Choosing Organic Pesticides over Synthetic Pesticides
May Not Effectively Mitigate Environmental Risk in
Christine A. Bahlai1, Yingen Xue1, Cara M. McCreary1, Arthur W. Schaafsma2, Rebecca H. Hallett1*
1School of Environmental Sciences, University of Guelph, Guelph, Ontario, Canada, 2Department of Plant Agriculture, University of Guelph, Ridgetown, Ontario, Canada
Background: Selection of pesticides with small ecological footprints is a key factor in developing sustainable agricultural
systems. Policy guiding the selection of pesticides often emphasizes natural products and organic-certified pesticides to
increase sustainability, because of the prevailing public opinion that natural products are uniformly safer, and thus more
environmentally friendly, than synthetic chemicals.
Methodology/Principal Findings: We report the results of a study examining the environmental impact of several new
synthetic and certified organic insecticides under consideration as reduced-risk insecticides for soybean aphid (Aphis
glycines) control, using established and novel methodologies to directly quantify pesticide impact in terms of biocontrol
services. We found that in addition to reduced efficacy against aphids compared to novel synthetic insecticides, organic
approved insecticides had a similar or even greater negative impact on several natural enemy species in lab studies, were
more detrimental to biological control organisms in field experiments, and had higher Environmental Impact Quotients at
field use rates.
Conclusions/Significance: These data bring into caution the widely held assumption that organic pesticides are more
environmentally benign than synthetic ones. All pesticides must be evaluated using an empirically-based risk assessment,
because generalizations based on chemical origin do not hold true in all cases.
Citation: Bahlai CA, Xue Y, McCreary CM, Schaafsma AW, Hallett RH (2010) Choosing Organic Pesticides over Synthetic Pesticides May Not Effectively Mitigate
Environmental Risk in Soybeans. PLoS ONE 5(6): e11250. doi:10.1371/journal.pone.0011250
Editor: Stephen J. Johnson, University of Kansas, United States of America
Received March 30, 2010; Accepted June 1, 2010; Published June 22, 2010
Copyright: ? 2010 Bahlai et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The authors acknowledge funding from the Natural Sciences and Engineering Council of Canada (http://www.nserc-crsng.gc.ca/), Agriculture and Agri-
Food Canada (AAFC) (http://www.agr.gc.ca/index_e.php) and the Ontario Ministry of Agriculture, Food and Rural Affairs - University of Guelph partnership (http://
www.uoguelph.ca/research/omafra/). The funders had no role in data collection and analysis, decision to publish, or preparation of the manuscript. AAFC
suggested the insecticide list for testing, and this is the only role any funders played in study design.
Competing Interests: In support of other projects unrelated to this study, the authors’ research group has received competitive research grants from grower
organizations and government bodies and contracts and/or in-kind contributions from manufacturers of both organic and synthetic pesticides. Grant sources for
other research projects within the last five years include: Natural Sciences and Engineering Research Council of Canada, Canada Foundation for Innovation,
Canada Food Inspection Agency, Agriculture and Agri-Food Canada, Ontario Ministry of Food, Agriculture, and Rural Affairs, United States Department of
Agriculture, Instituto Nacional de Investigacio ´n Agropecuaria (Uruguay), Grain Farmers of Ontario (formerly Ontario Soybean Growers), Ontario Grape and Wine
Research Inc., Ontario Wheat Producers Marketing Board, Ontario Corn Producers Association, Agricultural Adaptation Council of Canada, Romer Labs, Bayer
CropScience Canada, Bayer CropScience France, Monsanto Canada, Pioneer Hi-Bred Ltd., Dow AgroSciences, BASF Canada, Syngenta Crop Protection Canada,
Syngenta Seeds Canada, DuPont Canada Crop Protection, Natural Insect Control, Woodrill Seeds Ltd.
