Twice as easy to catch? A toxicant and a predator cue cause additive reductions in larval amphibian activity

Authors

  • Mari K. Reeves,

    Corresponding author
    1. United States Fish and Wildlife Service, Anchorage Fisheries and Ecological Services Office, 605 West 4th Avenue, Room G-61, Anchorage, Alaska 99501 USA
    2. Graduate Group in Ecology and Department of Environmental Science and Policy, University of California, 1 Shields Avenue, Davis, California 95616 USA
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  • Margaret Perdue,

    1. United States Fish and Wildlife Service, Anchorage Fisheries and Ecological Services Office, 605 West 4th Avenue, Room G-61, Anchorage, Alaska 99501 USA
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  • Gareth D. Blakemore,

    1. United States Fish and Wildlife Service, Anchorage Fisheries and Ecological Services Office, 605 West 4th Avenue, Room G-61, Anchorage, Alaska 99501 USA
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  • Daniel J. Rinella,

    1. Environment and Natural Resources Institute and Alaska Natural Heritage Program, University of Alaska, 3211 Providence Drive, Anchorage, Alaska 99508 USA
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  • Marcel Holyoak

    1. Graduate Group in Ecology and Department of Environmental Science and Policy, University of California, 1 Shields Avenue, Davis, California 95616 USA
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  • Corresponding Editor: J. Benstead.

Abstract

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.

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