published: 31 October 2019
Frontiers in Environmental Science | www.frontiersin.org 1October 2019 | Volume 7 | Article 177
Annemarie Van Wezel,
University of Amsterdam, Netherlands
Jane A. Entwistle,
Carsten A. Brühl
This article was submitted to
Toxicology, Pollution and the
a section of the journal
Frontiers in Environmental Science
Received: 03 April 2019
Accepted: 16 October 2019
Published: 31 October 2019
Brühl CA and Zaller JG (2019)
Biodiversity Decline as a
Consequence of an Inappropriate
Environmental Risk Assessment of
Pesticides. Front. Environ. Sci. 7:177.
Biodiversity Decline as a
Consequence of an Inappropriate
Environmental Risk Assessment of
Carsten A. Brühl 1
*and Johann G. Zaller 2
1Community Ecology and Ecotoxicology, iES Landau, Institute for Environmental Sciences, University of Koblenz-Landau,
Landau, Germany, 2Department of Integrative Biology and Biodiversity Research, Institute of Zoology, University of Natural
Resources and Life Sciences (BOKU), Vienna, Austria
Keywords: ecotoxicology, plant protection products, agroecology, regulatory, EU
The widespread contamination of ecosystems with plant protection products (pesticides in this
text) around the world is evident (Hoferkamp et al., 2010; Shunthirasingham et al., 2011; Stehle
and Schulz, 2015a; Ferrario et al., 2017; Hvˇ
ezdová et al., 2018; Silva et al., 2019). Pesticide eﬀects
on the physiology, activity and diversity of various aquatic and terrestrial non-target organisms
is addressed by numerous studies, and many new aspects are also described in a recent Frontiers
We currently observe a deterioration of biodiversity in agricultural landscapes, and the dramatic
losses are increasingly discussed by the public (European Commission, 2018a). Declines of
insect biomass of more than 70% in the last few decades in Germany, the halving of farmland
bird populations in Europe and eﬀects on pollinators are widely known (Donald et al., 2001;
Potts et al., 2010; Hallmann et al., 2017). Out of a set of recorded parameters of agricultural
intensiﬁcation (such as ﬁeld size, fertilizer application, landscape heterogeneity) a unique, pan-
European study identiﬁed pesticide application as the responsible factor for lower biodiversity
of plants, ground beetles, and birds in wheat ﬁelds (Geiger et al., 2010). Recently, a review
recognized chemical pollution including pesticides as the second most important driver for the
worldwide decline in insect populations (Sánchez-Bayo and Wyckhuys, 2019). Other drivers were
habitat loss and conversion to intensive agriculture, fertilizer inputs, introduced species, and
There is agreement in the scientiﬁc community that pesticides are a central responsible factor
for the observed terrestrial biodiversity declines. However, pesticides are perceived also as the
chemicals with the strictest regulation, requiring an in-depth Environmental Risk Assessment
(ERA) for registration in the European Union (European Parliament, 2009). This procedure
includes the performance of a set of toxicity studies and calculations using predicted exposure
values to calculate a risk. If the risk is deemed acceptable pesticides can be placed on the market
(for an overview see.g. Storck et al., 2017). Interestingly during this step of the authorization
process the “acceptable risk” is leading to pesticides considered “safe” for the environment (EFSA,
2019). Farmers, assuming they are using “safe” pesticides, are currently confronted with the public,
blaming them for the observed declines of biodiversity. It seems that the ERA for pesticide
regulation as currently carried out is inappropriate since it cannot prevent that registered and
commonly used pesticides have detrimental eﬀects on our environment.
In the last decade we have seen an increasing complexity in ERA of pesticides. The European
Food Safety Authority (EFSA), as the responsible authority for pesticide registration in Europe,
published guidance documents describing the required studies for diﬀerent groups of aquatic and
terrestrial organisms and their implementation in risk calculations (EFSA, 2010, 2013a). For the
Brühl and Zaller Biodiversity Unprotected by Pesticide Regulation
terrestrial environment there are also speciﬁc documents for
birds and mammals as well as for bees (EFSA, 2009, 2013b).
Furthermore, EFSA also recently published scientiﬁc opinions
on in-soil organisms, non-target arthropods, amphibians, and
reptiles as well as non-target terrestrial plants calling for
improvement of ERA for the respective groups (EFSA, 2014,
2015, 2017, 2018). In some instances, such as for the currently
neglected amphibians and reptiles, standard toxicity studies to
produce reliable endpoints are lacking and the entire ERA is
not even outlined yet. Scientiﬁc opinions are documents that
highlight steps in ERA that need to be improved. However, the
ERA is still performed as before until a guidance document
The current scheme for ERA of pesticides was also
recently addressed by the group of chief scientiﬁc advisors,
recommending among others the setting of unambiguous and
quantiﬁable protection goals and structural changes of the
registration process in the EU (European Commission, 2018b).
