Ecological Stoichiometry for Parasitologists.

Ecological stoichiometry (ES) is an ecological theory used to study the imbalances of chemical elements, ratios, and flux rates among organisms and the environment to better understand nutrient cycling, energy flow, and the role of organisms in ecosystems. Parasitologists can use this framework to study phenomena across biological scales from genomes to ecosystems. By using the common currency of elemental ratios such as carbon:nitrogen:phosphorus, parasitologists are beginning to explicitly link parasite-host interactions to ecosystem dynamics. Thus, ecological stoichiometry provides a framework for studying the feedbacks of parasites on the environment as well as the effects of the environment on parasites and disease.

Parasite and host elemental content and parasite effects on host nutrient excretion and metabolic rate.

Ecological stoichiometry uses the mass balance of elements to predict energy and elemental fluxes across different levels of ecological organization. A specific prediction of ecological stoichiometry is the growth rate hypothesis (GRH), which states that organisms with faster growth or reproductive rates will require higher phosphorus content for nucleic acid and protein synthesis. Although parasites are found ubiquitously throughout ecosystems, little is understood about how they affect nutrient imbalances in ecosystems. We (1) tested the GRH by determining the carbon (C), nitrogen (N), and phosphorus (P) content of parasitic trematodes and their intermediate host, the freshwater snail Elimia livescens, and (2) used this framework to determine the trematode effects on host nutrient excretion and metabolism. Snail and parasite tissues were analyzed for elemental content using a CHN analyzer and soluble reactive phosphorus (SRP) methods. Ammonium and SRP assays were used to estimate N and P excretion rates. A respirometer was used to calculate individual snail metabolism. Trematode tissues contained lower C:P and N:P (more P per unit C and N) than the snail tissues. Snail gonadal tissues more closely resembled the elemental content of parasite tissues, although P content was 13% higher in the gonad than the trematode tissues. Despite differences in elemental content, N and P excretion rates of snails were not affected by the presence of parasites. Parasitized snails maintained faster metabolic rates than nonparasitized snails. However, the species of parasite did not affect metabolic rate. Together, this elemental imbalance between parasite and host, and the altered metabolic rate of infected snails may lead to broader parasite effects in stream ecosystems.

The effects of the psychiatric drug carbamazepine on freshwater invertebrate communities and ecosystem dynamics.

Freshwater ecosystems are persistently exposed to pharmaceutical pollutants, including carbamazepine. Despite the ubiquity and recalcitrance of carbamazepine, the effects of this pharmaceutical on freshwater ecosystems and communities are unclear. To better understand how carbamazepine influences the invertebrate community and ecosystem dynamics in freshwaters, we conducted a mesocosm experiment utilizing environmentally relevant concentrations of carbamazepine (200 and 2000 ng/L). Mesocosms were populated with four gastropod taxa (Elimia, Physa, Lymnaea and Helisoma), zooplankton, filamentous algae and phytoplankton. After a 31 d experimental duration, structural equation modeling (SEM) was used to relate changes in the community structure and ecosystem dynamics to carbamazepine exposure. Invertebrate diversity increased in the presence of carbamazepine. Additionally, carbamazepine altered the biomass of Helisoma and Elimia, induced a decline in Daphnia pulex abundance and shifted the zooplankton community toward copepod dominance. Lastly, carbamazepine decreased the decomposition of organic matter and indirectly altered primary production and dissolved nutrient concentrations. Changes in the invertebrate community occurred through both direct (i.e., exposure to carbamazepine) and indirect pathways (i.e., changes in food resource availability). These data indicate that carbamazepine may alter freshwater community structure and ecosystem dynamics and could have profound effects on natural systems.

Relationships between the psychiatric drug carbamazepine and freshwater macroinvertebrate community structure.

Pharmaceutical pollutants are commonly detected in surface waters and have the potential to affect non-target organisms. However, there is limited understanding of how these emerging contaminants may affect macroinvertebrate communities. The pharmaceutical carbamazepine is ubiquitous in surface waters around the world and is a pollutant of particular concern due to its recalcitrance and toxicity. To better understand the potential effects of carbamazepine on natural macroinvertebrate communities, we related stream macroinvertebrate abundance to carbamazepine concentrations. Macroinvertebrate and water samples were collected from 19 streams in central Indiana in conjunction with other stream physiochemical characteristics. Structural equation modeling (SEM) was used to relate macroinvertebrate richness to carbamazepine concentrations. Macroinvertebrate richness was positively correlated with increasing concentrations of carbamazepine. From the SEM we infer that carbamazepine influences macroinvertebrate richness through indirect pathways linked to Baetidae abundance. Baetidae abundance influenced ephemeropteran abundance and FBOM percent organic matter, both of which altered macroinvertebrate richness. The pharmaceutical carbamazepine may alter freshwater macroinvertebrate species composition, which could have significant consequences to ecosystem processes.

