Ecosystem bioelement variability is associated with freshwater animal aggregations at the aquatic-terrestrial interface.

The impacts of animals on the biogeochemical cycles of major bioelements like C, N, and P are well-studied across ecosystem types. However, more than 20 elements are necessary for life. The feedbacks between animals and the biogeochemical cycles of the other bioelements are an emerging research priority. We explored how much freshwater mussels (Bivalvia: Unionoida) were related to variability in ecosystem pools of 10 bioelements (Ca, Cu, Fe, K, Mn, Na, Mg, P, S and Zn) in streams containing a natural mussel density gradient in the US Interior Highlands. We studied the concentrations of these bioelements across the aquatic-terrestrial interface-in the porewater of riverine gravel bars, and the emergent macrophyte Justicia americana. Higher mussel density was associated with increased calcium in gravel bars and macrophytes. Mussel density also correlated with variability in iron and other redox-sensitive trace elements in gravel bars and macrophytes, although this relationship was mediated by sediment grain size. We found that two explanations for the patterns we observed are worthy of further research: (1) increased calcium availability in gravel bars near denser mussel aggregations may be a product of the buildup and dissolution of shells in the gravel bar, and (2) mussels may alter redox conditions, and thus elemental availability in gravel bars with fine sediments, either behaviorally or through physical structure provided by shell material. A better understanding of the physical and biogeochemical impacts of animals on a wide range of elemental cycles is thus necessary to conserve the societal value of freshwater ecosystems.

Mussels and Local Conditions Interact to Influence Microbial Communities in Mussel Beds.

Microbiomes are increasingly recognized as widespread regulators of function from individual organism to ecosystem scales. However, the manner in which animals influence the structure and function of environmental microbiomes has received considerably less attention. Using a comparative field study, we investigated the relationship between freshwater mussel microbiomes and environmental microbiomes. We used two focal species of unionid mussels, Amblema plicata and Actinonaias ligamentina, with distinct behavioral and physiological characteristics. Mussel microbiomes, those of the shell and biodeposits, were less diverse than both surface and subsurface sediment microbiomes. Mussel abundance was a significant predictor of sediment microbial community composition, but mussel species richness was not. Our data suggest that local habitat conditions which change dynamically along streams, such as discharge, water turnover, and canopy cover, work in tandem to influence environmental microbial community assemblages at discreet rather than landscape scales. Further, mussel burrowing activity and mussel shells may provide habitat for microbial communities critical to nutrient cycling in these systems.

Animal aggregations promote emergent aquatic plant production at the aquatic-terrestrial interface.

The roles mobile animals and abiotic processes play as vectors for resource transfers between ecosystems ("subsidies") are well studied, but the idea that resources from animals with limited mobility may be transported across boundaries through intermediate taxa remains unexplored. Aquatic plants ("macrophytes") are globally distributed and may mediate transfers of aquatic-derived nutrients from aggregations of aquatic animals to terrestrial ecosystems when consumed by terrestrial herbivores. We used mesocosms (94 × 44 cm) to test whether aquatic animal-generated biogeochemical hotspots increase growth and nutrient content in macrophytes using the macrophyte Justicia americana and freshwater mussels. Justicia americana biomass production increased and belowground biomass allocation changed with increasing mussel density. At high mussel density, water-column phosphorus increased and carbon:phosphorus ratios in J. americana tissues decreased. We deployed motion-sensing cameras to explore herbivory on J. americana growing along the margins of the Kiamichi River, Oklahoma, and documented feeding by large mammals (Odocoileus virginianus, Sus scrofa, and Bos taurus). Thus, biogeochemical hotspots generated by aquatic animal aggregations can promote macrophyte production that subsequently is transferred to terrestrial animals. More broadly, this suggests that reductions in aquatic animal biomass may have bottom-up impacts that indirectly affect terrestrial ecosystems via plant-animal interactions bridging ecosystem boundaries.

Overlapping anthropogenic effects on hydrologic and seasonal trends in DOC in a surface water dependent water utility.

