An unforeseen chain of events: Lethal effects of pesticides at sublethal concentrations

Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania 15260 USA.
Ecological Applications (Impact Factor: 4.09). 11/2008; 18(7):1728-42. DOI: 10.1890/08-0454.1
Source: PubMed


The field of toxicology has traditionally assessed the risk of contaminants by using laboratory experiments and a range of pesticide concentrations that are held constant for short periods of time (1-4 days). From these experiments, one can estimate the concentration that causes no effect on survival. However, organisms in nature frequently experience multiple, applications of pesticides over time rather than a single constant concentration. In addition, organisms are embedded in ecological communities that can propagate indirect effects through a food web. Using outdoor mesocosms, we examined how low concentrations (10-250 microg/L) of a globally common insecticide (malathion) applied at various amounts, times, and frequencies affected aquatic communities containing zooplankton, phytoplankton, periphyton, and larval amphibians (reared at two densities) for 79 days. All application regimes caused a decline in zooplankton, which initiated a trophic cascade in which there was a bloom in phytoplankton and, in several treatments, a subsequent decline in the competing periphyton. The reduced periphyton had little effect on wood frogs (Rana sylvatica), which have a short time to metamorphosis. However, leopard frogs (Rana pipiens) have a longer time to metamorphosis, and they experienced large reductions in growth and development, which led to subsequent mortality as the environment dried. Hence, malathion (which rapidly breaks down) did not directly kill amphibians, but initiated a trophic cascade that indirectly resulted in substantial amphibian mortality. Importantly, repeated applications of the lowest concentration (a "press treatment" consisting of seven weekly applications of 10 microg/L) caused larger impacts on many of the response variables than single "pulse" applications that were 25 times as great in concentration. These results are not only important because malathion is the most commonly applied insecticide and is found in wetlands, but also because the mechanism underlying the trophic cascade is common to a wide range of insecticides, offering the possibility of general predictions for the way in which many insecticides impact aquatic communities and the populations of larval amphibians.