* E-mail: firstname.lastname@example.org
A public call for sustainability in agriculture has resulted in
numerous government initiatives to develop environmentally
friendly agricultural practices [1,2,3,4,5,6]. In 2003, the Canadian
government initiated the Pesticide Risk Reduction Program to
provide infrastructure for the development and implementation of
reduced-risk approaches for managing pests in crops . This
program, similar to ones in the UK  and USA , sought to
reduce environmental risk associated with older chemical
insecticides by replacing them with low risk alternatives. Though
generalizations about the relative safety of natural and synthetic
chemicals have been questioned in the past , these sustainability
programs often continue to emphasize the development of organic
and natural insecticides for pest control. These programs make the
assumption that natural insecticides present less risk to the
environment than synthetic insecticides, aligning with public
opinion  and influential scientific papers purporting greater
sustainability of organic practice .
The sustainability of agricultural practices is a subject of
ongoing debate in the literature [10,11,12,13]. Many studies have
compared organic, conventional and integrated pest management
(IPM) production systems as a whole, but even within a
commodity system, the conclusions reached in these studies are
widely divergent. A 1999 study  of New Zealand apple
production suggested an integrated approach was more sustain-
able, but a 2001 study  of the same system in Washington
favoured an organic management approach. Differing outcomes
may be attributed partially to differing geography, climate and
pest complexes at the two locations, but it is likely that differences
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in assessment methodology and the inconsistencies between
specific practices classed as organic or conventional at each
location were also influential in obtaining the observed results.
Comparing organic, conventional and integrated agriculture is not
as simple as it may initially appear : each system is
characterized by a suite of practices which are ideologically,
rather than empirically defined , these systems are not
mutually exclusive from each other [9,12], and vary from region
to region depending on regulations . Because of these
variations, generalizations about the overall sustainability of one
system over another are never universal . Pest management
practices are often specifically highlighted in the sustainability of
organic versus conventional agriculture debate, but much of the
debate is fuelled by a fundamental misconception that organic
farms do not use pesticides . In fact, organic farms, like
conventional farms, have access to a suite of pesticides [15,16]; the
primary difference is that organic regulations prohibit all synthetic
(i.e.: human-made) chemicals but allow a vast array of mineral and
botanical pesticides , whereas conventional pesticides can be
both naturally and synthetically derived and are regulated
individually, on a per active ingredient, per formulation basis .
Generalizations about the relative sustainability of one suite of
practices over another are dangerous when integrated into policy:
government regulations based on faulty assumptions about
agricultural systems are expensive and do not effectively reduce
the environmental risks they are designed to mitigate . It is
thus more productive, and more broadly applicable, to evaluate a
given tactic for environmental sustainability on its individual
properties and build policy based on results of these individual
Many national and international initiatives exist to develop
environmentally sustainable strategies for managing outbreaks of
soybean aphid, including Agriculture and Agri-Food Canada’s
(AAFC) Pesticide Risk Reduction Program . Soybean aphid is a
severe pest of cultivated soybean in North America , and
approximately 1.2 million hectares of soybean are cultivated each
year in Canada alone . Since its introduction to North
America 10 years ago , numerous studies have examined the
role of biological control agents in managing populations of aphids
[22,23,24,25,26], but foliar insecticides remain necessary when
populations of aphids exceed economic thresholds. The need for
reduced risk pesticides in this system is profound: only two foliar
insecticides are currently registered for soybean aphid control in
Canada , one of which is currently under review for re-
registration . A broader suite of insecticides with varied
mechanisms of action are needed to ensure effective insecticide
resistance management can occur .
Working with AAFC, we identified four novel products to
evaluate as potential reduced risk insecticides to include in
integrated pest management programs for soybean aphid
(Table 1). Two of these insecticides contained synthetic active
ingredients, the other two are natural insecticides permitted for use
in certified organic crops in Canada . We included
formulations of the two currently registered insecticides in the
experiments as conventional controls.