The majority of the members of the European parliament agreed
on a motion for a resolution on the authorization procedure for
pesticides that mentions concern regarding the widespread use
of pesticides and a lack of public knowledge about hazard and
risk of pesticide use (European Parliament, 2018). A few scientiﬁc
assessments of the European ERA scheme and its shortcomings
exist (e.g. Newman et al., 2006; Schäfer et al., 2011; Stehle and
Schulz, 2015b; Storck et al., 2017). Main points that are often
raised are the inclusion of new test or surrogate species, the
extension of studies to more realistic scenarios, the validity of
the used uncertainty (assessment) factors, the lack of including
sublethal endpoints in risk assessments and the need to address
ignored groups of organisms (e.g. Jänsch et al., 2006; Desneux
et al., 2007; Stahlschmidt and Brühl, 2012; Brühl et al., 2013). The
consideration of interactions of pesticide eﬀects with additional
stressors such as nutrients or climate change was also pointed out
(Köhler and Triebskorn, 2013; Baier et al., 2016).
But instead of highlighting all the open questions on various
stages of a complex ERA scheme we consider it necessary to step
back and address its entire structure. The observed biodiversity
declines in European agricultural landscapes are mostly discussed
for terrestrial organisms and not for aquatic systems. We will
therefore speciﬁcally focus on the terrestrial part of ERA.
APPLICATION SEQUENCES IN PESTICIDE
The existing ERA is performed for one active substance or
pesticide product that is applied once or a few times in a
speciﬁc crop. However, the current cropping systems do not
only receive one application of a pesticide. Their seeds might
be already treated with a mixture of multiple systemic pesticides
and several further products are applied on the growing plants
or fruits during the season. In Germany in 2016 on average
there were 6 pesticides applied (treatment index) in wheat,
7 in oilseed rape, 14 in potatoes, 22 in vine orchards, and
32 in apple production orchards (JKI, 2019). In the UK even
more pesticides were used for the same crops: 11 pesticides
for wheat, 13 for oilseed rape, and 21 for potatoes (FERA,
2017). Outside the EU maximum pesticide inputs as in banana
in Costa Rica, where aerial applications are conducted in
conventional plantations every 4 days, result in volumes of
over 75 kg of active molecules/ha/year. It is obvious to every
ecotoxicologist and ecologist that multiple, sequential ﬁeld
applications of biologically active chemicals are likely to cause
more severe eﬀects on a population of organisms than a single
application event. However, the current risk assessment assumes
that populations only face a single impact from a speciﬁc
pesticide, with suﬃcient time following after application to
allow the population to recover to former levels. In reality the
same population is facing multiple pesticide impacts during the
growing season. This is a worrying underestimation of the actual
risk for biodiversity in the agricultural landscape resulting from
pesticide use. Similar concerns of an underestimation of eﬀects
of contamination with multiple pesticides and other chemicals
are also raised for human health (Leu and Shiva, 2014).
The current ERA scheme addresses the eﬀects of a pesticide
on each group of organisms separately. There are ERA sections
on plants, on insects and spiders (arthropods) and birds.
Field studies are sometimes performed for arthropods, where
interactions between predatory insects and their prey is recorded.
However, ERA does not include so-called indirect eﬀects or
interactions between trophic levels of diﬀerent organism groups.
An example can be seen in an herbicide that has no acute toxic
eﬀect on insects as well as birds and therefore passes the current
risk assessment for both groups. However, the application of
the herbicide leads to a reduction of “weeds” (as intended in
the ﬁeld) and of “non-target plants” (the same plant species
growing outside the ﬁeld), therefore reducing the amount of
food for pollinators and herbivorous insects. This depletion can
lead to further impacts on birds since herbivorous insect larvae,
such as caterpillars, are smaller and less abundant after herbicide
treatments (Hahn et al., 2014), reducing the insect biomass
available to feed the birds oﬀspring. Trophic interactions are
fundamental features of ecosystems and therefore need to be
considered in ERA.
IN-FIELD EFFECTS ON BIODIVERSITY
The European ERA focusses on environmental eﬀects that can
occur in semi-natural structures outside the agricultural ﬁelds.
