compounds is guided by their short-term effi-
cacy; the indirect and subtler effects on their target species, namely arthropod
pest species, have been neglected. Curiously, comprehensive risk assessments
have increasingly explored effects on nontarget species, contrasting with the
majority of efforts focused on the target arthropod pest species. The present
review mitigates this shortcoming by hierarchically exploring within an eco-
toxicology framework applied to integrated pest management the myriad
effects of insecticide use on arthropod pest species.
43
Click here to view this article's
online features:
• Download figures as PPT slides
• Navigate linked references
• Download citations
• Explore related articles
• Search keywords
ANNUAL
REVIEWS
Further
Annu. Rev. Entomol. 2016.61:43-62. Downloaded from www.annualreviews.org
Access provided by Universidade Federal de Vicosa on 04/23/18. For personal use only.

EN61CH03-Guedes ARI 13 February 2016 7:45
CONCEPTUAL FRAMEWORK
Pesticides, particularly insecticides and acaricides, are toxicants deliberately released into the envi-
ronment to reduce target species populations. As such, pesticides are also environmental contam-
inants, as their presence in the environment occurs at levels higher than their natural background
levels. Furthermore, pesticides can be justifiably recognized as pollutants because they are envi-
ronmental contaminants that adversely affect living species. Although pesticides are pollutants of
deliberate use, this characterization does not minimize their importance in agriculture, animal
husbandry, and public health (1, 31, 104). However, this perception facilitates recognition of the
negative and positive impacts of these compounds. In this review, we hierarchically explore within
an ecotoxicology framework the multitude of responses sparked by pesticide use against arthropod
pest species.
(Mis)Conceptions About an Influential Tool
Pesticides are arguably the most influential pest management tool since the onset of their wide-
scale use in the late 1940s. This range of influence surpasses their realm of practical use, encom-
passing the general public and adding pressure to regulatory agencies. Despite their recognized
importance for food production as well as human and animal health (31, 104, 120), the layperson’s
perception of pesticides is largely negative, especially when synthetic compounds are considered
(11, 15, 18, 29).
The enduring prominence of pesticides has led to divergent conceptualizations of these com-
pounds, which convey the equivocated notion that particular pesticides are safe for humans and
the environment. Biopesticides, for instance, refer to the natural origin of the compounds (38, 135,
137), not their toxicity or safety (29, 72). Reduced-risk pesticides refer to compounds exhibiting at
least one of six advantageous traits when compared with existing pesticides (134); thus, it is not a
particularly stringent definition. In the present review, we make no distinction between the neolo-
gisms, pleonasms, and/or misnomers used when referring to pesticides, including pesticidal toxins.
Pesticide Use, Exposure, and Assessment Limitations
Despite the high overall costs of use and the worldwide drive toward sustainable agricultural
production, pesticide use is increasing (47, 51, 117). Insecticides and the acaricides of the older
generation, encompassing four pesticide groups, were replaced in part by a plethora of 25 main
groups of nonpersistent compounds with distinct modes of action and improved safety profiles
(25, 52). These new groups, however, are amenable to a higher number of applications per year,
resulting in higher amounts of pesticides being applied, particularly under intensive agriculture
production and vector control (105, 117, 120).
Efficacy studies usually focus on the short-term mortality of target arthropod pest species.
Similarly, regulatory agencies focus mostly on short-term endpoints when deciding to register
compounds. Nevertheless, long-term effects may occur, and even short-term mortality in arthro-
pod pest complexes may not be the primary endpoint to consider (4, 40, 115), a point too often
neglected by academia and regulators alike. Ecotoxicology studies do not usually focus on arthro-
pod pest species, and the few studies that do are physiologically oriented and use short-term
mortality assessments, in contrast to the abundant comprehensive studies focusing on nontarget
arthropods, such as the honey bee (Apis mellifera L.) and the natural enemies of pest species (39,
41, 78).
44 Guedes et al.
Annu. Rev. Entomol. 2016.61:43-62. Downloaded from www.annualreviews.org
Access provided by Universidade Federal de Vicosa on 04/23/18. For personal use only.

