Supplementary Material

1. Species groups and test species in current ERA of pesticides

Fish cover different ecological niches, but mainly as predators they play an important role for community dynamics in most surface waters. In the early days of ecotoxicology, dead fish (besides dying birds) were the most obvious sign of problems caused by chemicals in the environment. They have been used as test species for more than three decades. However, testing in pesticide ERA is performed with very few indicator species (mainly trout, carp, zebra fish and fat-head minnow) under laboratory conditions. Due to their size and predatory efficiency, fish are only rarely used in semi-field studies.

Aquatic invertebrates have been used as indicators for water quality for more than 100 years (Saprobic-Index (Kolkwitz and Marsson 1909), RIVPACS (Wright 2000)). Usually, Daphnia magna and one additional aquatic invertebrate (e.g. Chironomid larvae) are used to evaluate the risk for aquatic invertebrates (European Commission 2013).As primary producers, algae play an important role in most aquatic ecosystems. Taxonomically, it is a diverse group. Generally, a growth inhibition test on a green algae is required (European Commission 2013). In the present study we regard Cyanophyceae as algae as it is also current practice in pesticide risk assessment. The protection goal regards populations or functional groups and not individual species (EFSA PPR Panel 2010, 2013).

Higher aquatic plants (aquatic macrophytes) occur in high densities and biomass in many limnic habitats. In the ERA of pesticides floating plants (i.e. species of the genus Lemna) are usually tested, but a test with a plant rooting (Myriophyllum sp.) in the sediment has also been developed (Feiler et al. 2004).

The diversity of aquatic micro-organisms is high; they perform important ecosystem functions and provide essential services. Currently, the evaluation of pesticides effects on aquatic microorganisms is not explicitly required for authorization (European Parliament and European Council 2009). However, due to their important role in the aquatic nutrient and organic matter cycle, the impairment of their ecosystem functions certainly belong to “unacceptable effects on the environment” aimed to be prevented by Regulation (EC) No. 1107/2009 (EC 2009) (EFSA PPR Panel 2010).

Amphibians are globally under considerable threat (Stuart et al. 2004) without one single factor being exclusively responsible. The majority of European amphibians are protected by Council Directive 92/43/EEC ("Habitat Directive"; European Council 1992). Available data on the effects of pesticides on amphibians should be submitted for pesticide registration according to the new data requirements for pesticide authorization (European Commission 2013). However, commonly agreed upon risk assessment guidelines are not yet available, which may explain the low number of studies with amphibians and pesticides found in the literature.

Birds and mammals are handled differently than other terrestrial organisms in the pesticide risk assessment. Clearly, the protection goal is the population, but individuals must be protected as well (EFSA PPR Panel 2010). The risk assessment for birds and mammals is based on a combination of laboratory test data, sometimes supported by ecological information and field observations (e.g. for identifying focal species for a specific crop).

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Bees have enormous ecological and economic importance for agriculture as pollination is probably the best example of the monetary valuation of an ecosystem service (Hassan et al. 2005). This function can be performed by a wide-range of organisms (most often insects like butterflies or bees, but also birds or bats). Until recently, however, usually one species, the honey bee (Apis mellifera), has been scrutinized for the purpose of assessing the risk of pesticides (European Parliament and European Council 2009). Pollinating taxa require special protection, which has been highlighted in recent EFSA opinions (EFSA PPR Panel 2010, 2012). Furthermore, pesticide exposure has been related to negative impacts on bees (Lu et al. 2001, Desneux et al. 2007, Henry et al. 2012Tapparo, 2012 #102).

The group of non-target arthropods (NTAs), mainly consisting of insects and arachnids, is highly diverse both taxonomically and in terms of their function. Likewise, the migration ability can differ extremely between species, depending on whether they can fly (e.g. a lace-wing: Chrysoperla carnea) or not (e.g. a predatory mite: Typhlodromus pyri). Today, up to ten tests are more or less regularly performed in pesticide risk assessment (Candolfi et al. 2000). Any NTAs risk assessment starts with just two species (the predatory mite Typhlodromus pyri and the parasitoid Aphidius rhopalosiphi) in tier 1. In the case that these tests indicate concern, at higher-tiers it is possible to refine the risk assessment based on local or regional species in a field study representing the intended use (Candolfi et al. 2000, de Jong et al. 2010). In addition, in NTAs higher-tier studies (e.g. a field test with predatory mites), recovery within one season/year is already the decisive criterion of whether application of a certain pesticide at a specific time may be permitted or not.

