Caryn C. Vaughn

Community and foodweb ecology of freshwater mussels

Abstract Freshwater mussel (Superfamily Unionoidea) communities are important components of food webs, and they link and influence multiple trophic levels. Mussels filter food from both the water column and sediment with ciliated gills. Differences in cilia structure and arrangement might allow mussel species to partition food resources. Mussels are omnivores that feed across trophic levels on bacteria, algae, detritus, zooplankton, and perhaps, dissolved organic matter. Living mussels and their spent shells provide or improve habitat for other organisms by providing physical structure, stabilizing and bioturbating sediments, and influencing food availability directly and indirectly through biodeposition of organic matter and nutrient excretion. Effects of mussel communities on nutrient translocation and cycling depend on mussel abundance, species composition, and environmental conditions. Nutrient-related mussel effects influence multiple trophic levels. Healthy mussel communities occur as multispecies assemblages in which species interactions are probably very important. Food limitation and competition among species have been documented, but so have positive species interactions, and rare species have been shown to benefit energetically from living in species-rich communities. Effects of mussel species on ecosystem services and food webs vary across spatial and temporal scales, and the relative importance of competition and facilitation might change at different scales.

Biodiversity Losses and Ecosystem Function in Freshwaters: Emerging Conclusions and Research Directions

Six conclusions have emerged from recent research that complicate the ability to predict how biodiversity losses may affect ecosystem function: (1) species traits determine ecosystem function, (2) species within functional groups are not always ecological equivalents, (3) biodiversity losses include declines in the abundance of common species, (4) biodiversity losses affect wholefood webs, (5) the effects of biodiversity losses depend on abiotic and biotic context and spatial and temporal scales, and (6) successfully predicting linkages between biodiversity and ecosystem function requires using multiple empirical approaches across scales. Nutrient recycling by freshwater mussel communities illustrates these conclusions. Nutrient excretion rates depend on the expression of mussel species traits, which vary with flow, temperature, and community structure. Nutrient contributions from mussels depend on which mussel species are dominant, but common species of mussels are declining, leading to shifts in species dominance patterns and thus nutrient recycling. These changes are very likely affecting the rest of the benthic food web because mussel excretion stimulates primary, and subsequently secondary, production.

Ecosystem Processes Performed by Unionid Mussels in Stream Mesocosms: Species Roles and Effects of Abundance

Unionid mussels are a guild of freshwater, sedentary filter-feeders experiencing a global decline in both species richness and abundance. To predict how these losses may impact stream ecosystems we need to quantify the effects of both overall mussel biomass and individual species on ecosystem processes. In this study we begin addressing these fundamental questions by comparing rates of ecosystem processes for two common mussel species, Amblema plicata and Actinonaias ligamentina, across a range of abundance levels and at two trophic states (low and high productivity) in stream mesocosms. At both low and high productivity, community respiration, water column ammonia, nitrate, and phosphorus concentrations, and algal clearance rates were all linearly related to overall mussel biomass. After removing the effects of biomass with ANCOVA, we found few differences between species. In a separate series of experiments, nutrient excretion (phosphorus, ammonia, and molar N:P) and biodeposition rates were only marginally different between species. For the species studied here, functional effects of unionids in streams were similar between species and linearly related to biomass, indicating the potential for strong effects when overall mussel biomass is high and hydrologic residence times are long.

Predator-Avoidance Responses in Freshwater Decapod-Gastropod Interactions Mediated by Chemical Stimuli

Previous studies on single species of snails reached conflicting conclusions regarding the importance of chemical cues in predator-avoidance behavior. We performed laboratory experiments to determine if chemically mediated, predator-avoidance behavior, such as crawling out of the water by freshwater gastropods, occurred among prey of different species from several geographic sources: Oklahoma, Oregon, and Wisconsin. We compared responses of eight gastropod populations when they were exposed to predation by three species of crayfish. We observed no crawl-out from two prosobranch species. Individuals from four of six populations of pulmonates responded to crayfish predators; physid and lymnaeid populations consistently responded whereas some planorbid populations did not respond. We also examined individual variation in response to predators and the proximate costs and benefits to prey associated with crawling out of the water. Trade-offs between risks of immediate, direct mortality from aquatic, amphibious, or terrestrial predation relative to delayed, indirect mortality associated with desiccation, are influenced by shell size, thickness, and morphology, as well as physiological adaptations among various pulmonate populations. If water depth is sufficient to provide spatial refuge from crayfish, smaller snails can reduce their losses to predation by moving to the surface of the water or by crawling out. In previous studies, Physella virgata and Planorbella trivolvis frequently used predator-avoidance behavior when young, but as shell size and strength increased with age, the larger individuals spent less time crawling out of the water. In this study none of the planorbids (Helisoma anceps or Gyraulus parvus) crawled out, even when young. These differences are apparently due to differences in selection pressures caused by differences in use of various microhabitats where risk of predation varies over time.

