Toxicants may harm predators or prey differentially, hindering clear determination of multiple stressor effects on predation dynamics in polluted aquatic systems. We built on a prior field study in which we demonstrated that a chemical contaminant, copper (Cu) and odonate predators were correlated with more frequent observations of skeletal abnormalities in Alaskan wood frog (Rana sylvatica) tadpoles. Our prior study established a multiple stressor effect linked to an important environmental phenomenon (malformed amphibians) but did not provide clear mechanisms that might guide management. We here investigated behavioral mechanisms because of their potential to produce large changes in predation dynamics, and because in published studies low concentrations of Cu produced behavioral changes in predator-detection in fish. Surprisingly, low but environmentally relevant concentrations of Cu (5 μg/L) combined with chemical cues from a predator (Aeshna sitchensis) to produce large changes in the behavior of larval amphibians. Experiments demonstrated that a low concentration of Cu did not inhibit the ability of wood frog tadpoles to detect chemical cues of predators by olfactory means, but produced strong behavioral effects, causing tadpoles to reduce activity and alter microhabitat use. These results occurred with Cu at an exposure level lower than any we could find reported as toxic to amphibians in the literature. When Cu and predator cues were administered together, the activity reduction was additive and stronger at earlier life stages. We suggest that Cu intoxication would be disadvantageous to larval amphibian prey with prolonged exposure to predators during development, and we present field data from 2010 that support this assertion. Our study demonstrates the need to use sensitive behavioral assays and to investigate multiple stressor mechanisms to understand how multiple threats combine to affect organisms in nature.