Effects of mosquito control using the microbial agent Bacillus thuringiensis israelensis (Bti) on aquatic and terrestrial ecosystems: a systematic review

Background The bacterium Bacillus thuringiensis serovar israelensis (Bti) is commercially produced in various formulations for use as a larvicide worldwide, targeting especially the aquatic larval stage of mosquitoes. However, there is a concern that repeated Bti treatments may have both direct and indirect impacts on non-target organisms (NTOs) and the ecosystems they inhabit. This review evaluates the evidence for such impacts.Methods Literature was searched using six bibliographic databases, two search engines, and on specialist web sites. Eligibility screening was performed in two steps on (1) title/abstract, with consistency among reviewers assessed by double-screening 557 articles and (2) full text. Articles included after full text screening were critically appraised independently by two reviewers. Disagreements were reconciled through discussions. Key parameters of included studies are presented in narrative synthesis tables, including risk of bias assessments. Meta-analyses comparing treated with untreated ecosystems and using either the raw mean difference or log response ratio as effect size were performed.Review findings Ninety-five articles covering 282 case studies were included in the review. From these, we identified 119 different response variables, which were divided into nine outcome categories. Most studies investigated NTO abundance or life history (reproduction related outcomes), but diversity and community composition are also well represented as outcome categories. The studies are highly variable in methodology, rigor, and spatiotemporal scale, spanning 1 day to 21 years and from 10,000 m(2). Our metanalyses revealed a consistent negative effect of Bti treatment on abundances of Chironomidae and Crustacea, and also on chironomid emergence, although from a more restricted set of studies and regions. For most remaining response variables, we judged meta-analysis unfeasible, due to low study numbers or insufficient reporting of methods and results.Conclusions There is now a significant body of studies documenting effects of mosquito control using Bti on NTOs or other ecosystem properties, especially associated with negative effects on Chironomidae, as apparent from our meta-analyses. Accordingly, we suggest the potential for negative NTO or other ecosystem effects of Bti treatment should not be discounted a priori. Once a decision to proceed with Bti treatment has been taken, priority should be given to a well-designed program of ongoing monitoring and assessment. The paucity of rigorous studies conducted with low bias risk for most response variables undermines our capacity for evaluating how common many of the effects documented might be. Future research would benefit from a rigorous and well-replicated approach to studying Bti impacts in semi-field mesocosms or in the field, combined with a greater rigor in reporting key methodological details. A greater focus is needed on understanding the environmental factors which regulate the wider effects of mosquito control using Bti on NTOs and ecosystems, to enhance our capacity for predicting where and when Bti is most likely to have additional, negative and indirect ecological impacts

Ecological effects of mosquito control with Bti: evidence for shifts in the trophic structure of soil- and ground-based food webs

The microbial control agent Bacillus thuringiensis var. israelensis (Bti) has been successfully used worldwide to reduce abundances of biting Nematocera (Diptera), often with little direct impact on non-target organisms observed. However, the potential for additional indirect effects on other ecosystem properties, including on trophic linkages within food webs, is poorly known. We investigated the effects of multiple-year mosquito control treatments using the Bti product VectoBac((R))-G on the stable isotope composition of epigeal and soil-based consumers inhabiting replicate floodplains along the River Dalalven, Sweden. We observed significant changes in the isotopic composition of detritivores feeding at the base of floodplain food webs. Enchytraeid worms were characterised by 3.5% higher delta C-13 values in treated floodplains, suggesting increased consumption of delta C-13-enriched food. The overall range of community-wide delta N-15 values was 56% greater in the treated floodplains, whilst delta N-15 values of oribatid mites were elevated by 97%. These results suggest extra fractionation in the transfer of nitrogen through floodplain food chains. We conjecture that the ecological mechanisms driving these food web shifts are (1) the mass mortality of high delta C-13 A. sticticus larvae, which leaves high concentrations of dead mosquito biomass deposited on soils at local scales, after the floodwaters have receded and (2) incorporation of the very high delta C-13-enriched corn particles comprising the bulk of the VectoBac((R))-G product into floodplain food webs. Our results suggest that repeated applications of Bti might have wider, still largely unknown implications for nutrient and energy cycles within floodplain ecosystems

Ecological effects of mosquito control with Bti: evidence for shifts in the trophic structure of soil- and ground-based food webs