A trait-based approach to species' roles in stream ecosystems: climate change, community structure, and material cycling

The sustained decline in habitat quality and community integrity highlights the importance of understanding how communities and environmental variation interactively contribute to ecosystem services. We performed a laboratory experiment manipulating effects of acclimation temperature (5, 15, 25, and 35°C) on resource acquisition, assimilation and subsequent ecosystem services provided by eight freshwater mussel species. Our results suggest that although freshwater mussels are broadly categorized as filter feeders, there are distinct nested functional guilds (thermally tolerant and sensitive) associated with their thermal performance. At 35°C, thermally tolerant species have increased resource assimilation and higher rates of contributed ecosystem services (nutrient excretion, benthic–pelagic coupling). Conversely, thermally sensitive species have decreased assimilation rates and display an array of functional responses including increased/decreased benthic–pelagic coupling and nutrient excretion. Although thermally sensitive species may be in poorer physiological condition at warmer temperatures, their physiological responses can have positive effects on ecosystem services. We extrapolated these results to real mussel beds varying in species composition to address how shifts in community composition coupled with climate change may shift their contributed ecological services. Comparative field data indicate that two co-existing, abundant species with opposing thermal performance (Actinonaias ligamentina, Amblema plicata) differentially dominate community biomass. Additionally, communities varying in the relative proportion of these species differentially influence the magnitude (benthic–pelagic coupling) and quality (N:P excretion) of ecosystem services. As species are increasingly threatened by climate change, greater emphasis should be placed on understanding the contribution of physiological stress to the integrity and functioning of ecosystems.

Unionid mussels influence macroinvertebrate assemblage structure in streams

Abstract Unionid mussels often occur as multispecies aggregates called mussel beds and in dense patches within the mussel beds themselves. Thus, their distributions are patchy at 2 spatial scales. We examined the association between mussel assemblage structure and macroinvertebrate assemblage structure at these 2 spatial scales in rivers of the Ouachita Highlands, Arkansas and Oklahoma, USA. We used multivariate variation partitioning techniques to relate variation in benthic macroinvertebrate distribution and abundance to variation in mussel assemblages, environmental variables, spatial variables, and overlapping or shared variation between these components. At the patch scale, total densities of macroinvertebrates and dominant groups (Oligochaeta, Chironomidae, Ephemeroptera, and Trichoptera) were significantly higher in patches containing mussels than where mussels were absent, and densities of macroinvertebrates were positively correlated with unionid density. In variation partitioning analyses, mussel assemblages explained almost ½ of the variation in macroinvertebrate assemblages at both spatial scales, even after removing effects of similar habitat (environmental variables) and biogeographic history (spatial variables).

Complex hydraulic and substrate variables limit freshwater mussel species richness and abundance

Abstract We examined how substrate and complex hydraulic variables limit the distribution of freshwater mussels. We sampled mussels and measured substrate and hydraulic variables (at low and high flows) at 6 sites in the Little River, Oklahoma. To test which variables were most limiting to mussel species richness and abundance, we evaluated univariate and multiple 95th-, 90th-, and 85th-quantile regression models using a model selection approach. Across all 3 quantiles analyzed, hydraulic variables related to substrate stability (relative shear stress ratio [RSS] and shear stress) at high flows most limited mussel species richness and abundance. High-flow substrate stability models performed the best, but models that used substrate variables (substrate size and heterogeneity) also performed relatively well. Models that used complex hydraulic variables estimated at low flows performed poorly compared to those using the same variables estimated at high flows, a result suggesting that hydraulic conditions at low flows do not limit mussel habitat in our system. Our results demonstrate that substrate stability at high flows is an important factor governing mussel distributions. Last, our quantile regression approach successfully quantified the limiting-factor relationships of substrate and hydraulic characteristics on mussel habitat, and this approach could be used in other studies investigating habitat requirements of aquatic organisms.