With regard to soil invertebrates, the most important groups are Oligochaeta (earthworms and enchytraeids), Collembola (springtails), and Acari (mites) due to their influence on nutrient cycling and soil properties, or their diversity (mainly the arthropods) (Brussaard 2012). Other groups such as Nematoda have rarely been studied. With the exception of earthworms they are not regularly used in field or monitoring studies. Micro-arthropods (i.e. mainly springtails or mites) are an important group of soil invertebrates in terms of diversity, biomass and ecological relevance (Turbé et al. 2010). The nematodes are by far the most abundant and diverse (taxonomically and ecologically) group of soil invertebrates, including saprophagous, fungivorous and bacteriovorous, predatory, or parasitic species. Saprophagous earthworms (in temperate regions mainly species of the family Lumbricidae) and, to a lesser extent, potworms (Enchytraeidae), are the most important taxa in soil ecotoxicology due to their ecological relevance and (often) high sensitivity towards chemicals (Paoletti 1999, Römbke and Egeler 2009).

The numbers of taxonomic units of soil microbes is extremely high (e.g. Dequiedt et al. 2011, Griffiths et al. 2011). Various methods are available for assessment, usually using the indigenous microbial community or some of their functions (Philippot et al. 2012). Like in the aquatic compartment, testing of individual “species” is not common as the protection goal is usually the function and not the structure of these communities.

Plants are the only group in which more than one species has to be regularly tested (usually 6 to 10, almost always crop species (OECD 2006b, 2006a)). There is evidence that on average the sensitivity of crop and comparable wild species does not differ considerably (e.g. Carpenter and Boutin 2010).

Reptiles are a widely distributed and often highly endangered group of vertebrates. Available data on pesticide effects should be submitted for pesticide registration, but no agreed risk assessment approach is yet available (European Commission 2013).

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References

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Candolfi, M., Blümel, S., Forster, R., Bakker, F.M., Grimm, C., Hassan, S.A., Heimbach, U., Mead-Briggs, M., Reber, B., Schmuck, R. and Vogt, H. 2000. Guidelines to evaluate side-effects of plant protection products to non-target arthropods. Gent, IOBC-WPRS.

Carpenter, D. and Boutin, C. 2010. Sublethal effects of the herbicide glufosinate ammonium on crops and wild plants: Short-term effects compared to vegetative recovery and plant reproduction. Ecotoxicology 19(7): 1322-1336.

de Jong, F.M.W., Bakker, F.M., Brown, K., Jilesen, C.J.T.J., Posthuma-Doodeman, C.J.A.M., Smit, C.E., van der Steen, J.J.M. and van Eekelen, G.M.A. 2010. Guidance for summarising and evaluating field studies with non-target arthropods. RIVM report 601712006: 73.

Desneux, N., Decourtye, A. and Delpuech, J.-M. 2007. The sublethal effects of pesticides on beneficial arthropods. In Annual Review of Entomology. Edited by. pp. 81-106.

EFSA PPR Panel 2010. Scientific Opinion on the development of specific protection goal options for environmental risk assessment of pesticides, in particular in relation to the revision of the Guidance Documents on Aquatic and Terrestrial Ecotoxicology (SANCO/3268/2001 and SANCO/10329/2002). EFSA Journal 8(10): 1821-1876.

EFSA PPR Panel 2012. Scientific Opinion on the science behind the development of a risk assessment of Plant Protection Products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA Journal 10(5): 2668.

EFSA PPR Panel 2013. Guidance on tiered risk assessment for plant protection products for aquatic organisms in edge-of-field surface waters. EFSA Journal 11(7): 3290.

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European Council 1992. Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. Last amended by Council Directive 2006/105/EC of 20 November 2006 (FFH Directive). Official Journal L 206 p. 7 22.07.1992: 66.

