A Modeled Comparison of Direct and Food Web-Mediated Impacts of Common Pesticides on Pacific Salmon

<div><p>In the western United States, pesticides used in agricultural and urban areas are often detected in streams and rivers that support threatened and endangered Pacific salmon. Although concentrations are rarely high enough to cause direct salmon mortality, they can reach levels sufficient to impair juvenile feeding behavior and limit macroinvertebrate prey abundance. This raises the possibility of direct adverse effects on juvenile salmon health in tandem with indirect effects on salmon growth as a consequence of reduced prey abundance. We modeled the growth of ocean-type Chinook salmon (<i>Oncorhynchus tshawytscha</i>) at the individual and population scales, investigating insecticides that differ in how long they impair salmon feeding behavior and in how toxic they are to salmon compared to macroinvertebrates. The relative importance of these direct vs. indirect effects depends both on how quickly salmon can recover and on the relative toxicity of an insecticide to salmon and their prey. Model simulations indicate that when exposed to a long-acting organophosphate insecticide that is highly toxic to salmon and invertebrates (e.g., chlorpyrifos), the long-lasting effect on salmon feeding behavior drives the reduction in salmon population growth with reductions in prey abundance having little additional impact. When exposed to short-acting carbamate insecticides at concentrations that salmon recover from quickly but are lethal to invertebrates (e.g., carbaryl), the impacts on salmon populations are due primarily to reductions in their prey. For pesticides like carbaryl, prey sensitivity and how quickly the prey community can recover are particularly important in determining the magnitude of impact on their predators. In considering both indirect and direct effects, we develop a better understanding of potential impacts of a chemical stressor on an endangered species and identify data gaps (e.g., prey recovery rates) that contribute uncertainty to these assessments.</p></div

Matrix transition element and sensitivity and elasticity values.

1<p>Values calculated from data in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Johnson1" target="_blank">[32]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Howell1" target="_blank">[33]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Healey1" target="_blank">[35]</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Greene1" target="_blank">[39]</a>.</p

Relationships used to link anticholinesterase exposure to the abundance of prey.

<p>A) Step pulse of exposure to an anticholinesterase pesticide. B) Sigmoidal relationship between exposure concentration and relative prey abundance defined by control abundance (Pc), sigmoid slope (prey slope), prey EC₅₀, and a minimum abundance (prey floor, Pf). C) Time course of prey abundance in response to a step exposure. Pc denotes the control prey abundance before the exposure. Pi denotes the reduced prey abundance at the start of the exposure.</p

List of values used for control parameters to model organismal growth and the model sensitivity to changes in the parameter.

1<p>mean value of a normal distribution used in the model or constant value when no corresponding error is listed.</p>2<p>standard deviation of the normal distribution used in the model.</p>3<p>mean sensitivity when baseline parameter is changed over range of 0.5 to 2-fold, S =  (change in final/baseline weight)/(change in parameter/baseline parameter).</p>4<p>other values relative to control.</p>5<p>derived from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Sandahl1" target="_blank">[4]</a>.</p>6<p>derived from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Brett1" target="_blank">[31]</a>.</p>7<p>data from Brett et al. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Brett1" target="_blank">[31]</a> has no variability (ration was the independent variable) so a variability of 1% was selected to introduce some variability.</p>8<p>consistent with field-collected data for juvenile Chinook <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Nelson1" target="_blank">[64]</a>.</p>9<p>estimated from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Ferrari1" target="_blank">[9]</a>.</p>10<p>0.25 days consistent with <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Labenia1" target="_blank">[8]</a>; 30 days from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Chambers1" target="_blank">[65]</a>.</p>11<p>range estimated from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Wallace1" target="_blank">[21]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Cuffney1" target="_blank">[41]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-VandenBrink2" target="_blank">[43]</a>.</p>12<p>range estimated from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Colville1" target="_blank">[24]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-VandenBrink2" target="_blank">[43]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Ward1" target="_blank">[44]</a>.</p>13<p>derived from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Brett1" target="_blank">[31]</a> and adapted for ocean-type Chinook.</p

Effects concentrations (μg/L) and slopes for salmon AChE activity, and prey abundance dose-response curves for several organophosphate (OP) and carbamate (CB) insecticides.

<p>The ratio of the AChE EC₅₀ to prey EC₅₀ illustrates the relative sensitivities of the salmon AChE activity and their prey abundances to the insecticide. Salmon AChE values are from Laetz et al. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436-Laetz2" target="_blank">[29]</a>. Details of how prey abundance values were derived are given in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone.0092436.s001" target="_blank">Supporting Information S1</a>.</p

Effect of sustained or pulsed exposure on prey abundance.

<p>Prey available per day (relative to control) for juvenile ocean-type Chinook salmon in scenarios in which fish and prey were exposed to carbaryl at the prey EC₅₀ (4.33 μg/L) for either 1, 16-day pulse starting at day 30 (dates noted by dotted line), or 4, 4-day pulses starting on days 2, 30, 58 and 86 (noted by solid lines). Prey floor and prey recovery rates were intermediate (0.2 and 1% per day, respectively) for both scenarios. Model output indicated %Δλs for 1, 16-day and 4, 4-day exposure scenarios were –3 (9.8) and –12 (8.9), respectively.</p

Model scenarios and the questions they aim to address.

<p>Parameters that were changed in each scenario are in bold.</p

Effect of prey recovery rate and prey floor on salmon population growth rates.

<p>Mean percent change in lambda (on the y-axes) between modeled populations of unexposed ocean-type Chinook salmon and those exposed to a single, 4-day exposure per generation of a carbamate insecticide (e.g., carbaryl). The nine scenarios vary in the prey recovery and prey floor parameters (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0092436#pone-0092436-t003" target="_blank">Table 3</a>). Prey recovery rates were 0.5%, 1% and 5% per day, or slow, intermediate and fast, respectively. Prey floors were 0.05, 0.20 and 0.50, or low, intermediate and high, respectively. The vertical dotted line in each panel marks where the exposure concentration equals the EC₅₀ of the prey (4.33 μg/L for carbaryl).</p

Relationships linking anticholinesterase exposure to individual ration and growth rate.

<p>A&B) Relationships describing the time course of the effects of exposure on the organisms ability to capture food (A, potential ration) and the availability of food (B, relative prey abundance). C) Linear model linking final ration (potential ration times relative prey abundance) to growth rate using a line passing through the control condition with a slope denoted by Mgr. D) Time course for effect of exposure on individual growth rate produced by combining A, B, & C. See text for details. Closed circles represent the control condition just prior to exposure, and open circles (e.g. Ai) represent the exposed (inhibited) condition at the end of the exposure.</p

Change in salmon population growth rates due to direct and indirect effects of pesticides.

<p>Mean percent change in population growth rates (%Δλ) between unexposed ocean-type Chinook salmon and those exposed to a single, 4-day exposure per generation of chlorpyrifos (A), diazinon (B), carbaryl (C), and a hypothetical carbamate (D) as generated by the model. Scenarios for each insecticide include one with only the direct effects on salmon and another with effects on both salmon and their prey.</p