CONTEXT‐DEPENDENT SPECIES IDENTITY EFFECTS WITHIN A FUNCTIONAL GROUP OF FILTER‐FEEDING BIVALVES

We asked whether species richness or species identity contributed more to ecosystem function in a trait-based functional group, burrowing, filter-feeding bivalves (freshwater mussels: Unionidae), and whether their importance changed with environmental context and species composition. We conducted a manipulative experiment in a small river examining the effects of mussel assemblages varying from one to eight species on benthic algal standing crop across two sets of environmental conditions: extremely low discharge and high water temperature (summer); and moderate discharge and water temperature (fall). We found strong species identity effects within this guild, with one species (Actinonaias ligamentina) influencing accrual of benthic algae more than other species, but only under summer conditions. We suspect that this effect is due to a combination of the greater biomass of this species and its higher metabolic and excretion rates at warm summer temperatures, resulting in increased nitrogen subsidies to benthic algae. We also found that Actinonaias influenced the condition of other mussel species, likely through higher consumption, interference, or both. This study demonstrates that species within trait-based functional groups do not necessarily have the same effects on ecosystem properties, particularly under different environmental conditions.

Burrowing behavior of freshwater mussels in experimentally manipulated communities

Abstract We experimentally manipulated mussel community structure and observed mussel burrowing behavior in mesocosms held in a greenhouse. Vertical positions, vertical movements, and horizontal movements of Actinonaias ligamentina, Amblema plicata, Fusconaia flava, and Obliquaria reflexa were recorded during five 11-d trials. Community structure was manipulated by constructing communities with 11 different diversity treatments crossed with 3 different density treatments. Vertical positions, vertical movements, and horizontal movements of mussels differed significantly among diversity treatments, and vertical movements differed among density treatments. Differences among diversity treatments were caused by differences in species composition because the burrowing activity of mussels in multispecies communities could be predicted additively from single-species communities. The species used in our study vary in body size, but differences among species were still significant after accounting for body length. We think that differences in species burrowing behavior might be a result of niche partitioning of vertical space, might be a result of differing effects of temperature between species, or might be related to mechanisms to avoid dislodgement during high flows. The burrowing behavior of freshwater mussels has implications for mussel sampling protocols, the sensitivity of mussels to zebra mussel attachment, and how mussels influence benthic ecosystems.

Aggregated filter-feeding consumers alter nutrient limitation: consequences for ecosystem and community dynamics.

Nutrient cycling is a key process linking organisms in ecosystems. This is especially apparent in stream environments in which nutrients are taken up readily and cycled through the system in a downstream trajectory. Ecological stoichiometry predicts that biogeochemical cycles of different elements are interdependent because the organisms that drive these cycles require fixed ratios of nutrients. There is growing recognition that animals play an important role in biogeochemical cycling across ecosystems. In particular, dense aggregations of consumers can create biogeochemical hotspots in aquatic ecosystems via nutrient translocation. We predicted that filter-feeding freshwater mussels, which occur as speciose, high-biomass aggregates, would create biogeochemical hotspots in streams by altering nutrient limitation and algal dynamics. In a field study, we manipulated nitrogen and phosphorus using nutrient-diffusing substrates in areas with high and low mussel abundance, recorded algal growth and community composition, and determined in situ mussel excretion stoichiometry at 18 sites in three rivers (Kiamichi, Little, and Mountain Fork Rivers, south-central United States). Our results indicate that mussels greatly influence ecosystem processes by modifying the nutrients that limit primary productivity. Sites without mussels were N-limited with -26% higher relative abundances of N-fixing blue-green algae, while sites with high mussel densities were co-limited (N and P) and dominated by diatoms. These results corroborated the results of our excretion experiments; our path analysis indicated that mussel excretion has a strong influence on stream water column N:P. Due to the high N:P of mussel excretion, strict N-limitation was alleviated, and the system switched to being co-limited by both N and P. This shows that translocation of nutrients by mussel aggregations is important to nutrient dynamics and algal species composition in these rivers. Our study highlights the importance of consumers and this imperiled faunal group on nutrient cycling and community dynamics in aquatic ecosystems.