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Scientific Opinion on the state of the science on pesticide risk assessment for amphibians and reptiles

2018; Wiley; Volume: 16; Issue: 2 Linguagem: Inglês

10.2903/j.efsa.2018.5125

1831-4732

Colin Ockleford, Paulien Adriaanse, Philippe Berny, T.C.M. Brock, Sabine Duquesne, Sandro Grilli, Antonio F. Hernández, Susanne Hougaard Bennekou, Michael Klein, Thomas Kühl, Ryszard Laskowski, Kyriaki Machera, Olavi Pelkonen, Silvia Pieper, Michael Stemmer, Ingvar Sundh, Ivana Teodorović, A. Tiktak, Christopher John Topping, Gerrit Wolterink, Annette Aldrich, Cecilia Berg, Manuel E. Ortiz‐Santaliestra, Scott M. Weir, Franz Streissl, Robert H. Smith,

Agricultural safety and regulations

EFSA JournalVolume 16, Issue 2 e05125 Scientific OpinionOpen Access Scientific Opinion on the state of the science on pesticide risk assessment for amphibians and reptiles EFSA Panel on Plant Protection Products and their Residues (PPR), EFSA Panel on Plant Protection Products and their Residues (PPR)Search for more papers by this authorColin Ockleford, Colin OcklefordSearch for more papers by this authorPaulien Adriaanse, Paulien AdriaanseSearch for more papers by this authorPhilippe Berny, Philippe BernySearch for more papers by this authorTheodorus Brock, Theodorus BrockSearch for more papers by this authorSabine Duquesne, Sabine DuquesneSearch for more papers by this authorSandro Grilli, Sandro GrilliSearch for more papers by this authorAntonio F Hernandez-Jerez, Antonio F Hernandez-JerezSearch for more papers by this authorSusanne Hougaard Bennekou, Susanne Hougaard BennekouSearch for more papers by this authorMichael Klein, Michael KleinSearch for more papers by this authorThomas Kuhl, Thomas KuhlSearch for more papers by this authorRyszard Laskowski, Ryszard LaskowskiSearch for more papers by this authorKyriaki Machera, Kyriaki MacheraSearch for more papers by this authorOlavi Pelkonen, Olavi PelkonenSearch for more papers by this authorSilvia Pieper, Silvia PieperSearch for more papers by this authorMichael Stemmer, Michael StemmerSearch for more papers by this authorIngvar Sundh, Ingvar SundhSearch for more papers by this authorIvana Teodorovic, Ivana TeodorovicSearch for more papers by this authorAaldrik Tiktak, Aaldrik TiktakSearch for more papers by this authorChris J Topping, Chris J ToppingSearch for more papers by this authorGerrit Wolterink, Gerrit WolterinkSearch for more papers by this authorAnnette Aldrich, Annette AldrichSearch for more papers by this authorCecilia Berg, Cecilia BergSearch for more papers by this authorManuel Ortiz-Santaliestra, Manuel Ortiz-SantaliestraSearch for more papers by this authorScott Weir, Scott WeirSearch for more papers by this authorFranz Streissl, Franz StreisslSearch for more papers by this authorRobert H Smith, Robert H SmithSearch for more papers by this author EFSA Panel on Plant Protection Products and their Residues (PPR), EFSA Panel on Plant Protection Products and their Residues (PPR)Search for more papers by this authorColin Ockleford, Colin OcklefordSearch for more papers by this authorPaulien Adriaanse, Paulien AdriaanseSearch for more papers by this authorPhilippe Berny, Philippe BernySearch for more papers by this authorTheodorus Brock, Theodorus BrockSearch for more papers by this authorSabine Duquesne, Sabine DuquesneSearch for more papers by this authorSandro Grilli, Sandro GrilliSearch for more papers by this authorAntonio F Hernandez-Jerez, Antonio F Hernandez-JerezSearch for more papers by this authorSusanne Hougaard Bennekou, Susanne Hougaard BennekouSearch for more papers by this authorMichael Klein, Michael KleinSearch for more papers by this authorThomas Kuhl, Thomas KuhlSearch for more papers by this authorRyszard Laskowski, Ryszard LaskowskiSearch for more papers by this authorKyriaki Machera, Kyriaki MacheraSearch for more papers by this authorOlavi Pelkonen, Olavi PelkonenSearch for more papers by this authorSilvia Pieper, Silvia PieperSearch for more papers by this authorMichael Stemmer, Michael StemmerSearch for more papers by this authorIngvar Sundh, Ingvar SundhSearch for more papers by this authorIvana Teodorovic, Ivana TeodorovicSearch for more papers by this authorAaldrik Tiktak, Aaldrik TiktakSearch for more papers by this authorChris J Topping, Chris J ToppingSearch for more papers by this authorGerrit Wolterink, Gerrit WolterinkSearch for more papers by this authorAnnette Aldrich, Annette AldrichSearch for more papers by this authorCecilia Berg, Cecilia BergSearch for more papers by this authorManuel Ortiz-Santaliestra, Manuel Ortiz-SantaliestraSearch for more papers by this authorScott Weir, Scott WeirSearch for more papers by this authorFranz Streissl, Franz StreisslSearch for more papers by this authorRobert H Smith, Robert H SmithSearch for more papers by this author First published: 23 February 2018 https://doi.org/10.2903/j.efsa.2018.5125Citations: 14 Correspondence: pesticides.ppr@efsa.europa.eu Requestor: EFSA