Copper Pollution Increases the Relative Importance of Predation Risk in an Aquatic Food Web

Abstract

Although the cascading impact of predators depends critically on the relative role of lethal predation and predation risk, we lack an understanding of how human-caused stressors may shift this balance. Emergent evidence suggests that pollution may increase the importance of predator consumptive effects by weakening the effects of fear perceived by prey. However, this oversimplification ignores the possibility that pollution may also alter predator consumptive effects. In particular, contaminants may impair the consumptive effects of predators by altering density-dependent interactions among prey conspecifics. No study has directly compared predator consumptive and non-consumptive effects in polluted versus non-polluted settings. We addressed this issue by using laboratory mesocosms to examine the impact of sublethal doses of copper on tri-trophic interactions among estuarine predator crabs Cancer productus, carnivorous whelk prey Urosalpinx cinerea, and the basal resource barnacles Balanus glandula. We investigated crab consumptive effects (whelks culled without crab chemical cues), non-consumptive effects (whelks not culled with crab chemical cues), and total effects (whelks culled with crab chemical cues) on whelks in copper polluted and non-polluted waters. Realistic copper concentrations suppressed the effects of simulated crab lethal predation (whelk culling) by removing density-dependent feeding by whelks. Specifically, reductions in conspecific density occurring in elevated copper levels did not trigger the normal increase in whelk consumption rates of barnacles. Weakened effects of fear were only observed at extremely high copper levels, suggesting consumptive effects were more sensitive to pollution. Thus, pollution may shape communities by altering the roles of predators and interactions among prey.

Fig 1. Effects of whelk conspecific density on whelk consumption rates.

Mean (±SEM) per capita whelk consumption of barnacles in 1, 2, 5, and 10 whelk density treatments (n = 5) after seven days. Different letters indicate significantly different groups (Tukey HSD tests, p < 0.05).

Fig 2. Effects of crab predator and copper concentrations on whelk consumption rates.

Mean (±SEM) total number of barnacles consumed by whelks under No Crab (empty circles; n = 5) and Crab (filled circles; n = 5) treatments when exposed to five different copper concentration treatments (n = 5). R² and p-values are from a linear regression of the five copper concentrations with either No Crab (solid line) or Crab (dashed line) treatments. Dashed line for Crab treatments shown for clarity although not a statistically significant regression.

Fig 3. Effects of copper, crab predator, and culling on whelk consumption rates.

Mean (±SEM) per capita whelk consumption of barnacles under Copper (No Copper, Copper; n = 5), Crab (Crab, No Crab; n = 5), and Culling (Cull, No Cull; n = 5) treatments. Empty bars represent No Copper treatments. Filled bars represent 50 ppb Copper treatments. Per capita whelk consumption of barnacles was calculated as total number of barnacles consumed by whelks divided with the average number of experimental whelks in each replicate. Different letters indicate significantly different groups (Tukey HSD tests, p < 0.05).

Fig 4. Effects of copper and crab predator effect type on whelk consumption rates.

Mean (±SEM) effect size of crab predator Consumptive Effects (whelk culling, CE; n = 5), Non-Consumptive Effects (crab cues, NCE; n = 5), and Total Effects (crabs cues and whelk culling, TE; n = 5) calculated with per capita whelk consumption of barnacles. Empty bars represent No Copper treatments (n = 5). Filled bars represent 50 ppb Copper treatments (n = 5). Different letters indicate significantly different groups (Tukey HSD tests, p < 0.05).