Elsevier

Aquatic Toxicology

Volume 186, May 2017, Pages 215-221
Aquatic Toxicology

Interactive effects of an insecticide and a fungicide on different organism groups and ecosystem functioning in a stream detrital food web

https://doi.org/10.1016/j.aquatox.2017.03.008Get rights and content

Highlights

  • We investigated effects of a representative fungicide and insecticide on the functioning of a model tritrophic stream food web.

  • Multiple interactions between food web complexity and the pesticides altered functioning from our a priori predictions.

  • Pesticides often had contrasting impacts on different endpoints, reflecting tradeoffs in responses of organisms and/or compensatory mechanisms

  • Our results highlight challenges in predicting, understanding and evaluating impacts of multiple chemical stressors on complex food webs in situ

Abstract

Freshwater ecosystems are often affected by cocktails of multiple pesticides targeting different organism groups. Prediction and evaluation of the ecosystem-level effects of these mixtures is complicated by the potential not only for interactions among the pesticides themselves, but also for the pesticides to alter biotic interactions across trophic levels. In a stream microcosm experiment, we investigated the effects of two pesticides targeting two organism groups (the insecticide lindane and fungicide azoxystrobin) on the functioning of a model stream detrital food web consisting of a detritivore (Ispoda: Asellus aquaticus) and microbes (an assemblage of fungal hyphomycetes) consuming leaf litter. We assessed how these pesticides interacted with the presence and absence of the detritivore to affect three indicators of ecosystem functioning – leaf decomposition, fungal biomass, fungal sporulation – as well as detritivore mortality. Leaf decomposition rates were more strongly impacted by the fungicide than the insecticide, reflecting especially negative effects on leaf processing by detritivores. This result most like reflects reduced fungal biomass and increased detritivore mortality under the fungicide treatment. Fungal sporulation was elevated by exposure to both the insecticide and fungicide, possibly representing a stress-induced increase in investment in propagule dispersal. Stressor interactions were apparent in the impacts of the combined pesticide treatment on fungal sporulation and detritivore mortality, which were reduced and elevated relative to the single stressor treatments, respectively. These results demonstrate the potential of trophic and multiple stressor interactions to modulate the ecosystem-level impacts of chemicals, highlighting important challenges in predicting, understanding and evaluating the impacts of multiple chemical stressors on more complex food webs in situ.

Introduction

The development of the “Green revolution” during the 20th century dramatically raised agricultural production, especially through the extensive use of fertilizers and pesticides (Tilman, 1998). Such pesticides comprise a wide variety of insecticides, herbicides and fungicides, targeting different pest organism groups on crops. During or following their application onto agricultural fields, pesticides can be transferred into adjacent aquatic ecosystems, especially via spray drift or surface runoff (Schulz, 2004). Once there, these “pesticide cocktails” may affect the structure and diversity of aquatic communities (Schulz and Liess, 1999), and also key ecosystem processes such as algal productivity (Villeneuve et al., 2011) and leaf litter decomposition (Schafer et al., 2007). These impacts arise not only from the potential for direct interactions among the pesticides, but also from “knock-on” (i.e. secondary indirect or cumulative) effects of those interactions on organisms and the ecosystem functions they perform (Norgaard and Cedergreen, 2010, Truchy et al., 2015).

The decomposition of terrestrially-derived leaf litter is a key process in the functioning of streams, involving multiple organism groups and trophic levels. Leaf litter decomposition in streams begins with the leaching of soluble compounds from freshly shed litter, followed by colonization of microbes, particularly aquatic hyphomycete fungi (Gessner et al., 1999). Microbial colonization facilitates leaf degradation through enzymatic hydrolysis that converts organic matter to CO2 and biomass (Gessner et al., 2010). This process, also known as “microbial conditioning”, increases the palatability of the litter for leaf-consuming detritivores (a.k.a. “shredders”) (Bärlocher, 1985, Cummins and Klug, 1979), which are responsible for the bulk of the physical fragmentation of leaves into fine particulate organic matter (Anderson and Sedell, 1979, Hieber and Gessner, 2002).