European Parliament and European Council 2009. Regulation (EC) No 1107/2009 of the European Parliament and of the Council of 21 October 2009 concerning the placing of plant protection products on the market and repealing Council Directives 79/117/EEC and 91/414/EEC.

Feiler, U., Kirchesch, I. and Heininger, P. 2004. A new plant-based Bioassay for aquatic sediments. J. Soils Sed. 4(4): 261-266.

Henry, M., Beguin, M., Requier, F., Rollin, O., Odoux, J.-F., Aupinel, P., Aptel, J., Tchamitchian, S. and Decourtye, A. 2012. A Common Pesticide Decreases Foraging Success and Survival in Honey Bees. Science 336(6079): 348-350.

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Kolkwitz, R. and Marsson, M. 1909. Ökologie der tierischen Saprobien. Beiträge zur Lehre von der biologischen Gewässerbeurteilung. Internationale Revue der gesamten Hydrobiologie und Hydrographie 2(1-2): 126-152.

Lu, C.S., Knutson, D.E., Fisker-Andersen, J. and Fenske, R.A. 2001. Biological monitoring survey of organophosphorus pesticide exposure among preschool children in the Seattle metropolitan area. Environ. Health Perspect. 109(3): 299-303.

Paoletti, M.G. 1999. The role of earthworms for assessment of sustainability and as bioindicators. Agriculture Ecosystems & Environment 74(1-3): 137-155.

Philippot, L., Ritz, K., Pandard, P., Hallin, S. and Martin-Laurent, F. 2012. Standardisation of methods in soil microbiology: progress and challenges. FEMS Microbiol. Ecol. 82(1): 1-10.

Römbke, J. and Egeler, P. 2009. Oligochaete worms for ecotoxicological assessment of soils and sediments. In Annelids in Modern Biology. Edited by D.H. Shain. Hoboken, USA, Wiley-Blackwell. pp. 228-241.

Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S.L., Fischman, D.L. and Waller, R.W. 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306(5702): 1783-1786.

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2. Literature Search

We performed a search in the data bases Web of Science (http://apps.webofknowledge.com) and Scopus (http://www.scopus.com.scopeesprx.elsevier.com) using the key words given in Table S1. To also cover information that is not formally published (“grey literature”) including reports, theses, working papers, etc., we searched Scirus (http://www.scirus.com) as well. However, almost no ”grey literature” entered the selection of studies for the final review because most studies were found to have been either also formally published or presented quality issues. The time span of the search covered the the period from the starting date of the data bases to December 2011. Newer publications were added on a case by case basis.

Table S1: Key words for the literature search. The blocks were combined with “and” between and with “or” within each other.

OR

pesticide*; herbicide*; insecticide*; fungicide*; nematicide*; molluscicide*; “plant protection product*”

AND

acarid*; alga*; amphibia*; annelid*; anthomedus*; arachnid*; arthropod*; apis; bee*; beetle*; bird*; bivalve*; bivalvia*; boatman; backswimmer*; bug*; bumblebee*; "bumble bee*"; bombus; caddis*; coleopter*; collembol*; crustacean; damselfl*; decapod*; diptera; dragonfl*; earthworm*; enchytra*; ephemeroptera*; fish*; *flies; *fly; gastropod*; hemiptera*; hirudin*; honeybee*; "honey bee*"; hydra; hydrozoa; insect*; invertebrate*; larvae; leech*; lumbricid*; macroinvertebrate*; macrophyt*; mammal*; mayfl*; megaloptera*; microb*; micro-organism*; microorganism*; midge*; mite*; mollusc*; mussel*; nematode*; neuropteran*; nontarget; non-target; "non target"; notonectidae; notonecta*; odonata; oligochaet*; ostracoda*; periphyt *; planar*; plant*; plecoptera*; potworm*; reptile*; rotatoria*; rotifer*; slug*; snail*; springtail*; stonefl*; trichoptera*; turbellari*; *worm*; zygoptera*; "ecosystem engineer*"; "keystone species"; "umbrella species"; "foundation species"

AND

recovery; recoloni*; long-term; “long term”; longterm; delayed; latent; indirect

AND

effect*

AND

population*; community; communities

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2. Experimental Setup and Modes of Action

Regarding the number of concentrations tested, for the aquatic compartment the majority of studies dealt with more than one concentration in addition to the control. In contrast, most of the field studies in the terrestrial compartment were performed with just one concentration (often the maximum application rate (MAR), which can differ according to crop type, country or the year in which the study was performed). The number of replicates per concentration was rather low for the aquatic compartment (only 27% used four or more replicates). Likewise, most of the terrestrial studies used three or four replicates.

