Carla L. Atkinson

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.

Stable isotopic signatures, tissue stoichiometry, and nutrient cycling (C and N) of native and invasive freshwater bivalves

Abstract Filter-feeding mussels historically comprised most of benthic biomass in many streams. They contribute to stream ecosystem functioning by linking the water column and benthic habitats. Both native and nonnative species coexist in many streams, but their ecological roles are not well quantified. The invasive bivalve, Corbicula fluminea, has the potential to alter profoundly organic matter dynamics and nutrient cycling in streams. We compared stable isotope ratios and tissue and biodeposit stoichiometry of the native freshwater mussel, Elliptio crassidens, and C. fluminea in a Coastal Plain stream (Ichawaynochaway Creek, a tributary to the lower Flint River, Georgia, USA) to assess their trophic niche space and potential effects on nutrient cycling. We hypothesized that C. fluminea would assimilate a larger range of materials than E. crassidens. To determine dietary overlap of C. fluminea and E. crassidens, we measured the elemental and stable isotopic compositions (δ13C and δ15N) of their tissue. Corbicula fluminea showed lower trophic fidelity than E. crassidens and was able to acquire and assimilate a wide range of resources, as illustrated by their wide range of δ13C values. Corbicula fluminea also might alter nutrient cycling in the benthic environment of streams because they retain less N than E. crassidens, as reflected by their higher tissue C∶N. In the laboratory, we measured C and N in biodeposits (feces and pseudofeces) from the 2 species. Corbicula fluminea released more N through their biodeposits relative to E. crassidens by mass, a result implying that C. fluminea might modify nutrient cycling in streams. Our results show important differences in the food resources assimilated and the nutrients deposited as feces and pseudofeces by these 2 bivalves. Furthermore, our results demonstrate how invasive species, such as C. fluminea, can alter aquatic environments through differences in species traits within a functional group.

Stream discharge and floodplain connections affect seston quality and stable isotopic signatures in a coastal plain stream

Abstract Connections of a stream to its floodplain are important ecological linkages that affect spatial and temporal dynamics of the basal resources available to primary consumers in streams. Suspended organic material and associated microorganisms (seston) vary in quality seasonally and interannually within streams because of changing inputs from riparian and floodplain sources. Researchers have investigated the quality of different size fractions of material, but these differences have not been assessed with respect to the hydrology and the geomorphic structure of streams. We investigated how quality, represented by the stoichiometric ratio C:N, and stable isotopic signature (δ13C and δ15N) of 3 seston size classes varied in Ichawaynochaway Creek, a 5th-order tributary of the lower Flint River in the Coastal Plain of southwestern Georgia, USA. Samples were collected throughout the basin during varying flow regimes to estimate the quality and source of materials available over different temporal and spatial scales. Our results indicate significant differences in quality and stable isotopic signature based on particle size, discharge, and geomorphic structure of the stream and floodplain (constrained vs unconstrained reaches). The constrained portions of this stream occur in the lower portions of the basin. During low flow conditions, seston had higher quality with less depleted δ13C and more enriched δ15N signatures in the constrained than in the unconstrained portions of the stream. However, during high flow conditions, higher quality seston entered the stream from the adjacent floodplain in all portions of the basin. Insights gained from our study indicate how terrestrial and aquatic linkages and the natural flow regime affect the dynamics of basal resources and their availability to primary consumers in streams.

Consumer-driven nutrient dynamics in freshwater ecosystems: from individuals to ecosystems

The role of animals in modulating nutrient cycling [hereafter, consumer‐driven nutrient dynamics (CND)] has been accepted as an important influence on both community structure and ecosystem function in aquatic systems. Yet there is great variability in the influence of CND across species and ecosystems, and the causes of this variation are not well understood. Here, we review and synthesize the mechanisms behind CND in fresh waters. We reviewed 131 articles on CND published between 1973 and 1 June 2015. The rate of new publications in CND has increased from 1.4 papers per year during 1973–2002 to 7.3 per year during 2003–2015. The majority of investigations are in North America with many concentrating on fish. More recent studies have focused on animal‐mediated nutrient excretion rates relative to nutrient demand and indirect impacts (e.g. decomposition). We identified several mechanisms that influence CND across levels of biological organization. Factors affecting the stoichiometric plasticity of consumers, including body size, feeding history and ontogeny, play an important role in determining the impact of individual consumers on nutrient dynamics and underlie the stoichiometry of CND across time and space. The abiotic characteristics of an ecosystem affect the net impact of consumers on ecosystem processes by influencing consumer metabolic processes (e.g. consumption and excretion/egestion rates), non‐CND supply of nutrients and ecosystem nutrient demand. Furthermore, the transformation and transport of elements by populations and communities of consumers also influences the flow of energy and nutrients across ecosystem boundaries. This review highlights that shifts in community composition or biomass of consumers and eco‐evolutionary underpinnings can have strong effects on the functional role of consumers in ecosystem processes, yet these are relatively unexplored aspects of CND. Future research should evaluate the value of using species traits and abiotic conditions to predict and understand the effects of consumers on ecosystem‐level nutrient dynamics across temporal and spatial scales. Moreover, new work in CND should strive to integrate knowledge from disparate fields of ecology and environmental science, such as physiology and ecosystem ecology, to develop a comprehensive and mechanistic understanding of the functional role of consumers. Comparative and experimental studies that develop testable hypotheses to challenge the current assumptions of CND, including consumer stoichiometric homeostasis, are needed to assess the significance of CND among species and across freshwater ecosystems.