Drinking water supplies are increasingly affected by overlapping anthropogenic global change processes. As a key currency of ecosystem function in aquatic ecosystems, dissolved organic carbon (DOC) concentration and composition is sensitive to many global change processes. However, DOC must also be removed to avoid the production of harmful disinfection byproducts as water is processed. Thus, understanding the effects of global change processes on the seasonal and long-term dynamics of DOC composition and concentration is critical for ensuring the sustainability of drinking water supplies. To understand these dynamics, we analyzed a novel 11-year time series of stream water DOC concentration and composition using Weighted Regressions on Time Discharge and Season (WRTDS) to understand the influences of co-occurring changes in climate and atmospheric deposition. We also discuss the implications for water supply provision and management. We found that, during our study period, overlapping global change processes in the watershed had the net effect of increasing the DOC aromaticity, as measured by SUVA254, at moderate to high discharge levels during the late spring and early summer and the autumn and early winter. However, changes in DOC concentration were more dynamic and we observed both increasing and decreasing trends depending on season and hydrologic state. During summer, at low to moderate flow levels we observed a significant (p < 0.05) increase in DOC concentration. During autumn, at moderate to high flow levels we observed a significant (p < 0.05) decrease in DOC concentration and an increase in SUVA254. For drinking water providers, our results suggest that close monitoring of source waters must be coupled with the development of plans accounting for season- and hydrology-specific long-term changes.

Biomass distribution of fishes and mussels mediates spatial and temporal heterogeneity in nutrient cycling in streams.

Animals can play important roles in cycling nutrients [hereafter consumer-driven nutrient dynamics (CND)], but researchers typically simplify animal communities inhabiting dynamic environments into single groups that are tested under relatively static conditions. We propose a conceptual framework and present empirical evidence for CND that considers the potential effects of spatially overlapping animal groups within dynamic ecosystems. Because streams can maintain high biomass of mussels and fish, we were able to evaluate this framework by testing if biogeochemical hotspots generated by stable aggregations of mussels attract fishes. We predicted that spatial overlap between these groups may increase the flux of mineralized nutrients. We quantified how different fish assemblage biomass was between mussel bed reaches and reaches without mussels. We compared fish and mussel biomass at mussel beds to test whether differences in animal biomass mediate their contributions to nutrient cycling through nitrogen and phosphorous excretion. We estimated areal excretion rates for each group by combining biomass estimates with measured excretion rates. Fish biomass was homogeneously distributed, except following a period of low flow when fish were more concentrated at mussel beds. Mussel biomass was consistently an order of magnitude greater than fish biomass and mussel areal excretion rates exceeded fish excretion rates. However, the magnitude of those differences varied spatially and temporally. Mussel excretion stoichiometry varied with changes in assemblage composition, while fish excretion stoichiometry varied little. Biogeochemical hotspots associated with mussels did not generally overlap with fish aggregations, thus, under these conditions, animal processes appear to exert additive ecosystem effects.

Trophic Strategies Influence Metal Bioaccumulation in Detritus-Based, Aquatic Food Webs.

Metal accumulation in aquatic food webs is mediated by physiochemical parameters of the environment and organismal traits. Trophic strategies influence an organisms' exposure to metal pollution, but links between trophic ecology and exposure to divalent metals are relatively understudied. While organically bound metals are typically considered unavailable for uptake, organisms directly consuming dissolved organic carbon (DOC) and bacteria-via the microbial loop-must also be consuming organically bound metals. Hence, we predicted animals feeding within the microbial loop would accumulate metals through their diet. To test this prediction, we exploited dietary differences between two organisms, Simulium vittatum, a filter-feeding black fly and Hyalella azteca, a shredding detritivore. We exposed both species to three treatments of DOC (labile, recalcitrant, and no additional DOC) that were crossed with exposure to variable copper (Cu) concentrations (2-14 µg L-1) in laboratory microcosms. As predicted, H. azteca experienced a buffering effect by DOC. However, this pattern was not apparent for S. vittatum. Our results highlight the importance of considering trophic strategies when examining the impacts of metal pollution on aquatic communities, and demonstrate the potential for the microbial loop to facilitate metal uptake in freshwater food webs.

