Aquatic Snails from Mining Sites Have Evolved to Detect and Avoid Heavy Metals

Abstract

Toxicants in polluted environments are often patchily distributed. Hence, rather than being passive absorbers of pollution, some organisms have evolved the ability to detect and avoid toxicants. We studied the avoidance behavior of Physella columbiana, an aquatic pulmonate snail, in a pond that has been polluted with heavy metals for more than 120 years. Populations of this snail are rare at reference sites and are only robust at heavy-metal-polluted sites. We hypothesized that the snails are able to persist because they have evolved the ability to minimize their exposure to metals by actively avoiding metals in their environment. Using a Y-maze flow tank, we tested the avoidance behavior of snails to heavy-metal-polluted sediments and single-metal solutions of cadmium, zinc, or lead. We also tested the avoidance behaviors of the snails' laboratory-reared offspring raised in nonpolluted conditions. In addition, we tested the avoidance behavior of a small population of snails from a reference pond. Although all the snails we tested were able to detect low concentrations of heavy metals, we found that snails from the polluted site were the most sensitive, that their offspring were somewhat less sensitive, and that snails from the reference site were the least sensitive. This suggests that the ability of polluted-site snails to avoid heavy metals is both genetic and environmental. The concentrations of metals avoided by the snails from the polluted site were below the levels found at hot spots within their natal pond. The snails may be able to persist at this site because they decrease their exposure by moving to less-polluted sections of the pond. One application of our findings is the use of aquatic snails and our Y-maze design as an inexpensive pollution detector. Environmental pollutants such as lead, zinc, and arsenic are a problem throughout the world. People in underdeveloped countries often lack sophisticated pollution detection devices. We have developed a behavioral assay of aquatic pollution that is easy to use, is extremely sensitive (detection below 10 ppb), and can be constructed for fewer than 100 US dollars. Pulmonate snails are widely distributed in tropical, subtropical, and temperate parts of the globe, and they are often common in polluted waters. For countries such as India and Bangladesh, which must test thousands of shallow wells for possible contamination with heavy metals, our assay would be a good initial test. Once snails detected metals, then those samples could be confirmed by spectrometers. We encourage scientists in underdeveloped nations to consider our assay as an option.

Avoidance of contaminated sediments by an amphipod (Melita plumulosa), A harpacticoid copepod (Nitocra spinipes), and a snail (Phallomedusa solida)

“…Therefore, significant changes to crucial behavioral traits of an organism (e.g., foraging behavior, social interaction, and locomotion) may pose a threat to the survival of a population [4,5]. Behavioral traits can be exploited as toxicity test endpoints and, in some cases, have been demonstrated to be sensitive to contaminant exposure [6,7]. Consequently, behavioral endpoints are increasingly being considered to have high ecological relevance as contaminantinduced changes to an organism's behavior offer insight into potentially major environmental impacts [3].…”

“…In the natural environment, individual organisms, and eventually populations, will migrate away from a contaminated site before the exposure results in the uptake of a harmful dose (sublethal or lethal). Hence, avoidance behavior is a significant factor in determining the extent of exposure [4,6], the magnitude of the hazard, and the overall risk the sediment poses to ecosystem health. Avoidance is often a rapid and easily measurable response, with some suggesting that it is more sensitive than commonly used lethal and sublethal endpoints [6,7].…”

“…Hence, avoidance behavior is a significant factor in determining the extent of exposure [4,6], the magnitude of the hazard, and the overall risk the sediment poses to ecosystem health. Avoidance is often a rapid and easily measurable response, with some suggesting that it is more sensitive than commonly used lethal and sublethal endpoints [6,7]. Behavioral endpoints, such as avoidance, also have the advantage of providing an early warning to potential contamination which may result in lethal impacts [12].…”

“…Behavioral endpoints, such as avoidance, also have the advantage of providing an early warning to potential contamination which may result in lethal impacts [12]. Avoidance behavior has been investigated for a diverse range of aquatic organisms including fish [13], amphipods [9], cladocerans [7], aquatic snails [6], and bivalves [14]. These studies have all reported the usefulness of contaminant avoidance as a behavioral ecotoxicological endpoint.…”

“…Contaminant avoidance is likely to be a defense mechanism against the effect of poor environmental conditions, eliminating the threat to survival caused by the presence of toxicants [6]. Contaminant avoidance may also be an adaptive behavior [15].…”