Hugh Lefcort

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.

Disease, predator avoidance, and vulnerability to predation in tadpoles

Many parasites alter the behaviour of their hosts. In most systems that have been studied, predation of the intermediate host by the definitive host is necessary for parasite transmission. Directly transmitted parasites have been studied less frequently and the fitness benefits from altering host behaviours that lead to the death of the host are not obvious. We examined the behavioural and ecological effects of the yeast Candida humicola, a directly transmitted parasite species in its natural host, the red-legged frog (Rana aurora). This parasite dies if its host dies. We used a mixture of field and laboratory experiments to test : 1) if infected tadpoles have altered thermal preferences (behavioural fevers), 2) the ability of infected tadpoles to detect and respond to chemical cues from predacious roughskinned newts (Taricha granulosa) and 3) the susceptibility of infected tadpoles to predation by newts. We found that infected tadpoles exhibited altered thermoregulatory behaviour, exhibited reduced ability to differentiate chemical cues of potentially dangerous from innocuous predators, and suffered increased predation. Behavioural by-products of the host response to infection may provide a mechanism by which behavioural alterations occur in some one and two-host parasite systems. Physiological changes associated with the host response to infection fight disease organisms, but behavioural aspects of the response may have negative effects on host survival.

ANTIPREDATORY BEHAVIOUR OF FEVERISH TADPOLES: IMPLICATIONS FOR PATHOGEN TRANSMISSION

In this paper we propose the hypothesis that pathogen-induced host defense responses result in altered host behaviors and enhanced predation. In particular we examine the effects of the acute phase response (whose effects include fever, reduced activity and malaise) on antipredatory behavior in bullfrog (Rana catesbeiana) tadpoles. This host response is associated with the preliminary stages of infection with many pathogens yet its behavioral effects have received little attention. Bullfrog tadpoles were injected with alcohol-killed bacteria to induce a response to infection and their ability to detect and avoid capture by predatory salamanders (Taricha granulosa) was explored. We predicted that acute phase responses increase tadpole vulnerability to predation by influencing thermoregulatory behavior and their ability to detect, and avoid capture by, salamanders. We found that the sterotypical effects of the acute phase response can lead to increased predation. Malaise affected the refuge seeking behavior of the tadpoles in the presence of salamanders. We suggest that for tadpoles provided with refuges, altered behaviors are a liability. This endogenous response may afford some parasites a potential pathway to their next host.

Hormetic Effects of Heavy Metals in Aquatic Snails: Is a Little Bit of Pollution Good?

Hormesis is the term to describe a stimulatory effects associated with a low dose of a potentially toxic substance or stress. We had anecdotal evidence of hormetic effects in some of our previous experiments concerning the influence of heavy metals on aquatic snail growth and recruitment. We therefore repeated a version of an earlier experiment but this time we expanded our low-dose treatments and increased our sample size. We also explored if metals had a hormetic effect on algae periphyton. We raised snails in outdoor mini-ecosystems containing lead, zinc, and cadmium-contaminated soil from an Environmental Protection Agency Superfund site in the Silver Valley of northern Idaho. The snails came from two sites. One population (Physella columbiana) has evolved for 120 years in the presence of heavy metals and one (Lymnaea palustris) has not. We found that P. columbiana exhibited hormesis with snails exposed to small amounts of metals exhibiting more reproduction and growth than snails not exposed to metals. Naturally occurring Oscillatoria algae also exhibited a hormetic effect of heavy metals but L. palustris did not display hormesis. Large doses negatively impacted all three species. Overall the levels of cadmium, lead, and zinc measured in the tissues of the snails were inversely correlated to the number of snails recruited into the tub populations. Only in comparisons of the lowest metal treatment to the control treatment is a positive effect detected. Indirect effects on competing species of snails, periphyton, and also fishermen, may be less favorable.

Terrestrial snails use predator-diet to assess danger

Some aquatic snails are able to use chemical cues (kairomones) to differentiate between predators that have fed on snails and predators that have eaten other prey. However, it is unknown if terrestrial snails are able to differentiate between snail-fed predators and predators that have not recently consumed snails. Here we document diet-based chemical discrimination of a predator, the ground beetle Carabus carabus, by a terrestrial snail Theba pisana. When exposed to the feces of snail-fed beetles, snails initially stopped all movements and then increased climbing speed. The snails also decreased the time to deposition of their egg clutch. The snails did not react to an extract of crushed snails. Snails had only a partial reaction to the feces of beetles that had fed on chicken (Gallus domesticus) livers—they decreased climbing speed but did not alter egg laying times. These responses may be adaptive in that they allow snails to differentiate between individual beetles that may pose an immediate threat and beetles that may not. This is one of only a few studies to examine predator-diet effects on reproductive behavior.

Toad tadpole kin recognition: recognition of half siblings and the role of maternal cues

In laboratory experiments, western toad (Bufo boreas) tadpoles preferentially associated with full siblings over paternal half siblings and with maternal half siblings over non-siblings. Tadpoles did not distinguish between full siblings and maternal half siblings or between paternal half siblings and non-siblings. These results suggest a maternal component to kin recognition. However, maternal half siblings were not preferred over paternal half siblings. Therefore, the effect of maternal cues may be complex. B. boreas tadpoles can probably use both direct and indirect familiarity to discriminate between kin classes.

Pre-Exposure to Heavy Metal Pollution and the Odor of Predation Decrease the Ability of Snails to Avoid Stressors

Many organisms appear to exhibit adaptive cost–benefit behaviors that balance foraging, safety, and pollution avoidance. However, what if the cognitive facilities needed to make decisions are compromised by industrial pollutants? Are the resulting decisions altered? Similarly, does exposure to kairomones from predators alter an organism’s ability to avoid toxicants? Furthermore, how long an exposure is necessary: A few minutes, hours, or even a lifetime? We wondered if there was an interaction between the ability to respond to a predatory event and the ability to avoid heavy metals.

Life in a Near-Future Atmosphere: Carbon Dioxide Enrichment Increases Plant Growth and Alters the Behavior of a Terrestrial Snail but not a Terrestrial Beetle

Abstract In addition to effects on climate and water acidification, anthropogenic atmospheric releases of carbon dioxide may also directly impact terrestrial organisms that use CO 2 as a chemical cue. We wondered how common organisms would respond to near-future levels of CO 2 – levels that may occur by 2025. We chose two common but taxonomically and ecologically dissimilar organisms ( Theba pisana helicid snails and Adesmia dilatata tenebrionid beetles) to examine the behavioral effects of a slight rise (~10 ppm) of CO 2 on animal abundance and plant growth in the Negev Desert of Israel. We found that plots with supplementary CO 2 exhibited greater plant growth than control plots over a 50-day experiment, but increased growth did not alter beetle or snail numbers.In laboratory experiments with higher levels of augmented CO 2 paired with food rewards, we found that snails did not change their climbing behavior when presented with CO 2 alone, but they avoided food and climbed away when CO 2 was paired with food. Beetles in the laboratory were attracted to food regardless of CO 2 levels although high levels of CO 2 (1200–1300 ppm) reduced movement.The direct effects of near-future CO 2 levels may augment plant growth but have only minor influence on terrestrial snails and beetles. However, the effects of CO 2 on climate change in desert habitats like the Negev may be more severe due to a predicted rise in temperature and a decline in precipitation.