Ecotoxicology of Rice Pesticides

Pesticide Risk Assessment in Rice Paddies: Theory and Practice E. Capri and D.G. Karpouzas (editors) © 2008 Elsevier B.V. All rights reserved

Chapter 5

Ecotoxicology of Rice Pesticides Jose V. Tarazona1 and G. Peter Dohmen2 1Department

of the Environment, Spanish National Institute for Agriculture and Food Research and Technology (INIA), 28040 Madrid, Spain 2BASF, Agricultural Center Limburgerhof, Ecotoxicology, D-67114 Limburgerhof, Germany

Contents 1. Introduction 2. Environmental and ecotoxicity data for risk assessment of pesticides 3. Specific issues associated with paddy rice 4. Ecotoxicological assessment of rice pesticides 4.1. Identification of relevant non-target populations and communities 4.2. Assessing the effects on the paddy community 4.3. Effects on associated communities and populations 4.3.1. Effects on bird populations 4.3.2. Effects on other terrestrial vertebrates and the use of mammalian toxicity data in ecotoxicological assessment 4.3.3. Effects on associated wetlands 4.4. Proposals for testing strategies and future needs 5. Conclusions References

69 71 74 77 80 81 84 84 85 85 87 87 88

1. INTRODUCTION Ecotoxicology can be defined as the study of the effects of substances (and physical agents according to some authors) on ecosystems. This covers the assessment, monitoring and diagnosis of effects on populations, communities and ecosystems including their structure and function and interactions with the physical and chemical environment, but also includes the development of methods for assessing the level of impact considered to not endanger the sustainability of ecosystems, the determination of conditions for the safe use of chemicals or agents and their management in order to achieve safe uses. Pesticides are biologically active substances intended to be effective against certain groups of organisms. Accordingly, some side effects next to the wanted activity can usually not be excluded. Regulatory decisions and management practices should limit such unwanted impact. However, as many other anthropogenic stressors on ecosystems, rice pesticides have caused unwanted and unpredicted ecological effects due to lack of knowledge or misuse. These effects have been reported and reviewed by other authors (Tejada et al., 1995; Abdullah et al., 1997). The objective of this chapter is to review the use of ecotoxicological methods for assessing the risk of rice pesticides and to explore new developments. As risk

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assessments offer the scientific basis for regulatory processes, this revision has been based on the current status of pesticide registration in the European Union. It should be noted that although almost all countries have established registration programmes for pesticides, there are significant differences in the requirements and capacities between developed and developing countries (Castillo et al., 1997). One of the main applications of ecotoxicology is to predict the potential environmental effects within the risk assessment context. This assessment is usually carried out in two subsequent steps, starting with the identification of the hazards potentially associated to a chemical followed by the establishment of dose/ response relationships (Pugh and Tarazona, 1998). In a subsequent step, the potential environmental concentrations of the substance are estimated and/or measured and compared to the toxicity (hazard) of the compound resulting in a prediction of risk. The protection goal in ecotoxicology is generally the sustainability of ecosystems and populations and not the individual organism, in contrast to human toxicology where effects on individuals are the main focus of the evaluation. As a consequence, the advance of ecotoxicology has required the development of new methodologies – starting from subcellular enzymatic bioindicator tests to complex community studies – and conceptual models for covering issues such as ecosystem redundancy and resilience, the assessment of indirect effects, or the potential for recovery (e.g. USEPA, 1998). Figure 1 summarises the ecotoxicological assessment process.

ECOSYSTEM

EFFECT MAGNIFICATION

ABIOTIC FACTORS COMMUNITY

ENVIRONMENTAL FACTORS

EFFECT MITIGATION

COMMUNITY +

POPULATIONS ENVIRONMENTAL FACTORS INDIVIDUALS

GEOGRAPHICAL DIMENSION Fig. 1. The ecotoxicological effect assessment requires the extrapolation of effects observed on individuals to consequences on populations, communities and ecosystems.

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As a matter of principle, the toxicological effects represent the response of the individual to the chemical exposure, while the goal of the assessment is to identify the consequences on populations and communities or on their functions. Thus, ecotoxicological approaches can use individual responses, and then estimate its consequences on populations and communities, or use directly higher tier assays measuring endpoints closer to ecology than to classical toxicology. Both approaches are complementary, and most risk assessment protocols are established on the basis of tiered levels. The initial or lower tier approaches are often based on single-species bioassays, resembling those developed by classical toxicology. In general, the lower tier tests are conducted under laboratory conditions; they are designed to provide clear, reproducible results with limited input of time and resources. At the same time, they only poorly reflect the reality. Higher tier tests are often designed to be closer to the real situation. This makes such studies often more complicated and expensive and reduces at the same time their replicability. Finally, field tests and monitoring studies provide insight into the real situation. However, the results are often only exactly true for this situation, although extrapolation to other situations is generally possible and valid, if certain limitations are considered. Such a tiered approach is applied frequently nowadays, when it is important to discover any significant, sometimes subtle impact relevant under environmental conditions, which may be small compared to other natural or anthropogenic impacts. For example, normal agricultural practice like ploughing, preparing the seed bed and harvesting often have a much stronger impact on soil organisms then the impact of pesticide use. During the 1960s and 1970s, the interpretation of the observed effects in hot spots, exploring the potential causal-effect relationships between measured concentrations and the observed ecological disasters, was rather straightforward. The clear evidence of pollution related effects, associated to a technological development with low environmental concern, expanded the role of ecotoxicology, and the 1970s and 1980s can be characterised by the development of ecological quality standards and objectives, setting maximum acceptable concentrations expected to be of insignificant impact to the environment. The methodology for setting these standards has been further developed and still represents a main request from the regulatory arena to the scientific community (Bro-Rasmussen et al., 1994) and for scientific debate (Tarazona, 1997; CSTEE, 2004). However, decision makers have to balance potential negative environmental impact, environmental costs, with the benefits of certain human activities. To do this the risk based approaches are the most appropriate tool. The decision-making process is only partly a scientific question, and depends mainly on societal, economic and political considerations. 2. ENVIRONMENTAL AND ECOTOXICITY DATA FOR RISK ASSESSMENT OF PESTICIDES Pesticides are mostly recognised as plant protection products, although other uses should be considered in some cases. In the particular case of rice pesticides, the use for vector control is particularly relevant in certain areas. Within this

