Available online at www.sciencedirect.
com
ScienceDirect
Newer characters, same story: neonicotinoid
insecticides disrupt food webs through direct and
indirect effects
John F Tooker and Kirsten A Pearsons
During the Green Revolution, older classes of insecticides
contributed to biodiversity loss by decreasing insect
populations and bioaccumulating across food webs.
Introduction of Integrated Pest Management (IPM) improved
stewardship of insecticides and promised fewer non-target
effects. IPM adoption has waned in recent decades, and
popularity of newer classes of insecticides, like the
neonicotinoids, has surged, posing new and unique threats to
insect populations. In this review, we first address how older
classes of insecticides can affect trophic interactions, and then
consider the influence of neonicotinoids on food webs and the
role they may be playing in insect declines. We conclude by
discussing challenges posed by current use patterns of
neonicotinoids and how their risk can be addressed.
Address
Department of Entomology, Merkle Lab, The Pennsylvania State Uni-
versity, University Park, PA, USA
Corresponding author: Tooker, John F (tooker@psu.edu)
Current Opinion in Insect Science 2021, 46:50–56
This review comes from a themed issue on Pollinator decline: human
and policy dimensions
Edited by Jeroen van der Sluijs, Stephane Foucart and Jérôme
Casas
https://doi.org/10.1016/j.cois.2021.02.013
2214-5745/ã 2021 Elsevier Inc. All rights reserved.
Introduction
Accounting for the majority of animal biodiversity, insects
are integral links in most terrestrial and freshwater food
webs. Potential declines in insect abundance and diver-
sity, however, may destabilize food webs across the globe.
Among drivers that could be contributing to insect
declines, climate change and habitat loss have, by some
measures, garnered most of the attention [1]. In contrast,
less attention has focused on insecticide use, despite
being a likely contributor to biodiversity losses generally
[2,3], and insect declines specifically [4,5]. Insecticides
were highlighted as the primary culprit for biodiversity
Current Opinion in Insect Science 2021, 46:50–56
loss in Silent Spring [6], yet widespread insecticide use and
contamination has only grown since the 1950s [1,7].
Insecticides can have great value for pest management,
particularly when used within the framework provided by
integrated pest management (IPM) [8,9]. As originally
envisioned, IPM relies on cultural tactics and natural-
enemy populations to help prevent pest populations from
causing economic damage, with insecticides reserved as
last resorts [8,10,11]. Unfortunately, the value of insecti-
cides as insurance against pests has driven a steady shift
away from IPM, and towards preventative seed-based
pest management options (e.g., transgenic traits, seed-
applied pesticides) [12,13], especially in large-acreage
crops (e.g., maize, soybeans, cotton, etc.). Because of this
insurance-based approach, insecticides are now applied
on more crop acres than at any time in history [1,7],
providing more opportunities for insecticides to affect
non-pest insects and other taxa. Non-target insects may
encounter insecticides directly at the time of application
or by coming into contact with contaminated media (e.g.,
soil, sediment, or water), or indirectly when insecticidal
compounds move via trophic connections in food webs.
Carson [6] revealed consequences of such effects of
insecticides on food webs, ranging from the direct loss
of animals at the base of food webs to the indirect loss of
animals on higher trophic levels that were vulnerable to
magnified insecticide concentrations in their prey.
Despite stoking public outrage and fueling environmen-
talism, Silent Spring appears to have done little to curb
enthusiasm for insecticides—usage in the U.S. continued
to increase after its publication and those increases con-
tinue today [1,14]. By the 1970s, as regulations limited use
of DDT and other organochlorines, insecticides from
other classes (e.g., organophosphates, carbamates, and
pyrethroids) were there to lessen the blow. More recently,
insecticide use has been driven by neonicotinoids, a class
of insecticides that is far more toxic to insects than its
predecessors, and whose toxicity to other groups of ani-
mals, including vertebrates and non-insect invertebrates,
needs to be clarified. The ubiquity of neonicotinoids
poses a threat to non-target insects, and may be playing
a role in some recently documented animal declines
[15,16].
In this paper, we will briefly review how older classes of
insecticides affect food webs, then, as a comparison, we
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will focus on neonicotinoids to consider their influences
on food webs and potential roles in insect declines.
General influence of insecticides on trophic
interactions and food webs
Any insecticide can disrupt a food web when susceptible
species directly encounter toxic residues at the time of
application or come into contact with contaminated
media. This environmental exposure, at lethal or suble-
thal levels, can weaken links in food webs and, depending
on the trophic level affected, can reduce prey availability,
alter competition, and release prey from top-down control
[15,17–27]. More nuanced is how insecticides can disrupt
food chains by moving up trophic levels.
Organochlorine insecticides (especially DDT) disrupt
food chains by limiting insect abundance and, more
notoriously, disturb trophic cascades [17,28]. Because
they bioaccumulate in fatty animal tissue, organochlorine
concentrations can increase as predators consume con-
taminated prey. In both aquatic and terrestrial systems,
this biomagnification phenomenon can burden top verte-
brate predators with much higher, toxic concentrations
than lower trophic levels [17,29,30].
Like organochlorines, other synthetic insecticides (e.g.,
certain organophosphates and pyrethroids) can biomag-
nify and endanger higher trophic levels [17,31–33],
although significant bioaccumulation is rare due to rapid
degradation (most carbamates and organophosphates)
[18,34], metabolism (most pyrethroids) [35] and elimina-
tion (most neonicotinoids) [36]. However, even com-
pounds that do not readily bioaccumulate can disrupt
trophic cascades when sensitive prey become scarce and
when sensitive predators (both invertebrate and verte-
brate) consume contaminated prey [18,32].