Drought-induced changes in flow regimes lead to long-term losses in mussel-provided ecosystem services

Extreme hydro-meteorological events such as droughts are becoming more frequent, intense, and persistent. This is particularly true in the south central USA, where rapidly growing urban areas are running out of water and human-engineered water storage and management are leading to broad-scale changes in flow regimes. The Kiamichi River in southeastern Oklahoma, USA, has high fish and freshwater mussel biodiversity. However, water from this rural river is desired by multiple urban areas and other entities. Freshwater mussels are large, long-lived filter feeders that provide important ecosystem services. We ask how observed changes in mussel biomass and community composition resulting from drought-induced changes in flow regimes might lead to changes in river ecosystem services. We sampled mussel communities in this river over a 20-year period that included two severe droughts. We then used laboratory-derived physiological rates and river-wide estimates of species-specific mussel biomass to estimate three aggregate ecosystem services provided by mussels over this time period: biofiltration, nutrient recycling (nitrogen and phosphorus), and nutrient storage (nitrogen, phosphorus, and carbon). Mussel populations declined over 60%, and declines were directly linked to drought-induced changes in flow regimes. All ecosystem services declined over time and mirrored biomass losses. Mussel declines were exacerbated by human water management, which has increased the magnitude and frequency of hydrologic drought in downstream reaches of the river. Freshwater mussels are globally imperiled and declining around the world. Summed across multiple streams and rivers, mussel losses similar to those we document here could have considerable consequences for downstream water quality although lost biofiltration and nutrient retention. While we cannot control the frequency and severity of climatological droughts, water releases from reservoirs could be used to augment stream flows and prevent compounded anthropogenic stressors.

Long‐lived organisms provide an integrative footprint of agricultural land use

Nitrogen (N) fertilizer runoff into rivers is linked to nutrient enrichment, hydrologic alteration, habitat degradation and loss, and declines in biotic integrity in streams. Nitrogen runoff from agriculture is expected to increase with population growth, so tracking these sources is vital to enhancing biomonitoring and management actions. Unionid mussels are large, long-lived, sedentary, primary consumers that transfer particulate material and nutrients from the water column to the sediments through their filter feeding. Because of these traits, mussels may provide a temporal integration of nitrogen inputs into watersheds. Our goals were to (1) establish a baseline delta15N signature for unionid mussels in watersheds not heavily influenced by agriculture for use in comparative analyses and (2) determine if mussels provide an integrative measure of N sources in watersheds with varying percentages of agriculture across large spatial scales. We compiled tissue delta15N data for 20 species of mussels from seven geographic areas, including 23 watersheds and 42 sample sites that spanned varying degrees of agricultural intensification across the eastern United States and Canada. We used GIS to determine land cover within the study basins, and we estimated net anthropogenic nitrogen inputs (NANI) entering these systems. We then determined the relationship between mussel tissue delta15N and percentage of land in agriculture (%AG) and net anthropogenic N loading. The delta15N of mussel tissue could be predicted from both %AG and net anthropogenic N loading, and one component of NANI, the amount of N fertilizer applied, was strongly related to the delta15N of mussel tissue. Based on our results, mussels occupying a system not affected by agricultural land use would have a baseline delta15N signature of approximately 2.0 pe thousand, whereas mussels in basins with heavy agriculture had delta15N signatures of 13.6 per thousand. Our results demonstrate that mussels integrate anthropogenic N input into rivers at a watershed scale and could be a good bioassessment tool for tracking agriculture N sources.

Implications of species addition and decline for nutrient dynamics in fresh waters

Abstract: In terrestrial and aquatic ecosystems, organisms directly affect nutrient storage and cycling by sequestering nutrients via growth and remineralizing nutrients via excretion and egestion. Therefore, species introductions and extirpations can profoundly affect nutrient storage and remineralization rates, and present a challenge for conserving ecosystem function in fresh waters. The literature of consumer-driven nutrient dynamics is growing rapidly, but studies of consumer effects on nutrient storage and remineralization across species and among ecosystems are limited. We compared the effects of 3 grazing taxa, nonnative armored catfish in Mexican streams, native mussels in Oklahoma streams, and native tadpoles in Panamanian streams, on nutrient storage and remineralization. We examined interactions among organismal stoichiometry and biomass, nutrient storage, remineralization rates, and ecosystem size across these 3 groups following species decline (tadpoles and mussels) or introduction (armored catfish) to gain a better understanding of organism-specific effects on nutrient dynamics among freshwater ecosystems. Collectively, our results suggest that the ecosystem-level effect of consumer-driven nutrient dynamics is strongly influenced by environmental variables and is taxon specific. Major changes in biomass of stoichiometrically distinctive organisms can lead to subsequent changes in the flux and storage of elements in an ecosystem, but the overall effect of aquatic animals on nutrient dynamics also is determined by discharge and nutrient-limitation patterns in streams and rivers.