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chapter, the assessment will focus on the use of rice pesticides as plant protection products. From a scientific perspective, the principles for the ecotoxicological assessment of other uses do not differ significantly; however, it should be recognised that the testing strategies, risk management and particularly, the cost/benefit assessment and decision-making, is directly related to the intended use, and may result in large differences in terms of the level of ecological risk considered to be acceptable. The environmental risk assessment of pesticides as plant protection products poses several particularities. Pesticides are designed to be biologically active compounds that can affect certain biota. Furthermore, the release of the chemical into the agricultural environment is intentional and the purpose is to affect organisms that are competitors, pathogens or pests for the crop. The intended release may also have consequences to organisms not intended to be affected – side effects on non-target organisms – and on adjacent and remote areas, where the pesticide is transported by/through air, water, soil or even living organisms. Both processes should be considered, but the approaches, protection aims and methodologies are different. In the off-crop area, exposure should be considered as a contamination event, resulting in the unintended presence of a potentially toxic chemical in environmental compartments. Exposure mitigation measures are feasible in some cases and welcomed. The consequences associated to the exposure and the ecotoxicological assessment should be based in the generic goal to avoid significant effects on the structure and functioning of the ecosystem. The in-crop assessment, however, must consider that the application of the pesticide is planned and intentional with the goal of altering the system and interspecies relationships in a way that is favourable to the crop, i.e. by reducing competition, herbivory and diseases (and thus intentionally reducing biodiversity). Thus, the assessment cannot be done on the basis of preventing biological/ ecological changes, but on restricting those changes to the intended ones. In addition, the assessment is not conducted on a (semi-)natural ecosystem but on human-managed agrobiosystems. The landscape, the abiotic compartments and the biodiversity of the biological community are heavily modified for improving crop productivity and reducing cost. Agricultural practices modify soil conditions and require severe adaptations of the soil community. The consequences for the above ground compartment are even higher, as the vegetation cover is replaced by the crop. Nevertheless, the agrobiosystems represent a relevant habitat for a large number of species. The relationships between the crop area and wild species is highly variable; in some cases, the crop area represent the predominant habitat for the species, while in others it is just a sporadic feeding zone. These reasons justify an in-crop effect assessment not based on the protection of the structure and function of undisturbed ecosystems. On the other hand, although being effective biological agents, undesired side effects should be minimised. As a direct consequence, pesticide effect assessment protocols require a new problem formulation for the in-crop assessment, which is based on the identification of non-target organisms. This identification is relatively easy in some cases. For example, some insecticides target very specific pests which can be identified at the species level for each crop. In these cases all other species,

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including other insect species, should be considered as non-target organisms. The assessment is not so clear in other cases, and a regulatory decision is required; for example, despite of their selectivity for some plant species, the European assessment consider that all plants within the crop area are target for herbicides (DGSANCO, 2002a). The situation can be even more complex, e.g. for fumigants and soil sterilisers, where the efficacy may be directly related not just to a reduction of a limited number of harmful species on the crop agrobiosystem but to intense structural changes. The in-crop level of protection also incorporates aspects associated to the beneficial effect of some species and taxa for soil protection and crop productivity. In fact, the protection of beneficial organisms used to be a main aim within the environmental safety assessment of pesticides. Although, nowadays, the goal has been extended in most regulatory schemes for covering all non-target groups independently of their agronomic implications, it must be recognised that the protection of well-known beneficial species is still a relevant aspect within the in-crop environmental assessment. Above ground invertebrates represent the most typical example. Although the final aim is theoretically established on ground, foliar and pollinator invertebrates as a whole, the reality in most cases is an assessment for honey bees and a few predatory and parasitoid species, which are considered sensitive and also posse agronomic relevance (Candolfi et al., 2001). There is also an intermediate level, which could be defined as an edge of field assessment, covering the non-crop areas surrounding the field. The level of agronomic impact in this zone is not as high as within the crop area, but it is not negligible and a pure ecological assessment is not possible. The first 1 m next to the field is often heavily disturbed by agricultural practices (in paddy rice, for example, the banks surrounding the field). The following 2 m (i.e. up to 3 m from the crop zone) are still disturbed by agricultural practices (e.g. turning areas for machinery) or removing vegetation (mowing). These areas may represent the transition between the agricultural land and the off-crop zone, and the level of protection should be established at least at the functional level, including as an ecological function the capability for re-colonisation of the crop area either between agronomic seasons or after abandoning the agricultural activity. These three levels have been summarised in Table 1. Using the European assessment scheme, taxonomic groups have been allocated to each area. Although some divergences may exist among the schemes developed in different world regions, the basis for the assessment are of generic nature and therefore worldwide applicable with just some differences related to regulatory settings or agricultural practices. The consequences of these different levels of protection are addressed in the methodology employed for the assessment but also on the margin of safety, or using a more proper definition the uncertainty factor, employed in the legislation. Larger factors are usually applied when the extrapolation is required for covering a wider set of taxonomic groups and/or ecological functions. The revision of the EU guidelines conducted by the Task Force for Harmonisation of Risk Assessment Procedures under the European Steering Scientific Committee offers several considerations on how these differences have been addressed within several European regulations (SSC, 2003).

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Table 1. Local assessment scenarios normally employed in the ecotoxicological assessment of pesticides Off-crop assessment Aquatic organisms including sediment and associated terrestrial systems

Edge of field

In-crop assessment

Terrestrial plants – ground and foliar invertebrates (non-target arthropods)

Birds and mammals – pollinators, non-target arthropods, soil dwelling organisms, soil function Protection level based on the Protection level based on Protection level based structure and functioning populations/communities on direct effects on of ecosystems including the potential non-target populations for recovery including the beneficial aspects of some species and groups, soil function and sustainability of the system

Regarding the methodological issues, the main difference in the lower tier assessment is the selection of the test system. The screening assessment of ecologically relevant effects is based on a simplistic assumption: the protection of the structure guarantees the protection of the ecosystem functions. The test systems should cover all relevant groups and, as discussed above, the uncertainty factor must be large enough for covering the non-tested groups. When the problem formulation excludes the target species, the selection of the proper non-target species in the lower tier screening assessment is required, and factors such as potential benefits (e.g. in the selection of bees and specific foliar arthropods) or citizen perception (e.g. in the selection of birds instead of reptiles) becomes more apparent. Probably, the main differences appear in the application of higher tier assessment, based on multispecies experiments, semi-field and field studies. Indirect effects are always relevant for ecosystem-based assessments, while they must be excluded in some population/community evaluations in the context of an agriculturally intended reduction of biodiversity with the aim to benefit the crop. For example, the use of non-selective herbicide will provoke in all cases a dramatic reduction of foliar arthropod biodiversity within the treated area. This effect is not intended, but is the unavoidable consequence of the effects on the target vegetation. Thus, while the potential direct toxicity of the herbicide for arthropods is included in the assessment as this could be considered an avoidable side effect, the indirect consequences are excluded.