EN61CH03-Guedes ARI 13 February 2016 7:45
Direct and Indirect Hierarchical Effects
The importance of the lethal effects of insecticides cannot be denied; however, underestimating
potential sublethal effects of pesticides on target organisms and their potential ecological conse-
quences is a mistake. Although pesticides are usually applied at concentrations that will result in
rapid death of pest species, residues degrade over time on plants, animals, water, and soils, resulting
in sublethal exposures (10, 42). Furthermore, nontarget species, including secondary arthropod
pest species, can be exposed to sublethal concentrations of pesticides for long periods, leading to
unforeseeable consequences such as pest outbreaks (34, 62).
An arthropod pest species may be directly and indirectly affected by a pesticide application.
Direct effects include mortality and various sublethal effects of pesticide exposure, and indirect
effects encompass habitat changes (e.g., food and shelter contamination) and changes to other
species within food webs that alter pest population viability (Figure 1). Both direct and indirect
effects of an applied pesticide could impair the physiology of an organism, reducing its survival
and/or reproduction. Other organisms that interact with the pest species in an ecosystem may
also be negatively affected, which may result in unpredictable outcomes in the demographic vital
rates of the pest species (48, 122). The population-level effect on a given species can translate
into a community-level effect, adding another hierarchical level of pesticide-induced stress and
emphasizing the complexity of effects that may potentially accrue from pesticide use (Figure 2).
Such effects may affect the original arthropod pest species targeted by the insecticide application,
leading to ecological backlashes that compromise integrated pest management.
INDIVIDUAL STRESS RESPONSES
Pesticides suppress arthropod populations by interacting with a primary site of action within an
individual organism and impairing at least one of its basic physiological processes, leading to its
demise (25, 52). This is the basis on which commercial pesticide molecules are developed for
managing arthropod pest populations. Nonetheless, any given pesticide is likely to interact with
secondary sites of action, which may not lead to the death of the organism but may produce
sublethal consequences that compromise its homeostasis and interfere with its survival and/or
reproduction. This is the case for the insecticide baits used against leafcutting ants, where forager
mortality is actually an undesirable trait because colony suppression is the objective. Colony
suppression requires the unaffected foragers to carry the toxic bait to the nest, impairing the
colony either by directly compromising the fungus garden (as a fungicide) and its cultivation by
the minor workers or by impairing progeny production by the ant queen (3, 4, 40).
Physiological Responses
Pesticides affect individual arthropods, the consequences of which may manifest at higher hier-
archical levels, i.e., populations and communities. Studies at the individual level elucidate how
a pesticide interacts with its target sites in the organism. Therefore, toxicological studies on the
mode of action of pesticidal compounds are the first step to understanding how pesticides work
on individual insects, as well as how they eventually lead to effects on the structure and function
of populations and communities (93).
Physiological responses to pesticide exposure at the individual level encompass not only the pes-
ticide toxic responses (both primary and secondary) mentioned above, but also nontoxic or protec-
tive responses (93). For example, pesticide-induced production of detoxification enzymes (46, 95)
www.annualreviews.org
•
Pesticide-Induced Stress in Arthropod Pests 45
Annu. Rev. Entomol. 2016.61:43-62. Downloaded from www.annualreviews.org
Access provided by Universidade Federal de Vicosa on 04/23/18. For personal use only.

EN61CH03-Guedes ARI 13 February 2016 7:45
a
b
Central
individual
Conspecics
Natural
enemies
Resources
Pesticide
Conspecics
Conspecics
Resources
Pesticide
Pesticide
Natural
enemies
Pesticide
Resources
Natural
enemies
Direct interactions Indirect interactions
1st order 2nd order nth order
Central
individual
Pesticide
Resources
(e.g., food, water,
shelter)
Pesticide
Conspecics
Pesticide
Resources
. . .
Natural enemies
. . .
Pesticide
Resources
. . .
Conspecics
. . .
Pesticide
Conspecics
. . .
Natural enemies
. . .
Pesticide
Resources
. . .
Conspecics
. . .
Pesticide
Conspecics
. . .
Natural enemies
. . .
Pesticide
Resources
. . .
Natural enemies
. . .
Natural enemies
Conspecics
(mates and
intraspecic
competitors)
Pesticide
Resources
Natural enemies
Natural
enemies
(interspecic
competitors,
parasitoids,
predators,
pathogens)
Pesticide
Resources
Conspecics
Figure 1
(a) Weblike
representation of
potential direct and
indirect effects o f
pesticides departing
from a central
organism, and the
major environmental
components that
might influence the
central organism’s
chance of surviving,
reproducing, and
irradiating to
subsequent
interrelated
components. The
dotted lines denote the
continued progression
ofeffectsasinthe
central components of
the web, the ellipse
delimits the direct
interactions, and the
rectangle in which
panel a is set delimits
the progressive range
of potential indirect
interactions with the
central organism.
(b) Horizontal
progression expanded
from the weblike
representation in panel
a illustrating potential
direct and indirect
effects of pesticides
affecting a given
central organism.
46 Guedes et al.
Annu. Rev. Entomol. 2016.61:43-62. Downloaded from www.annualreviews.org
Access provided by Universidade Federal de Vicosa on 04/23/18. For personal use only.