Question number: EFSA-Q-2011-00985 Panel members: Paulien Adriaanse, Philippe Berny, Theodorus Brock, Sabine Duquesne, Sandro Grilli, Antonio F Hernandez-Jerez, Susanne Hougaard, Michael Klein, Thomas Kuhl, Ryszard Laskowski, Kyriaki Machera, Colin Ockleford, Olavi Pelkonen, Silvia Pieper, Robert Smith, Michael Stemmer, Ingvar Sundh, Ivana Teodorovic, Aaldrik Tiktak, Chris J Topping and Gerrit Wolterink. Acknowledgements: The Panel wishes to thank the members of the Working Group on amphibian and reptile risk assessment: Paulien Adriaanse, Annette Aldrich, Cecilia Berg, Philippe Berny, Kyriaki Machera, Manuel Santaliestra Ortiz, Silvia Pieper, Robert H Smith, Chris J. Topping, Scott Weir, and the hearing experts: Carsten Brühl, Peter Dohmen, US-EPA colleagues: Brian Anderson, Catherine Aubee, Amy Blankenship, Kristina Garber, Edward Odenkirchen, Melissa Panger, Thomas Steeger, our short-term study visitor Lara Petschick and EFSA staff member: Franz Streissl for the support provided to this scientific output. Adopted: 22 November 2017 Reproduction of the images listed below is prohibited and permission must be sought directly from the copyright holder: Figure 1: © Stockphoto; Figure 5: © WHO This publication is linked to the following EFSA Supporting Publications article: http://onlinelibrary.wiley.com/doi/10.2903/sp.efsa.2018.EN-1357/full AboutSectionsPDF ToolsExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Abstract Following a request from EFSA, the Panel on Plant Protection Products and their Residues developed an opinion on the science to support the potential development of a risk assessment scheme of plant protection products for amphibians and reptiles. The coverage of the risk to amphibians and reptiles by current risk assessments for other vertebrate groups was investigated. Available test methods and exposure models were reviewed with regard to their applicability to amphibians and reptiles. Proposals were made for specific protection goals aiming to protect important ecosystem services and taking into consideration the regulatory framework and existing protection goals for other vertebrates. Uncertainties, knowledge gaps and research needs were highlighted. Summary Introduction The PPR Panel was tasked to provide a scientific opinion on the state of the science on pesticide risk assessment for amphibians and reptiles. Concerns had been raised that the current risk assessment of pesticides may not sufficiently cover the risk to amphibians and reptiles. The opinion should provide the scientific basis for potentially developing a guidance document for pesticide risk assessment for amphibians and reptiles. Some amphibians and reptiles do occur in agricultural landscapes, some species resident and some migrating through. Amphibians often breed in water bodies in or adjacent to agricultural fields. Laboratory, field and survey studies have linked pesticides with harm to amphibians. Especially, studies on terrestrial stages of amphibian have shown that currently approved substances and authorised pesticides can cause mortality in frogs and toads at rates corresponding to authorised field rates. Even when including possible interception by crop plants, deposited residues are expected to lead to high risks for amphibians. There are few studies on reptiles, but those that exist suggest that pesticides can cause harm and that further investigation is needed. Field studies also exist where no unacceptable effects from the authorised use of pesticides were observed. However, the absence of evidence is not necessarily considered as evidence of absence of effects. In addition to ecotoxicological concerns, amphibians are the most endangered group of vertebrates with faster decline rates than mammals and birds. Many of the European reptile species are threatened, with 42% of the reptile species exhibiting a declining population trend. The majority of species in both groups are protected species under European regulation. The Panel concludes that exposure of amphibians and reptiles to pesticides does occur, and that this exposure may lead to decline of populations and harm individuals, which would be of high concern. Therefore, a specific environmental risk assessment (ERA) scheme is needed for these groups. Ecology/biology of amphibians and reptiles Amphibians and reptiles are two phylogenetically distinct groups that show unique anatomical and physiological features compared with fish, birds and mammals. One common physiological feature of amphibians and reptiles is poikilothermy which differentiates them from birds or mammals. Sensitivity and exposure to pesticides, affected by poikilothermy through its influence on physiology, growth, development, behaviour or reproduction may be shared, but other factors, e.g. skins with increased permeability in amphibians, may also have a large influence on risks associated with pesticides. Potential for overspray, dermal exposure by contact with pesticidal active substances on soils or plants, and oral