Matthias Liess

Analyzing effects of pesticides on invertebrate communities in streams

The aim of this investigation was to find patterns in aquatic invertebrate community composition that are related to the effects of pesticides. Investigations were carried out in 20 central European streams. To reduce the site-specific variation of community descriptors due to environmental factors other than pesticides, species were classified and grouped according to their vulnerability to pesticides. They were classified as species at risk (SPEAR) and species not at risk (SPEnotAR). Ecological traits used to define these groups were sensitivity to toxicants, generation time, migration ability, and presence of aquatic stages during time of maximum pesticide application. Results showed that measured pesticide concentrations of 1:10 of the acute 48-h median lethal concentration (LC50) of Daphnia magna led to a short- and long-term reduction of abundance and number of SPEAR and a corresponding increase in SPEnotAR. Concentrations of 1:100 of the acute 48-h LC50 of D. magna correlated with a long-term change of community composition. However, number and abundance of SPEAR in disturbed stream sections are increased greatly when undisturbed stream sections are present in upstream reaches. This positive influence compensated for the negative effect of high concentrations of pesticides through recolonization. The results emphasize the importance of considering ecological traits and recolonization processes on the landscape level for ecotoxicological risk assessment.

Effects of neonicotinoids and fipronil on non-target invertebrates

We assessed the state of knowledge regarding the effects of large-scale pollution with neonicotinoid insecticides and fipronil on non-target invertebrate species of terrestrial, freshwater and marine environments. A large section of the assessment is dedicated to the state of knowledge on sublethal effects on honeybees (Apis mellifera) because this important pollinator is the most studied non-target invertebrate species. Lepidoptera (butterflies and moths), Lumbricidae (earthworms), Apoidae sensu lato (bumblebees, solitary bees) and the section “other invertebrates” review available studies on the other terrestrial species. The sections on freshwater and marine species are rather short as little is known so far about the impact of neonicotinoid insecticides and fipronil on the diverse invertebrate fauna of these widely exposed habitats. For terrestrial and aquatic invertebrate species, the known effects of neonicotinoid pesticides and fipronil are described ranging from organismal toxicology and behavioural effects to population-level effects. For earthworms, freshwater and marine species, the relation of findings to regulatory risk assessment is described. Neonicotinoid insecticides exhibit very high toxicity to a wide range of invertebrates, particularly insects, and field-realistic exposure is likely to result in both lethal and a broad range of important sublethal impacts. There is a major knowledge gap regarding impacts on the grand majority of invertebrates, many of which perform essential roles enabling healthy ecosystem functioning. The data on the few non-target species on which field tests have been performed are limited by major flaws in the outdated test protocols. Despite large knowledge gaps and uncertainties, enough knowledge exists to conclude that existing levels of pollution with neonicotinoids and fipronil resulting from presently authorized uses frequently exceed the lowest observed adverse effect concentrations and are thus likely to have large-scale and wide ranging negative biological and ecological impacts on a wide range of non-target invertebrates in terrestrial, aquatic, marine and benthic habitats.

Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: A review

Neonicotinoids, broad-spectrum systemic insecticides, are the fastest growing class of insecticides worldwide and are now registered for use on hundreds of field crops in over 120 different countries. The environmental profile of this class of pesticides indicate that they are persistent, have high leaching and runoff potential, and are highly toxic to a wide range of invertebrates. Therefore, neonicotinoids represent a significant risk to surface waters and the diverse aquatic and terrestrial fauna that these ecosystems support. This review synthesizes the current state of knowledge on the reported concentrations of neonicotinoids in surface waters from 29 studies in 9 countries world-wide in tandem with published data on their acute and chronic toxicity to 49 species of aquatic insects and crustaceans spanning 12 invertebrate orders. Strong evidence exists that water-borne neonicotinoid exposures are frequent, long-term and at levels (geometric means=0.13μg/L (averages) and 0.63μg/L (maxima)) which commonly exceed several existing water quality guidelines. Imidacloprid is by far the most widely studied neonicotinoid (66% of the 214 toxicity tests reviewed) with differences in sensitivity among aquatic invertebrate species ranging several orders of magnitude; other neonicotinoids display analogous modes of action and similar toxicities, although comparative data are limited. Of the species evaluated, insects belonging to the orders Ephemeroptera, Trichoptera and Diptera appear to be the most sensitive, while those of Crustacea (although not universally so) are less sensitive. In particular, the standard test species Daphnia magna appears to be very tolerant, with 24-96hour LC50 values exceeding 100,000μg/L (geometric mean>44,000μg/L), which is at least 2-3 orders of magnitude higher than the geometric mean of all other invertebrate species tested. Overall, neonicotinoids can exert adverse effects on survival, growth, emergence, mobility, and behavior of many sensitive aquatic invertebrate taxa at concentrations at or below 1μg/L under acute exposure and 0.1μg/L for chronic exposure. Using probabilistic approaches (species sensitivity distributions), we recommend here that ecological thresholds for neonicotinoid water concentrations need to be below 0.2μg/L (short-term acute) or 0.035μg/L (long-term chronic) to avoid lasting effects on aquatic invertebrate communities. The application of safety factors may still be warranted considering potential issues of slow recovery, additive or synergistic effects and multiple stressors that can occur in the field. Our analysis revealed that 81% (22/27) and 74% (14/19) of global surface water studies reporting maximum and average individual neonicotinoid concentrations respectively, exceeded these thresholds of 0.2 and 0.035μg/L. Therefore, it appears that environmentally relevant concentrations of neonicotinoids in surface waters worldwide are well within the range where both short- and long-term impacts on aquatic invertebrate species are possible over broad spatial scales.

