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Calibration of the Spearpesticides Ganatra et al. Environ Sci Eur (2021) 33:58 https://doi.org/10.1186/s12302-021-00497-9 RESEARCH Open Access Calibration of the SPEARpesticides bioindicator for cost-efective pesticide monitoring in East African streams Akbar A. Ganatra1,2, Faith Jebiwot Kandie1,3,4,5, Ulrike Fillinger1, Francis McOdimba1,2, Baldwyn Torto1, Werner Brack3,5, Matthias Liess6,7* , Henner Hollert7 and Jeremias M. Becker6,7 Abstract Background: Pesticides are washed from agricultural felds into adjacent streams, where even short-term exposure causes long-term ecological damage. Detecting pesticide pollution in streams thus requires the expensive monitor- ing of peak concentrations during run-of events. Alternatively, exposure and ecological efects can be assessed using the SPEARpesticides bioindicator that quantifes pesticide-related changes in the macroinvertebrate community compo- sition. SPEARpesticides has been developed in Central Europe and validated in other parts of Europe, Australia and South America; here we investigated its performance in East African streams. Results: With minimal adaptations of the SPEARpesticdes index, we successfully characterized pesticide pollution in 13 streams located in Western Kenya. The East African SPEARpesticides index correlated well with the overall toxicity of 30 pesticides (maximum toxic unit maximum environmental vs. median lethal concentration) measured in stream 2 = water (R 0.53). Similarly, the SPEARpesticides index correlated with the risk of surface run-of from agricultural felds (as identifed= based on ground slope in the catchment area and the width of protective riparian strips, R2 0.45). Unlike = other bioindicators designed to indicate general water pollution, SPEARpesticides was independent of organic pollution and highly specifc to pesticides. In 23% of the streams, pesticides exceeded concentrations considered environmen- tally safe based on European frst tiered risk assessment. Conclusions: Increasing contamination was associated with considerable changes in the macroinvertebrate community composition. We conclude that pesticides need to be better regulated also in developing countries. SPEARpesticides provides a straightforward and cost-efcient tool for the required monitoring of pesticide exposure in small to medium streams. Keywords: Ecotoxicology, Bio-indicator, Pesticide pollution Background and birds [2–4]. Tere is increasing evidence that the In 2020, the worldwide application of agricultural pes- pesticide-driven impairment of biocenoses also afects ticides is expected to increase from 2 million tonnes valuable ecosystem services ranging from pollination to 3.5 million tonnes annually [1]. Pesticide pollution [5] to leaf-litter degradation [6] and to the biological is considered one of the main drivers for the global control of agricultural pests [7, 8] and of pathogens decline in the abundance and diversity of insects, plants in freshwater [9]. For the United States and the Euro- pean Union, where pesticides are used on a large scale, *Correspondence: [email protected] extensive literature on exposure and efects in the envi- 6 Department of System-Ecotoxicology, Helmholtz Centre ronment is available from academic research and from for Environmental Research GmbH – UFZ, 04318 Leipzig, Germany regulatory risk assessment [1]. In developing countries, Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Ganatra et al. Environ Sci Eur (2021) 33:58 Page 2 of 15 regulation of plant protection products is often poor pollution in small to medium streams that may be spe- and information on pesticide pollution is scarce, cifcally valuable in developing countries. though recent evidence suggests that pesticide usage SPEARpesticides has been developed for temperate has been increasing [1]. As agricultural producers grow streams in Central Europe. Tus, the studied species more conscious about the use of synthetic pesticides composition, pesticide exposure patterns and ecologi- and their toxic efects [10], more efort in the assess- cal conditions may difer from those in other continents ment and mitigation of pesticide pollution is urgently such as in sub-Saharan Africa. Malherbe et al. [22] found needed. only a non-signifcant response of SPEAR pesticides values Freshwater macroinvertebrates in small streams are at to pesticide pollution in South African streams. In con- particular risk, since streams collect pesticide loads from trast, SPEARpesticides has been successfully applied and agricultural felds in the catchment area [11]. Moreover, validated to assess pesticide pollution in various streams many freshwater arthropods are highly sensitive to insec- ranging from Southern to Northern Europe [20], and ticides and fungicides [12–14]. However, the detection (after minor modifcation) in Australia [23] and Argen- and quantifcation of pesticides in streams is challeng- tina [24]. Te SPEARpesticides concept is based on ecotoxi- ing, as exposure occurs typically in short pulses due to cological traits rather than taxonomic relations and thus spray drift and particularly due to surface run-of from provides a mechanistic linkage of pesticide stress and the agricultural felds following heavy rainfall [15]. Such community response; in contrast to classical taxonomy- short-term exposure peaks (in the range of hours) drive based bioindicators, trait-based approaches can over- long-term efects on the macroinvertebrate community come issues with natural taxonomic variability and may for months [16–18]. Terefore, pesticide measurements thus be applicable even across diferent climatic regions from grab samples of stream water and sediment at ran- [25]. For freshwater macroinvertebrates in the South- dom time points tend to considerably underestimate the ern hemisphere, information on ecotoxicological traits magnitude of pesticide exposure. Realistic environmental is very scarce [22, 23]. However, Wang et al. [26] found monitoring in streams must capture the exposure peaks that related saltwater invertebrates from temperate and by run-of event-triggered sampling [15] or by continu- tropical regions difer only slightly in their acute sensitiv- ous passive sampling over extended periods of time [11]. ity to toxicants. Moreover, SPEAR pesticides can be applied However, such studies are labor-intensive and expensive at the family taxonomic level [27], and palearctic and [19]. In addition to the chemical analysis of samples for afrotropical streams share most of their macroinverte- many compounds, samplers need to be installed, pro- brate families [28]. Assuming that families of freshwater tected and regularly accessed in remote areas. Tese macroinvertebrates from temperate and tropical streams challenges limit the feasibility of monitoring pesticide may generally share their vulnerability to pesticides, pollution based on chemical analyses, particularly in SPEARpesticides may be, therefore, used also in sub-Saha- developing countries. ran Africa. As an alternative approach, pesticide exposure can Here we applied the SPEAR pesticides bioindicator to be indirectly derived from its observed efects on macroinvertebrate samples from 13 small to medium the macroinvertebrate community composition. Te streams in Western Kenya. Te SPEARpesticides values SPEARpesticides (“SPEcies At Risk”) bioindicator has been were compared to the toxic pressure of 30 pesticides in developed to quantify decreases in the proportion of water samples concurrently collected during the rainy those taxa considered to be vulnerable to pesticides, as season [29]. Additionally, we tested the specifcity of the compared to reference conditions [20, 21]. For this task, SPEARpesticides index for pesticide efects and compared stream macroinvertebrates have been classifed as vul- its performance to alternative bioindicators for environ- nerable or non-vulnerable taxa based on ecotoxicologi- mental stressors. cal traits (see methods). Because the SPEAR pesticides index describes the proportion of vulnerable taxa (weighted by Materials and methods individual number), it has no unit and does not facili- Study area tate the identifcation of individual toxic compounds in Te Lake Victoria South Basin in the western part of the environment. However, SPEARpesticides values can be Kenya (Fig. 1) is characterized by a tropical climate with translated to an estimated toxic pressure for macroin- a major rainy season between March and June and a vertebrates in the more informative form of toxic units minor rainy season between October and December. Te (see methods). Since the SPEARpesticides value is driven by rainy seasons are separated by dry months, particularly long-term efects,
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