3. SPECIFIC ISSUES ASSOCIATED WITH PADDY RICE The assessment of any particular crop requires some adaptations of the assessment scenario. The environmental conditions of rice paddies are so unique, however, that a different conceptual model is required for addressing the problem formulation. It should be noticed that in some areas rice is grown on dry arable

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soil instead of paddies; obviously, in those circumstances the assessment of rice pesticides becomes similar to the one for other cereals. There are four main issues associated to the paddy that should be considered and will be described below: ● ● ● ●

the specific conditions in rice semi aquatic/terrestrial ecosystem, fate considerations, the presence of specific communities, and the specific ecological value and in some regions the close connection to natural, ecologically important nature reserves.

An additional specificity of rice paddies is the use of pesticides for vector control instead of for crop protection. These assessments offer fundamental differences when compared to conventional pesticide evaluations. The main obvious difference focus on risk/benefit considerations, as Public Health, not farmer economy, is involved in this case. In addition, the efficacy of these measures requires a different geographical dimension, which must cover a significant part of the vector distribution area and do not distinguishes between in-crop and off-crop assessments. Furthermore, taxonomic groups traditionally considered as “non-target” standard species, such as chironomids, the most typical sediment dwelling organisms in ecotoxicity test design at the OECD level, can be the target for pesticide applications in rice paddies (Stevens and Warren, 1995). Focusing on plant protection products, as a matter of principle, the basic concept of in-crop and edge of field assessments based on terrestrial organisms and an off-crop assessment for aquatic ecosystems is not applicable to rice. Rice paddies are certainly agrobiosystems and not wetland ecosystems, but the artificial flooding of rice paddies creates a sequence of aquatic and terrestrial communities, which obviously is not observed in other crops. As a consequence, the in-crop assessment for rice paddies requires the definition of non-target effects for the paddy community, as well as a reconsideration of the relevance of the potential effects on pollinators, foliar and ground arthropods and on soil dwelling organisms. The second relevant group of differences between rice paddies and other crops are those regarding the fate processes. These aspects have received particular attention in other chapters within this volume. In the following the ecotoxicological consequences associated to these fate differences are highlighted. For the in-crop assessment, the application patterns, flooded or drainage conditions; will determine how and when the aquatic paddy community will be exposed, as well as the sequence of soil/sediment dwelling communities that should be considered in the assessment. Although heavily modified by the agricultural practices, the below ground community should be assimilated to that observed in Mediterranean wetlands, which, in a simplified approach could be described as a succession of soil, flooded soil, sediment, drained sediment and back to soil dwelling communities. The exposure assessment for mammals and birds also requires some adaptations with respect to the exposure patterns and in particular the food items to be considered. Regarding the off-crop assessment the most significant exposure difference is related to the routes regulating the transfer of the applied chemical from the

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treated area to adjacent aquatic ecosystems. Drift during application is obviously as relevant for rice as for other crops, while the relevance of the drainage to surface water and leaching to groundwater processes mostly depends on the specific paddy conditions. In addition a new emission route should be considered: the direct discharge of paddy water into associated water bodies. This route appears as a consequence of the need for maintaining a water flow in the paddy system and it may constitute the most relevant route in some cases. The third and fourth specific aspects are connected and directly linked to the biology of the paddy system and associated environments. The paddies constitute a very rich agrobiosystem in terms of biodiversity and large numbers of species are expected in these systems (Hidaka, 1998). Rice cultivation in Europe and other parts of the world can be divided in two main subgroups, showing clear differences in term of the associated biological community. The first subgroup corresponds to paddies associated to wetlands, mostly in coastal areas such as those of La Albufera, the Ebro delta or the Guadalquivir in Spain or the Camargue in France. The paddy community in these systems is directly related to the wetland community. Birds represent a particularly relevant group. Elphick (2000) studied Californian paddies and concluded that flooded fields apparently provide equivalent foraging habitat to semi-natural wetlands to bird species; similar situations have been observed in Europe (Hafner et al., 1986; Fasola et al., 1996). The second subgroup corresponds to inland arable land transformed into rice paddies through irrigation practices. The rice area in the Po valley represents a typical example similar to that observed in Zaragoza and Badajoz in Spain. These conditions create new habitats to be colonised by adapted species. The suitability of rice paddies as foraging habitats for aquatic bird species is not restricted to paddies associated to wetlands. Perez-Chiscano (1975) studied the changes in avifauna that followed the transformation of agricultural land into rice paddies in Badajoz (Spain). He found a dramatic change in the avifauna composition and distribution, with 60 birds species directly associated to the paddies and several others associated to the irrigation channels; most of them not reported in that area before. Maeda (2001) studied the avifauna of rice paddies in Japan and recorded 19 waterbird species and 31 landbird species over the study year. Waterbird occurrence was largely restricted to the flooded season, confirming the direct relationship between rice agricultural practices and the associated avian community. Other particularly relevant species expected in rice paddies are fish, amphibians and reptiles among the vertebrates, and crayfish among the macroinvertebrates (Hidaka, 1998). In summary, the same vertebrate and invertebrate groups are relevant for all paddies, associated to natural or to artificial (irrigated) wetlands systems. However, from an ecological perspective the value in term of biodiversity and nature protection may be very different and thus also the protection goals. In fact, wetland associated paddies are sometime part of the natural wetland ecosystems and in several areas are directly related to nature reserves. The actual situation is obviously relevant for site-specific assessments. Therefore, in addition to the generic assessment, such as required for national registrations of commercial products, a further