The effects of the pharmaceutical carbamazepine on life history characteristics of flat-headed mayflies (Heptageniidae) and aquatic resource interactions.

Pharmaceutical pollutants are commonly detected in freshwater ecosystems around the world and have biological effects on aquatic organisms. However, current understanding of the influence this contaminant class has on freshwater communities and ecosystems is lacking. Recently the scientific community has called for research focusing on certain pharmaceuticals due to their ubiquity and potential toxicity. Carbamazepine is one of these pharmaceuticals. To better understand the effect carbamazepine has on life history characteristics of aquatic organisms and consumer-resource interactions, we quantified the influence of carbamazepine on the development, growth and behavior of mayfly nymphs (Stenonema sp.) and the alterations in food consumer-resource interactions between Stenonema and algae (Chaetophora). Microcosms were assembled in a factorial design containing algae and mayfly nymphs native to central Indiana and dosed with environmentally relevant concentrations of carbamazepine. From this ecotoxicological experiment we were able to infer that carbamazepine at 2,000 ng/L influenced the development and behavior of Stenonema nymphs and the body dimensions of adult individuals. However, it appears that carbamazepine does not influence consumer-resource interactions at concentrations found in surface waters. The pharmaceutical carbamazepine may influence the behavior, growth and development of mayflies, which could have significant consequences at the population, community and ecosystem level.

The influence of TCS on the growth and behavior of the freshwater snail, Physa acuta.

Triclosan (TCS) is among the top 10 most persistent contaminants found in U.S. rivers, streams, lakes, and aquifers. Although TCS has not been found to be hazardous to humans, it can be toxic to aquatic environments and animals. The effects of TCS on growth rates and the locomotive behavior of the freshwater snail, Physa acuta, were studied by exposing snails to a range of environmentally-relevant trace concentrations previously documented in freshwater ecosystems. Effects of TCS on snail growth were calculated using a non-linear regression model, and effects on behavior were determined using a two-way analysis of variance. Environmentally relevant concentrations of TCS (0.5 to 1.0 µg/L) enhanced Physa growth rates at low concentrations, but slowed growth rates at concentrations greater than 5 µg/L. Acute exposure did not affect immediate snail behavior; however, chronically exposed snails moved more slowly than naïve snails. These data indicate that concentrations of TCS currently found in freshwater ecosystems can potentially affect the growth and behavior of snails.

Effects of ionic liquids on the survival, movement, and feeding behavior of the freshwater snail, Physa acuta.

Room-temperature ionic liquids (ILs) are being promoted as environmentally friendly alternatives to volatile organic solvents currently used by industry. Because ILs are novel and not yet in widespread use, their potential impact on aquatic organisms is unclear. We studied the effects of several ILs on the survivorship and behavior (movement and feeding rates) of the freshwater pulmonate snail, Physa acuta. Median lethal concentrations (LC50s) of ILs with imidazolium- and pyridinium-based cations and Br- and PF6- as anions ranged from 1 to 325 mg/L. Toxicity was greatest for ILs with eight-carbon alkyl chains attached to both imidazolium and pyridinium rings and declined with shorter alkyl chains, indicating a positive relationship between alkyl chain length and toxicity. Compared to controls, snails moved more slowly when exposed to butyl- and hexyl-cation ILs at 1 to 3% of LC50 concentrations but were not affected at higher IL concentrations (4-10% of LC50), which is characteristic of U-shaped dose-response curves. Snail movement was not affected by ILs with octyl alkyl groups. Grazing patterns, however, indicated that snails grazed less at higher IL concentrations. Physa acuta egestion rates were reduced in the presence of ILs at 3 to 10% of LC50 concentrations. Thus, nonlethal IL concentrations affected P. acuta behaviors, potentially impacting individual fitness and food web interactions. These results provide initial information needed to assess the potential hazards of ILs should they reach freshwater ecosystems.