Influence of neonicotinoids on trophic
interactions and food webs
Through ubiquitous use and unique chemistry, neonicoti-
noids are poised to distort food webs by significantly
decreasing insect abundance and diversity [37,38]. Indeed,
widespread adoption of neonicotinoids, mainly in large-
acreage row-crop agriculture, has turned regions of North
America and Europe into increasingly less hospitable, even
toxic, landscapes for insects [39,40,41,42]. Moreover, the
chemical characteristics of neonicotinoids (e.g., higher
water solubility and persistence in soil) [43] facilitate con-
tamination of unintended locations (e.g., aquatic environ-
ments, natural habitats, organic crop fields) [44,45,46,47],
where these toxic insecticides [48] can negatively affect
sensitive taxa [37,38].
To address the influence of neonicotinoids on food webs,
we review how sensitive arthropod taxa come into contact
with toxic doses of neonicotinoids, and how such expo-
sure can spread through food webs.
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Neonicotinoids and food webs Tooker and Pearsons 51
Routes of exposure for primary invertebrate
consumers
Primary consumers, especially insect herbivores and omni-
vores, will encounter neonicotinoids when they feed on
treated plants (Figure 1). Primary consumers can receive
lethal and sublethal doses of neonicotinoids by feeding on
the roots, leaves, xylem, phloem, pollen, nectar, and extra-
floral nectar of treated plants [48,49,50,51] (Exposure
routes for pollinators have been addressed in detail
elsewhere [52–55]). Untreated plants can also pose a
risk, because the chemical characteristics that allow neoni-
cotinoids to translocate into treated plants also allow move-
ment into untreated plants from contaminated soil or water
(Figure 1) [56–60]. Even mycophagous insects can encoun-
ter lethal doses when feeding on plant-parasitic fungi that
absorbed neonicotinoids from their host plants [61].
Primary consumers of dead plant material can also
encounter lethal and sublethal doses of neonicotinoids
when feeding on senesced tissues of treated plants
(Figure 1) [62–64]. Earthworms specifically can accu-
mulate neonicotinoids to levels that impair their
behavior and ecological function [47,65–68]. For
decomposers and detritivores in general, exposure to
neonicotinoids via substrates can be just as important as
dietary exposures [69]; neonicotinoid residues in soil,
sediment, and water can disrupt decomposition pro-
cesses in both terrestrial [37,38,70] and aquatic systems
[64,71–74].
Routes of exposure for secondary
invertebrate consumers
Secondary consumers, such as predaceous and parasitic
insects, can also encounter lethal and sublethal doses of
neonicotinoids through multiple routes (Figure 1). As with
primary consumers, predators and omnivores can encounter
neonicotinoid residues when they feed on contaminated
plant tissues such as floral resources, extrafloral nectar, or
guttationdroplets[51,75–77].Predatorscanalsoingesttoxic
doses of neonicotinoids via trophic interactions, such as
when they prey on or scavenge herbivorous invertebrates
that acquired neonicotinoids from plants. This trophic
transfer can facilitate pest outbreaks by releasing herbivore
populations from top-down control; such effects have been
documented with both non-insect herbivores that have low
susceptibility to neonicotinoids (e.g., mites and slugs)
[24,67] and herbivorous insects that received sublethal
doses of neonicotinoids (e.g., scale insects, aphids, crickets)
[78–80]. Secondary consumers can also encounter neoni-
cotinoids when feeding on contaminated honeydew
produced by phloem-feeding, hemipteran insects, such
as aphids, mealybugs, and scales [50,81]. For highly
omnivorous and opportunistic consumers like ants, neoni-
cotinoid exposure can be cumulative; when utilizing
contaminated prey, floral resources, extrafloral nectar, hon-
eydew, even seeds from non-target plants, ants can be
burdened with compounding exposure to neonicotinoids,
Current Opinion in Insect Science 2021, 46:50–56
52 Pollinator decline: human and policy dimensions
Figure 1
Routes of exposures for primary and secondary consumers to neonicotinoid insecticides applied to crop plants via coated seeds or trees via soil
drenches.
which can reduce colony fitness and alter ant community
composition [82,83].
Influence of neonicotinoids on food webs
Despite their unique chemistry and toxicity, neonicoti-
noids influence food webs via the same two mechanisms
that are seen for older insecticide classes: directly simpli-
fying food webs and indirectly by moving within food
webs. First, neonicotinoids can influence food webs by
directly reducing the abundance and diversity of consu-
mers [37,38]. When lower trophic levels are directly
affected, members of higher trophic levels (especially
specialists) may suffer from prey scarcity. Evidence for
this mechanism comes from various systems (e.g., crop-
lands, forests, and waterways), where neonicotinoids have
simplified and depopulated insect communities, reducing
abundance of animals at higher trophic levels (e.g.,
insects, birds, and fishes) [15,64,72,73,84–86,87,88].
One of the more notable of these examples resulted from
neonicotinoid use in rice, where neonicotinoid contami-
nation in agricultural runoff greatly decreased abundance
Current Opinion in Insect Science 2021, 46:50–56
Current Opinion in Insect Science
of zooplankton and aquatic insects in a large lake, causing
commercial fisheries to collapse by about 90% [87].