The microbial control agent Bacillus thuringiensis var. israelensis (Bti) has been successfully used worldwide to reduce abundances of biting Nematocera (Diptera), often with little direct impact on non-target organisms observed. However, the potential for additional indirect effects on other ecosystem properties, including on trophic linkages within food webs, is poorly known. We investigated the effects of multiple-year mosquito control treatments using the Bti product VectoBac®-G on the stable isotope composition of epigeal and soil-based consumers inhabiting replicate floodplains along the River Dalälven, Sweden. We observed significant changes in the isotopic composition of detritivores feeding at the base of floodplain food webs. Enchytraeid worms were characterised by 3.5% higher δ13C values in treated floodplains, suggesting increased consumption of δ13C-enriched food. The overall range of community-wide δ15N values was 56% greater in the treated floodplains, whilst δ15N values of oribatid mites were elevated by 97%. These results suggest extra fractionation in the transfer of nitrogen through floodplain food chains. We conjecture that the ecological mechanisms driving these food web shifts are (1) the mass mortality of high δ13C A. sticticus larvae, which leaves high concentrations of dead mosquito biomass deposited on soils at local scales, after the floodwaters have receded and (2) incorporation of the very high δ13C-enriched corn particles comprising the bulk of the VectoBac®-G product into floodplain food webs. Our results suggest that repeated applications of Bti might have wider, still largely unknown implications for nutrient and energy cycles within floodplain ecosystems

A long-established invasive species alters the functioning of benthic biofilms in lakes

Invasive species often transform environmental conditions, exclude native species and alter ecosystem functioning, including key ecosystem processes underpinning nutrient and energy cycles. However, such impacts have been most documented during periods of invasive species dominance; their influences on functioning at lower relative abundances and after long-term establishment are less well-known.We investigated the effects of Elodea canadensis, a macrophyte native to North America with a long invasion history in many regions of the world, on the biomass accrual and metabolism of littoral zone biofilms growing on organic and inorganic substrates.We deployed nutrient diffusing substrates (NDS) in 18 replicate transects distributed across six lakes, comprising three invaded by E. canadensis and three uninvaded reference lakes. NDS were amended with nitrogen (N), phosphorus (P) or N + P together, or were deployed as unamended controls. E. canadensis relative abundance varied widely in the invaded transects, ranging from 13% to 93% of all macrophyte cover.On control substrates, algal biomass, quantified as Chlorophyll-a, and gross primary production (GPP) were 42% and 78% greater in the invaded compared to uninvaded lakes, respectively. Respiration rates, attributable to responses of both autotrophs and heterotrophs, were 45% greater on control substrates in invaded lakes. By contrast, N-limitation of both biofilm GPP and respiration was 25% and 35% greater in uninvaded compared with invaded lakes.There was no evidence for differences in nutrients, light availability or grazing pressure between invaded and uninvaded transects. Rather, the observed differences in metabolism suggest that the presence of E. canadensis increases availability of N at local scales, reducing N-limitation of biofilms and resulting in elevated rates of biofilm productivity.Our results demonstrate that invasive elodeids might have significant impacts on biofilms and processes associated with the cycling of nutrients, even when long-established and present at lower relative abundances

Interactive effects of land use, river regulation, and climate on a key recreational fishing species in temperate and boreal streams

Numerous anthropogenic stressors, including river regulation, excess loadings of nutrients and sediment, channelisation, as well as thermal and hydrological stressors driven by climate change impact riverine ecosystems worldwide. In a time when freshwater degradation and the rate of global warming are faster than ever, understanding the potential interactive effects of local and catchment-scale stressors with large-scale climatic conditions is essential to enhance our ability to plan effective conservation, restoration, and mitigation measures. In this study we analysed a dataset spanning the whole of Sweden using a space-for-time approach to investigate interactive effects of land use, river regulation, and climate on brown trout (Salmo trutta) abundance in streams. We found that in warmer regions trout populations were negatively affected in catchments with more intense river regulation by hydropower dams (i.e. >= 10 m(3)/km(2) total reservoir storage volume). In such catchments, a 7 degrees C warmer mean summer air temperature was associated with an average between 44% and 83% decline in trout abundance. In catchments with less intense river regulation, trout abundance instead increased moderately with increasing temperature. We also found that brown trout abundance declined with increasing areal extent of urban areas when found in combination with >= 20% agricultural land use. When agricultural land use reached maximum values (84%), brown trout abundance decreased from an average of 13 individuals per 100 m(2) in catchments with no urban areas to values = 5% urban land use. Also, brown trout abundance declined with increasing agricultural land use in catchments with >= 3% urban land use. Our study brings innovative empirical evidence of interactive effects between river regulation, land use and climate on brown trout populations. From a management perspective our findings suggest that: (1) restoring natural flows (e.g. through dam removal) and riparian vegetation could mitigate adverse effects of climate change; and (2) restoration measures that minimise the effects of agriculture and urban land use (e.g. reduction of nutrient levels and restored riparian buffer zones) could help rehabilitate brown trout in catchments with high anthropogenic land use change. However, given the large observed variation between streams, we advise for bespoke management actions stemming from sound knowledge of local habitat conditions and target populations, whenever possible, using an ecosystem management-based approach