Pesticides reduce regional biodiversity of stream invertebrates

The biodiversity crisis is one of the greatest challenges facing humanity, but our understanding of the drivers remains limited. Thus, after decades of studies and regulation efforts, it remains unknown whether to what degree and at what concentrations modern agricultural pesticides cause regional-scale species losses. We analyzed the effects of pesticides on the regional taxa richness of stream invertebrates in Europe (Germany and France) and Australia (southern Victoria). Pesticides caused statistically significant effects on both the species and family richness in both regions, with losses in taxa up to 42% of the recorded taxonomic pools. Furthermore, the effects in Europe were detected at concentrations that current legislation considers environmentally protective. Thus, the current ecological risk assessment of pesticides falls short of protecting biodiversity, and new approaches linking ecology and ecotoxicology are needed.

Relative sensitivity distribution of aquatic invertebrates to organic and metal compounds

In the field, a multitude of species can be exposed to numerous toxicants; thus, the sensitivity of individual species to particular toxicants must be known to predict effects and to analyze changes in species composition. For most species, no information about their toxicant sensitivity is available. To address this limitation, we have grouped the available information to assign sensitivities to aquatic invertebrate taxa relative to Daphnia magna. With respect to organic compounds, most taxa of the orders Anisoptera, Basommatophora, Coleoptera, Decapoda, Diptera, Ephemeroptera, Eulamellibranchiata, Heteroptera, Hirudinea, Isopoda, Oligochaeta, Prosobranchia, Trichoptera, Tricladida, and Zygoptera are less sensitive than D. magna. Some taxa of the Amphipoda, Plecoptera, and Cladocera (other than D. magna) are significantly more sensitive. For organic compounds, approximately 22% of the investigated taxa were more sensitive than D. magna. Most taxa of the orders Amphipoda, Basommatophora, Diptera, Ephemeroptera, Eulamellibranchiata, Heteroptera, Isopoda, Oligochaeta, and Tricladida are significantly less sensitive than D. magna to metal compounds. The taxa belonging to the Crustacea, with the exception of the order Isopoda, are much more sensitive. For metal compounds, approximately 30% of the investigated taxa were more sensitive than D. magna. Hence, D. magna is among the most sensitive taxa regarding both groups of toxicants. The sensitivities for several taxa are listed, and use of the relative sensitivity distribution to link toxicant effects in mesocosm studies and field investigations is discussed.

Combined and interactive effects of global climate change and toxicants on populations and communities

Increased temperature and other environmental effects of global climate change (GCC) have documented impacts on many species (e.g., polar bears, amphibians, coral reefs) as well as on ecosystem processes and species interactions (e.g., the timing of predator–prey interactions). A challenge for ecotoxicologists is to predict how joint effects of climatic stress and toxicants measured at the individual level (e.g., reduced survival and reproduction) will be manifested at the population level (e.g., population growth rate, extinction risk) and community level (e.g., species richness, food-web structure). The authors discuss how population- and community-level responses to toxicants under GCC are likely to be influenced by various ecological mechanisms. Stress due to GCC may reduce the potential for resistance to and recovery from toxicant exposure. Long-term toxicant exposure can result in acquired tolerance to this stressor at the population or community level, but an associated cost of tolerance may be the reduced potential for tolerance to subsequent climatic stress (or vice versa). Moreover, GCC can induce large-scale shifts in community composition, which may affect the vulnerability of communities to other stressors. Ecological modeling based on species traits (representing life-history traits, population vulnerability, sensitivity to toxicants, and sensitivity to climate change) can be a promising approach for predicting combined impacts of GCC and toxicants on populations and communities. Environ. Toxicol. Chem. 2013;32:49–61.

The footprint of pesticide stress in communities-Species traits reveal community effects of toxicants

The predictive power of the current risk-assessment framework for pesticides remains uncertain. This is because any extrapolation towards landscape-level effects encounters considerable uncertainties: (i) when proceeding from the level of individual single-species tests to populations and communities, biological interactions are not considered; (ii) from mesocosms to field communities, environmental factors and stressors that determine the effects of pesticides in the field are not considered; and (iii) most monitoring investigations are restricted spatially and do not consider recolonisation, and lack an adequate means of distinguishing confounding factors from natural variation. We advocate using species traits as community descriptors, to determine quantitative links between pesticide toxicity and community alterations. Recently, a trait-based indicator system was developed to identify SPEcies At Risk (SPEAR) of being affected by pesticides, with reference to life-history and physiological traits. This SPEAR system has now been successfully employed to link pesticide exposure and effects in Finland, France and Germany. The effect of pesticides on the structure of communities described with SPEAR was independent of the biogeographical region. We then extrapolated and visualised the anticipated risk for aquatic communities in small agricultural streams within Europe in a risk map. With this information we identified a potential risk from pesticide runoff in a high proportion of streams. By focusing on the ecological effect of selected environmental factors, trait-based approaches offer an increased realism for risk assessment of toxicants on the ecosystem level.

