Kaarina Foit

Climate change, agricultural insecticide exposure, and risk for freshwater communities

Climate change exerts direct effects on ecosystems but has additional indirect effects due to changes in agricultural practice. These include the increased use of pesticides, changes in the areas that are cultivated, and changes in the crops cultivated. It is well known that pesticides, and in particular insecticides, affect aquatic ecosystems adversely. To implement effective mitigation measures it is necessary to identify areas that are affected currently and those that will be affected in the future. As a consequence, we predicted potential exposure to insecticide (insecticide runoff potential, RP) under current conditions (1990) and under a model scenario of future climate and land use (2090) using a spatially explicit model on a continental scale, with a focus on Europe. Space-for-time substitution was used to predict future levels of insecticide application, intensity of agricultural land use, and cultivated crops. To assess the indirect effects of climate change, evaluation of the risk of insecticide exposure was based on a trait-based, climate-insensitive indicator system (SPEAR, SPEcies At Risk). To this end, RP and landscape characteristics that are relevant for the recovery of affected populations were combined to estimate the ecological risk (ER) of insecticides for freshwater communities. We predicted a strong increase in the application of, and aquatic exposure to, insecticides under the future scenario, especially in central and northern Europe. This, in turn, will result in a severe increase in ER in these regions. Hence, the proportion of stream sites adjacent to arable land that do not meet the requirements for good ecological status as defined by the EU Water Framework Directive will increase (from 33% to 39% for the EU-25 countries), in particular in the Scandinavian and Baltic countries (from 6% to 19%). Such spatially explicit mapping of risk enables the planning of adaptation and mitigation strategies including vegetated buffer strips and nonagricultural recolonization zones along streams.

SPEAR indicates pesticide effects in streams - Comparative use of species- and family-level biomonitoring data

To detect effects of pesticides on non-target freshwater organisms the Species at risk (SPEAR(pesticides)) bioindicator based on biological traits was previously developed and successfully validated over different biogeographical regions of Europe using species-level data on stream invertebrates. Since many freshwater biomonitoring programmes have family-level taxonomic resolution we tested the applicability of SPEAR(pesticides) with family-level biomonitoring data to indicate pesticide effects in streams (i.e. insecticide toxicity of pesticides). The study showed that the explanatory power of the family-level SPEAR(fm)(pesticides) is not significantly lower than the species-level index. The results suggest that the family-level SPEAR(fm)(pesticides) is a sensitive, cost-effective, and potentially European-wide bioindicator of pesticide contamination in flowing waters. Class boundaries for SPEAR(pesticides) according to EU Water Framework Directive are defined to contribute to the assessment of ecological status of water bodies.

Culmination of Low-Dose Pesticide Effects

Pesticides applied in agriculture can affect the structure and function of nontarget populations at lower doses and for longer timespans than predicted by the current risk assessment frameworks. We identified a mechanism for this observation. The populations of an aquatic invertebrate (Culex pipiens) exposed over several generations to repeated pulses of low concentrations of the neonicotinoid insecticide (thiacloprid) continuously declined and did not recover in the presence of a less sensitive competing species (Daphnia magna). By contrast, in the absence of a competitor, insecticide effects on the more sensitive species were only observed at concentrations 1 order of magnitude higher, and the species recovered more rapidly after a contamination event. The underlying processes are experimentally identified and reconstructed using a simulation model. We conclude that repeated toxicant pulse of populations that are challenged with interspecific competition may result in a multigenerational culmination of low-dose effects.