We completed laboratory assays to estimate the direct contact
toxicity of these insecticides to several natural enemy species when
applied at field rates (Table 2). We used two of the soybean aphid’s
primary predator species in this study, multicoloured Asian
ladybeetle Harmonia axyridis and insidious flower bug Orius insidiosus
[25,26]. There were significant differences in mortality by
treatment applied for all insect groups F6,657=325.25, P,.0001
for ladybeetle adults; F6,993=1069.34, P,.0001 for ladybeetle
larvae; F6,277=228.11, P,.0001 for flower bug adults), but
generally, the two currently registered insecticides were most toxic
to natural enemies under laboratory conditions. The other four
insecticides were much less toxic to the ladybeetle, though it was
found that one of the organic insecticides, Beauveria bassiana, was
slightly more toxic to adults, and one novel synthetic, flonicamid,
was slightly more toxic to larvae than the remaining novel
insecticides. The four novel pesticides all caused some mortality to
the insidious flower bug, but the two organic insecticides had
significantly higher toxicity than the two novel synthetic
We conducted a two year, five site study to examine the
performance of these insecticides against aphids, and selectivity
with respect to natural enemies under field conditions (Fig. 1). In
addition to efficacy, it is desirable for an insecticide to have a high
selectivity for its target pests in order to minimize environmental
impact, and to conserve biological control services provided by
other organisms residing in the treated area. All synthetic
insecticides had similar efficacy one week after treatment
(F6,148=7.48, P,0.0001), though dimethoate efficacy was reduced
in the second assessment week (Fig. 1a), and yield in plots treated
with synthetic insecticides did not differ significantly (F6,90=3.51,
P=0.0036) (Fig. 2). The two organic insecticides had lower
efficacy than the synthetic insecticides (Fig. 1a) at one week
P,0.0001) post-treatment and did not offer significant yield
protection over the untreated control (Fig. 2). Field selectivity was
highest amongst synthetic insecticides, and lowest amongst organic
insecticides included in this experiment (F1,119=9.00, P=0.0033),
Table 1. Insecticides evaluated for use in control of the soybean aphid.
(ai) Trade name (Supplier)Mode of action%ai Rate per haEIQ*
Conventional (synthetic) Cyhalothrin-l
Matador 120EH (Syngenta)Neurotoxin- sodium channels 13.1 83 mL47.20.4
Conventional (synthetic)Dimethoate Lagon 480H (Cheminova)Neurotoxin- acetylcholine esterase inhibitor 43.55 1,000 mL33.5 12.5
Novel (synthetic)SpirotetramatMoventoH (Bayer)Fatty acid biosynthesis inhibitor 22.4 196 mL34.2 1.3
Novel (synthetic)Flonicamid BeleafH (FMC) Neurotoxin- potassium channels50196 g 8.70.8
Mineral oil Superior 70 oilH (UAP) Oxygen exchange99 11,000 mL30.1280.2
Beauveria bassianaBotanigardH (Laverlam) Entomopathogenic fungus221,000 g 16.73.3
*per unit weight environmental impact quotient (EIQ).
**predicted EIQ-field use rating (EIQ-FUR) for a single application of the insecticide, converted to lbs/ac, as convention dictates.
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and though dimethoate had the numerically lowest selectivity
amongst the synthetic insecticides, it was still numerically more
selective than the organic insecticides (Fig. 1b).
Net environmental impact of applying each insecticide at given
rates was estimated using an Environmental Impact Quotient
analysis . The per-unit-EIQ was highest for cyhalothrin-l, a
conventional synthetic insecticide (Table 1), but the EIQ-field use
ratings were highest amongst the older synthetic, dimethoate, and
the two organic insecticides. The high EIQ-field use rating of
dimethoate was due to both a high application rate and a relatively
high per-unit EIQ. The EIQ-field use rating for the mineral oil
insecticide, though, was more than an order of magnitude higher
than that of dimethoate, due to its relatively high per-unit-EIQ
and its extremely high application rate. The remaining four
insecticides had relatively low EIQ-field use ratings compared with
mineral oil and dimethoate.
EIQ allows relative impact of various control strategies within a
crop to be ranked; it is a standard method for indexing the total
environmental impact of an application of a given pesticide. EIQ
relies on data which is commonly available on MSDS sheets,
incorporates the application rate of a pesticide, and is not site or
pest-specific, so it provides a less biased estimation than other
pesticide ranking systems used to quantify environmental impact
[15,30]. Because EIQ is based on a rating system and does not rely
on field obtained data, some authors have criticized its use .