Disentangling the roles of plant functional diversity and plaint traits in regulating plant nitrogen accumulation and denitrification in freshwaters

1. There is a growing recognition that functional measures of diversity, based on quantification of functionally important species traits, are useful for explaining variation in ecosystem processes. However, the mechanisms linking functional diversity to different processes remain poorly understood, hindering development of a predictive framework for ecosystem functioning based on species traits.2. The current understanding of how the functional traits of aquatic plants (macrophytes) affect nitrogen (N) cycling by regulating microbial communities and their activity in freshwater habitats is particularly limited. Denitrifying bacteria are typically associated with the roots of both aquatic and terrestrial plants and denitrification is the main cause of loss of N from ecosystems. Disentangling the interplay between plants and microbial denitrifiers is key to understanding variation in rates of denitrification from local to landscape scales.3. In a mesocosm experiment, we varied the species richness (monocultures or two-species mixtures) and composition of macrophytes. We quantified effects of both macrophyte functional diversity, quantified as functional trait dissimilarity, and functional trait composition, quantified as community weighted mean trait values, on N removal in wetlands. We used structural equation modelling to disentangle the direct and indirect influences of traits on N accumulation in plant biomass, denitrification activity and abundance of key bacterial denitrification genes (nirS and nirK).4. Both functional diversity and functional trait composition regulated N removal, explaining 70%-94% variation in the underlying ecosystem processes. Increased macrophyte functional diversity increased plant N accumulation, and indirectly enhanced denitrification by increasing denitrification gene abundance. Among traits, greater plant relative growth rates, specific leaf area and above-ground biomass increased plant N accumulation. Denitrification activity increased with increasing below-ground biomass but decreased with increasing root diameter.5. These findings improve our understanding of N removal in freshwater wetlands dominated by macrophytes, and have broad ecological implications for wetland management targeting enhanced ecosystem services. Our results highlight the potential for optimizing denitrification and plant N accumulation in wetlands and thereby improving water purification by increasing macrophyte functional diversity and ensuring the presence of key traits in macrophyte assemblages

Comparing effects of microplastic exposure, FPOM resource quality, and consumer density on the response of a freshwater particle feeder and associated ecosystem processes

Fine particulate organic matter (FPOM) is an important basal resource in stream ecosystems for deposit- and filter-feeding macroinvertebrates (collectively 'particle feeders'). Microplastics (MP) share many characteristics with FPOM (e.g. size range, surface area to volume ratios) and are potentially consumed by particle feeders. Accordingly, MP contamination of natural FPOM pools might affect particle feeder growth and survival, particularly when background FPOM resource quality is low, or intraspecific competition is high. We conducted a microcosm experiment to evaluate how a realistic (1400 particles/kg sediment) polyethylene MP (o = 45-53 mu m) concentration interacts with FPOM (o = 63-250 mu m) resource quality (low versus high nutrient content) and consumer density (10 versus 20 individuals per microcosm) to affect growth and survival of larval Chironomus riparius (Diptera: Chironomidae), a model particle feeder. We additionally quantified community respiration, based on three hour measurements of oxygen consumption in the microcosms at the end of the experiment. MP exposure reduced larval body lengths by 26.7%, but only under the low consumer density treatment. MPs reduced community respiration by 26.2%, but only in the absence of chironomids, indicating an impact on microbial respiration. In comparison, low resource quality and high consumer density were associated with 53.5-70.2% reductions in community respiration, chironomid body length and/or body mass. These results suggest that effects of contamination of FPOM with MPs at environmentally realistic concentrations on the life histories of particle feeders such as C. riparius might be limited, especially relative to the effects of resource quality and consumer density. However, the reduction in microbial respiration when MPs were present highlights the need for further research addressing MP impacts on microbes, given their key roles in ecosystem functioning