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site-specific assessment (e.g. within the Biodiversity Management Plans) for the use of pesticides in those protected areas with special concerns may be appropriate. This should include also a range of other management practices of importance for the protection of biodiversity and ecological values in protected wetlands, such as the paddy water regime, fertilisation, management of associated canals, etc. A frequently applied practice is to drain paddies before pesticide application. This management enhance the performance of the product, and also may reduce the risk to aquatic organisms in off-crop situations. On the other hand, draining will have a major impact on the animals living within the paddy, which usually depend on water, including for example, amphibia. Thus, in these areas good agricultural practice should be specifically designed for minimising the effects, and the overall consequences of the different alternatives should be evaluated in a holistic approach. Depending on regional demands, special emphasis could be on management plans to enhance the protection of, wetland plants, amphibia, fish, birds or plant species. 4. ECOTOXICOLOGICAL ASSESSMENT OF RICE PESTICIDES When the assessment is conducted within a regulatory framework, the test requirements, at least for the initial level, are generally specified, allowing some flexibility specifically at higher levels. As for other chemicals or pesticides, the ecotoxicological assessment of rice pesticides should be conducted through a tiered testing strategy. The initial lower tier testing is done using single-species laboratory bioassays under worst case condition. If the results of these studies indicate a risk, then additional, higher tier tests can be performed, which should produce relevant information and thus reduce uncertainties associated with the risk assessment process based on a limited set of data. They include studies to reflect more realistic exposure conditions, additional species testing and at the highest tier microcosms, mesocosms and field studies. The lower tier testing is mostly conducted on a set of “typical” laboratory species and based as much as possible on standardised testing conditions. The selected species should cover a variety of taxonomic groups representing the key ecological receptors. The endpoints are selected through a combination of ecological relevance, appropriateness and feasibility. The standardisation of testing conditions by international and/or national organisations provides the level of reproducibility required for a regulatory process and the exchange of data at the international level. Table 2 offers a summary of the main regulatory ecotoxicological requirements in the European Union under Directive 91/414/EC and in USA under FIFRA Subdivision E, Part 158; test are conducted according to the OECD, EU or USA guidelines. As shown in the Table 2, the selected species and assays present large similarities in both regulatory assessments. Mammals are not included as the mammalian toxicity assays requested for the health assessment are used for the environmental assessment. The OECD runs harmonisation programmes for the guidelines and for the mutual recognition of ecotoxicological results. OECD guidelines include

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Table 2. Standard ecotoxicity tests required for the registration of pesticides in the EU and USA, OECD guideline are generally relevant in both regions (and worldwide) Ecotoxicity test Avian acute oral Avian dietary Avian reproduction-chronic toxicity Simulated or actual field test mammals and birds Freshwater fish acute (two species) Freshwater invertebrate acute Estuarine/marine fish, shellfish, shrimp acute Chronic toxicity test on juvenile fish (growth) Freshwater or marine/estuarine fish early life stage chronic toxicity Freshwater invertebrate life cycle chronic toxicity Effects on sediment dwelling organisms Full fish life cycle Simulated or actual aquatic field study Bioconcentration in fish Effects on algal growth Tier I seed germination – single dose Tier I seedling emergence – single dose Tier I vegetative vigor – single dose Tier I aquatic plant growth – single dose Tier II seed germination – multi-dose Tier II seedling emergence – multi-dose Tier II vegetative vigor – multi-dose Tier II aquatic plant growth – multi-dose Honey bee acute contact LD50 Honey bee acute oral LD50 Honey bee toxicity of residues on foliage Bee brood feeding test Other arthropods Acute toxicity for earthworms: artificial soil test. Chronic toxicity for earthworms: growth, reproduction and behaviour Soil non-target microorganisms Effects on other non-target organisms (flora and fauna) believed to be at risk Effects on biological methods for sewage treatment

EU guideline

USA guideline

SETAC, 1995 OECD 205 OECD 206

71-1 71-2 71-4 71-5

OECD 203, EU C1 OECD 202, EU C2

72-1 72-2 72-3

OECD 215 OECD 210

72-4a

OECD 211

72-4b

OECD 218, 219

OPPTS 850.1790 ASTM E83-93 72-5 OPPTS 850.1500

Protocol to be discussed case-by-case

72-7 OECD 305E OECD 201, EU C3

Not relevant OECD 208 OECD 201, 221 OECD 214, EPPO 170 OECD 213, EPPO 170

122-1 122-1 122-1 122-2 123-1 123-1 123-1 123-2 141-1 141-2

ICPBR Guidance documents OECD 207, EU C OECD 222 OECD 216, 217, SETAC Not defined Not defined

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several of the assays for which the current EU regulation does not present a specific own guideline. In practice, most studies are principally based on OECD guidelines. However, the assays conducted under equivalent specific guidelines (e.g. USA guidance for European submissions) are usually accepted and the guidance documents (e.g. DGSANCO, 2002a, b) offer additional information on which guidelines are comparable and proposals on appropriate methodologies for conducting those assays for which a guideline is not specified in the regulation. As expected, the species selection was done under generic aspects and do not focus on the particularities of rice paddies. Nevertheless, the overall picture offers a reasonable selection of key taxonomic groups relevant for a standard first tier paddy and wetland assessment, may be with two main exceptions: aquatic macroinvertebrates and wetland plants, although there are discrepancies in this point. There are various options for higher tier testing depending on the specific concerns or uncertainties that need to be addressed. Studies can be performed simulating more realistic exposure conditions and covering processes such as degradation and dissipation of the substance. Time to event studies may help to more realistically address short-term exposure. Additional species testing reduces the uncertainty with respect to sensitivity differences between species. Population studies cover different life stages of a species. All these tests are usually performed with a single species in the laboratory. Community studies are more complex and cover a range of species. Usually such studies are conducted as micro–mesocosm or as (semi-)field studies. These studies provide the most realistic and complex results including information on indirect effects, interactions and recovery, but they are also least reproducible. Such approaches are in principle similar in the different compartments, aquatic and terrestrial. Obviously, aquatic microcosms, mesocosms and semi-field/field studies are usually employed for covering aquatic ecosystems. Higher tier soil laboratory studies with communities focus on soil microcosms with two main approaches, the use of soil cores with its biological community, such as the terrestrial model ecosystem (TME) approach (Knacker et al., 2004), and the use of artificial soil assemblages, such as the MS·3 approach, (Boleas et al., 2005a,b; Fernández et al., 2005). The next step moves directly to semi-field/field studies which may also cover other terrestrial groups, such as bees, foliar arthropods, birds and mammals. The appropriateness of these designs for covering the specific conditions of rice paddies is limited. Aquatic micro and mesocosms may be relevant for the assessment of the adjacent water bodies, but its biological structure is clearly different from that expected for the paddy. On the other hand, the information obtained in mesocosm studies with a large diversity of species will also provide relevant data on potential effects in paddies if the specific fate and climatic conditions of paddies are considered. Due to the significant proportion of rice paddies located in coastal areas, estuaries may become particularly relevant, and estuarine mesocosms have been used for higher tier testing of rice pesticides (Wirth et al., 2004). The soil microcosms are obviously of low value, as the specific paddy conditions are very different from that observed in pasture areas or arable land. The peculiarity of rice paddies conditions and the economic, social, public health and ecological relevance of this crop has conferred a significant

