Leo Posthuma

Heavy-metal adaptation in terrestrial invertebrates: A review of occurrence, genetics, physiology and ecological consequences

Abstract 1. The occurrence of genetic adaptation to heavy metals in natural populations of terrestrial invertebrates is evaluated from literature data. Five criteria for adaptation evidence are applied, with concepts from ecotoxicology, ecology, life-history theory and quantitative genetics. 2. There is strong evidence for the occurrence of adaptation in natural populations of the isopod Porcellio scaber (Isopoda), the springtails Isotoma notabilis , Onychiurus armatus and Orchesella cincta (Collembola), the blowfly Lucilia cuprina and the fruit fly Drosophila melanogaster (Diptera). Adaptation to metal-containing pesticides has been demonstrated in ticks (Acarina). Population divergence indicates acclimation or adaptation in many other species. 3. Metal adaptation has been achieved within a few generations under laboratory conditions in some species; adapted populations occur at field sites that have been polluted for decades, or longer. 4. Genetic variation for tolerance and life-history characteristics, allowing for adaptation, was quantified in a reference population of Orchesella cincta . Tolerance and life-history patterns in exposed field populations matched predictions from genetic variation. 5. Adaptation involves modification and intensification of existing physiological mechanisms for metal assimilation, excretion, immobilization or compartmentalized storage. There are indications ofinter-population divergence in metal-binding proteins in a snail. In the fruit fly Drosophila melanogaster metal adaptation is achieved by duplication of the metallothionein gene. 6. An altered life-history is often part of the complex adaptation syndrome. Metal-adapted invertebrates have a shorter life-cycle and a higher reproductive effort. 7. Possible consequences of adaptation, consisting of costs of tolerance determined by genetic correlations, and probably of reduced genetic variation for tolerance and other features, are discussed. Reduced genetic variation is suggested by results for the springtail Orchesella cincta . 8. The distinction between “costs of tolerance” on the one hand and linkage disequilibrium or direct selection for altered life-history patterns on the other hand is discussed. 9. Species with high sensitivity (i.e. a low NOEC), that do not have populations maintaining sufficient genetic variation to evolve tolerance or modified life-history characteristics, or that have costly tolerance mechanisms, or both, are most at risk for extinction at sites with increasing metal pollution. 10. Metal adaptation in terrestrial invertebrates appears to be of degree rather than of kind: indications for a specific metal-fauna, equivalent to metal-vegetation, are lacking.

Complex mixture toxicity for single and multiple species: Proposed methodologies

Methods for the assessment of ecological risks associated with exposure to defined mixtures of toxicants are reviewed and formalized for single-species toxicity. Depending on the modes of action of toxicants in a mixture, these methods apply either the model for concentration additivity (CA) or the model for response additivity (RA). For complex mixtures, the present paper advocates the use of a new, two-step, mixed-model approach as a logical extension of model selection: Mixture toxicity for individual modes of action is evaluated with the CA model, and the toxicities of different modes of action are combined using the RA model. Using comparable mixture toxicity strategies in combination with the concept of species-sensitivity distributions, we develop a method to address and predict the risk for direct effects on the composition of species assemblages and biodiversity. The data needed for modeling can be obtained from existing databases, and lack of data can, in part, be addressed by the use of toxicity patterns in those databases. Both single- and multiple-species methods of mixture risk prediction are useful for risk management, because they allow ranking of polluted sites and affected species as well as identification of the most hazardous contaminants, at least in a comparative way. Validation of the proposed methods is feasible but currently limited because of a lack of appropriate data.