With regard to the study duration, aquatic invertebrates and algae were most often investigated for durations between two weeks and two months (Table S2). Few studies spanned four months up to one year and only two studies lasted more than one year. For aquatic microbes, all investigations were shorter than two months, presumably due to the short generation times of these taxa. For the terrestrial taxa, 40% of all studies lasted longer than four months, including 19% with a duration of more than a year. When comparing the different taxa groups, there were astonishingly small differences in test duration between the groups, as opposed to the aquatic environment. Even microbes, having usually very short generation times, were tested as long as non-target arthropods or other soil invertebrates.

The majority of the aquatic studies investigated were conducted under semi-field conditions (51 out of 106), mainly in outdoor pond mesocosms, while 34 were conducted in the laboratory and 21 in the field, most often as enclosures in lakes. In contrast, most of the terrestrial studies were conducted in the field (52 out of 76), followed by laboratory (18, 16 of those with microbes) and semi-field studies (5) and one greenhouse study.

See Tables S3, S4 and S5 for information on the different substance groups tested, the most common substances and the modes of action.

Table S2: Study durations for the different taxa groups; d=days, w=weeks, m=months, y=year.study duration> 2d-1w > 1w-2w > 2w-1m > 1m-2m > 2m-3m > 3m-4m > 4m-1y > 1y

Aquatic environmentInvertebrates 2 5 23 16 13 9 9 2Algae 6 14 10 9 2 12 1Microbes 3 2 2 5Macrophytes 1 4SUM 5 13 40 31 22 11 25 3% Total 3 9 27 21 15 7 17 2Terrestrial environmentBirds 1Bees 1NTAs 1 2 4 3 8 5 1Invertebrates 4 3 2 10 4Microbes 1 1 6 6 1 1 1Plants 1 3 2 2SUM 1 2 6 9 11 2 11 10% Total 1 4 13 19 22 5 20 15

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Table S3: Number of studies per substance class and the most common substances.number of studies most common substances (n)

Aquatic environmentInsecticides 61 chlorpyrifos (12), carbaryl (9),

esfenvalelrate (5), temephos (5)Herbicides 27 atrazine (9), diuron (4), glyphosate (4),

isoproturon (4),Fungicides 14 azoxystrobin (5), carbendazim (5)

Terrestrial environmentInsecticides 38 dimethoate (5), triflumuron (4)Herbicides 23 glyphosate (6), paraquat (6), simazine (4)Fungicides 19 benomyl (4), captan (3)

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Table S4: Modes of action of substances used in studies on aquatic systems.

 Mode of action Number of studies

Number of substances

InsecticidesInhibition of Acetylcholinesterase 29 6Inhibitor of Cholinesterase 1 1Agonist of Ecdysone receptor 1 1Agonist of GABA-gated chloride channel 4 4Inhibition of chitin biosynthesis 2 1Inhibition of nicotinic acetylcholine receptors 2 1Inhibition of mitochondrial complex I electron transport 1 1Modulation of sodium channel 14 5Modulation of sodium channel modulator; inhibition of Acetylcholinesterase 1 1Modulation of sodium channel, nerve action 3 1

LarvicidesMicrobial disruptors of insect midgut membranes 3 1Activation of Nicotinic acetylcholine receptor (nAChR) allosteric, nerve action 3 1

FungicidesEnergy disruption in fungus at multiple sites 1 1Inhibition of fungal mitotic microtubule formation 5 1Inhibition of mitochondrial respiration 5 1Inhibition of sterol biosynthesis 2 2

HerbicidesInhibition of Acetolactate synthase 1 1Inhibition of cell division 2 1Inhibition of photosynthesis at photosystem I 1 1Inhibition of photosynthesis at photosystem II 17 7Inhibition of synthesis of amino acids 4 1

Fungicide, insecticide and herbicideInhibition of mitochondrial ATP-ase activity 1 1

BiocidesInhibition of photosynthesis at photosystem II 2 1

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Table S5: Modes of action of substances used in studies on terrestrial systems.