Acute and chronic toxicity of imidazolium-based ionic liquids on Daphnia magna.

Room-temperature ionic liquids (ILs) are considered to be green chemicals that may replace volatile organic solvents currently used by industry. However, IL effects on aquatic organisms and ecosystems are currently unknown. We studied the acute effects of imidazolium-based ILs on survival of the crustacean Daphnia magna and their chronic effects on number of first-brood neonates, total number of neonates, and average brood size. Lethal concentrations of imidazolium ILs with various anions (X-) ranged from a median lethal concentration (LC50) of 8.03 to 19.91 mg L(-1), whereas salts with a sodium cation (Na+ X-) were more than an order of magnitude higher (NaPF6 LC50, 9,344.81 mg L(-1); NaBF4 LC50, 4765.75 mg L(-1)). Thus, toxicity appeared to be related to the imidazolium cation and not to the various anions (e.g., Cl-, Br-, PF6-, and BF4-). The toxicity of imidazolium-based ILs is comparable to that of chemicals currently used in manufacturing and disinfection processes (e.g., ammonia and phenol), indicating that these green chemicals may be more harmful to aquatic organisms than current volatile organic solvents. We conducted 21-d chronic bioassays of individual D. magna exposed to nonlethal IL concentrations at constant food-resource levels. Daphnia magna produced significantly fewer total neonates, first-brood neonates, and average neonates when exposed to lower concentrations (0.3 mg L(-1)) of imidazolium-based ILs than in the presence of Na-based salts at higher concentrations (400 mg L(-1)). Such reductions in the reproductive output of Daphnia populations could cascade through natural freshwater ecosystems. The present study provides baseline information needed to assess the potential hazard that some ILs may pose should they be released into freshwater ecosystems.

Predator identity and trait-mediated indirect effects in a littoral food web.

Perturbations to the density of a species can be propagated to distant members of a food web via shifts in the density or the traits (i.e. behavior) of intermediary species. Predators with differing foraging modes may have different effects on prey behavior, and these effects may be transmitted differently through food webs. Here we test the hypothesis that shifts in the type of predator present in a food web indirectly affect the prey's resource independent of changes in the density of prey. We assessed the importance of predator identity in mediating the grazing effects of the freshwater snail Physa integra on its periphyton resources using field and mesocosm studies. Field observations showed that Physa used covered habitats more in ponds containing fish than in ponds containing crayfish or no predators at all. A field experiment confirmed that snail behavior depended on predator identity. Physa placed near caged pumpkinseed sunfish (Lepomis gibbosus) selected covered habitats, but Physa placed near caged crayfish (Orconectes rusticus) moved to the surface of the water. The effects of predator identity on periphtyon were then examined in a mesocosm experiment, using caged predators. Habitat use of Physa was similar to their habitat use in the field experiment. In the presence of caged sunfish, periphyton standing crop in covered habitats was reduced to 34% of the standing crop in the presence of crayfish. In contrast, periphyton in near-surface habitats was 110% higher in the presence of fish than in the presence of crayfish. Thus, the effects of predator identity on Physa behavior cascaded through the food web to affect the abundance and spatial distribution of periphyton.

Predator identity and consumer behavior: differential effects of fish and crayfish on the habitat use of a freshwater snail.

Predators can alter the outcome of ecological interactions among other members of the food web through their effects on prey behavior. While it is well known that animals often alter their behavior with the imposition of predation risk, we know less about how other features of predators may affect prey behavior. For example, relatively few studies have addressed the effects of predator identity on prey behavior, but such knowledge is crucial to understanding food web interactions. This study contrasts the behavioral responses of the freshwater snail Physellagyrina to fish and crayfish predators. Snails were placed in experimental mesocosms containing caged fish and crayfish, so the only communication between experimental snails and their predators was via non-visual cues. The caged fish and crayfish were fed an equal number of snails, thereby simulating equal prey mortality rates. In the presence of fish, the experimental snails moved under cover, which confers safety from fish predators. However, in the presence of crayfish, snails avoided benthic cover and moved to the water surface. Thus, two species of predators, exerting the same level of mortality on prey, induced very different behavioral responses. We predict that these contrasting behavioral responses to predation risk have important consequences for the interactions between snails and their periphyton resources.