Second, neonicotinoids can move across trophic levels
within food webs, causing sublethal and lethal effects
along the way. We presented some of this evidence above
(Routes of exposure for secondary invertebrate consumers), but,
because neonicotinoids are generally not thought to
bioaccumulate, these examples mostly involved move-
ment of neonicotinoids between taxa occupying adjacent
trophic levels. Recently, however, a few studies appear to
have found evidence for neonicotinoid bioaccumulation
[47,89]. Imidacloprid used to protect hemlock trees was
found in benthic invertebrates and salamanders collected
from nearby streams [88]; higher-than-expected imida-
cloprid levels in the salamanders suggested that salaman-
ders were accumulating toxic levels of imidacloprid
through their invertebrate-rich diet [89]. Moreover,
earthworms may accumulate neonicotinoids from soil
[47], which is concerning given previous research doc-
umenting sub-lethal effects of neonicotinoids on
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earthworms [65,66,68] and their role as an important prey
resource for a diversity of insects and birds. However,
even in the more common situations where neonicoti-
noids do not bioaccumulate, these highly toxic com-
pounds can still disrupt food webs when sensitive taxa
occupy higher trophic levels.
Conclusions
Based on their ubiquity and available evidence, neonicoti-
noids are likely to be playing a role in insect declines [4,5]
via direct and indirect effects on food webs. The scale of their
influence, however, is unclear. Although neonicotinoids can
move across trophic levels, their main influence on food webs
is likely through simplification, where direct exposure to
neonicotinoids decreases abundance of sensitive taxa, caus-
ing effects that can ripple through food webs [15,87].
These simplifying effects are reinforced and exacerbated
by 1) annual inputs of neonicotinoids over large areas
[39,40,41,42], 2) the likelihood that sensitive taxa in these
areas will encounter neonicotinoids through multiple routes
of exposure (Figure 1), and 3) their time-cumulative toxicity,
which increases sensitivity of taxa with repeated exposure
[90].
While older classes of insecticides affected food webs via
broad toxicity and/or biomagnification, the effect of neo-
nicotinoids appears to result from a combination of the
unprecedented scale of their use and their more insidious,
but perhaps just as broad toxicity to invertebrate and
vertebrate animals. Neonicotinoids have been deployed
over the past two decades at a remarkable scale
[39,40,41,42,91,92], and many ecological concerns
attributable to neonicotinoids would be greatly dimin-
ished if they were simply used less frequently and over
smaller areas. Frequent and widespread use, coupled with
relatively high water solubility, means that significant
movement of neonicotinoids into non-target habitats is
virtually inevitable [44,45,46,47]. When neonicotinoids
arrive in non-target habitats, the traits that make them
valuable for pest control (i.e., high insect specificity and
toxicity) [48] become a liability. These traits allow neo-
nicotinoids to weaken insect populations and simplify
food web, but perhaps with fewer apparent effects on
vertebrates (e.g., fish, and mammals) that, in the past,
signaled the ecological risks posed by insecticides (but
see [93,94]). Nevertheless, neonicotinoids appear to be
more toxic to some taxa than expected, causing serious
problems for some vertebrates, particularly birds, which
appear to be suffering from prey scarcity and direct
exposure, and these concerns need to be taken seriously
[15,95,96].
As widespread use of neonicotinoids is driving their
influence on insect declines and food webs, the best path
forward is to decrease the scale and frequency of neoni-
cotinoids use, particularly where their preventative
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Neonicotinoids and food webs Tooker and Pearsons 53
deployment as seed coatings clearly outstrips their need
[97,98]. Such decreases could be facilitated by wider
adoption of IPM, hewing more closely to its original
vision of embracing natural enemies as allies in pest
control, and embracing risk assessment and pest control
alternatives provided by some conservation-based farm-
ing methods [8,9,99–102]. Although reducing neonicoti-
noid use through IPM could help growers maintain profits
and would protect the long-term viability of neonicoti-
noids, a widespread return to IPM, at least in the U.S.,
seems unlikely in the short term given ongoing increases
in insecticide use and financial incentives of large agri-
cultural companies to maintain the status quo [1,14].
Unfortunately, the alternative is to implement stronger
regulatory controls on neonicotinoids. This option, which
has been put into effect in Europe [103], is understand-
ably distasteful for many farmers and their allies, but
stronger regulations may become necessary if use patterns
do not change voluntarily and evidence of the negative
influence of neonicotinoids on animal populations con-
tinues to mount [104].
Declarations of interests
None.
Acknowledgements
We thank the editors for the invitation to contribute this manuscript.
Thanks to N. Sloff (Penn State) for creating the figure. Funding for this
article was provided by USDA AFRI competitive grant 2017-67013-26594
and the College of Agricultural Sciences at Penn State via the National
Institute of Food and Agriculture and Hatch Appropriations under Project
#PEN04606 and Accession #1009362.
References and recommended reading
Papers of particular interest, published within the period of review,
have been highlighted as
 of special interest
 of outstanding interest
1. Bernhardt ES, Rosi EJ, Gessner MO: Synthetic chemicals as
agents of global change. Front Ecol Environ 2017, 15:84-90.
2. McLaughlin A, Mineau P: The impact of agricultural practices on
biodiversity. Agric Ecosyst Environ 1995, 55:201-212.
3. Hayes TB, Hansen M: From silent spring to silent night:
agrochemicals and the anthropocene. Elementa 2017, 5:57.