uptake of pesticides through ingestion of contaminated materials exists for both groups. Exposure of amphibians and reptiles when inhabiting a treated area can be prolonged, especially in the case of territorial reptile species or of amphibian aquatic stages. The amphibian life cycle has a major influence on exposure, which is difficult to predict from data generated from other taxa. Amphibians possess some structures typical of higher vertebrates that do not occur in fish (e.g. the Müllerian ducts as precursors of sexual organs). Impacts of pesticides on these structures cannot be identified through assessment based on fish toxicity endpoints and require specific assessment at specific, sensitive time windows in the amphibian's aquatic development. Based on ecological, biological and population distribution traits, a list of potential focal species that are also suitable to develop population models to support specific protection goals (SPGs) is suggested. Selection based on traits leading to potential high exposure and sensitivity to pesticides is proposed. Risk assessment should include adequate numbers of species representing diverse taxa that exhibit a considerable range of important life histories and ecologies. Preliminary proposed species are the great crested newt (Triturus cristatus), the natterjack toad (Epidalea calamita), the common tree frog (Hyla arborea), the Hermann's tortoise (Testudo hermanni), the sand lizard (Lacerta agilis) and the smooth snake (Coronella austriaca). Spatial aspects Pesticide exposure depends on behaviour of individuals. Realistic risk assessments should take spatial behaviour within a season into account, which is particularly important for migrating amphibians. Population structure and spatio-temporal dynamics can have other important implications for pesticide impacts on amphibian and reptile populations. There is considerable evidence that many amphibians exist in unstable spatially substructured populations of various types (e.g. mainland–island), which may be sensitive to pesticide disturbance. Spatial dynamics necessary to support spatially structured population in the long term is dependent on landscape structure. Therefore, for inclusion of both the spatial and temporal implications of pesticide usage, and to take the ecological state of the population into account, a systems approach to ERA is recommended. Population dynamics and population modelling Population dynamics informs the risk assessment primarily through a description of changes in animals' distribution and abundance in space and time. This is justified from basic principles. For the modelling of these dynamics to be useful for the risk assessment, trading off generality for the realism of the systems approach will have to be addressed. The system approach integrates environment, ecology and pesticide use and fate, providing baseline population states against which the impact of the use of the pesticide is assessed. Multiple and varied baseline scenarios may be needed to ensure that the realistic worst-case baseline situation is represented. An illustrative model of great crested newt is presented, demonstrating potential uses in amphibian ERA. Models such as this can help to translate toxicity data to population modelling endpoints at landscape-scales. However, landscape structure, farming assumptions and weather conditions can be important factors influencing overall population-level effects and must be considered carefully in regulatory scenarios. Endpoints from population modelling that can be used in the risk assessment and in support of SPG definitions are population impact on abundance and occurrence, as well as changes in total population size with time expressed as relative population growth rates. These endpoints facilitate the assessment of impacts, possible recovery and long-term population viability. To assess risk, landscape-scale spatially explicit mechanistic models for the six focal species need to be developed and tested. This will provide support for the general risk assessment framework suggested below. If possible, to address the complications of poikilothermy and mobility, a toxicodynamics/toxicokinetic (TK/TD) modelling component might be directly integrated into the behavioural simulation. Simulation results should be included in lower tiers as look-up tables of presimulated regulatory scenario results. These models can then also be used for higher tier risk assessment and to support the setting of tolerable magnitude of effect for the protection goals. Specific protection goals SPG options were developed based on the legislative requirements in place for non-target vertebrates. The need to encompass the endangered status of a great proportion of amphibian and reptile species and the importance of amphibians and reptiles as drivers of valuable ecosystem services in agricultural landscapes was also taken into account. Ecosystem services considered were the provision of genetic resources and biodiversity, maintenance