Competition increases toxicant sensitivity and delays the recovery of two interacting populations

We investigated how persistent competitive pressure alters toxicant sensitivity and recovery from a pesticide pulse at community level. Interacting populations of Daphnia (Daphnia magna) and Culex larvae (Culex pipiens molestus) were pulse-exposed (48 h) to the pyrethroid fenvalerate. The abundance and biomass of the populations were monitored by non-invasive image analysis. Shortly after exposure, Daphnia showed a concentration-response relationship with the toxicant with an LC₅₀ of 0.9 μg/L. Culex larvae were slightly less sensitive with an LC₅₀ of 1.7 μg/L. For both species, toxicant sensitivity increased with the population biomass of the respective species before exposure, which is explained by intraspecific competition. Several weeks after exposure to the highest treatment concentration of 1 μg/L, the slight differences in sensitivity between the two species were amplified to contrasting long-term effects due to interspecific competition: high interspecific competition impaired the recovery of Daphnia. Subsequently, Culex larvae profited from the slow recovery of Daphnia and showed an increased success of emergence. We conclude that, in natural systems where competition is present, such competitive processes might prolong the recovery of the community structure. Hence, natural communities might be disturbed for a longer period by toxic exposure than predicted from single-species tests alone.

Intraspecific competition delays recovery of population structure

Ecotoxicological field studies have shown that total abundance and biomass often recover shortly after pulsed toxicant stress. In contrast, population structure showed comparatively long-term alterations before reaching pre-treatment conditions. We investigated two mechanisms that may explain the prolonged recovery of population structure: latent toxicant effects on life-history traits on the individual level and competition on the population level. To test these hypotheses we exposed populations of Daphnia magna to a pulse of the pyrethroid Fenvalerate. For several generations the populations were kept at two different degrees of competition: strong competition at carrying capacity and reduced competition maintained by simulated predation. After disturbance due to Fenvalerate exposure, biomass recovered after 14-17 days. In contrast, size structure characterised by a lack of large and dominance of small organisms recovered after 43 days in populations with strong competition. Size structure recovered twice faster in populations with reduced competition. We explain this as follows: due to toxicant induced mortality, food availability and consequently birth rate increased and populations were dominated by small individuals. In populations without predation, these cohorts grew and eventually exerted high intraspecific competition that (i) stopped further growth of juveniles and (ii) increased mortality of adults. These demographic processes were mainly responsible for the prolonged recovery of size structure. In contrast, for populations with predation, the regular harvest of individuals reduced competition. Juveniles developed continuously, allowing a fast recovery of size structure in these dynamic populations. In risk assessment the duration for populations to recover from (toxicant) stress, is crucial for the determination of ecological acceptable effects. We conclude that competition needs to be considered in order to understand and predict recovery of size structure.

Predicting the synergy of multiple stress effects

Toxicants and other, non-chemical environmental stressors contribute to the global biodiversity crisis. Examples include the loss of bees and the reduction of aquatic biodiversity. Although non-compliance with regulations might be contributing, the widespread existence of these impacts suggests that for example the current approach of pesticide risk assessment fails to protect biodiversity when multiple stressors concurrently affect organisms. To quantify such multiple stress effects, we analysed all applicable aquatic studies and found that the presence of environmental stressors increases individual sensitivity to toxicants (pesticides, trace metals) by a factor of up to 100. To predict this dependence, we developed the “Stress Addition Model” (SAM). With the SAM, we assume that each individual has a general stress capacity towards all types of specific stress that should not be exhausted. Experimental stress levels are transferred into general stress levels of the SAM using the stress-related mortality as a common link. These general stress levels of independent stressors are additive, with the sum determining the total stress exerted on a population. With this approach, we provide a tool that quantitatively predicts the highly synergistic direct effects of independent stressor combinations.

Pesticides from wastewater treatment plant effluents affect invertebrate communities