4. Sánchez-Bayo F, Wyckhuys KA: Worldwide decline of the
 entomofauna: a review of its drivers. Biol Conserv 2019,
232:8-27.
This extensive review offers assessments of potential drivers of insect
declines around the world.
5. Wagner DL: Insect declines in the Anthropocene. Annu Rev
 Entomol 2020, 65:457-480.
This comprehensive review of insect declines addresses a wide range of
potential causes, including agricultural intensification and insecticide use.
Topics also include declines of insect-eating animals, reporting biases,
and the challenge of measuring declines over time.
6. Carson R: Silent Spring. Houghton Mifflin Company; 1962.
7. Stehle S, Schulz R: Agricultural insecticides threaten surface
waters at the global scale. Proc Natl Acad Sci U S A 2015,
112:5750-5755.
Current Opinion in Insect Science 2021, 46:50–56
54 Pollinator decline: human and policy dimensions
8. Stern VM, Smith R, Van den Bosch R, Hagen K: The integration of
chemical and biological control of the spotted alfalfa aphid:
the integrated control concept. Hilgardia 1959, 29:81-101.
9. Kogan M: Integrated pest management: historical
perspectives and contemporary developments. Annu Rev
Entomol 1998, 43:243-270.
10. Smith R, Hagen K: The integration of chemical and biological
control of the spotted alfalfa aphid: impact of commercial
insecticide treatments. Hilgardia 1959, 29:131-154.
11. Stern V, van den Bosch R: The integration of chemical and
biological control of the spotted alfalfa aphid: field
experiments on the effects of insecticides. Hilgardia 1959,
29:103-130.
12. Gray ME: Relevance of traditional integrated pest
management (IPM) strategies for commercial corn producers
in a transgenic agroecosystem: a bygone era? J Agric Food
Chem 2011, 59:5852-5858.
13. Hurley TM, Sun H: Softening shock and awe pest management
in corn and soybean production with IPM principles. J Integr
Pest Manag 2019, 10:7.
14. Pesticides M: A Love Story: America’s Enduring Embrace of
Dangerous Chemicals. University Press of Kansas; 2015.
15. Hallmann CA, Foppen RP, van Turnhout CA, de Kroon H,
Jongejans E: Declines in insectivorous birds are associated
with high neonicotinoid concentrations. Nature 2014,
511:341-343.
16. Hallmann CA, Sorg M, Jongejans E, Siepel H, Hofland N,
Schwan H, Stenmans W, Müller A, Sumser H, Hörren T, Goulson D:
More than 75 percent decline over 27 years in total flying
insect biomass in protected areas. PLoS One 2017, 12:
e0185809.
17. Brown AW: Ecology of Pesticides. John Wiley & Sons; 1978.
18. Hill EF: Wildlife toxicology of organophosphorus and
carbamate pesticides. In Handbook of Ecotoxicology, edn 2.
Edited by Hoffman DJ. Lewis Publishers; 2003:281-312.
19. Kenne M, DjiéJito-Lordon C, Orivel J, Mony R, Fabre A, Dejean A:
Influence of insecticide treatments on ant-hemiptera
associations in tropical plantations. J Econ Entomol 2003,
96:251-258.
20. Fleeger JW, Carman KR, Nisbet RM: Indirect effects of
contaminants in aquatic ecosystems. Sci Total Environ 2003,
317:207-233.
21. Boatman ND, Brickle NW, Hart JD, Milsom TP, Morris AJ,
Murray AW, Murray KA, Robertson PA: Evidence for the indirect
effects of pesticides on farmland birds. Ibis 2004, 146:131-143.
22. Relyea RA, Diecks N: An unforeseen chain of events: lethal
effects of pesticides on frogs at sublethal concentrations. Ecol
Appl 2008, 18:1728-1742.
23. Markó V, Keresztes B, Fountain MT, Cross JV: Prey availability,
pesticides and the abundance of orchard spider communities.
Biol Control 2009, 48:115-124.
24. Szczepaniec A, Creary SF, Laskowski KL, Nyrop JP, Raupp MJ:
Neonicotinoid insecticide imidacloprid causes outbreaks of
spider mites on elm trees in urban landscapes. PLoS One 2011,
6:e20018.
25. Kerby JL, Sih A: Effects of carbaryl on species interactions of
the foothill yellow legged frog (Rana boylii) and the Pacific
treefrog (Pseudacris regilla). Hydrobiologia 2015, 746:255-269.
26. Rogers HA, Schmidt TS, Dabney BL, Hladik ML, Mahler BJ, Van
Metre PC: Bifenthrin causes trophic cascade and altered
insect emergence in mesocosms: implications for small
streams. Environ Sci Technol 2016, 50:11974-11983.
27. Schroeder-Spain K, Smee DL: Dazed, confused, and then
hungry: pesticides alter predator–prey interactions of
estuarine organisms. Oecologia 2019, 189:815-828.
28. Hickey JJ, Keith JA, Coon FB: An exploration of pesticides in a
Lake Michigan ecosystem. J Appl Ecol 1966, 1:141-154.
Current Opinion in Insect Science 2021, 46:50–56
29. Barker RJ: Notes on some ecological effects of DDT sprayed
on elms. J Wildl Manage 1958, 22:269.
30. Okoniewski JC, Stone WB, Hynes KP: Continuing
organochlorine insecticide mortality in wild birds in New York,
2000–2004. Bull Environ Contam Toxicol 2006, 77:726-731.