of cultural services, provision of food and pharmaceutical resources, support of nutrient cycling and soil structure formation, regulation of pest and disease outbreak, invasion resistance and the support of food webs. It is proposed that SPG options be agreed on the individual level for the survival of adult amphibians and reptiles; risks to the long-term persistence of populations should be considered for all other impacts. Attributes of population persistence relate to the assessment of abundance/biomass of amphibian and reptile species, but also to the landscape occupancy of these species, and to changes in population growth rates. The limits of operation for amphibians and reptiles in agricultural landscapes were considered to be negligible effects on mortality and small effects of up to months on population impacts for both groups. Toxicological endpoints and effect assessment A range of toxicological responses related to population fitness in amphibians and reptiles have been shown in laboratory experiments to be potentially useful as test endpoints (e.g. impaired embryo/larval survival, developmental rate, time to metamorphosis, gonadal differentiation, spermatogenesis, oogenesis, fertility rate and behaviour). Possible endpoints for reproductive and endocrine toxicity testing in amphibians and reptiles include changes in sex ratio and ovotestis frequency, reproductive organ development and fertility, use of biomarkers for estrogenic compounds and secondary sex characteristics such as sexually dimorphic characteristics or sexual behaviour. For amphibians there are standardised tests available, of which the following are more often performed: (a) the Larval Amphibian Growth and Developmental Assay (LAGDA), (b) the Amphibian Metamorphosis Assay (AMA) and (c) the Frog Embryo Teratogenesis Assay – Xenopus (FETAX). Of these, LAGDA is the most extensive test with an experimental design that allows detection of disrupted metamorphosis as well as sexual development in the model species Xenopus laevis. None of the above tests, however, cover the reproductive ability of amphibians. A full life cycle test with amphibians (e.g. with Xenopus tropicalis which has a shorter generation time than X. laevis) could be very useful in a risk assessment context because it enables the identification of impaired reproductive function following exposure during a sensitive window of development. All standardised tests with amphibians are conducted in the aquatic environment, and no such tests exist for testing terrestrial stages. For reptiles, there are no existing standard test guidelines; there is also little toxicity data for this group of vertebrates. This makes it very difficult to compare the toxicological sensitivity among different reptile species. Efforts should be made to investigate the toxicity of active substances and plant protection on reptiles in order to close these knowledge gaps in future. Differences in sensitivity among life stages, especially within amphibians, should be considered when determining the toxicity of pesticides, since the morphological and physiological differences among them are considerable. Regarding terrestrial amphibian life stages, no agreed guideline exist. However, tests to detect toxicity of pesticides via dermal exposure routes have been carried out, consisting of housing animals in a terrarium and applying the chemical at a realistic rate with a device simulating a professional pesticide application. The Panel stresses the importance of research efforts in the identification of in vitro test endpoints, in order to minimise animal testing. However, dermal exposure routes are particularly crucial for terrestrial stages of amphibian, since the skin has vital functions in gas and water exchange. These actively steered processes might be difficult to be mimicked in vitro. Exposure routes As a general approach, Exposure Assessment Goals and associated Ecotoxicologically Relevant Exposure Quantities (EREQs) in exposure relevant environmental matrices provide the basis for calculating Predicted Exposure Quantities (PEQs) in the field. EREQs enable a coherent linking between exposure in ecotoxicological experiments and exposure in the field. A final decision on EREQs is possible after agreement on the ecotoxicological effect assessment for amphibians and reptiles (e.g. in test protocols). The main routes of exposure for amphibians in the aquatic system are via contact to pond water and sediment and to a lesser extent via oral uptake. Main entry routes for pesticides into ponds in agricultural areas are spray-drift deposition, runoff or drainage. Sediment may accumulate pesticide residues and in such cases exposure of tadpoles by uptake of sediment may be an important route. The analysis of the dimensions of the Spanish and Swiss amphibian ponds and the CountrySide Survey ponds in the UK and their comparison to the FOrum for Co-ordination of pesticide fate models and their USe (FOCUS) surface water bodies