Assessing and managing freshwater ecosystems vulnerable to environmental change

Freshwater ecosystems are important for global biodiversity and provide essential ecosystem services. There is consensus in the scientific literature that freshwater ecosystems are vulnerable to the impacts of environmental change, which may trigger irreversible regime shifts upon which biodiversity and ecosystem services may be lost. There are profound uncertainties regarding the management and assessment of the vulnerability of freshwater ecosystems to environmental change. Quantitative approaches are needed to reduce this uncertainty. We describe available statistical and modeling approaches along with case studies that demonstrate how resilience theory can be applied to aid decision-making in natural resources management. We highlight especially how longterm monitoring efforts combined with ecological theory can provide a novel nexus between ecological impact assessment and management, and the quantification of systemic vulnerability and thus the resilience of ecosystems to environmental change

Forested riparian buffers change the taxonomic and functional composition of stream invertebrate communities in agricultural catchments

Riparian zones form the interface between stream and terrestrial ecosystems and play a key role through their vegetation structure in determining stream biodiversity, ecosystem functioning and regulating human impacts, such as warming, nutrient enrichment and sedimentation. We assessed how differing riparian vegetation types influence the structural and functional composition (based on species traits) of stream invertebrate communities in agricultural catchments. We characterized riparian and stream habitat conditions and sampled stream invertebrate communities in 10 independent site pairs, each comprising one “unbuffered” reach lacking woody riparian vegetation and a second downstream reach with a woody riparian buffer. Forested riparian buffers were associated with greater shading, increased gravel content in stream substrates and faster flow velocities. We detected changes in invertebrate taxonomic composition in response to buffer presence, with an increase in sensitive Ephemeroptera, Plecoptera and Trichoptera (EPT) taxa and increases in key invertebrate species traits, including species with preference for gravel substrates and aerial active dispersal as adults. Riparian vegetation independently explained most variation in taxa composition, whereas riparian and instream habitat together explained most variation in functional composition. Our results highlight how changes in stream invertebrate trait distributions may indirectly reflect differences in riparian habitat, with implications for stream health and cross-ecosystem connectivity

Agricultural land use weakens the relationship between biodiversity and ecosystem functioning

Leaf litter decomposition is a significant ecosystem process for streams' energy provisioning, while species-specific decomposition rates often form a continuum from slow to fast decomposing species allowing for resources' availability to stream consumers over a longer time period after leaf fall. Leaf litter mixtures in streams typically comprise leaf species varying in their traits, allowing for litter diversity effects on decomposition. At the same time, agricultural land use, habitat characteristics, water quality and invertebrate composition modulate leaf litter decomposition. To identify leaf litter diversity effects and disentangle the roles of agricultural intensity, habitat characteristics, water quality and invertebrate composition for leaf litter processing in streams, we quantified leaf litter decomposition of three leaf species covering a gradient from slow to fast decomposing species, tested either individually or as a three-species mixture. The study was conducted over 21 days across 18 streams with a gradient of agricultural intensity (percent agricultural land use) in their catchments. We found leaf litter diversity effects in terms of complementarity under low to intermediate agricultural intensity, given that slow decomposing leaf species decomposed almost twice as fast in the three-species mixture compared to the observations on individual leaf species. This leaf litter diversity effect decreased with increasing agricultural intensity, suggesting that agriculture weakens the biodiversity-ecosystem functioning relationship. However, pathways by which agriculture affected decomposition differed between single-species and mixed-species scenarios. For the single-species scenario, negative effects of agriculture appeared to be mediated through effects on the proportion of sensitive detritivore species and altered habitat characteristics. For the mixed-species scenario, altered water quality negatively affected the proportion of sensitive detritivore species, in turn reducing the diversity effect on functioning. Our results suggest that the weakened biodiversity-ecosystem functioning relationship under increasing agricultural intensity might be a significant factor threatening carbon cycling and food web integrity in streams