31. Favari L, López E, Martı’nez-Tabche L, Dıaz-Pardo E: Effect of
insecticides on plankton and fish of Ignacio Ramirez reservoir
(Mexico): a biochemical and biomagnification study.
Ecotoxicol Environ Saf 2002, 51:177-186.
32. Elliott JE, Wilson LK, Vernon R: Controlling wireworms without
killing wildlife in the Fraser River Delta. In Wildlife
Ecotoxicology. Edited by Elliott JE, Bishop CA, Morrissey C.
Springer; 2011:213-237.
33. Corcellas C, Eljarrat E, Barceló D: First report of pyrethroid
bioaccumulation in wild river fish: a case study in Iberian river
basins (Spain). Environ Int 2015, 75:110-116.
34. Downing AL, DeVanna KM, Rubeck-Schurtz CN, Tuhela L,
Grunkemeyer H: Community and ecosystem responses to a
pulsed pesticide disturbance in freshwater ecosystems.
Ecotoxicology 2008, 17:539-548.
35. You J, Brennan A, Lydy MJ: Bioavailability and
biotransformation of sediment-associated pyrethroid
insecticides in Lumbriculus variegatus. Chemosphere 2009,
75:1477-1482.
36. Lewis KA, Tzilivakis J, Warner DJ, Green A: An international
database for pesticide risk assessments and management.
Hum Ecol Risk Assess 2016, 22:1050-1064.
37. Pisa LW, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Downs CA,
Goulson D, Kreutzweiser DP, Krupke C, Liess M, McField M,
Morrissey CA: Effects of neonicotinoids and fipronil on non-
target invertebrates. Environ Sci Pollut Res 2015, 22:68-102.
38. Pisa L, Goulson D, Yang EC, Gibbons D, Sánchez-Bayo F,
Mitchell E, Aebi A, van der Sluijs J, MacQuarrie CJ, Giorio C,
Long EY: An update of the Worldwide Integrated Assessment
(WIA) on systemic insecticides. Part 2: impacts on organisms
and ecosystems. Environ Sci Pollut Res 2017, 9:1-49.
39. Goulson D, Thompson J, Croombs A: Rapid rise in toxic load for
bees revealed by analysis of pesticide use in Great Britain.
PeerJ 2018, 6:e5255.
40. DiBartolomeis M, Kegley S, Mineau P, Radford R, Klein K: An
 assessment of acute insecticide toxicity loading (AITL) of
chemical pesticides used on agricultural land in the United
States. PLoS One 2019, 14:e0220029.
Based on publicly available pesticide-use data, this study calculated the
acute insecticide toxicity loading for U.S. agricultural areas. They found
that from 1992 to 2014 that toxicity relative to honey bees increased by as
much as 48-fold, largely due to use of neonicotinoids as seed coatings on
large acreage crops.
41. Douglas MR, Sponsler DB, Lonsdorf EV, Grozinger CM: County-
 level analysis reveals a rapidly shifting landscape of
insecticide hazard to honey bees (Apis mellifera) on US
farmland. Sci Rep 2020, 10:797.
By integrating data from several public sources, this study reveals that
landscape-level ‘oral-based toxic load’ for honey bees has increased
ninefold in recent decades. This toxic load varies across different regions
of the U.S., and appears to be driven by neonicotinoids coated on large-
acreage crops
42. Malaj E, Freistadt L, Morrissey CA: Spatio-temporal patterns of
crops and agrochemicals in Canada over 35 years. Front
Environ Sci 2020, 8:208.
43. Wood TJ, Goulson D: The environmental risks of neonicotinoid
pesticides: a review of the evidence post 2013. Environ Sci
Pollut Res 2017, 24:17285-17325.
44. Morrissey CA, Mineau P, Devries JH, Sanchez-Bayo F, Liess M,
Cavallaro MC, Liber K: Neonicotinoid contamination of global
surface waters and associated risk to aquatic invertebrates: a
review. Environ Int 2015, 74:291-303.
45. Hladik ML, Vandever M, Smalling KL: Exposure of native bees
foraging in an agricultural landscape to current-use
pesticides. Sci Total Environ 2016, 542:469-477.
www.sciencedirect.com

46. Humann-Guilleminot S, Binkowski ŁJ, Jenni L, Hilke G, Glauser G,
 Helfenstein F: A nation-wide survey of neonicotinoid
insecticides in agricultural land with implications for agri-
environment schemes. J Appl Ecol 2019, 56:1502-1514.
This study sampled soil and plants from organic farms and habitats set
aside for ecological protection, and screened them for neonicotinoids.
Neonicotinoids were detected in 93% of samples from organic farms and
80% of set-aside habitats. Calculated hazard quotients revealed that up
to 9% and 41% of beneficial invertebrate species could encounter lethal
and sublethal doses, respectively, of clothianidin.
47. Pelosi C, Bertrand C, Daniele G, Coeurdassier M, Benoit P,
 Nélieu S, Lafay F, Bretagnolle V, Gaba S, Vulliet E, Fritsch C:
Residues of currently used pesticides in soils and
earthworms: a silent threat? Agric Ecosyst Environ 2020,
305:107167.
This study sampled earthworms in agricultural fields in France and found
them to contain mixtures of insecticides, fungicides, and herbicides.
Earthworms contained elevated concentrations of neonicotinoids relative
to the soil in which they were found, suggesting that these insecticides
can bioaccumulate in some scenarios.