EN61CH03-Guedes ARI 13 February 2016 7:45
Increasing response time
Pesticide
Population
Organism
Endosymbiont
Physiological
process
Assemblage/
community
Inferential strength to assign causation
Figure 2
Schematic hierarchical representation of the chain of potential effects of pesticides.
provides the mechanistic basis of pesticide-induced stress tolerance and resistance. Protective
responses may also involve shifts in metabolism, particularly digestive and energy metabolism,
allowing physiological trade-offs that favor protective mechanisms leading to survival at the ex-
pense of body growth and/or reproduction (74, 136), as is apparently the case for the maize weevil
(Sitophilus zeamais) (6, 60, 89).
Differing pesticide target-site sensitivity, detoxification, sequestration, excretion, and pene-
tration allow for the differential physiological toxicity of pesticides, a subject widely explored in
insecticide resistance and selectivity studies (35, 36, 140). In addition to these physiological mech-
anisms, reduced pesticide exposure based on behavior should also be considered because it may
play a fundamental role in pesticide efficacy and its consequences (53, 68). Both physiological and
behavioral responses may also be non-self-determined when considering the individual arthropod
as a symbiont-inhabited ecocosm in which endosymbionts play relevant roles, allowing their host
better adaptation to the external environment (44, 127). Evidence of endosymbiont-mediated
arthropod adaptation to chemical plant defenses should not be a surprise (126); therefore, en-
dosymbionts are also likely to play significant roles mediating arthropod responses to insecticidal
stress (21, 77, 129). The latter issue has received little attention and is worthy of further study.
www.annualreviews.org
•
Pesticide-Induced Stress in Arthropod Pests 47
Annu. Rev. Entomol. 2016.61:43-62. Downloaded from www.annualreviews.org
Access provided by Universidade Federal de Vicosa on 04/23/18. For personal use only.

Frequently asked questions

Q1. What contributions have the authors mentioned in the paper "Pesticide-induced stress in arthropod pests for optimized integrated pest management programs" ?

The present review mitigates this shortcoming by hierarchically exploring within an ecotoxicology framework applied to integrated pest management the myriad effects of insecticide use on arthropod pest species. 43 Click here to view this article 's online features: • Download figures as PPT slides • Navigate linked references • Download citations • Explore related articles • Search keywords ANNUAL REVIEWS Further A nn u. R ev. In this review, the authors hierarchically explore within an ecotoxicology framework the multitude of responses sparked by pesticide use against arthropod pest species. Furthermore, pesticides can be justifiably recognized as pollutants because they are environmental contaminants that adversely affect living species. The importance of the lethal effects of insecticides can not be denied ; however, underestimating potential sublethal effects of pesticides on target organisms and their potential ecological consequences is a mistake. Furthermore, nontarget species, including secondary arthropod pest species, can be exposed to sublethal concentrations of pesticides for long periods, leading to unforeseeable consequences such as pest outbreaks ( 34, 62 ). The population-level effect on a given species can translate into a community-level effect, adding another hierarchical level of pesticide-induced stress and emphasizing the complexity of effects that may potentially accrue from pesticide use ( Figure 2 ). Colony suppression requires the unaffected foragers to carry the toxic bait to the nest, impairing the colony either by directly compromising the fungus garden ( as a fungicide ) and its cultivation by the minor workers or by impairing progeny production by the ant queen ( 3, 4, 40 ). 

Q2. What are the main factors that influence the toxicity of pesticides?