 Mode of action Number of studies

Number of substances

InsecticidesInhibition of Acetylcholinesterase - 22 18Inhibition of chitin synthesis 6 2Modulation of sodium channel 8 5Acetylcholine receptor (nAChR) agonist 2 1Excitation insect nervous system 1 1GABA-antagonist 2 2

MolluscicidesInhibition of Acetylcholinesterase 3 1

NematicidesInhibition of Acetylcholinesterase 2 1

FungicidesInhibition of mitosis 4 2Inhibition of Acetylcholinesterase 2 1Cell-division 1 1Disruption of membrane function 1 1Disruption of lipid metabolism 3 1Inhibition of spore germination 3 2Disruption of membrane 1 1Inhibition of respiration 1 1Suppression growth + sporangial formation 1 1

HerbicidesInhibition of photosynthesis 12 8Hormone-like growth regulator 2 1Inhibition of lycopene cyclase 2 1Synthetic auxin 6 5Inhibition of Acetolactate synthase 3 2Inhibition of lycopene cyclase 2 2

BiocidesAcceleration of aerobic metabolism 2 1

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3. All references used in the formal evaluation

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Caquet, T., Hanson, M.L., Roucaute, M., Graham, D.W. and Lagadic, L. 2007. Influence of isolation on the recovery of pond mesocosms from the application of an insecticide. II. Benthic macroinvertebrate responses. Environmental Toxicology and Chemistry 26(6): 1280-1290.

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Castro, A.A., Lacerda, M.C., Zanuncio, T.V., de S. Ramalho, F., Polanczyk, R.A., Serrão, J.E. and Zanuncio, J.C. 2011. Effect of the insect growth regulator diflubenzuron on the predator Podisus nigrispinus (Heteroptera: Pentatomidae). Ecotoxicology: 1-8.

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Chang, K.H., Sakamoto, M. and Hanazato, T. 2005. Impact of pesticide application on zooplankton communities with different densities of invertebrate predators: An experimental analysis using small-scale mesocosms. Aquatic Toxicology 72(4): 373-382.

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Daam, M.A., Crum, S.J.H., van den Brink, P.J. and Nogueira, A.J.A. 2008. Fate and effects of the insecticide chlorpyrifos in outdoor plankton-dominated microcosms in Thailand. Environmental Toxicology and Chemistry 27(12): 2530-2538.

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Daam, M.A., Satapornvanit, K., van den Brink, P.J. and Nogueira, A.J.A. 2010. Direct and Indirect Effects of the Fungicide Carbendazim in Tropical Freshwater Microcosms. Arch. Environ. Contam. Toxicol. 58(2): 315-324.

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DeLorenzo, M.E., Pennington, P.L., Chung, K.W., Finnegan, M.C. and Fulton, M.H. 2009. Effects of the antifouling compound, Irgarol 1051, on a simulated estuarine salt marsh ecosystem. Ecotoxicology 18(2): 250-258.

Duchet, C., Caquet, T., Franquet, E., Lagneau, C. and Lagadic, L. 2010. Influence of environmental factors on the response of a natural population of Daphnia magna (Crustacea: Cladocera) to spinosad and Bacillus thuringiensis israelensis in Mediterranean coastal wetlands. Environ. Pollut. 158(5): 1825-1833.

Duchet, C., Larroque, M., Caquet, T., Franquet, E., Lagneau, C. and Lagadic, L. 2008. Effects of spinosad and Bacillus thuringiensis israelensis on a natural population of Daphnia pulex in field microcosms. Chemosphere 74(1): 70-77.

Duffield, S.J. and Aebischer, N.J. 1994. The effect of spatial scale of treatment with dimethoate on invertebrate population recovery in winter-wheat. J. Appl. Ecol. 31(2): 263-281.

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