PREDICTIVE MODELS ATTRIBUTE EFFECTS ON FISH ASSEMBLAGES TO TOXICITY AND HABITAT ALTERATION

Biological assessments should both estimate the condition of a biological resource (magnitude of alteration) and provide environmental managers with a diagnosis of the potential causes of impairment. Although methods of quantifying condition are well developed, identifying and proportionately attributing impairment to probable causes remain problematic. Furthermore, analyses of both condition and cause have often been difficult to communicate. We developed an approach that (1) links fish, habitat, and chemistry data collected from hundreds of sites in Ohio (USA) streams, (2) assesses the biological condition at each site, (3) attributes impairment to multiple probable causes, and (4) provides the results of the analyses in simple-to-interpret pie charts. The data set was managed using a geographic information system. Biological condition was assessed using a RIVPACS (river invertebrate prediction and classification system)-like predictive model. The model provided probabilities of capture for 117 fish species based on the geographic location of sites and local habitat descriptors. Impaired biological condition was defined as the proportion of those native species predicted to occur at a site that were observed. The potential toxic effects of exposure to mixtures of contaminants were estimated using species sensitivity distributions and mixture toxicity principles. Generalized linear regression models described species abundance as a function of habitat characteristics. Statistically linking biological condition, habitat characteristics including mixture risks, and species abundance allowed us to evaluate the losses of species with environmental conditions. Results were mapped as simple effect and probable-cause pie charts (EPC pie diagrams), with pie sizes corresponding to magnitude of local impairment, and slice sizes to the relative probable contributions of different stressors. The types of models we used have been successfully applied in ecology and ecotoxicology, but they have not previously been used in concert to quantify impairment and its likely causes. Although data limitations constrained our ability to examine complex interactions between stressors and species, the direct relationships we detected likely represent conservative estimates of stressor contributions to local impairment. Future refinements of the general approach and specific methods described here should yield even more promising results.

Predicted effects of toxicant mixtures are confirmed by changes in fish species assemblages in Ohio, USA, rivers

The purposes of this study were to investigate whether exposure to toxicant mixtures is associated with fish assemblage characteristics in the field and to describe the relationships between predicted chronic and acute mixture risks and observed impacts. Fish abundance and abiotic monitoring data from Ohio, USA, surface waters were compiled and analyzed. Variability of biotic and abiotic parameters was large. Exposure assessment, risk assessment with species-sensitivity distributions, and mixture toxicity rules were used to calculate a relative risk predictor: The multisubstance potentially affected fraction of species (msPAF). Predicted acute and chronic risks ranged from low values to more than 10 and 50% of species potentially affected, respectively. Pearson correlations between predicted risk and observed assemblage characteristics were nonsignificant for total abundance, number of species, Shannon-Weaver index, and evenness. Moderately significant correlations were found between predicted risk and abundance for 23% of individual species. Both abundance increases and decreases were observed. Generalized linear model (GLM) regressions revealed significant nonlinear associations between predicted risk and the abundance for 50% (metals and ammonia) and 55% (household product ingredients) of the species. Local ecological impact was expressed as the fraction of species expected but not observed, both with and without attribution of impact to mixture exposure. The association between predicted impacted fraction and the fraction of species expected but not observed was not significant. Predicted acute and chronic impacted fractions were associated significantly with the observed fraction of species likely lost by the action of toxicant mixtures under field conditions, with wide confidence bounds. These findings confirm the view that higher mixture impacts are expected in the field at higher msPAF.

Genetic variation and covariation for characteristics associated with cadmium tolerance in natural populations of the springtail Orchesella cincta (L.)

Heavy metals can be strong and stable directional selective agents for metal‐exposed populations. Genetic variation for the metal‐tolerance characteristic “cadmium excretion efficiency” was studied in populations of the collembolan Orchesella cincta from a reference‐ and a metal‐contaminated forest soil. Previously it has been shown that “excretion efficiency” influences tolerance through midgut‐mediated immobilization and excretion of toxic metal ions, and that an increased mean excretion efficiency is present in animals inhabiting metal‐contaminated litter. In the present research, offspring‐parent regressions showed that additive genetic variation for cadmium excretion efficiency was present in the population from the reference site. The heritability estimate was 0.33. In the natural population exposed to heavy metals from an industrial source, additive genetic variation was not significantly different from zero. Differences in the heritability between the reference and the exposed population were not significant. Genetic variation for cadmium excretion efficiency allows for a response to selection in the reference population. Such a response has probably occurred in the metal‐exposed population. Half‐sib analysis with animals from the reference population was used to estimate genetic variation and maternal effects for excretion efficiency, relative growth rate and molting frequency, and to determine genetic correlations between these characteristics. Additive genetic variation was demonstrated for all three characteristics, heritability estimates were 0.48, 0.75 and 0.46, respectively. Maternal effects were low for excretion efficiency and molting frequency, but may be present for relative growth rate. Phenotypic and genetic correlations among these characteristics were positive. The environmental correlation between relative growth rate and molting frequency was positive, others were negative. Direct selection for any of the characteristics, or genetic correlations between tolerance characteristics and growth characteristics, or both may have caused the responses previously observed in field populations.

