Towards a more realistic chemical risk assessment for fish: development and use of population models
Lara Ibrahim, PhD project, Fraunhofer IME, Schmallenberg, Germany c/o RWTH, Aachen, Germany
Fish are considered under all the European Union (EU) directives and regulations that are related to the environmental risks of chemicals. The assessment of potential effects of chemicals on fish is usually based on highly standardized bio-tests on the level of the organism (e.g. effects on survival, growth, reproduction), using a limited set of standard test species under controlled conditions. However, the environmental protection goals are related to mortality on the level of individuals (visible mortality) as well adverse effects on the level of populations (in the case of sub-lethal effects) in the field.
Thus, extrapolations from laboratory test results to the situation in the field are needed for the risk assessment for fish and ecological modelling can contribute to this need in various aspects including extrapolations from one species to another, from the individual to the population level and between environmental conditions while considering the spatio-temporal variability of exposure and other environmental factors and stressors. The Fish-2 project aims to contribute to the aspect of extrapolations from sub-lethal effects measured on test individuals to the population level of ecologically relevant species.
Population studies with fish are not practical in the regulatory process because of the relatively long generation-time, high costs, and ethical issues, and thus, the most detailed and relevant information stem from life-cycle tests. However, standard test species for chronic tests are chosen based on the practicality of handling in the laboratory and thus are generally small in size, have a short life-span and reproduce frequently e.g. Rainbow trout. Species in the field can be long-lived and vary greatly in survival rates and reproductive output.
Current practice in Environmental Risk Assessment (ERA) extrapolates test results to the field situation using safety factors, and this approach is designed to be conservative although the associated uncertainties cannot be quantified and thus over- or under-protection may result. Ecological modelling of field populations, in addition to standard toxicity tests, can help achieve a more ecologically relevant ERA since it can take into account ecological aspects that are not usually handled in laboratories. At this point, the choice of the species of fish which is to be modelled is a critical point which needs investigation.
For extrapolating sub-lethal effects on fish to the population level in an ecologically relevant way, the envisioned way forward is to identify vulnerable species which are representative of the ones exposed in the field and to build population models for focal species selected from them. Pesticide effects which are measured on the level of test individuals in standard bio-tests are expected to be used as input to these population models after performing interspecies extrapolations. Interspecies extrapolation can be achieved in various ways including predicting toxicity to fish based on in vitro data and toxico-kinetic / toxico-dynamic models (Fish-1 project). Population models which are built around the important life history and ecological aspects of the identified focal species would then extrapolate individual-level effects to the population level allowing the assessment and estimation of realistic worst-case effects on fish populations in the field.
A specific framework for the needed identification of representative vulnerable species and focal species has not yet been established and there are a multitude of possible approaches. This project primarily aims to contribute to this issue by making use of the rich and readily available data on geographical distribution, habitat preference and life cycle of freshwater fish in Europe in peer-reviewed publications and grey literature. Within a practical time-frame, this project scientifically investigates and suggests candidates for detailed modelling in service of an ecologically more relevant assessment of the effects of pesticides on fish, and lays ground for an individual based model (IBM) for the focal species which was concluded as representative in case of sub-lethal effects of pesticides on fertility.
Thus, the project addresses the following objectives, via a tiered filtering and modelling approach, while focusing on pesticides in the EU:
- To comprehensively identify and list potentially exposed freshwater fish living in edge-of-field water bodies in agricultural landscapes in the EU
- To assess how their different life histories reflect on their responses to toxicants on the population level (using population multiplication rates as endpoints)
- To identify the species which can be representative of field conditions (representative vulnerable species) considering different possible adverse effects of pesticides. We considered possible lethal effects on juveniles or adults or sub-lethal effects on fertility.
- To develop an IBM for a chosen focal species from the representative vulnerable species regarding cases of sub-lethal effects on fertility since sub-lethal effects are currently of primary interest for population level ERA of pesticides for fish. This IBM would provide the means for extrapolating sub-lethal effect data derived from standard toxicity tests to the population level of this species for a more ecologically relevant risk assessment.
Materials, Methods and Results
The concept of population vulnerability was adopted for the identification of vulnerable representative species whereby vulnerability is determined by the species’ susceptibility to exposure to the pollutant, their potential to sustain their populations if adversely affected (population resilience) and their sensitivity to the toxicant (Ibrahim et al. 2013, 2014).
- Susceptibility to exposure
Freshwater fish species were comprehensively listed, that are native to Europe, widespread in the European Union, and which inhabit streams, ditches or ponds in agricultural landscapes (Ibrahim et al. 2013). Starting with 579 fish species occurring in European freshwater, 27 species met the filtering criteria and were thus considered at an elevated risk of being exposed to pesticides. The resulting list was verified based on monitoring studies that had been conducted in agricultural landscapes over the past 20 years.