48. Jeschke P, Nauen R: Neonicotinoids—from zero to hero in
insecticide chemistry. Pest Manag Sci 2008, 64:1084-1098.
49. Moscardini VF, Gontijo PC, Michaud JP, Carvalho GA: Sublethal
effects of chlorantraniliprole and thiamethoxam seed
treatments when Lysiphlebus testaceipes feed on sunflower
extrafloral nectar. BioControl 2014, 59:503-511.
50. Calvo-Agudo M, González-Cabrera J, Picó Y, Calatayud-
 Vernich P, Urbaneja A, Dicke M, Tena A: Neonicotinoids in
excretion product of phloem-feeding insects kill beneficial
insects. Proc Nat Acad Sci U S A 2019, 116:16817-16822.
Phloem-feeding insects often excrete honeydew, which can be a source
of carbohydrates for beneficial insect species. This lab-based study
demonstrated that honeydew produced by mealybugs feeding on neo-
nicotinoid-treated trees can expose natural enemies to these insecti-
cides, causing significant mortality.
51. Zioga E, Kelly R, White B, Stout JC: Plant protection product
residues in plant pollen and nectar: a review of current
knowledge. Environ Res 2020, 189:109873.
52. Blacquiere T, Smagghe G, Van Gestel CA, Mommaerts V:
Neonicotinoids in bees: a review on concentrations, side-
effects and risk assessment. Ecotoxicology 2012, 21:973-992.
53. Whitehorn PR, O’connor S, Wackers FL, Goulson D:
Neonicotinoid pesticide reduces bumble bee colony growth
and queen production. Science 2012, 336:351-352.
54. Rundlöf M, Andersson GK, Bommarco R, Fries I, Hederström V,
Herbertsson L, Jonsson O, Klatt BK, Pedersen TR, Yourstone J,
Smith HG: Seed coating with a neonicotinoid insecticide
negatively affects wild bees. Nature 2015, 521:77-80.
55. Woodcock BA, Bullock JM, Shore RF, Heard MS, Pereira MG,
Redhead J, Ridding L, Dean H, Sleep D, Henrys P, Peyton J:
Country-specific effects of neonicotinoid pesticides on honey
bees and wild bees. Science 2017, 356:1393-1395.
56. Botı́as C, David A, Horwood J, Abdul-Sada A, Nicholls E, Hill E,
Goulson D: Neonicotinoid residues in wildflowers, a potential
route of chronic exposure for bees. Environ Sci Technol 2015,
49:12731-12740.
57. Main AR, Michel NL, Headley JV, Peru KM, Morrissey CA:
Ecological and landscape drivers of neonicotinoid insecticide
detections and concentrations in Canada’s prairie wetlands.
Environ Sci Technol 2015, 49:8367-8376.
58. Mogren CL, Lundgren JG: Neonicotinoid-contaminated
pollinator strips adjacent to cropland reduce honey bee
nutritional status. Sci Rep 2016, 6:1-10.
59. Bredeson MM, Lundgren JG: Neonicotinoid insecticidal seed-
treatment on corn contaminates interseeded cover crops
intended as habitat for beneficial insects. Ecotoxicology 2019,
28:222-228.
60. Alford AM, Krupke CH: Movement of the neonicotinoid seed
treatment clothianidin into groundwater, aquatic plants, and
insect herbivores. Environ Sci Technol 2019, 53:14368-14376.
www.sciencedirect.com
Neonicotinoids and food webs Tooker and Pearsons 55
61. Choudhury RA, Sutherland AM, Hengel MJ, Parrella MP,
Gubler WD: Imidacloprid movement into fungal conidia is lethal
to mycophagous beetles. Insects 2020, 11:496.
62. Kreutzweiser D, Good K, Chartrand D, Scarr T, Thompson D: Non-
target effects on aquatic decomposer organisms of
imidacloprid as a systemic insecticide to control emerald ash
borer in riparian trees. Ecotoxicol Environ Saf 2007, 68:315-325.
63. Kreutzweiser DP, Good KP, Chartrand DT, Scarr TA,
Thompson DG: Are leaves that fall from imidacloprid-treated
maple trees to control Asian Longhorned beetles toxic to
non-target decomposer organisms? J Environ Qual 2008,
37:639-646.
64. Lima-Fernandes E, Bundschuh M, Bakanov N, Englert D, Schulz R,
Schäfer RB: Effects of a systemic pesticide along an aquatic
tri-trophic food chain. Bull Environ Contam Toxicol 2019,
103:507-514.
65. Dittbrenner N, Triebskorn R, Moser I, Capowiez Y: Physiological
and behavioural effects of imidacloprid on two ecologically
relevant earthworm species (Lumbricus terrestris and
Aporrectodea caliginosa). Ecotoxicology 2010, 19:1567-1573.
66. Dittbrenner N, Moser I, Triebskorn R, Capowiez Y: Assessment of
short and long-term effects of imidacloprid on the burrowing
behaviour of two earthworm species (Aporrectodea caliginosa
and Lumbricus terrestris) by using 2D and 3D post-exposure
techniques. Chemosphere 2011, 84:1349-1355.
67. Douglas MR, Rohr JR, Tooker JF: Neonicotinoid insecticide
travels through a soil food chain, disrupting biological control
of non-target pests and decreasing soya bean yield. J Appl
Ecol 2015, 52:250-260.