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    • "However, despite the relative lack of toxicity of malathion to macroarthropods in this study, malathion concentrations of 101 lg/L were sufficient to significantly alter zooplankton community composition and ecosystem properties in mesocosms seeded with organisms from the same area as the current study (Halstead et al., 2014). Likewise, malathion has been observed to have lethal and sublethal effects on a variety of other aquatic organisms (Relyea and Diecks, 2008; Rohr et al., 2008a; USEPA, 2014b; Verbruggen and van den Brink, 2010). Toxicity of organophosphates or pyrethroids to B. flumineum has not been previously reported. "
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    ABSTRACT: As agricultural expansion and intensification increase to meet the growing global food demand, so too will insecticide use and thus the risk of non-target effects. Insecticide pollution poses a particular threat to aquatic macroarthropods, which play important functional roles in freshwater ecosystems. Thus, understanding the relative toxicities of insecticides to non-target functional groups is critical for predicting effects on ecosystem functions. We exposed two common macroarthropod predators, the crayfish Procambarus alleni and the water bug Belostoma flumineum, to three insecticides in each of two insecticide classes (three organophosphates: chlorpyrifos, malathion, and terbufos; and three pyrethroids: esfenvalerate, λ-cyhalothrin, and permethrin) to assess their toxicities. We generated 150 simulated environmental exposures using the US EPA Surface Water Contamination Calculator to determine the proportion of estimated peak environmental concentrations (EECs) that exceeded the US EPA level of concern (0.5×LC50) for non-endangered aquatic invertebrates. Organophosphate insecticides generated consistently low-risk exposure scenarios (EECs<0.5×LC50) for both P. alleni and B. flumineum. Pyrethroid exposure scenarios presented consistently high risk (EECs>0.5×LC50) to P. alleni, but not to B. flumineum, where only λ-cyhalothrin produced consistently high-risk exposures. Survival analyses demonstrated that insecticide class accounted for 55.7% and 91.1% of explained variance in P. alleni and B. flumineum survival, respectively. Thus, risk to non-target organisms is well predicted by pesticide class. Identifying insecticides that pose low risk to aquatic macroarthropods might help meet increased demands for food while mitigating against potential negative effects on ecosystem functions. Copyright © 2015. Published by Elsevier Ltd.
    Chemosphere 05/2015; 135:265-271. DOI:10.1016/j.chemosphere.2015.03.091 · 3.34 Impact Factor
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    • "Although the effects of biocides and pesticides, in general, on single or multiple species at micro and mesocosm experiments are well described in the literature (e.g. Cripe, 1994; Boone et al., 2004; Emmanuel et al., 2004; Relyea and Diecks, 2008; Tlili et al., 2011), the effects of such toxicants on community structure level are rarely assessed (Beketov and Liess, 2012) (but see e.g. Rohr and Crumrine, 2005; Schaefer et al., 2007), despite numerous pleas for a shift in this approach (e.g. "
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    ABSTRACT: Contamination is a particular harmful type of chemical disturbance and predicting their effects on natural systems is very complex. Effects of disturbances vary in space and time and depend, among other things, on the type and age of organisms, the habitat being studied and the complex interactions occurring in the systems. Most impact analyses of contaminants are however still done with limited number of selected organisms under laboratory conditions. Manipulative experiments done in situ are important to measure ecologically relevant responses of contaminant effects on marine systems. Ecological approaches on contamination studies, accounting for interactions among species and the environment are essential to understand how such disturbances affect systems. We evaluated the effects of bleach and permethrin, two common and pervasive contaminants, on intertidal benthic assemblages in two different successional stages, mature and young. There were no impacts on the overall structure of assemblages, regardless of their age. The lack of effects on the structure of assemblages might be due to the intrinsic characteristic of the habitat studied, which provide few sinks for contaminants, as well as the inherent features of the organisms themselves. Bleach did cause, however, a decrease in the abundance of limpets, which can have further consequences to these systems. This study shows the importance of studies on chemical disturbances done under relevant natural scenarios and that efficient management policies of natural systems will only achieve successful responses with properly designed experiments under natural conditions.
    Science of The Total Environment 02/2015; 506-507:10-17. DOI:10.1016/j.scitotenv.2014.10.095 · 4.10 Impact Factor
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    • "However, the present results contrast with those of several studies on repeated exposure in zooplankton (Daam et al. 2008; Hanazato and Yasuno 1990) and amphibians (Boone et al. 2001; Relyea and Diecks 2008). For example, a study on frogs comparing single and multiple exposures showed that small weekly applications of the insecticide malathion caused greater impacts on many of the examined response variables than single-pulse applications at a 25-fold higher concentration (Relyea and Diecks 2008). This finding was explained by the fact that the multiple pulses held the community in a state of continued disturbance, which further reinforced the trophic cascade initiated by the direct toxic effect of the insecticide on the zooplankton assemblage in the community. "
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    ABSTRACT: Ecosystems are subject to a combination of recurring anthropogenic and natural disturbances, such as climate change and pesticide exposure. Biological com- munities are known to develop tolerance to recurring dis- turbances due to successive changes at both the community and organismal levels. However, information on how additional stressors may affect the development of such community tolerance is scarce to date. We studied the influence of hydrological disturbance on the reaction of zooplankton communities to repeated insecticide pulses in outdoor microcosms. The communities were exposed to three successive pulses of the insecticide esfenvalerate (0.03, 0.3, and 3 lg/L) and to the gradual removal of water and its subsequent replacement over three cycles or to a constant water level. Except at the highest esfenvalerate concentration, the communities developed tolerance to the toxicant, as indicated by their decreasing reaction to sub- sequent insecticide applications, and this development was enhanced by hydrological disturbance. The pronounced decline of the key taxa Daphnia spp. through the combined action of the two stressors was identified as the main mechanism responsible for the increase in community tolerance under a fluctuating water level. Under a constant water level, the abundance of Daphnia spp. did not decrease significantly without the insecticide treatment, indicating that other mechanisms were responsible for the observed community tolerance. The present study shows that additional stressors can facilitate the development of community tolerance and that such facilitation is propa- gated through community-level mechanisms.
    Ecotoxicology 11/2014; in press(9). DOI:10.1007/s10646-014-1308-5 · 2.71 Impact Factor
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