demonstrates that the most vulnerable 10% of the surveyed ponds are significantly smaller than the FOCUS ponds (Appendix C). This means that we expect peak concentrations in FOCUS ponds not to be conservative estimates for the exposure concentrations in the ponds in the surveys. It is more complicated to compare the peak concentrations in FOCUS ditches and streams with the ponds in the surveys; therefore, the Panel was unable to make a general statement on whether or not peak concentrations in FOCUS ditches and streams are conservative for the ponds in the surveys. In view of the higher flow-through rates in the FOCUS ditches and streams, however, the pesticide concentrations are expected to decline more rapidly in the FOCUS ditches and streams than in the ponds of the surveys and thus they probably underestimate chronic exposure in the surveyed ponds. The Panel therefore expects that the FOCUS ditches and streams are not conservative for the chronic risk assessment of exposure in ponds used by amphibians in the European Union (EU). The FOCUS scenarios for use in amphibian ERA therefore need to be modified and this may entail the gathering of data via surveys of amphibian use of water bodies along with chemical monitoring. It is important to note that small surface waters are not routinely monitored and thus chemical monitoring should be extended. In their terrestrial environment, dermal exposure via direct overspray and contact to residues on soil and plant surfaces are important exposure routes as well as oral uptake of contaminated food. The main exposure routes for reptiles are food intake, contact to residues on soil and plants and contact of eggs to contaminated soil. As reptiles have a high site fidelity, dermal uptake may be more important for reptiles residing in treated fields than amphibians migrating though treated fields although their skin is less permeable than the skin of amphibians. Coverage of amphibians and reptiles by existing RA It is important to distinguish between the predictability, i.e. the coverage of existing test results with other non-target organisms as a surrogate for toxicological sensitivity of amphibians and reptiles and the protectivity of existing risk assessment procedures as a surrogate for the protection of amphibians and reptiles towards risks from plant protection product (PPP) intended uses. The potential of relying on other vertebrates as surrogates for amphibians and reptiles to cover toxicity of pesticides is compromised by some particular biological processes typical of these animals, including metamorphosis in amphibians or hormone dependent sex determination. Thus, impacts of pesticides need to be assessed for specific, sensitive time windows within the animals' development. Exposure through water: Several studies indicate that the acute endpoints for aquatic life stages of amphibians (eggs, embryos, tadpoles and adults) are lower than the acute endpoints for fish in about 30% of the cases. Therefore, if a higher percentage of all cases should be covered, an extrapolation factor needs to be applied on the acute fish endpoint if it has to be used in the risk assessment of amphibians. Uncertainty with regard to representativeness of X. laevis for European amphibian species and species sensitivity distribution needs to be addressed further to suggest extrapolation factors. No conclusion can be drawn for the coverage of the chronic sensitivity of amphibians by fish because of limitations in comparability of chronic studies and endpoints observed in those studies. Furthermore, the chronic fish studies do not address relevant sublethal endpoints effects on metamorphosis, reproduction or immunosuppression in amphibians. The amount of data relative to reptiles in the aquatic system is too limited to run any comparison in toxicity. Oral and dermal exposure in terrestrial environment: The oral exposure estimates from the screening steps in the risk assessment for birds and mammals may cover the oral exposure estimate for amphibians and reptiles. In order to estimate oral exposure, allometric equations as in the bird and mammal risk assessment could be applied with amphibian and reptile specific parameters. One existing model is the US-EPA T-herps model, which would need to be adjusted for European species. Whether the risk to amphibians and reptiles is covered by the risk assessment of birds and mammals depends on the differences in toxicological sensitivity and assessment factors applied. The comparisons of the daily dietary exposure and dermal exposure from overspray (assuming 100% uptake) give an indication that both exposure pathways are of high importance for amphibians and reptiles and hence both should be addressed in the risk assessment. The risk from dermal exposure is not assessed for birds and mammals and dermal exposure might lead to different effects than oral exposure. Therefore, protection of amphibians and reptiles by the risk assessment for birds and mammals is highly uncertain. The