68. Van Hoesel W, Tiefenbacher A, König N, Dorn VM, Hagenguth JF,
Prah U, Widhalm T, Wiklicky V, Koller R, Bonkowski M, Lagerlöf J:
Single and combined effects of pesticide seed dressings and
herbicides on earthworms, soil microorganisms, and litter
decomposition. Front Plant Sci 2017, 8:215.
69. Englert D, Zubrod JP, Pietz S, Stefani S, Krauss M, Schulz R,
Bundschuh M: Relative importance of dietary uptake and
waterborne exposure for a leaf-shredding amphipod exposed
to thiacloprid-contaminated leaves. Sci Rep 2017, 7:1-10.
70. Pearsons KA, Tooker JF: Preventive insecticide use affects
arthropod decomposers and decomposition in field crops.
Appl Soil Ecol 2021, 157:103757.
71. Wettstein FE, Kasteel R, Garcia Delgado MF, Hanke I, Huntscha S,
Balmer ME, Poiger T, Bucheli TD: Leaching of the neonicotinoids
thiamethoxam and imidacloprid from sugar beet seed
dressings to subsurface tile drains. J Agric Food Chem 2016,
64:6407-6415.
72. Miles JC, Hua J, Sepulveda MS, Krupke CH, Hoverman JT:
Effects of clothianidin on aquatic communities: evaluating the
impacts of lethal and sublethal exposure to neonicotinoids.
PLoS One 2017, 12:e0174171.
73. Cavallaro MC, Liber K, Headley JV, Peru KM, Morrissey CA:
Community-level and phenological responses of emerging
aquatic insects exposed to 3 neonicotinoid insecticides: an in
situ wetland limnocorral approach. Environ Toxicol Chem 2018,
37:2401-2412.
74. Frame ST, Pearsons KA, Elkin KR, Saporito LS, Preisendanz HE,
Karsten HD, Tooker JF: Assessing surface and subsurface
transport of neonicotinoid insecticides from no-till crop fields.
J Environ Qual 2021:1-9 http://dx.doi.org/10.1002/jeq2.20185.
75. Smith SF, Krischik VA: Effects of systemic imidacloprid on
Coleomegilla maculata (Coleoptera: Coccinellidae). Environ
Entomol 1999, 28:1189-1195.
76. Girolami V, Mazzon L, Squartini A, Mori N, Marzaro M, Di
Bernardo A, Greatti M, Giorio C, Tapparo A: Translocation of
neonicotinoid insecticides from coated seeds to seedling
guttation drops: a novel way of intoxication for bees. J Econ
Entomol 2009, 102:1808-1815.
77. Moser SE, Obrycki JJ: Non-target effects of neonicotinoid seed
treatments; mortality of coccinellid larvae related to
zoophytophagy. Biol Control 2009, 51:487-492.
Current Opinion in Insect Science 2021, 46:50–56
56 Pollinator decline: human and policy dimensions
78. Grafton-Cardwell EE, Gu P: Conserving vedalia beetle, Rodolia
cardinalis (Mulsant) (Coleoptera: Coccinellidae), in citrus: a
continuing challenge as new insecticides gain registration. J
Econ Entomol 2003, 96:1388-1398.
79. Seagraves MP, Lundgren JG: Effects of neonicitinoid seed
treatments on soybean aphid and its natural enemies. J Pest
Sci 2012, 85:125-132.
80. Uhl P, Bucher R, Schäfer RB, Entling MH: Sublethal effects of
imidacloprid on interactions in a tritrophic system of non-
target species. Chemosphere 2015, 132:152-158.
81. Quesada CR, Scharf ME, Sadof CS: Excretion of non-
metabolized insecticides in honeydew of striped pine scale.
Chemosphere 2020, 249:126167.
82. Penn HJ, Dale AM: Imidacloprid seed treatments affect
individual ant behavior and community structure but not egg
predation, pest abundance or soybean yield. Pest Manag Sci
2017, 73:1625-1632.
83. Schläppi D, Kettler N, Straub L, Glauser G, Neumann P: Long-
term effects of neonicotinoid insecticides on ants. Commun
Biol 2020, 3:1-9.
84. Dilling C, Lambdin P, Grant J, Rhea R: Community response of
insects associated with eastern hemlock to imidacloprid and
horticultural oil treatments. Environ Entomol 2009, 38:53-66.
85. Douglas MR, Tooker JF: Meta-analysis reveals that seed-
applied neonicotinoids and pyrethroids have similar negative
effects on abundance of arthropod natural enemies. PeerJ
2016, 4:e2776.
86. Disque HH, Hamby KA, Dubey A, Taylor C, Dively GP: Effects of
clothianidin-treated seed on the arthropod community in a
mid-Atlantic no-till corn agroecosystem. Pest Manag Sci 2019,
75:969-978.
87. Yamamuro M, Komuro T, Kamiya H, Kato T, Hasegawa H,
 Kameda Y: Neonicotinoids disrupt aquatic food webs and
decrease fishery yields. Science 2019, 366:620-623.
By capitalizing on insecticide sales data and long-term sampling history
of aquatic invertebrates and fish population, this study reveals a strong
influence of neonicotinoid insecticides on aquatic invertebrates that
support different populations of fishes. Notably, declines in key zoo-
plankton and insect species results in collapse of two commercial
fisheries.
88. Becker JM, Ganatra AA, Kandie F, Mühlbauer L, Ahlheim J,
Brack W, Torto B, Agola EL, McOdimba F, Hollert H, Fillinger U:
Pesticide pollution in freshwater paves the way for
schistosomiasis transmission. Sci Rep 2020, 10:1-3.