We quantified pesticide contamination and its ecological impact up- and downstream of seven wastewater treatment plants (WWTPs) in rural and suburban areas of central Germany. During two sampling campaigns, time-weighted average pesticide concentrations (cTWA) were obtained using Chemcatcher® passive samplers; pesticide peak concentrations were quantified with event-driven samplers. At downstream sites, receiving waters were additionally grab sampled for five selected pharmaceuticals. Ecological effects on macroinvertebrate structure and ecosystem function were assessed using the biological indicator system SPEARpesticides (SPEcies At Risk) and leaf litter breakdown rates, respectively. WWTP effluents substantially increased insecticide and fungicide concentrations in receiving waters; in many cases, treated wastewater was the exclusive source for the neonicotinoid insecticides acetamiprid and imidacloprid in the investigated streams. During the ten weeks of the investigation, five out of the seven WWTPs increased in-stream pesticide toxicity by a factor of three. As a consequence, at downstream sites, SPEAR values and leaf litter degradation rates were reduced by 40% and 53%, respectively. The reduced leaf litter breakdown was related to changes in the macroinvertebrate communities described by SPEARpesticides and not to altered microbial activity. Neonicotinoids showed the highest ecological relevance for the composition of invertebrate communities, occasionally exceeding the Regulatory Acceptable Concentrations (RACs). In general, considerable ecological effects of insecticides were observed above and below regulatory thresholds. Fungicides, herbicides and pharmaceuticals contributed only marginally to acute toxicity. We conclude that pesticide retention of WWTPs needs to be improved.

Short-term disturbance of a grazer has long-term effects on bacterial communities - relevance of trophic interactions for recovery from pesticide effects.

Little is known about the transfer of pesticide effects from higher trophic levels to bacterial communities by grazing. We investigated the effects of pulse exposure to the pyrethroid Fenvalerate on a grazer-prey system that comprised populations of Daphnia magna and bacterial communities. We observed the abundance and population size structure of D. magna by image analysis. Aquatic bacteria were monitored with regard to abundance (by cell staining) and community structure (by a 16S ribosomal RNA fingerprinting method). Shortly after exposure (2 days), the abundance of D. magna decreased. In contrast, the abundance of bacteria increased; in particular fast-growing bacteria proliferated, which changed the bacterial community structure. Long after pulse exposure (26 days), the size structure of D. magna was still affected and dominated by a cohort of small individuals. This cohort of small D. magna grazed actively on bacteria, which resulted in low bacterial abundance and low percentage of fast-growing bacteria. We identified grazing pressure as an important mediator for translating long-term pesticide effects from a grazer population on its prey. Hence, bacterial communities are potentially affected throughout the period that their grazers show pesticide effects concerning abundance or population size structure. Owing to interspecific interactions, the recovery of one species can only be assessed by considering its community context.

Modelling aquatic exposure and effects of insecticides--application to south-eastern Australia.

Agricultural pesticides are widely used and can affect freshwater organisms. We applied a spatially explicit exposure model, validated for central Europe, to estimate exposure to insecticides through runoff for streams in south-eastern Australia. The model allows the identification of streams potentially affected by insecticide runoff located in 10×10 km grid cells. The computation of runoff relies on key environmental factors such as land use, soil texture, slope and precipitation. Additionally, the model predicted the ecological effect of insecticides on the macroinvertebrate community. We predicted insecticide surface runoff that results in a moderate to poor ecological quality for streams in half of the grid cells containing agricultural land. These results are in good accordance with the results obtained by estimating pesticide stress with a biotic index (SPEAR(pesticides)) based on macroinvertebrate monitoring data. We conclude that the exposure and effect model can act as an effective and cost-saving tool to identify high risk areas of insecticide exposure and to support stream management.

Automated Nanocosm test system to assess the effects of stressors on two interacting populations.

There is a great need in environmental research for test systems that include ecologically important factors and that are also easy to use. We present here the automated test system Nanocosm, which is composed of populations of Daphnia magna and Culex pipiens molestus. The Nanocosm system allows the investigation of stressed populations in the presence of interspecific competition, which is a very important factor involved in the dynamics of ecosystems. With the Nanocosm system, the abundance and size structure of populations of both species are quantified by image analysis. The technique enables a time-efficient, non-invasive and reliable long-term monitoring of interactions between two aquatic populations. We recommend the Nanocosm system as a novel tool for the simplified integration of competition into environmental and ecotoxicological research as well as for the assessment of risk due to stressors.