However, we found a clear inverse relationship between field
selectivity and EIQ for insecticides tested in this study when
applied at field rates (Fig. 3), suggesting that EIQ rankings are
relevant predictors of at least some in-field parameters for
environmental impact, and our results strongly support the
continued use of EIQ for ranking pesticide impact. Responses of
natural enemy communities are strong indicators of ecological
impact of an insecticide, because they are arthropods, like the
targets, and are thus likely to be biologically similar to the target of
the insecticide, and because they are often found alongside the pest
at the time of an insecticide application, heightening their
exposure compared to other non-target organisms.
Looking at the issue empirically, our results show that with
regards to environmental impact, target selectivity and efficacy,
the novel synthetic insecticides we tested have better performance
than organic insecticides; suggesting that certain organic manage-
ment practices are not more environmentally sustainable than
conventional ones. It has been purported that organic systems are
not just better for the environment, but are more economically
sustainable because of the price premiums associated with organic
food . Consumers are often willing to pay more for products
they believe are produced in the most sustainable way possible, but
we have shown that the organic methods available are not always
the most sustainable choice. Carefully designed integrated pest
management systems are likely the best strategy for minimizing
environmental impact of agriculture: where certified organic
systems may reject the technology with the smallest environmental
impact based on ideology , IPM maintains the flexibility to
incorporate any strategy empirically determined to have the
smallest impact. In fact, it has been argued that studies which have
concluded that IPM has a greater impact than organic
management  have simply tested a poorly designed IPM
strategy in which the efficacy and impact of individual tactics
included in the program were not effectively examined , did
not accurately reflect IPM practice, or employed biased methods
of evaluation . Though IPM practice does not typically come
with price premiums associated with the production of organic
food, IPM strategies are still commonly used by many conven-
tional farmers , and given increased consumer awareness of
the benefits of IPM practice, adoption rates are likely to rise.
It is for these reasons that we reject the organic-conventional
dichotomy and emphasize that, in order to optimize environmen-
tal sustainability, individual tactics must be evaluated for their
environmental impact in the context of an integrated approach,
and that policy decisions must be based on empirical data and
objective risk-benefit analysis, not arbitrary classifications.
Materials and Methods
Selection of insecticides for inclusion in experiments
In May 2008, the Pest Management Centre at AAFC provided
us with a list of 14 potential insecticides for inclusion in our
experiments. We reviewed each insecticide and eliminated those
which had the same mode of action as any other insecticide
registered for use against soybean aphid in Canada, and then
contacted the suppliers to assess the economic feasibility of using
these insecticides in field crops. Two novel synthetic and two
organic insecticides were identified to be tested for management of
soybean aphid, and the two registered insecticides were included
in the experiment as conventional controls. Experimental
Table 2. Relative direct contact mortality of natural enemies treated with six insecticides at field rate.
Relative H-T adjusted % mortality*
TreatmentHarmonia axyridis adults Harmonia axyridis larvae Orius insidiosus adults
Mineral oil 2.6d 6.3d60.7c
Beauveria bassiana 10.9c2.7e 59.5c
*Insecticides were applied at 0.5, 1 and 26field rate using an airbrush sprayer. Mortality was assessed at 18, 24 and 48 h post treatment for O. insidiosus, and every 24 h
for 7d for H. axyridis adults and larvae. Mortality data were Henderson-Tilton adjustedand subjected to a mixed model ANOVA by species and life stage, with relative
rate incorporated into the model, and assessment time treated as a repeated measure. Observed mortality within a species and life stage followed by the same letter are
not significantly different at a=0.05 (LSD).
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application rates for novel insecticides were developed in
consensus with supplier companies (Table 1). Table S1 provides
a complete list of insecticides considered for inclusion in this
experiment, and the rationale for products selected.
Determination of direct contact toxicity to natural
Adults and larvae of multicoloured Asian ladybeetle Harmonia
axyridis and adults of insidious flower bug Orius insidiosus were
treated with formulated insecticides at the equivalent of 0.5, 1 and
26field rate using an airbrush spray tower. The untreated control
consisted of 1 mL of distilled water. Groups of insects (8–10) were
anesthetized using CO2then placed in a 50 mm glass Petri plate
lined with a piece of 47 mm qualitative filter paper, treated using
the spray tower, and then placed in post-treatment containers.