89. Crayton SM, Wood PB, Brown DJ, Millikin AR, McManus TJ,
 Simpson TJ, Ku KM, Park YL: Bioaccumulation of the pesticide
imidacloprid in stream organisms and sublethal effects on
salamanders. Glob Ecol Conserv 2020, 24:e01292.
This study provides evidence that imidacloprid used to protect hemlock
trees against an invasive pest species can leach into nearby streams,
where it and its toxic degradates enter the aquatic food web, eventually
bioaccumulating in salamanders with negative effects.
90. Tennekes HA, Sánchez-Bayo F: The molecular basis of simple
relationships between exposure concentration and toxic
effects with time. Toxicology 2013, 309:39-51.
91. Douglas MR, Tooker JF: Large-scale deployment of seed
treatments has driven rapid increase in use of neonicotinoid
insecticides and preemptive pest management in US field
crops. Environ Sci Tech 2015, 49:5088-5097.
92. Tooker JF, Douglas MR, Krupke CH: Neonicotinoid seed
treatments: limitations and compatibility with integrated pest
management. Agric Environ Lett 2017, 2:1-5.
Current Opinion in Insect Science 2021, 46:50–56
93. Gibbons D, Morrissey C, Mineau P: A review of the direct and
indirect effects of neonicotinoids and fipronil on vertebrate
wildlife. Environ Sci Pollut Res 2015, 22:103-118.
94. Berheim EH, Jenks JA, Lundgren JG, Michel ES, Grove D,
Jensen WF: Effects of neonicotinoid insecticides on
physiology and reproductive characteristics of captive female
and fawn white-tailed deer. Sci Rep 2019, 9:1-10.
95. Eng ML, Stutchbury BJ, Morrissey CA: A neonicotinoid
 insecticide reduces fueling and delays migration in songbirds.
Science 2019, 365:1177-1180.
This study of white-crowned sparrows used controlled dosing and auto-
mated telemetry to study migratory behavior of birds. Those birds that
ingested field-relevant amounts of neonicotinoid-coated seeds lost
weight and their migratory flights were significantly delayed.
96. Li Y, Miao R, Khanna M: Neonicotinoids and decline in bird
 biodiversity in the United States. Nat Sustain 2020, 10:1-9.
By comparing datasets on pesticide use and bird abundance, this study
demonstrates statistically that neonicotinoid insecticides are likely to be
causing decreases in bird populations in the U.S.
97. Labrie G, Gagnon AÈ, Vanasse A, Latraverse A, Tremblay G:
 Impacts of neonicotinoid seed treatments on soil-dwelling
pest populations and agronomic parameters in corn and
soybean in Quebec (Canada). PLos One 2020, 15:e0229136.
Agronomic trials in Quebec over four years revealed that <5% of corn and
soybean fields benefited from use of neonicotinoid coated seeds. The
results were driven by low pest populations and suggest that prophylactic
use of neonicotinoid was not warranted.
98. Smith JL, Baute TS, Schaafsma AW: Quantifying early-season
 pest injury and yield protection of insecticide seed treatments
in corn and soybean production in Ontario, Canada. J Econ
Entomol 2020, 113:2197-2212.
This four-year study in Ontario assessed the value of seed-applied
pesticides for corn and soy production. Their results indicated that only
8 and 6% of fields, respectively, experienced yield benefits from neoni-
cotinoid use, and a minority of the sites recovered the costs of deploying
neonicotinoid-coated seeds. Authors concluded that ‘there is little
demonstrate benefit’ to current use rates of neonicotinoids.
99. Furlan L, Contiero B, Chiarini F, Colauzzi M, Sartori E, Benvegnù I,
Fracasso F, Giandon P: Risk assessment of maize damage by
wireworms (Coleoptera: Elateridae) as the first step in
implementing IPM and in reducing the environmental impact
of soil insecticides. Environ Sci Pollut Res 2017, 24:236-251.
100. Furlan L, Pozzebon A, Duso C, Simon-Delso N, Sánchez-Bayo F,
Marchand PA, Codato F, van Lexmond MB, Bonmatin JM: An
update of the Worldwide Integrated Assessment (WIA) on
systemic insecticides. Part 3: alternatives to systemic
insecticides. Environ Sci Pollut Res 2018, 25:1-23.
101. Veres A, Wyckhuys KAG, Kiss J, Tóth F, Burgio G, Pons X, Avilla C,
Vidal S, Razinger J, Bazok R et al.: An update of the Worldwide
Integrated Assessment (WIA) on systemic pesticides. Part 4:
alternatives in major cropping systems. Environ Sci Pollut Res
2020, 27:29867-29899.
102. Busch AK, Douglas MR, Malcolm GM, Karsten HD, Tooker JF: A
high-diversity/IPM cropping system fosters beneficial
arthropod populations, limits invertebrate pests, and
produces competitive maize yields. Agric Ecosyst Environ 2020,
292:106812.
103. Klatt BK, Rundlöf M, Smith HG: Maintaining the restriction on
neonicotinoids in the European Union–benefits and risks to
bees and pollination services. Front Ecol Evol 2016, 4:4.
104. Krupke C, Tooker JF: Beyond the headlines: the influence of
insurance pest management on an unseen, silent
entomological majority. Front Sustain Food Syst 2020, 4:251.
www.sciencedirect.com