Currently no ERA for the in-ﬁeld risk is mandated. However,
the scientiﬁc opinion for non-target arthropods, mentions
“biodiversity has to be supported to a certain degree in the
in-ﬁeld areas (. . . ) in order to provide important ecosystem
services (EFSA, 2015).” However, the respective guideline is
not addressing this issue and negative eﬀects on biodiversity
are therefore deliberately accepted in the cropping area where
pesticides are directly applied at biologically eﬀective rates.
The agricultural cropping area that receives pesticide inputs in
Europe represents 22% of the total land area, reaching more
Frontiers in Environmental Science | www.frontiersin.org 2October 2019 | Volume 7 | Article 177
Brühl and Zaller Biodiversity Unprotected by Pesticide Regulation
than 30% for example in Germany and France (for 2015,
Eurostat, 2019). Therefore, in countries with a high proportion
of cropped area almost a third of the terrestrial land surface
is not evaluated regarding negative eﬀects of pesticides on its
biodiversity. To explain the observed decline in insect biomass
in the agricultural landscape of Germany (Hallmann et al., 2017)
the most parsimonious explanation (Occam’s razor) is the annual
application of insecticides on more than 30% of Germanys land
area, the entire cropping area, since the 1970s. No other factor
such as the suggested light pollution or soil sealing needs to be
invoked to explain the observed reductions (BMU, 2018).
The ERA required for pesticide regulation is in most cases
not addressing the impact of pesticide use in agricultural
ﬁelds and does not include food-web related ecosystem eﬀects.
This fundamental misconception leads to an ERA scheme
and a resulting pesticide regulation that is not protective for
biodiversity. If we remain working with the ERA scheme in place,
in our opinion we will continue to observe further declines of
many groups of organisms such as farmland birds and insects in
the agricultural landscape. Neglecting the three described factors
can have far-reaching consequences at the ecosystem level that
are likely larger than an underestimation of risk due to a lower
uncertainty factor or a ﬂaw in the experimental design of a
ﬁeld study. The misconception can also not be compensated
by additional studies including new surrogate species or groups
of organisms. The banning of certain insecticides or broad-
band herbicides will also hardly improve the situation. We
therefore urgently need to rethink our basis for the regulation
of these biologically active substances and develop a holistic
approach to include indirect eﬀects caused by multiple pesticides
applied in the agricultural productive land area of Europe.
Since the current ERA for the regulation of pesticides is not
addressing the real-world situation we ought to accept that
the current practice of pesticide use in European agriculture
is not suﬃciently protective and therefore not safe for the
RISK MANAGEMENT INSTEAD OF
The development of a new systemic approach for ERA will
take considerable time and require substantial resources. We
therefore also need to discuss other options to at least halt the
negative eﬀects of pesticides on biodiversity of the agricultural
landscape. Risk management to mitigate negative pesticide eﬀects
might be a helpful alternative until we are able to assess the
true environmental risk of pesticide usage. Reducing pesticides
in agricultural practice is an obvious option. It was estimated that
total pesticide use could be reduced by more than 40% in almost
60% of 946 evaluated farms in a French network without any
negative eﬀects on both productivity and proﬁtability (Lechenet
et al., 2017). Integrated pest management should focus on
using natural enemies of pests and crop rotations and agree
on pesticides as a last option instead of current practices,
where pesticides are prophylactically implemented in farming
practices (e.g., seed-treatments of cereals). We additionally could
extend the proportion of semi-natural habitats without pesticide
inputs in the agricultural landscape, increase agri-environmental
schemes and enlarge the area of organic farming. Many options
are on the table and a strengthening of the greening of the
common agricultural policy (CAP) is currently discussed for the
coming period of European policy (Erjavec and Erjavec, 2015;
Solazzo et al., 2016; Alons, 2017). Risk mitigation of pesticides
needs to be implemented eﬀectively and at a large scale to bend
the curve of biodiversity decline in agricultural landscapes now. If
we delay to change agricultural practice and its current pesticide
use our eﬀorts to stop the current biodiversity decline and restore
it to former levels need to be much larger at a later stage.
All authors listed have made a substantial, direct and intellectual
contribution to the work, and approved it for publication.
CB thanks colleagues and the students of the Ecotoxicology
courses at the iES in Landau and at Universidad Nacional
Costa Rica in Heredia for many intense discussions. Special
thanks go to Marjon Belderbos and Clemes Ruepert for their
hospitality and the tranquility of the garden house with the
motmot that inspired this text. We also thank the reviewers and
editor for helpful comments on earlier versions of this opinion.
Open access publication was supported by BOKU (University
of Natural Resources and Life Sciences) Vienna Open Access
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Conﬂict of Interest: The authors declare that the research was conducted in the
absence of any commercial or ﬁnancial relationships that could be construed as a
potential conﬂict of interest.
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