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interest to the paddy situations, and specific higher tier test designs are available (Dennet et al., 2003; Sanchez et al., 2006; Sanchez-Bayo and Goka, 2006). The general principles for assessing these higher tier studies, such as those recommended in the Society of Environmental Toxicology and Chemistry (SETAC) workshops HARAP and CLASSIC (Campbell et al., 1999; Giddings et al., 2002) are generally applicable, although the specific conditions of the rice paddy should be considered. Some issues are addressed below. 4.1. Identification of relevant non-target populations and communities The use of pesticides in rice paddy may have two main objectives, as plant protection products, for improving rice yield and control pests and diseases, or for controlling vectors and pests in public health programmes. Accordingly, the problem definition or problem formulation of the risk assessment can differ significantly. They determine which organisms should be considered as target, non-target and also the protection goals of the environmental risk assessment. In this chapter, we will focus mostly on the use of rice pesticides as plant protection products. As mentioned above, the ecotoxicological assessment for vector control programmes is not significantly different in the lower tier level assessment. The main difference may be that the treatment should cover all the wetland area, not just the rice paddies, and therefore the transfer of the pesticide from the paddy to the adjacent water bodies becomes irrelevant as these water bodies will be also directly treated. As a consequence, the distinction between the paddy community and the associated wetland communities of the paddy neighbourhood is useless. At the higher tier level, significant differences may arise due to the particularities of other parts of the risk assessment protocol, basically, the efficacy assessment and the risk characterisation. Vector control programmes usually require a long-term planning approach to be effective, and the geographical scale is usually wider than for plant protection products. The assessment of long-term effects in the case of persistent pesticides and the consequences on biodiversity for repeated applications become essential. In addition, the public health benefits expected from this control are so relevant that the question is usually not whether to use a pesticide but which one should be applied at least until a significant level of control is achieved and/or other control measures are implemented. Thus, the risk characterisation tends to be a comparative risk characterisation, analysing the different alternatives and the risk/benefits of each option. Finally, in most countries these programmes are handled by public authorities, not as a private decision from the farmers, and require site-specific impact and risk assessments adapted to the local particularities (e.g. Stevens and Warren, 1995). Going back to the use of rice pesticides as plant protection products, the “classical” in-crop versus off-crop assessment is applicable, as all intended effects are related to the paddy itself and any effect outside the paddy should be considered as undesired. Some regulatory guidelines have conferred a low relevance to the paddy community (e.g. MEDRice, 2003) as heavily disturbed in-crop area, but from an ecological perspective, the paddy community is clearly relevant, as presented above, and this circumstance requires an additional consideration of the

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level of protection required for the paddy and the associated communities, ensuring efficient crop production while avoiding unacceptable levels of effect. 4.2. Assessing the effects on the paddy community The complex paddy rice community is subjected to continuous changes. The typical paddies located around wetlands should be considered as modified wetland communities, typical for non-permanently flooded systems, where the vegetation cover is replaced by the crop. Rice pesticides are mostly applied during the flooding period, and therefore the in-paddy effect assessment should focus mostly on the aquatic paddy community, including sediment. Sometimes, the paddies are also drained before pesticide application with the loss of a large part of the aquatic community, modifying the risk assessment (i.e. reducing the risk of the outflow and increasing the effects on the paddy community). In addition to the contribution of the in-crop paddy community to the overall biodiversity, a major role is to serve as food for other organisms with particular relevance, for example, to many bird species. The main groups to be considered for the in-paddy assessment are phytoplankton, zooplankton, macroinvertebrates, sediment/soil microorganisms and birds. Within the crop, other wetland plants are generally considered weeds, and therefore potential targets for the pesticide, however, for endangered and/or endemic species a site-specific assessment is required. The situation is more complex with respect to phytoplankton. This is the main basis for the aquatic food chain; in addition some blue-green algae are useful due to their nitrogen fixation capability. On the other hand, from an agronomic perspective, algae compete for nutrients with the rice plant and can impede the water management; thus rice yield is usually better if strong algal growth (particularly that of large filamentous species) is avoided. Not surprisingly, the main risks for aquatic plants and algae are expected from the use of herbicides. The effects assessment usually considers that all plants within the crop area are target species for herbicides. On the other hand, endangered species are frequently found in wetland areas and paddies and, depending on the water management, a protection at the paddy level may be essential when designing the species conservation strategy. As a corollary, a generic assessment may assume a low relevance for in-paddy wetland plants, while a site-specific assessment may be required for endangered species in the prevalent areas. Some herbicides are also expected to be particularly toxic for phytoplankton, while, not surprisingly insecticides tend to be particularly risky for zooplankton species. Both communities play a key role in paddy systems but, at the same time, present a large variability regarding the special and temporal composition due to, among other factors, agronomic water management. Typical characteristics of these communities are their very high potential for rapid colonisation and/or for biological cycles with resistance forms or other mechanisms allowing the species to remain inactive during the dry season and recover quickly as soon as the conditions allow a proper development. In addition, the water inflow brings new populations, which can develop very rapidly under the conditions