The SOLUTIONS project: Challenges and responses for present and future emerging pollutants in land and water resources management

SOLUTIONS (2013 to 2018) is a European Union Seventh Framework Programme Project (EU-FP7). The project aims to deliver a conceptual framework to support the evidence-based development of environmental policies with regard to water quality. SOLUTIONS will develop the tools for the identification, prioritisation and assessment of those water contaminants that may pose a risk to ecosystems and human health. To this end, a new generation of chemical and effect-based monitoring tools is developed and integrated with a full set of exposure, effect and risk assessment models. SOLUTIONS attempts to address legacy, present and future contamination by integrating monitoring and modelling based approaches with scenarios on future developments in society, economy and technology and thus in contamination. The project follows a solutions-oriented approach by addressing major problems of water and chemicals management and by assessing abatement options. SOLUTIONS takes advantage of the access to the infrastructure necessary to investigate the large basins of the Danube and Rhine as well as relevant Mediterranean basins as case studies, and puts major efforts on stakeholder dialogue and support. Particularly, the EU Water Framework Directive (WFD) Common Implementation Strategy (CIS) working groups, International River Commissions, and water works associations are directly supported with consistent guidance for the early detection, identification, prioritisation, and abatement of chemicals in the water cycle. SOLUTIONS will give a specific emphasis on concepts and tools for the impact and risk assessment of complex mixtures of emerging pollutants, their metabolites and transformation products. Analytical and effect-based screening tools will be applied together with ecological assessment tools for the identification of toxicants and their impacts. The SOLUTIONS approach is expected to provide transparent and evidence-based candidates or River Basin Specific Pollutants in the case study basins and to assist future review of priority pollutants under the WFD as well as potential abatement options.

Determination of Field Effects of Contaminants—Significance of Pollution-Induced Community Tolerance

The concept of pollution-induced community tolerance (PICT) consists of the phenomenon that communities in an ecosystem exhibit increased tolerance as a result of exposure to contaminants. Although a range of ‘classic’ ecological principles explains the processes that increase tolerance of a community, the value of PICT for ecological risk assessment was recognized only recently (Blanck et al. 1988). The following issues are recognized: First, regarding the question on the role of suspect compounds causing ecological effects, the PICT approach covers the issue of causality better than ‘classical’ ecological community response parameters like species densities or species diversity indices. This relates to the fact that the level of PICT is assumed to be relatively constant (compared to density and diversity), whereas the suspect compound causing the observed effect can be deduced with relative clear inference from artificial exposure experiments. Second, PICT directly addresses a level of biological organization (the community), the level of concern for many ecological risk assessment methods. Other methods for risk assessment, like toxicity testing or bioassays, focus on individual or population-level effects, and need extrapolation of the results to the field. Such extrapolation step may pose problems regarding validity of the outcome of risk assessment. The occurrence of PICT is, however, not (yet) a community endpoint that is sufficiently underpinned to trigger risk mitigation activities. This paper especially focuses on the possibility to improve risk assessment approaches by incorporation of PICT assessments, especially focusing on the issue of causality and on the ecological meaning of PICT. Despite the advantages over ‘classical’ parameters, literature analysis suggests that the PICT approach may be strengthened by determining to which degree the PICT approach relates to ecological changes, like shifts in community structure, functioning, and stability. The aim of this paper is to summarize some literature, putting the emphasis on terrestrial studies, to get insights whether PICT is a sensitive and powerful tool to quantify ecological effects in field conditions, to link them to toxicant stress, and thus to determine whether PICT may be taken into consideration in risk assessment.

Metal uptake from soils and soil-sediment mixtures by larvae of Tenebrio molitor (L.) (Coleoptera).