Organized Oral Session 44: Impacts of Species Addition and Species Loss on Ecosystem Function in Freshwater Systems

Understanding the role of species as drivers of ecosystem processes is imperative to preserve, utilize, and sustain ecosystems globally. Addition of species through invasion and loss of species through extirpation or extinction can have profound effects on ecosystem structure and function (Zavaleta et al. 2009). This is especially true for freshwater ecosystems in which a preponderance of native species are threatened with extinction and where nonnative species are frequently introduced (Dudgeon and Smith 2006). Commonly, anthropogenic activities result in the loss of biodiversity and enhance the ability of exotic species to invade and persist in novel habitats (Dudgeon and Smith 2006). Because these activities are expected to increase through time, advances in understanding the consequences of species loss and addition on ecosystem function are needed to guide appropriate management and conservation decisions. The loss and addition of organisms may render habitats functionally impaired (Covich et al. 2004); therefore, understanding the consequences of such change is imperative to manage, mitigate, and restore freshwater ecosystems.

Consumer Aggregations Drive Nutrient Dynamics and Ecosystem Metabolism in Nutrient-Limited Systems

Differences in animal distributions and metabolic demands can influence energy and nutrient flow in an ecosystem. Through taxa-specific nutrient consumption, storage, and remineralization, animals may influence energy and nutrient pathways in an ecosystem. Here we show these taxa-specific traits can drive biogeochemical cycles of nutrients and alter ecosystem primary production and metabolism, using riverine systems that support heterogeneous freshwater mussel aggregations. Freshwater unionid mussels occur as distinct, spatially heterogeneous, dense aggregations in rivers. They may influence rates of production and respiration because their activities are spatially concentrated within given stream reaches. Previous work indicates that mussels influence nutrient limitation patterns, algal species composition, and producer and primary consumer biomass. Here, we integrate measures of organismal rates, stoichiometry, community-scaled rates, and ecosystem rates, to determine the relative source–sink nutrient dynamics of mussel aggregations and their influence on net ecosystem processes. We studied areas with and without mussel aggregations in three nitrogen-limited rivers in southeastern Oklahoma, USA. We measured respiration and excretion rates of mussels and collected a subset of samples for tissue chemistry and for thin sectioning of the shell to determine growth rates at each site. This allowed us to assess nutrient remineralization and nutrient sequestration by mussels. These rates were scaled to the community. We also measured stream metabolism at three sites with and without mussels. We demonstrated that mussel species have distinct stoichiometric traits, vary in their respiration rates, and that mussel aggregations influence nutrient cycling and productivity. Across all mussel aggregations, we found that mussels excreted more nitrogen than they sequestered into tissue and excreted more phosphorus than they sequestered except at one site. Furthermore, gross primary productivity was significantly greater at reaches with mussels. Collectively, our results indicate that mussels have ecosystem-level impacts on nutrient availability and production in nutrient-limited rivers. Within these streams, mussels are affecting the movement of nutrients and altering nutrient spiralling.

Benthic algal community composition across a watershed: coupling processes between land and water

One of the main goals of ecology is to understand how the abiotic environment influences the biotic characteristics of the ecosystem. Various processes at multiple scales interact to affect the physical and chemical environments that are experienced by organisms, which ultimately influence community composition. We aimed to understand the processes that control benthic algae community composition within a watershed. We investigated the impact of both land cover and physiochemical variables on benthic algal community composition. We sampled benthic algae along with multiple habitat and water chemistry parameters within three microhabitats across eight sites along the mainstem of the Kiamichi River in southeastern Oklahoma. We used the benthic light availability model to assess the amount of light reaching the bottom of the stream. Additionally, we conducted a GIS analysis of the watershed to determine the land cover affecting each of these sites. Several of the in-stream site-scale variables that were measured (e.g., conductivity, pH and canopy cover) were strongly correlated with both position within the watershed and percent agriculture within the watershed. The physiochemical parameters that were correlated with watershed position and land cover were then used to understand the linkage with algae community composition. Algae genera composition was strongly correlated with both light reaching the bottom of the stream and conductivity. Our results suggest a hierarchy of factors that determine species composition and show the dependence of community composition on differing light regimes.