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typically prevailing in paddy systems, such as high temperature and sufficient nutrients. These characteristics also reduce the impact of rice agricultural practices where the water level is artificially controlled and the paddies are flooded or drained as needed. As a consequence, the effect assessment of pesticides within the system should consider the high potential for recovery/re-colonisation of the paddy community. Populations of copepods, cladocerans and ostracods fluctuate during the paddy-growing season in response to flooding, field drainage, ploughing and other practices (Tejada et al., 1995; Abdullah et al., 1997). There is also a tendency within taxonomic groups with communities dominated initially by phytophagous species, gradually giving way to predators and scavengers (Sanchez-Bayo and Goka, 2006). Under these circumstances it can be assumed that the ecological relevance of the plankton communities should focus on their function, while structural changes are expected to be acceptable within the crop if the function is maintained. The main consequence for that assumption is the reduction in the uncertainty/assessment factor. Among macroinvertebrates, crayfish are considered particularly relevant in rice paddies and have received a significant attention. Part of this relevance is related to its role as food source not only for wild vertebrates but also for humans. In certain areas, rice paddies are used for a commercial cultivation of crayfish, stocking crayfish in the paddy when rice reaches the green ring stage (Huner and Barr, 1991). Figure 2 shows a comparison of the acute toxicity of several pesticides for daphnids and crayfish. The information available for crayfish is too limited for allowing a range estimation for this group, while for most pesticides, several daphnid species have been tested. The figure presents for each pesticide

Acute toxicity crayfish

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Fig. 2. Comparison of the acute toxicity of several pesticides to crayfish versus daphnids. The graph gives one value for crayfish, which is either the only available result or a geometric average. Daphnids data are presented as the lowest value (symbol) and the range (line).

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the reported acute toxicity data for crayfish and the lowest and highest acute EC50 for daphnids, combining information from several databases (USEPA, EU, INIA, etc.). The figure confirms the highest toxicity of insecticides and shows that crayfish are in most cases, but not always, less sensitive than daphnids. Part of this apparent difference simply reflects the fact that the database is larger for daphnids than for crayfish. Differences of one and even two orders of magnitude in the acute toxicity of the same pesticide for daphnids are relatively frequent as observed by the bars. There are several insecticides in use at present, which are potentially toxic to fish, crayfish or which may have a negative impact on birds feeding in the paddy. Those will need a very careful evaluation and eventually a risk/benefit analysis to determine whether, when and where their use can be considered acceptable or not. The bioaccumulation of pesticides in crayfish and other aquatic invertebrates is receiving a significant attention (Chaton et al., 2002; Klosterhaus et al., 2003; Maenpaa et al., 2003). Although there are not sufficient data for sound conclusions yet; a conceptual comparison of the bioaccumulation mechanisms in fish and invertebrates suggests two potential issues that require further assessment on the role of invertebrates in bioaccumulation and transfer of pesticides into the food chain, particularly for chemicals with a relatively fast dissipation from the water column: the highest bioaccumulation potential of invertebrates compared to fish for short-term exposures due to lower depuration rates (e.g. for chemicals metabolised through cytochrome P450 related routes) and the potential for accumulation related not to the liphophilicity of the chemical but to reactivity with exoskeleton structures. The latest is an adsorption-like phenomena that although does not affect the internal body burden may contribute to the overall exposure of those predators swallowing the whole crayfish. An interesting aspect of the paddy non-target community is its beneficial role for controlling pests and vectors (Dennett et al., 2003); which provides additional arguments for protecting the aquatic community. This assessment may be compared to the beneficial role of some non-target terrestrial arthropods in other crops. A distinction between the protection goals to be applied to in-crop and off-crop non-target arthropods has been suggested (Candolfi et al., 2001) and accepted in the regulatory arena (DGSANCO, 2002a). The ecotoxicological assessment of the sediment/soil microbial community is based on functional parameters related to the nutrient cycles: respiration and nitrification. These roles are essential for a sustainability assessment. However, the evaluation is more difficult in the specific paddy situation, as the flooding conditions by themselves, independently of the potential pesticide effects, may interfere with these processes. The current guidelines (OECD, 2004a,b) and the decision criteria for agricultural soils accept a significant effect if a recovery is observed in 100 days. Similar criteria are considered acceptable for the paddy assessment while specific conditions on paddy soil should be used if become available (MEDRice, 2003). In summary, the relevant ecotoxicological effects to be specifically highlighted for the assessment of the paddy community are those related to the plankton function and the role as food source for birds. The plankton assessment can be covered through the standard ecotoxicological tests as the selected organisms

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may be considered representative. The protection of function alone, allowing structural changes, allows a reduction of the uncertainty/assessment factors. It has been suggested that in a first tier assessment the lack of effects on representative species such as green algae and daphnids may be enough for the required level of protection and, therefore, the EC50 (alga) and NOECs (fish, Daphnia) from the standard tests without additional factors could be sufficient for the protection of plankton function (Tarazona and Sanchez, 2006). The main goal for the in-crop assessment should be the potential for recovery of the community. As a difference to the arable situation, where recovery has to be demonstrated until the following season, and considering the ecological importance of such artificial wetlands the recovery should preferably occur within the same season. It must also be considered that in some tropical countries fishes are cultured in the rice paddy, and therefore the effects on fish populations should be also covered (Abdullah et al., 1997). The evaluation of the potential effects of pesticides on fish or crayfish populations may be done on the basis of similar methodologies than those employed for the ecotoxicological assessment. 4.3. Effects on associated communities and populations The complement of the paddy community assessment must cover the “users” of the paddy environment and the surrounding ecosystems that may be exposed during or after the application. These assessments cover birds and mammals feeding in the paddy and the aquatic bodies and wetland areas that may receive the spray drift or the paddy water drainage. 4.3.1. Effects on bird populations

As explained previously, the assessment of the potential effects on birds is a critical aspect in the assessment of rice pesticides. Due to animal welfare and ethical issues the possibilities for toxicity testing on birds are limited. Typical testing strategies for birds cover two species from different families, usually Bobwhite quail (Colinus virginianus) and Mallard duck (Anas platyrhynchos). A single dose acute lethality tests, a short-term dietary test with oral exposure from food during five days and reproduction tests are presently required for covering the risk assessment of acute mortality and reproduction effects that may impair populations. This data set is considered the minimum for getting acceptable risk estimations. The endpoints to be measured in avian reproduction studies and the interpretation and extrapolation of the observed results is receiving significant attention nowadays. Several proposals have been published suggesting better alternatives for data handling (Mineau, 2005) and for using the data in risk assessments (Bennett et al., 2005; Shore et al., 2005). The bird assessment in the European Union is moving to the identification of key species, representative of specific crops and to focus the assessment in a species-specific risk characterisation for the selected species (compare DGSANCO, 2002b). The application of this approach to complex systems, such as rice paddies, with hundred of species with very different feeding habits seems to be problematic with the current