Each insecticide-concentration combination was repeated four
times. The spray tower was rinsed with acetone, then distilled
water, between each application.
obtained from commercial suppliers (BioBest Biological Systems
Canada and MGS Horticultural Inc.). Repetitions of 10 adult O.
insidiosus were treated, and then placed, post-treatment, in 10 cm
plastic Petri plates lined with filter paper moistened with distilled
water, and containing 1–2 washed baby spinach leaves, and an
excess of frozen Ephistia eggs (BioBest Biological Systems Canada)
for food. Mortality was recorded at 18, 24 and 48h post treatment.
Harmonia axyridis adult assays.
obtained from aggregations on buildings in Guelph, Ontario,
Canada, and were reared in laboratory cultures using procedures
described by Xue et al . Repetitions of 10 adult H. axyridis
were treated, and then placed in 10 cm plastic Petri plates lined
with filter paper moistened with distilled water, and containing
Harmonia axyridis were
Figure 1. Field efficacy and selectivity observed for six insecticides for aphid control. A) Observed efficacy. Aphid count data were
Henderson-Tilton adjusted  and subjected to a mixed model ANOVA by post-treatment sampling period with year of experiment, block, pass of
tractor, site, and interaction terms between block and pass, block and site, and pass and site incorporated into the model. b) Observed selectivity.
Field selectivity was determined using the natural enemy-to-aphid ratio in treatment plots, for exact calculation see Materials and Methods. Observed
efficacy and selectivity within sampling period marked by the same letter are not significantly different at a=0.05 (LSD).
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several barley leaves infested with bird-cherry oat aphid (Aphid
excess of frozen Ephistia eggs (BioBest Biological Systems Canada) for
food. Mortality was recorded every 24h for 168 h (7 d).
Harmonia axyridis larvae assays.
H. axyridis were obtained from the laboratory culture described
above. Assays were performed as adult assays above, except
repetitions consisted of 8 individuals and instead of being placed
Second and third instar
Figure 2. Least-square mean soybean yield in fields treated with six insecticides, 2009. Data were subjected to a mixed model ANOVA
with block, site, treatment incorporated into the model. Observed yields marked by the same letter are not significantly different at a=0.05 (LSD).
Data from 2008 were excluded from analysis because of low overall aphid populations.
Figure 3. Relationship between observed field selectivity and the inverse of Environmental Impact Quotient at field rates. Field
selectivities presented as least square means (6 SE) of field selectivities observed at four sites in 2009. Equation of regression line is Field
selectivity=(3.361.7)/EIQ+(0.363.1)+site effect, with F93=4.23, p=0.0035.
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together in a Petri plate, were placed individually into cells of a
rearing tray (BIO-RT-32, C-D International, Inc.) with Ephistia
eggs and aphid-infested barley to avoid cannibalism.
Statistical analysis of bioassay data.
normalized using the Henderson-Tilton adjustment , and
subjected to a mixed model ANOVA accounting for concentration
(relative to field rate), treatment, and assessment time. Assessment
time was treated as a repeated measure in the analysis.
Mortality data was
Determination of field efficacy and selectivity
In 2009, four soybean fields in southwestern Ontario with aphid
populations approaching the action threshold of 250 aphids per
plant were identified in collaboration with government extension
personnel in July and August, 2009. After obtaining permission
from landowners, sites were assessed once weekly until aphid
populations exceeded 250 aphids per plant. Upon reaching this
threshold, field experiments were initiated. In our initial screening
trial in 2008, treatments were applied to a single site with a
moderate density of aphids (,120 aphids per plant), due to low
aphid populations across our region during that year.