Due to the interconnected nature of stream food webs, pesticides targeting one group of organisms can have knock-on effects on other trophic levels and organism groups (Bundschuh and McKie, 2016). Such effects can propagate both “bottom-up”, where effects on the composition and activity of organisms at the base of the food web impact higher trophic levels, and “top-down”, where impacts on higher trophic levels (i.e. primary or secondary consumers) strongly influence lower trophic levels (Gotelli and Ellison, 2006, Jabiol et al., 2013). For example, fungicides that impact biomass and activities of microbes are likely to also impair microbial conditioning and thereby reduce detritivore feeding, further reducing overall rates of leaf decomposition (Fernandez et al., 2015, Gardeström et al., 2016). Insecticides can impact decomposition mediated through effects on the feeding behavior, abundance (mortality) and/or diversity (selective mortality) of invertebrate detritivores (Schafer et al., 2007). However, impacts of insecticides on leaf processing by microbes are difficult to predict (Chung and Suberkropp, 2008) – given that detritivores themselves consume microbes, a negative effect on detritivore feeding activity may even favor greater microbial activity (Graça et al., 1993). Unraveling the individual and joint consequences of pesticides targeting different types of organisms might aid our understanding of the relevance of the different functions provided by these trophic levels for the ecosystem process of, for example, leaf litter decomposition.

We investigated the effects of two pesticides (a fungicide and insecticide) on the functioning of a tritrophic (detrital resource – microbial decomposers – invertebrate detritivore) stream food web in laboratory microcosms, as a model system for investigating complex multiple stressor and -trophic interactions. In a factorial experiment, these microcosms were subjected either to (i) a pesticide free control, (ii) an insecticide only treatment, (iii) a fungicide only treatment, or (iv) a combined pesticide treatment with the fungicide and insecticide applied jointly. The presence or absence of the detritivore Asellus aquaticus (Crustacea: Isopoda) was also varied among microcosms. Our response variables included rates of leaf mass loss, the mortality and leaf processing efficiency (LPE) of detritivores, as well as the biomass and sporulation activity of fungi. We hypothesized that the fungicide as single stressor would affect microbially-mediated decomposition, fungal biomass and fungal sporulation activity negatively, which may have knock-on effects arising from the bottom-up on the responses of detritivores, reflecting impaired microbial conditioning. In contrast, we expected that the insecticide would affect the detrital food web from top-down, by reducing LPE of detritivores, but possibly enhancing some microbial responses due to a reduction in detritivore feeding pressure. Finally, we hypothesized that the joint application of the fungicide and insecticide would reflect the combined impacts of impaired microbial activity caused by the fungicide and impaired detritivore feeding caused by the insecticide.

Section snippets

The pesticide treatments

Our selected model pesticides were the fungicide azoxystrobin and insecticide lindane. Azoxystrobin is primarily used to prevent foliar diseases of vegetable and fruit crops caused by pathogenic fungi (Ascomycota, Deutermyctoa, Basidomycota) and fungi-like organisms (Oomycetes) (Bartlett et al., 2002). Azoxystrobin affects fungal reproduction and development by disturbing the energy production for spore germination and zoospore motility (Bartlett et al., 2002). Azoxystrobin is frequently

Pesticide-induced mortality of A. aquaticus

The insecticide lindane did not cause acute toxicity of A. aquaticus at 5 μg/l, with average mortality (0.4 ± 0.2 deaths per microcosm, ±SE; n = 5) barely higher than in the controls (with no individuals dead, Table 1). The lack of acute lindane toxicity over thirteen days is in line with earlier studies reporting acute toxicity of lindane in the amphipod shredder Hyalella azteca over ten days of exposure, at a factor of five above the concentrations tested during the present study (Blockwell et

Acknowledgements

Märit Peterson prepared the fungicide stock solutions, and ergosterol analyses were run by Margareta Zetherström. Funding was provided by FORMAS grants to WG (216-2004-1971) and BGM (DESTRESS, 2014-886), with additional material support from the Centre for Chemical Pesticides at the Swedish University of Agricultural Sciences.

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