Differing pesticide target-site sensitivity, detoxification, sequestration, excretion, and penetration allow for the differential physiological toxicity of pesticides, a subject widely explored in insecticide resistance and selectivity studies (35, 36, 140). 

Q3. What are the components of the arthropod behavioral avoidance response to pesticide exposure?

Repellence (i.e., the behavioral response after extensive contact with a pesticide) and irritability (i.e., the behavioral response with little or no pesticide contact) are two components of the arthropod behavioral avoidance response to pesticide exposure that are usually neglected in studies of arthropod pest species, unlike natural enemies (26, 41, 54, 88). 

Q4. What is the intriguing and counterintuitive consequence of pesticide use?

An intriguing and counterintuitive consequence of pesticide use (or overuse) for pest management programs is increased pest abundance, leading to pest outbreaks. 

Q5. What is the widely studied ecological backlash of the pesticide paradox?

Insecticide resistance is a long-term (evolutionary) consequence of insecticide overuse and is the best-known and most widely studied ecological backlash of the pesticide paradox (e.g., 87, 140). 

Q6. What are the main topics of interest in pesticide-induced stress?

5. Pesticide-induced hormesis and behavior-mediated responses are current topics of interest and might explain pesticide-induced outbreaks of arthropod pest species. 

Q7. Why is pesticide-mediated competition a potential mechanism of secondary pest outbreaks?

Because pesticide exposure may shift the dominance of competing species sharing the same niche (32, 50, 128), pesticidemediated competition is another potential mechanism of secondary pest outbreaks that deserves attention. 

Q8. What are some of the other traits that are important for determining population size?

other life-history traits, such as fertility, life span, and age at which first reproduction occurs, are important for determining population size, and these traits vary among species and are potentially affected by pesticide exposure (123). 

Q9. What is the current toxicity endpoint of interest for arthropod pests?

Current regulatory processes of pesticide risk assessment and pesticide registration in both the United States and the European Union encourage the use of acute mortality as the toxicity endpoint of interest for both target and nontarget species. 

Q10. What is the definition of a quantal dose-response relationship?

A quantal dose-response relationship represents the variation in response due to increased doses of a compound, translating the effect from each individual, in which the response is assessed, to the population (i.e., an interbreeding group of individuals within the same species). 

Q11. What is the primary endpoint used to estimate the response to pesticide-induced stress?

Regarding the response to pesticide-induced stress, mortality is the primary endpoint used to estimate prevalent toxicological endpoints, namely the median lethal dose (LD50) (or concentration, LC50), or analogous estimates, and eventually the no observable effect dose (NOED) (or concentration, NOEC). 

Q12. What is the role of pesticides in creating the initial community context?

Pesticides themselves may not only affect a community but may also play a relevant role in creating the initial community context, such as influencing the pattern of species colonization of a contaminated area, a possibility that has also been largely neglected (138). 

Q13. What are the main reasons for the lack of impact of pesticides on arthropod communities?

their nontarget impacts and their potential to negatively affect arthropod communities associated with agroecosystems, for instance, may compromise pollinators and detritivorous arthropods important for enhancing crop yield (10, 41, 67, 119). 

Q14. What are the challenges for pesticide use in arthropod pest management?

The role of endosymbionts in arthropod pesticide-induced stress, the increased use of pesticide mixtures for plant and animal protection, and landscape diversity pose new challenges for pesticide use in arthropod pest management when most of the existing challenges remain broadly unrecognized. 

Q15. What is the common focus of pesticide-induced stress in arthropod pest species?

The prevailing focus of pesticide-induced stress in arthropod pest species is usually circumscribed to short-term mortality effects on the pest species and some natural enemies, which are either perceived as important for control or used as surrogate species in these assessments, although the latter use is often dubious, if not questionable (12, 13). 

Q16. What are the main concerns of pesticide use?

Pesticide use poses concerns for human health and environmental safety, which are broadly recognized, but also poses risks to agriculture, disease prevention, and pest management, which are not frequently recognized. 

Q17. What are the main effects of pesticides on arthropods?

Pesticides affect individual arthropods, the consequences of which may manifest at higher hierarchical levels, i.e., populations and communities. 

Q18. What are the effects of pesticides on the physiology of an organism?

Both direct and indirect effects of an applied pesticide could impair the physiology of an organism, reducing its survival and/or reproduction.