Invasive Species Mediate Insecticide Effects on Community and Ecosystem Functioning

Abstract

Anthropogenic activities increase pesticide contamination and biological invasions in freshwater ecosystems. Understanding their combined effects on community structure and on ecosystem functioning presents challenges for an improved ecological risk assessment. This study focuses on an artificial stream mesocosms experiment testing for direct and indirect effects of insecticide (chlorantraniliprole - CAP) exposure on the structure of a benthic macroinvertebrate freshwater community and on ecosystem functioning (leaf decomposition, primary production). To understand how predator identity and resource quality alter the community responses to chemical stress, the mediating effects of an invasive predator species (crayfish Procambarus clarkii) and detritus quality (tested by using leaves of the invasive Eucalyptus globulus) on insecticide toxicity were also investigated. Low concentrations of CAP reduced the abundance of shredders and grazers, decreasing leaf decomposition and increasing primary production. Replacement of autochthonous predators and leaf litter by invasive species decreased macroinvertebrate survival, reduced leaf decomposition, and enhanced primary production. Structural equation modeling (SEM) highlighted that CAP toxicity to macroinvertebrates was mediated by the presence of crayfish or eucalypt leaf litter which are now common in many Mediterranean freshwaters. In summary, our results demonstrate that the presence of these two invasive species alters the effects of insecticide exposure on benthic freshwater communities. The approach used here also allowed for a mechanistic evaluation of indirect effects of these stressors and of their interaction on ecosystem functional endpoint, emphasizing the value of incorporating biotic stressors in ecotoxicological experiments.

The Importance of Ecological Networks in Multiple-Stressor Research and Management

“…Indirect stressor effects mediated by biotic interactions are particularly relevant in a multiple-stressor context given the potential of stressors to ripple through communities and ecological networks, resulting in stressors interactions at distant groups of organisms (see examples above). Stressors change the availability of basal resources, consumer biomass, and behavioral or morphological traits, all affecting the intensity of consumption and energy flows (Brodin et al, 2014;Alexander et al, 2016;Rodrigues et al, 2018). Stressors may also increase susceptibility to infectious organisms (e.g., parasites; Studer and Poulin, 2013;Hofmann et al, 2016), with potential knock-on effects on host phenotype and ecological processes (Frainer et al, 2018).…”

“…Biotic interactions also underlie masking effects that might occur when measuring species as independent endpoints of the analysis. Masking effects may be based on adaptation in resource use by consumers when measuring their biomass (Alexander et al, 2013), functional redundancy of consumers when measuring resource use (Rodrigues et al, 2018), or cascading effects across more than two trophic levels (Alexander et al, 2013;Rodrigues et al, 2018). Masking may erroneously be interpreted as organisms being insensitive or resistant toward the stressors.…”

“…These may occur if stressors cause functional or density changes in organisms, thus triggering trait or density-mediated alterations of non-trophic interactions, e.g., competition and facilitation (Clements et al, 1989;Brooks and Crowe, 2018;Rodrigues et al, 2018). Specifically testing biotic interactions can reveal such indirect stressor effects, novel stressor combinations, and their ecosystem-level consequences.…”

“…This effect interacted synergistically with raising water temperatures (a direct stressor) in increasing fish mortality. In a similar experiment, Rodrigues et al (2018) used SEM to quantify direct and indirect effects of an insecticide and of invasive species on a stream food web. In their study, indirect effects explained a positive effect of an invasive top-predator (Louisiana crayfish, Procambarus clarkii) on algal growth through cascading effects, and a positive effect of the insecticide on invertebrate prey survival due to behavioral changes, which reduced cues used by the predator.…”

“…[1]Kortsch et al (2015),[2] Tylianakis et al (2007), [3] Bruder et al (2017), [4] Schrama et al (2017), [5] Alexander et al (2016), [6] Bakker et al (2013), [7] Bentivoglio et al (2016), [8] Brittain and Strecker (2018), [9] Frainer and McKie (2015), [10] Schuwirth et al (2016), [11] Gardeström et al (2016), [12] Borgå et al (2001), [13] Fu et al (2018), [14](Alexander et al, 2013),[15] (Rodrigues et al, 2018).…”