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level of information. The worst case assumption of a significant number of individual birds feeding almost exclusively in the rice paddies seems to be realistic (Hafner et al., 1986; Fasola et al., 1996; Elphick, 2000), and the feeding behaviour is very variable and clearly controls the environmental exposure of birds to pesticides, with large differences even within the same family (Albanis et al., 1996). As a consequence, the environmental fate properties of the pesticide will trigger which species will receive the highest exposure. The suitability of the generic residue estimations in plants, seeds, arthropods, etc., used for other crops (e.g. DGSANCO, 2002b) must be re-evaluated depending on the pesticide application practice. For example, the generic assessment employed for a pesticide applied in drained paddies which are re-flooded immediately after treatment should be checked carefully. The direct consumption of paddy soil/sediment and the exposure via aquatic invertebrates including crayfish should be also considered. A potential concern based on the avian toxicity studies and the expected level of residues should require a further assessment, considering relevant exposure routes, such as the crop, soil/ sediment, other plants, algae, invertebrates and fish. As already mentioned, the bioaccumulation assessment should consider not only fish but also algae, zooplankton, crayfish and sediment dwelling invertebrates. 4.3.2. Effects on other terrestrial vertebrates and the use of mammalian toxicity data in ecotoxicological assessment

Birds and mammals toxicity data are usually employed for a generic assessment of all vertebrates, including amphibians and reptiles. Both groups have a greater relevance in rice paddies than mammals. The decline of amphibian populations all over the world is creating a significant concern. Depending on the species and developmental status, the main exposure route for amphibians may be water, either through the respiratory system or by dermal exposure, food or a combination of both. The basic assumption that an assessment based on fish for water exposure and birds and mammals for oral exposure is also protective for amphibians and reptiles has been demonstrated to be true for the limited number of cases in which information on data-rich chemicals has allowed a comparison. With the current level of knowledge and before specific assays are developed and standardised this assumption seems to be the only pragmatic solution to be applied also for the assessment of rice pesticides. Nevertheless, it should be clear that this is a pragmatic solution for the time being, not sufficiently scientifically established, and that this should be revisited as soon as additional information may be provided. As a direct consequence, a generic risk assessment for mammals based on worst case exposure estimations should be conducted for rice pesticides, regardless of the relevance of mammals feeding on the paddy systems, as a method for covering the oral exposure of vertebrates in general. 4.3.3. Effects on associated wetlands

In several areas of Europe and elsewhere, rice paddies are directly connected to wetland areas of high ecological value. These areas include some of the most significant biodiversity reservoirs, receiving the highest possible level of protection.

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A direct relationship between the use of pesticides in rice paddies and the contamination of these natural reservoirs has been described (Manosa et al., 2001). In addition to drift and drainage, the direct discharge of paddy water into the surrounding water bodies constitutes the main exposure route for these wetland ecosystems. As these systems mostly comprise low-flow systems, the dilution is limited and the concentrations expected at the discharge sites may reach levels that clearly require a specific assessment, as depending on the pesticide fate properties and the management situations this route may be much more relevant than spray drift. A standard risk assessment for off-crop areas focusing on the effects on both structure and function of the ecosystem is appropriate for these systems. This is the same situation addressed for other crops and their adjacent water bodies; thus, the same methodologies may be applied. With respect to nontarget plant testing this may need some adaptation to cover wetland plants, too. Nevertheless, there is a specific aspect with paddy rice concerning its relevance for rare and/or threatened species, which is not covered in a generic assessment for registration purposes. The use of pesticides in areas where endangered and/or rare species may be at risk requires an additional specific evaluation for those particular species in the form of an impact or a risk assessment in addition to the generic regulatory evaluation. In fact, this is a common practice in rice cultivations located in the vicinity of ecological reserves; such assessments on “endangered species” in specific areas is nowadays also practiced in the USA. The effect assessment for wetland plants should be at least partially covered in the generic risk assessment. The assessment of pesticide risks for non-target plants has traditionally differentiated aquatic and terrestrial systems. The aquatic compartment has been covered by algae and one aquatic vascular plants, Lemna spp., as species selected for the standard ecotoxicity tests in the first tier. The risk assessment for terrestrial plants has been introduced later on, with the development of specific proposals. Basically, the assessment is only relevant for herbicides, as other pesticides show in general low toxicity for plants. The generic assessment usually considers spray drift in the vicinity of the crop as the major relevant exposure route. The possibility for medium-term transport related to volatility and subsequent atmospheric deposition in other areas has also been considered in certain cases. Both routes may be relevant in rice paddies, however, in most cases the already mentioned discharge of contaminated paddy water into the wetland would be the predominant path of potential contamination. This route of exposure may be reduced by spraying the herbicide on the drained paddy, which is often done anyway to increase efficacy of the treatment. There are no standard ecotoxicity tests, other than those on Lemna spp., for covering this potential risk, however the evaluation of the efficacy, selectivity and mode of action of the herbicide may provide enough information for this assessment. Basically, the required information is a set of toxicity thresholds or concentration/response relationships for a set of wetland relevant species covering a wide range of taxonomic groups and considering exposures from spray/drift, from water and from soil/sediment when relevant, which may produce enough information even for the application of probabilistic risk assessments.