Bioassays were performed to evaluate the impact of soil characteristics on Cd, Cu, Pb, and Zn uptake by larvae of Tenebrio molitor. Metal accumulation was determined in 13 natural field soils, one metal-spiked field soil, four soil-sediment mixtures, and Cd- or Zn-spiked OECD artificial soil. Statistical analyses were used to investigate covariation of accumulation patterns with various soil metal pools and soil properties. Body concentrations of Cu and Zn in Zn-spiked OECD soils, field soils, and soil-sediment mixtures mostly remained constant. Considerable variation was noted for all Cd and Pb steady-state body concentrations among field soils and soil-sediment mixtures. For the spiked field soil and in the Cd-spiked OECD soil, body concentrations increased almost linearly with time. For the nonessential metals Cd and Pb, larval body concentrations correlated mainly to the total metal pool of the soil. Cd uptake at similar total Cd concentrations was within the same range among spiked OECD soils, field soils, and mixtures. A comparison of the findings with studies on other soil-inhabiting species shows that metal uptake patterns depend on metal type, soil type, and exposed species. It is suggested that soil organisms can be categorized according to gross divergence in ecophysiological characteristics, determined by, for instance, (non)permeability of the outer integument. These characteristics appear as similarities among multivariate functions as derived for the beetle.

Uncertainty in msPAF‐based ecotoxicological effect factors for freshwater ecosystems in life cycle impact assessment

Abstract Ecotoxicological effect factors are part of the analysis of relative impacts by chemical contaminants on ecosystems. Uncertainty distributions, represented by the 90% confidence interval, belonging to ecotoxicological effect factors for freshwater ecosystems were determined. This study includes 869 high production volume chemicals, related to 7 nonspecific toxic modes of action (TMoAs). The ecotoxicological effect factors are divided into a TMoA-specific part and a chemical-specific part. The 90% confidence interval of the TMoA-specific part of the effect factor ranges from 23 orders of magnitude for acrylate toxicity to 2 orders of magnitude for nonpolar narcosis. The range in the TMoA-specific part of the effect factor is mainly caused by uncertainty in the spread in toxic sensitivity between species (σj). Average uncertainty in the chemical-specific part of the effect factors depends on the number of species tested and ranges on average from a factor of 5 for more than 3 species tested to a factor of about 1,000 for 2 species tested. Average uncertainty in the ecotoxicological effect factors ranges from a factor of 100 for more than 3 species tested to a factor of nearly 10,000 for 2 species tested. It is recommended that the ecotoxicological effect factor of a chemical is based on toxicity data of at least 4 species.

Predicted mixture toxic pressure relates to observed fraction of benthic macrofauna species impacted by contaminant mixtures

Species sensitivity distributions (SSDs) quantify fractions of species potentially affected in contaminated environmental compartments using test species sensitivity data. The present study quantitatively describes associations between predicted and observed ecological impacts of contaminant mixtures, based on monitoring data of benthic macroinvertebrates. Local mixture toxic pressures (multisubstance potentially affected fraction of species [msPAF]) were quantified based on measured concentrations of 45 compounds (eight metals, 16 chlorinated organics, mineral oil, 16 polycyclic aromatic hydrocarbons, four polychlorinated biphenyls), using acute as well as chronic 50%-effective concentration-based SSD-modeling combined with bioavailability and mixture modeling. Acute and chronic toxic pressures were closely related. Generalized linear models (GLMs) were derived to describe taxon abundances as functions of environmental variables (including acute toxic pressure). Acute toxic pressure ranged from 0 to 42% and was related to abundance for 74% of the taxa. Habitat-abundance curves were generated using the GLMs and Monte Carlo simulation. Predicted abundances for the taxa were associated with acute mixture toxic pressure in various ways: negative, positive, and optimum abundance changes occurred. Acute toxic pressure (msPAF) was associated almost 1:1 with the observed fraction of taxa exhibiting an abundance reduction of 50% or more. The findings imply that an increase of mixture toxic pressure associates to increased ecological impacts in the field. This finding is important, given the societal relevance of SSD model outputs in environmental policies.