The influence of land cover on the sensitivity of streams to metal pollution.

Identifying freshwater systems that are at risk from anthropogenic stressors is a pressing management problem. In particular, the detection of metal pollution is often constrained by data availability and resources. To address this challenge and develop a tool to identify susceptible systems, we tested whether land cover could be predictive of stream sensitivity to metal pollution, as determined by the biotic ligand model (BLM). We used water chemistry data from the conterminous United States to estimate metal sensitivity in streams using two BLMs (i.e., HydoQual, Bio-Met). Subsequently, we combined the sensitivity estimates with land cover and physiochemical data from the GAGES-II database to build predictive models of sensitivity to metals in streams. When combined, our predictor variables (e.g., land cover, mean annual temperature, mean annual precipitation) generally explained about half of the variation in our dataset. In each model, the percent of wetlands in a watershed was strongly correlated with reduced sensitivity to metals, likely due to increased concentrations of dissolved organic carbon associated with wetlands. To validate the utility of the models, we used them to predict metal sensitivity in sites where metal concentrations had been collected, but where the full suite of BLM parameters were unknown. We were able to classify several hundred sites which are likely at risk to metal pollution. Our work highlights the value in considering metal toxicity at the landscape-scale and describes a new approach to estimate metal sensitivity when site-specific chemical parameters are unknown.

Chemical Force Spectroscopy Evidence Supporting the Layer-by-Layer Model of Organic Matter Binding to Iron (oxy)Hydroxide Mineral Surfaces.

The adsorption of dissolved organic matter (DOM) to metal (oxy)hydroxide mineral surfaces is a critical step for C sequestration in soils. Although equilibrium studies have described some of the factors controlling this process, the molecular-scale description of the adsorption process has been more limited. Chemical force spectroscopy revealed differing adhesion strengths of DOM extracted from three soils and a reference peat soil material to an iron (oxy)hydroxide mineral surface. The DOM was characterized using ultrahigh-resolution negative ion mode electrospray ionization Fourier Transform ion cyclotron resonance mass spectrometry. The results indicate that carboxyl-rich aromatic and N-containing aliphatic molecules of DOM are correlated with high adhesion forces. Increasing molecular mass was shown to decrease the adhesion force between the mineral surface and the DOM. Kendrick mass defect analysis suggests that mechanisms involving two carboxyl groups result in the most stable bond to the mineral surface. We conceptualize these results using a layer-by-layer "onion" model of organic matter stabilization on soil mineral surfaces.

Molecular composition and biodegradability of soil organic matter: a case study comparing two new England forest types.

Soil organic matter (SOM) is involved in many important soil processes such as carbon sequestration and the solubility of plant nutrients and metals. Ultrahigh resolution mass spectrometry was used to determine the influence of forest vegetation type and soil depth on the molecular composition of the water-extractable organic matter (WEOM) fraction. Contrasting the upper 0-5 cm with the 25-50 cm B horizon depth increment, the relative abundance of lipids and carbohydrates significantly increased, whereas condensed aromatics and tannins significantly decreased for the deciduous stand WEOM. No significant abundance changes were found for the coniferous stand DOM. Kendrick mass defect analysis showed that the WEOM of the 25-50 cm B horizon was depleted in oxygen-rich and higher mass components as compared to the 0-5 cm B horizon WEOM, suggesting that higher mass WEOM components with oxygen-containing functionality show greater reactivity in abiotic and/or biotic reactions. Furthermore, using an inoculated 14-day laboratory incubation study and multivariate ordination methods, we identified the WEOM components with H:C > 1.2 and O:C > 0.5 as being correlated most strongly with biodegradability. Our findings highlight the importance of understanding soil depth differences for various forest types in the chemical composition of SOM and the processes governing SOM production and transformations to fully understand the ecological implications of changes in forest composition and function in a changing climate.