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As explained above, if endangered wetland species are present in the area, a specific assessment at the local level should be conducted and methods have been developed for this ecotoxicological evaluation (e.g. Luo and Ikeda, 2005). 4.4. Proposals for testing strategies and future needs Due to the complexity of rice paddies, the ecotoxicological assessment of rice pesticides and its further development into a risk characterisation can be highly benefited by the development of a specific conceptual model. A methodology based on versatile conceptual models which are adapted to the characteristics of each chemical were initially developed for terrestrial systems (Tarazona et al., 2002; Tarazona and Vega, 2002) and has been adapted to the paddy situation for the assessment of rice pesticides (Tarazona and Sanchez, 2006). The option covers a full set of possibilities, maximising the use of first tier data whenever possible. This proposal has been completed with the development/adaptation of specific testing proposals, including off-site toxicity testing of treated paddy water and rice paddy mesocosms-type studies (Sanchez et al., 2006). The use of experimental rice paddies, either in ad hoc facilities or using compartments build within rice paddies, offers large possibilities for conducting higher tier ecotoxicity tests (Dennet et al., 2003; Sanchez-Bayo and Goka, 2006) and it is feasible to combine fate and ecotoxicological parameters in semi-field paddy assays measuring simultaneously realistic exposure estimations and the effects on the paddy community (Sanchez et al., 2006). The development of some guidance for conducting ecotoxicological assays on experimental paddies should be considered for facilitating the regulatory use of these tools. In addition, one of the main needs for the future is the development of scenarios and exposure models for birds feeding on the paddy, reviewing the extensive literature available on the ecology of most of the relevant species.

5. CONCLUSIONS The ecotoxicological assessment of rice pesticides is particularly complex due to the specificities of this crop where aquatic and terrestrial communities are mixed in a human-managed wetland-type agrobiosystem. Any assessment must cover at least three main aspects, potential effects on the paddy community, potential effects on associated wetlands and water bodies, and the potential risks for vertebrates, particularly birds, feeding on the paddy. The initial lower tier assessment may be conducted using the generic approaches derived for other crops. For a higher tier risk assessment it is recommended to develop a specific conceptual model for identifying the key elements that should be addressed. Proposals for constructing these models on the basis of the characteristics of the pesticide are available and may allow a proper selection of the essential combinations of: compartment → exposure route → ecological receptor

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These combinations can be then prioritised and should be considered in the refinement. Specific tools, and in particular, experimental paddies, which can be easily created in rice fields, offer a perfect higher tier experimental tool for assessing exposure, including bioaccumulation, and effects under realistic conditions. Further site-specific considerations and management practices may become relevant with respect to nature conservation issues or where dual use of paddies for (cray)fish production is intended. REFERENCES Abdullah, A. R., Bajet, C. M., Matin, M. A., Nhan, D. D. and Sulaiman, A. H. (1997). Ecotoxicology of pesticides in the tropical paddy field ecosystem. Environ. Toxicol. Chem. 16, 59–70. Albanis, T. A., Hela, D., Papakostas, G. and Goutner, V. (1996). Concentration and bioaccumulation of organochlorine pesticide residues in herons and their prey in wetlands of Thermaikos Gulf, Macedonia, Greece. Sci. Total Environ. 182, 11–19. Bennett, R. S., Dewhurst, I. C., Fairbrother, A., Hart, A. D., Hooper, M. J., Leopold, A., Mineau, P., Mortensen, S. R., Shore, R. F. and Springer, T. A. (2005). A new interpretation of avian and mammalian reproduction toxicity test data in ecological risk assessment. Ecotoxicology 14, 801–815. Boleas, S., Alonso, C., Pro, J., Babín, M. M., Fernández, C., Carbonell, G. and Tarazona, J. V. (2005a). Effects of sulfachlorpyridazine in MS·3-arable land: A multispecies soil system for assessing the environmental fate and effects of veterinary medicines. Environ. Toxicol. Chem. 24, 811–819. Boleas, S., Alonso, C., Pro, J., Fernández, C., Carbonell, G. and Tarazona, J. V. (2005b). Toxicity of the antimicrobial oxytetracycline to soil organisms in a multispecies-soil system (MS·3) and influence of manure co-addition. J. Hazard. Mater. 122, 233–241. Bro-Rasmussen, F., Calow, P., Canton, J. H., Chambers, P. L., Silva Fernandes, A., Hoffmann, L., Jouany, J. M., Klein, W., Persoone, G., Scoullos, M., Tarazona, J. V. and Vighi, M. (1994). EEC water quality objectives for chemicals dangerous to aquatic environment (List 1). Rev. Environ. Contam. Toxicol. 137, 83–110. Campbell, P. J., Arnold, D. J. S., Brock, T. C. M., Grandy, N. J., Heger, W., Heimbach, F., Maund, S. J. and Streloke, M. (Eds), (1999). Guidance Document on Higher-tier Aquatic Risk Assessment for Pesticides (HARAP). SETAC-Europe Publications, Brussels, Belgium. Candolfi, M. P., Barrett, K. L., Campbell, P. J., Forster, R., Grandy, N., Huet, M. C., Lewis, G., Oomen, P. A., Schmuck, R. and Vogt, H. (Eds), (2001). Guidance document on regulatory testing and risk assessment procedures for plant protection products with non-target arthropods. From the ESCORT 2 workshop (p. 46). SETAC, Pensacola. Castillo, L. E., De La Cruz, E. and Ruepert, C. (1997). Ecotoxicology and pesticides in tropical aquatic ecosystems of Central America. Environ. Toxicol. Chem. 16, 41–51. Chaton, P. F., Ravanel, P., Tissut, M. and Meyran, J. C. (2002). Toxicity and bioaccumulation of fipronil in the nontarget arthropodan fauna associated with subalpine mosquito breeding sites. Ecotoxicol. Environ. Saf. 52, 8–12. CSTEE (2004). Opinion on the Setting of Environmental Quality Standards for the Priority Substances included in Annex X of Directive 2000/60/EC in Accordance with Article 16 thereof (p. 32). CSTEE, SANCO C7/GF/csteeop/ WFD/280504 D(04). Brussels. Dennett, J. A., Bernhardt, J. L. and Meisch, M. V. (2003). Operational note effects of fipronil and lambda-cyhalothrin against larval Anopheles quadrimaculatus and nontarget aquatic mosquito predators in Arkansas small rice plots. J. Am. Mosq. Control Assoc. 19, 172–174. DGSANCO (2002a). Guidance Document on Terrestrial Ecotoxicology under Council Directive 91/414/EEC. SANCO, 10329/2002rev.2 final. DGSANCO (2002b). Guidance Document on Risk Assessment for Birds and Mammals Under Council Directive 91/414/ EEC. SANCO/4145/2000rev.6 – final. Elphick, C. S. (2000). Functional equivalency between rice fields and semi-natural wetland habitats. Conserv. Biol. 14, 181–191.

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