- Population resilience
It was possible to build simple population models around the life cycles of 21 of the 27 fish species listed in step (1) in order to compare the life histories of the different species and their associated population resilience (Ibrahim et al. 2014). Such a comparison needed a uniform study environment which is of an adequate level of complexity and yet not highly data demanding and therefore we used time-invariant Leslie matrix models which uniformly assumed birth-pulse populations and pre-breeding censuses. We compared the population resilience and hence the potential of species to sustain their populations in cases of exposure to pesticides of different modes of action, namely pesticides causing hypothetical reductions in fertility, juvenile survival or adult survival. Life history characteristics of the species which had the least resilient populations to each of the considered modes of action were identified and three candidate species were suggested as focal species for modelling.
- Intrinsic sensitivity
Interspecies variability in intrinsic sensitivity was not handled in this project for several reasons including unavailability of toxic effect data for most of the listed species, ethical limits on toxicity testing on vertebrates, and the fact that intrinsic sensitivity is toxicant-specific making the conclusion of a generally most intrinsically sensitive species to pesticides impossible. Instead, conventional and developing approaches may be used for interspecies extrapolations as needed.
- Individual based population model
Since this project aims to contribute to a more ecologically relevant extrapolation of sub-lethal effects of pesticides on fish to the population level, an individual based model is currently being developed for the Eurasian minnow, Phoxinus phoxinus. This species was found to have the least resilient populations for the considered possible sub-lethal effects of pesticides (sub-lethal effects on fertility) in step (2). The version of the IBM which is currently under development handles the minnow population dynamics by accounting for individual variability and the effect of population density on individual growth and of habitat preference and reproductive behavior on individual survival. Model design and parametrization are based on field data and demographic patterns which had been reported since 1940 and till this day, for minnow populations in general while focusing on temperate populations. Work on this step is ongoing.
Conclusions and Outlook
Within Fish-2, it was possible to identify the freshwater fish species that are susceptible to exposure to pesticides in the EU. We could apply population modelling to link the life-cycle traits of these species to their population vulnerability and to suggest focal field species which are suitable for modelling in service of population-level extrapolation in higher-tier ERA for pesticides in Europe. We did not address the interspecies variability of intrinsic sensitivities of these species to pesticides, however we suggest using the approaches which are available or under development in the field for the interspecies extrapolation of intrinsic sensitivities.
The matrix population models which we have used for the comparison of population resilience of the different species allowed the projection of effects on vital rates on population multiplication rates, but they do not allow the precise prediction of toxic effects and the future population structure and dynamics, which would be needed in ERA. Therefore, more detailed population models which can account for important mechanisms such as behavior and density dependence should be developed for the identified focal species. Depending on the final protection goals, such a population model would at least be needed for the extrapolation of sub-lethal effects to the population level i.e. a detailed model for P. phoxinus.
As a short-term aim, this project aims to lay foundations for an IBM for the minnow as a tool which can take toxicity data from bio-tests as input and extrapolate them to the population level with a certain quantified degree of certainty. A fundamental ground is to develop first an adequately simple ecological IBM for the minnow and to evaluate and validate its output against long-term population dynamics which have been observed in the field. As a result, case studies can reflect reality with a certain degree of precision since the further implementation of the measured effects from standard fish bio-tests as a sub-model in this IBM would not result in real estimations of true risks rather it would result in more certain estimations and a protective and ecologically relevant assessment for field conditions in Europe.
As long-term possibilities which can be further expanded in the minnow IBM, spatially explicit variants of the IBM can be considered whereby environmental aspects of minnow habitats such as climate and limitations of spawning grounds, as well as behavioral aspects of the minnow such as shoaling and the resulting local population densities and their effect on population dynamics, as well as different exposure scenarios to pesticides in space may be explored and incorporated if found important. Also, it can be tested if the population model may be linked to TK/TD models which allow a more mechanistic description of the effect on the organism level; relating effects on life cycle traits not directly to the time-variable test item concentration in the water, but to internal concentrations and modes of action.
Ibrahim L, Preuss TG, Ratte HT, Hommen U (2013) A list of fish species that are potentially exposed to pesticides in edge-of-field water bodies in the European Union—a first step towards identifying vulnerable representatives for risk assessment. Environmental Science and Pollution Research 20 (4): 2679-2687. DOI: 10.1007/s11356-013-1471-x
Ibrahim L, Preuss TG, Schaeffer A, Hommen U (2014) A contribution to the identification of representative vulnerable fish species for pesticide risk assessment in Europe—A comparison of population resilience using matrix models. Ecological Modelling 280: 65-75. DOI: 10.1016/j.ecolmodel.2013.08.001
PhD Fellow: Lara Ibrahim (IME)
Project Supervisor: Udo Hommen (IME)
Co-Supervisors: Roman Ashauer (Eawag) , Pernille Thorbek (Syngenta)
Supervisor of the PhD Thesis: Prof. Dr. Andreas Schaeffer (RWTH)
Associated partners: Bayer, BASF
Last updated: 02.04.2014