RAMIFICATIONS OF PREDATOR AVOIDANCE: PREDATOR AND HEAVY- METAL-MEDIATED COMPETITION BETWEEN TADPOLES AND SNAILS

We examined how the effects of competition between snails (Lymnaea pulustris) and Columbia spotted frog (Rana luteiventris) tadpoles are mediated by predatory bluegill sunfish (Lepomis macrochirus) and heavy metals. We raised snails and tadpoles in outdoor mini-ecosystems containing lead-, zinc-, and cadmium-contaminated soil from the EPA Superfund site in the Silver Valley of northern Idaho. To some treatments we added water from the tanks of sunfish that had fed on tadpoles and snails. Unexpected indirect effects occurred in polluted environments. We found a habitat shift by snails and tadpoles due to the response of tadpoles to predaceous fish odor. This shift decreased tadpole ingestion of metal-rich sediments and increased metal ingestion by snails. Heavy metals and fish odor therefore altered competitive interactions between snails and tadpoles. Metal-exposed tadpoles metamorphosed at an older age than non-metal-exposed animals. Metal exposure did not affect snail survival, growth, or recruitment. In the absence of heavy metals tadpoles reduced snail recruitment. Because heavy metals disproportionately harmed tadpoles, the negative effects of tadpoles on snails were ameliorated in polluted environments. The presence of snails did not alter tadpole development but did increase metal loads in tadpoles. We also tested the ability of snails to detect and respond to chemical cues emanating from crushed snails, an extract of crushed snails, and sunfish. Snails changed their behavior in response to crushed snails, but not to sunfish. Heavy-metal-exposed snails did not alter their behavior. Tadpoles altered their behavior when exposed to sunfish that had fed on tadpoles but did not respond to sunfish that had not fed on tadpoles. We found that heavy metal toxicants and predator odor cause behavioral changes and can alter competitive interactions between snails and tadpoles. We also showed that, due to indirect effects, pollution exposure for a given species may be modified both by the presence of competitors, and also by species that are neither competitors nor perceived as predators.