The agricultural use of pesticides leads to environmentally relevant pesticide concentrations that cause adverse effects on stream ecosystems. These effects on invertebrate community composition can be identified by the bio-indicator SPEARpesticides. However, refuge areas have been found to partly confound the indicator. On the basis of three monitoring campaigns of 41 sites in Central Germany, we identified 11 refuge taxa. The refuge taxa, mainly characterized by dispersal-based resilience, were observed only nearby uncontaminated stream sections and independent of the level of pesticide pressure. Through incorporation of this information into the revised SPEARpesticides indicator, the community structure specifically identified the toxic pressure and no longer depended on the presence of refuge areas. With regard to ecosystem functions, leaf litter degradation was predicted by the revised SPEARpesticides and the median water temperature at a site (R2 = 0.38, P = 0.003). Furthermore, we designed the bio-indicator SPEARrefuge to quantify the magnitude of general recolonization at a given stream site. We conclude that the taxonomic composition of aquatic invertebrate communities enables a specific indication of anthropogenic stressors and resilience of ecosystems.

Introduction

The intensive use of pesticides worldwide results in high pesticide concentrations in streams (Malaj et al., 2014; Stehle and Schulz, 2015) and causes negative effects on the structure (Liess and von der Ohe, 2005; Münze et al., 2017), ecological functions (Schäfer et al., 2012) and biodiversity (Beketov et al., 2013) of freshwater communities. This widespread degradation of aquatic ecosystems is further accelerated by climate change, increasing exposure to agricultural pesticides (Kattwinkel et al., 2011) and increasing pesticide vulnerability of populations by unfavorable temperatures (Dinh et al., 2016). The use of effect-based indicators is a powerful tool for identifying the toxic pressure of pesticides. The invertebrate-based indicator SPEARpesticides uses trait information of taxa to identify pesticide pressure and the ecological effects in streams. SPEARpesticides was developed by Liess and von der Ohe (2005) and successfully applied to indicate pesticide pressure in streams of different geographical regions worldwide including Europe (Schäfer et al., 2007; Liess et al., 2008; Orlinskiy et al., 2015; Münze et al., 2015; Münze et al., 2017), Russia (Beketov and Liess, 2008), Australia (Schäfer et al., 2011), USA (Chiu et al., 2016) and South America (Hunt et al., 2017). However, as described in several studies (Orlinskiy et al., 2015; Liess and von der Ohe, 2005), the indicator value of SPEARpesticides not only is related to the toxic pressure but also is partly confounded by the presence of uncontaminated stream sections. Such stream sections serve as refuge areas for those invertebrates that recolonize affected stream sections mainly by downstream drift. The influence of refuge areas on toxicant effects has been observed particularly under weak to medium pesticide pressure (Orlinskiy et al., 2015; Liess and von der Ohe, 2005). In contrast, high pesticide pressure impeded the successful recolonization of refuge taxa. Consequently, the presence of refuge areas was taken into account to accurately predict the toxic pressure of pesticides with the SPEARpesticides indicator system. The influence of external sources of recolonizing organisms on disturbed communities has also been recognized in experimental freshwater studies. For example, in a mesocosm experiment, Caquet et al. (2007) have shown that isolation from external populations highly delays the recovery of sensitive insects from pesticide exposure. Trekels et al. (2011) have concluded from a semi-field study with the insecticide endosulfan that external recovery via adult dispersal is particularly important for univoltine compared with multivoltine aquatic invertebrates. Despite the knowledge on the general effects of refuge areas, it is unknown which taxa in freshwater streams are strongly linked to the presence of refuge areas under pesticide exposure and which traits mainly characterize those taxa. However, this knowledge is crucial to increase the stressor specificity and spatial independence of indicators such as SPEARpesticides.