Field experiments employed a RCBD consisting of four blocks
of 15 3.7615.2m beds, with 3 untreated controls per block (one for
each tractor pass required), our six insecticides and six other
products or formulations not reported in this study. Insecticides
were applied using a Teejet Duo nozzle configuration with spray
tips #TT11002 at a height of 50cm above the canopy. Spray
pressure at the nozzle was 276 kPa and the tractor travelled at a
ground speed of 9.7km/h. Fluid delivery rate was maintained at
187 L/ha for all treatments. 2–3 soybean plants were destructively
sampled from each bed at each assessment, and assessments were
completed 1) immediately before treatment, 2) one week after
treatment and 3) two weeks after treatment. Total numbers of
aphids, ladybeetles, lacewings, parasitized aphid mummies,
syrphid larvae, and flower bugs were assessed on each plant.
Aphid counts were transformed using Henderson-Tilton
adjustments to account for population changes in the control
between time of treatment and time of assessment, then subjected
to a mixed model ANOVA accounting for site, year, tractor pass,
replicate, and treatment.
Field Selectivity Calculation
Field selectivity of each insecticide was estimated by calculating
the change in the ratio of natural enemies to aphids in each plot,
and subjecting these data to a mixed model ANOVA as above. We
defined field selectivity as the relative change in the natural-
enemy-to-pest population ratio observed after treatment. We
standardized the counts of natural enemies of different species by
defining a Natural Enemy Unit (NEU), where 1 NEU is the
number of predators or parasitoids required to kill 100 pest insects
in 24h. Thus,
where N is the total number of natural enemy species, niis the total
number of individuals of natural enemy species i observed on 10
plants, and Viis the average voracity of natural enemy species i,
that is, the number of pest insects it can kill in 24 h divided by 100.
Using functional response data obtained by Xue et al. , we
defined our soybean aphid ecosystem specific calculation as:
where nladybeetles is the total number of adult and larvae of
ladybeetles of Harmonia axyridis or Coccinella septempunctata, nmummies
is the total number of parasitized aphids, nsyrphids is the total
number of Syrphidae larvae, nOriusis the total number of Orius spp.,
and nlacewingsis the total number of Chrysopidae observed on 10
Field selectivity was defined as the ratio of NEU/Aphids (NEU/
A) after treatment to NEU/A before treatment, normalized by the
control, as in the Henderson-Tilton adjustment , and took the
This selectivity index results in values ,1 if a treatment kills
more natural enemies than target pests, and values .1 if a
treatment kills more target pests than natural enemies. Larger
numbers will indicate a more target-selective pesticide. The
selectivity index assumes the applied treatment has at least some
efficacy against the target pest.
Environmental Impact Assessment
EIQs were estimated using established methodology [29,33]
incorporating data from MSDS sheets provided by the supplier of
the insecticides, an EIQ-field use rating was calculated for each
insecticide, using the assumption that one application at field rate
per season would provide equivalent aphid control. See Table 3
Table 3. Toxicity ratings used to calculate Environmental Impact Quotient for Beauveria bassiana, which does not have a
published EIQ value.
Variables from EIQ Equation*
*Ratings were developed in accordance with methodology presented in Kovach et al. .
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for values used in the calculation of EIQ for Beauveria bassiana, Download full-text
which does not have an existing published EIQ value.
provided by Agriculture and Agri-Food Canada (AAFC).
Found at: doi:10.1371/journal.pone.0011250.s001 (0.04 MB
Complete list of insecticides under consideration
We sincerely thank L. Des Marteaux, D. Makynen, J. Smith,T. Phibbs, D.
Hooker, A. Gradish and T. Baute for technical assistance on this project,
R. Norris and B. Stirling for the use of their respective farms, C. Scott-
Dupree for use of the airbrush spray tower, M.K. Sears and J.A. Newman
for providing comments on this manuscript, and C. Petzoldt and D.
Marvin for providing support with the EIQ method. We would also like to
thank Syngenta, Bayer, FMC, UAP, and Laverlam for providing
insecticides for our experiments, and BioBest Canada and MGS
Horticultural for providing insects.
Conceived and designed the experiments: CB AWS RHH. Performed the
experiments: CB YX CMM. Analyzed the data: CB. Contributed
reagents/materials/analysis tools: CB YX. Wrote the paper: CB RHH.
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Organic Isn’t Risk-Free
PLoS ONE | www.plosone.org7 June 2010 | Volume 5 | Issue 6 | e11250