Thresholds for the Effects of Pesticides on Invertebrate Communities and Leaf Breakdown in Stream Ecosystems

We compiled data from eight field studies conducted between 1998 and 2010 in Europe, Siberia, and Australia to derive thresholds for the effects of pesticides on macroinvertebrate communities and the ecosystem function leaf breakdown. Dose-response models for the relationship of pesticide toxicity with the abundance of sensitive macroinvertebrate taxa showed significant differences to reference sites at 1/1000 to 1/10,000 of the median acute effect concentration (EC50) for Daphnia magna, depending on the model specification and whether forested upstream sections were present. Hence, the analysis revealed effects well below the threshold of 1/100 of the EC50 for D. magna incorporated in the European Union Uniform Principles (UP) for registration of single pesticides. Moreover, the abundances of sensitive macroinvertebrates in the communities were reduced by 27% to 61% at concentrations related to 1/100 of the EC50 for D. magna. The invertebrate leaf breakdown rate was positively linearly related to the abundance of pesticide-sensitive macroinvertebrate species in the communities, though only for two of the three countries examined. We argue that the low effect thresholds observed were not mainly because of an underestimation of field exposure or confounding factors. From the results gathered we derive that the UP threshold for single pesticides based on D. magna is not protective for field communities subject to multiple stressors, pesticide mixtures, and repeated exposures and that risk mitigation measures, such as forested landscape patches, can alleviate effects of pesticides.

ACUTE AND DELAYED EFFECTS OF THE NEONICOTINOID INSECTICIDE THIACLOPRID ON SEVEN FRESHWATER ARTHROPODS

Ecotoxicological risk assessment of contaminants often is based on toxicity tests with continuous-exposure profiles. However, input of many contaminants (e.g., insecticides) to surface waters typically occurs in pulses rather than continuously. Neonicotinoids are a new group of insecticides, and little is known about their toxicity to nontarget freshwater organisms and potential effects on freshwater ecosystems. The aim of the present research was to assess effects of short-term (24-h) exposure to the neonicotinoid insecticide thiacloprid, including a postexposure observation period. A comparison of several freshwater insect and crustacean species showed an increase of sensitivity by three orders of magnitude in the following order: Daphnia magna < Asellus aquaticus = Gammarus pulex < Simpetrum striolatum < Culex pipiens = Notidobia ciliaris = Simulium latigonium, with median lethal concentrations (LC50s) of 4,400, 153, 190, 31.2, 6.78, 5.47, and 5.76 mug/L, respectively (postexposure observation 11-30 d). Thiacloprid caused delayed lethal and sublethal effects, which were observed after 4 to 12 d following exposure. Reduction in LC50s found when postexposure observation was extended from 1 d to a longer period (11-30 d) was up to >50-fold. Hence, delayed effects occurring after short-term exposure should be considered in risk assessment. The 5% hazardous concentration (HC5) of thiacloprid obtained in the present study (0.72 microg/L) is more than one order of magnitude below the currently predicted worst-case environmental concentrations in surface water. Concerning the selection of test organisms, we observed that the widely employed test organism D. magna is least sensitive among the arthropods tested and that, for neonicotinoid insecticides, an insect like the mosquito C. pipiens would be more suitable for predicting effects on sensitive species.

The significance of entry routes as point and non-point sources of pesticides in small streams

In an agricultural catchment area in Germany we analyzed water samples from five entry routes for 2 insecticides. 5 fungicides and 13 herbicides. The sewage plant outlet and the emergency overflow of a sewage sewer contained only herbicides. In each farmyard runoff we found on average 24 g pesticides during application period, presumably caused by cleaning the spraying equipment. In comparison, the field runoff and the rainwater sewer contained less load, but also insecticides, fungicides and herbicides. The sewage plant caused 65.9% of the total herbicide load, the sewage sewer 19.8% and the farmyard runoff 12.8%. The farmyards also caused 83.7% of total insecticide and 83.8% of fungicide load. The total load of all entry routes is correlated with the amount of pesticides applied in the catchment area and the Ko/w value for each pesticide (mult. regress. r2: 0.82; p<0.0001; n = 14). In stream A the sewage plant caused a slight but continuous contamination by herbicides with 82% of the total load found during low-water phases. In comparison, stream B had only farmyard runoff and non-point sources, which caused high peaks of herbicide and a contamination by insecticides. Consequently, high-water phases generated 70% of the total pesticide load.