exposure model for workers or alternatively the dermal exposure models for birds from US-EPA TIM could be used to estimate the systemic exposure via dermal uptake in terrestrial stages of amphibians and reptiles from contact to residues on plants or soil after adjusting with amphibian and reptile specific factors such as the dermal absorption fraction (DAF), the surface area of the animal and foliar contact rate. For the time being, 100% dermal absorption of substances is suggested. It may be possible to refine this value once data on dermal absorption become available for different active substances. Data need to be generated on the body surface area in contact with the soil and in contact with plant surfaces when they move, the speed of movement and time when they are actively moving vs resting. It is recommended that experiments are performed to analyse the quantities taken up by the animals by the various routes of dermal contact to understand how these quantities add to the systemic exposure of the animals. Moreover, the effects of pesticides on the skin of amphibians as an organ actively regulating water and gas exchange should be investigated. General risk assessment framework The general risk assessment framework suggested is based on a tiered approach but is adapted to take account of parallel lines of assessment for local and landscape scale assessment which takes into account long-term population risks. In general, data are needed on the chronic toxicity of pesticides for amphibians, starting from the exposure in the aquatic stages up to and including reproductive stages. The determination of effects of pesticides on terrestrial stages via the dermal route of exposure is a central requirement for amphibians. Effects determinations in juvenile frogs are needed until development of surrogate in vitro tests is sufficiently advanced. For reptiles, toxicity data for both acute and chronic endpoints are lacking and there is insufficient data to support mammals or birds as surrogates for toxicity testing. Consequently, research is needed to allow any emerging relationships to existing tests (e.g. bird testing) to be sufficiently supported. All addressed endpoints should be determined in simple experiments allocated at the lower assessment tier. Inclusion of further animal testing at higher tiers (e.g. field effect studies) is not recommended as a standard risk refinement option. Higher assessment tiers should focus on refinement of exposure options and on the characterisation of generic ecological parameters. The risk assessment scheme comprises an evaluation of effects at the local scale and long-term effects at the landscape scale. At local scale, a risk assessment for all relevant environmental compartments in which different life stages occur would be performed. After an assessment of acute and chronic effects at local scale, the risks of intended pesticide uses have to be assessed at the landscape scale. At landscape scale, all life stages and compartments should be combined in a single risk assessment. The landscape scale also covers single population long-term risk assessment over years of pesticide use. This should be performed in a first step using prerun computer models that address the long-term repercussions of the effects of year-on-year use of pesticides on amphibian and reptile populations. Within each compartment, the impact of pesticides on amphibians and reptiles resulting from a combination of the main exposure routes should be performed. It is suggested that the outcome of exposure to pesticides by several routes is addressed in order to combine the risks of the main routes. As a pragmatic worst-case approach for the first-tier risk assessment, combination of the relevant terrestrial exposure routes following the approach used for mixture toxicity is suggested. Unlike other non-target groups, recovery may not be considered as an option for amphibians and reptiles since no long-term impact on populations is likely to be allowed. However, short-term recovery, e.g. by local density-dependent compensation during larval stages may still need to be considered as part of an integrated population assessment. It is suggested that management options to mitigate risks from pesticide use on amphibians and reptiles identified at lower tiers are considered and exhausted before higher tier assessment is performed, especially when higher tier approaches should include animal testing. Mitigation options would need to be locally specified to be successful. Two main areas where uncertainty needs to be generally addressed in the risk assessment of amphibians and reptiles are the calibration of a risk assessment scheme and the treatment of additional uncertainties in the assessment (e.g. use of surrogates). The aim of developing the local and landscape long-term assessments and supporting these with further data collection and ideally short-term use of toxicity testing is to reduce these uncertainties as quickly as possible. 1 Introdu