Long-term ecological research in freshwaters enabled by regional biodiversity collections, stable isotope analysis, and environmental informatics.

Biodiversity collections are experiencing a renaissance fueled by the intersection of informatics, emerging technologies, and the extended use and interpretation of specimens and archived databases. In this article, we explore the potential for transformative research in ecology integrating biodiversity collections, stable isotope analysis (SIA), and environmental informatics. Like genomic DNA, SIA provides a common currency interpreted in the context of biogeochemical principles. Integration of SIA data across collections allows for evaluation of long-term ecological change at local to continental scales. Challenges including the analysis of sparse samples, a lack of information about baseline isotopic composition, and the effects of preservation remain, but none of these challenges is insurmountable. The proposed research framework interfaces with existing databases and observatories to provide benchmarks for retrospective studies and ecological forecasting. Collections and SIA add historical context to fundamental questions in freshwater ecological research, reference points for ecosystem monitoring, and a means of quantitative assessment for ecosystem restoration.

Assessing relationships between onsite wastewater treatment system maintenance patterns and system-level variables.

Globally, millions of households rely on onsite wastewater treatment systems (OWTSs), such as septic systems, to safely treat and dispose of wastewater. Conventional subsurface OWTSs are a common and affordable option for many landowners, and effectively remove pathogenic and nutrient pollution from wastewater when properly sited and maintained. However, OWTSs can also be a source of nonpoint pollution in watersheds when they are not functioning properly. To better understand the drivers of OWTS maintenance and failure, we explored relationships between OWTS age, environmental characteristics (edaphic conditions, topographic wetness index, and distance to stream), and repair and pumping records for OWTSs in Athens-Clarke County, Georgia, USA. Repair records indicated that 7.8 % of the 8826 OWTSs in the study were repaired over a 78-year period and that the median age of a repaired OWTSs was 65 years old. Pumping records showed that 12.2 % of the OWTSs were pumped in a 38-month period (an annualized rate of 5.7 %). The suite of widely available environmental variables we used as predictors were likely not granular enough to detect patterns of individual system maintenance at this scale. However, we found that the oldest OWTSs (>50 years) had the highest probabilities of being repaired and exhibiting signs of hydraulic failure. Notably, new OWTSs (2-10 years) were nearly as likely as the oldest systems to exhibit signs of hydraulic failure. These findings suggest that repair and replacement efforts should target older systems that are at or near the end of their serviceable life, and, in addition to continually monitoring older systems, all OWTSs should be inspected one year after installation. By leveraging data that may already exist, practitioners in other localities can use this reproducible approach to estimate the performance of OWTSs. Our data and methods will support efforts to prioritize wastewater infrastructure investments and policies.

Non-point source fecal contamination from aging wastewater infrastructure is a primary driver of antibiotic resistance in surface waters.

Antibiotic resistance is a global threat to human health. Many surface water resources are environmental hotspots of antibiotic resistant gene (ARG) transfer, with agricultural runoff and human waste highlighted as common sources of ARGs to aquatic systems. Here we quantified fecal marker genes and ARGs in 992 stream water samples collected seasonally during a 5-year period from 115 sites across the Upper Oconee watershed (Georgia, USA), an area characterized by gradients of agricultural and urban development. Widespread fecal contamination was found from humans (48% of samples), ruminants (55%), and poultry (19%), and 73% of samples tested positive for at least one of the six targeted ARGs (ermB, tet(B), blaCTX-M-1, blaKPC, blaSHV, and qnrS). While ARGs were strongly correlated with human fecal markers, many highly contaminated samples were not associated with sewage outfalls, an expected source of fecal and ARG pollution. To determine sources of contamination, we synthesized ARG and fecal marker data with geospatial data on land use/land cover and wastewater infrastructure across the watershed. This novel analysis found strong correlations between ARGs and measures of sewer density, sewer length, and septic system age within sample watersheds, indicating non-point sources of fecal contamination from aging wastewater infrastructure can be critical disseminators of anthropogenic ARGs in the environment.

Six minutes to promote change: People, not facts, alter students' perceptions on climate change.

Anthropogenic climate change threatens the structure and function of ecosystems throughout the globe, but many people are still skeptical of its existence. Traditional "knowledge deficit model" thinking has suggested that providing the public with more facts about climate change will assuage skepticism. However, presenting evidence contrary to prior beliefs can have the opposite effect and result in a strengthening of previously held beliefs, a phenomenon known as biased assimilation or a backfire effect. Given this, strategies for effectively communicating about socioscientific issues that are politically controversial need to be thoroughly investigated. We randomly assigned 184 undergraduates from an environmental science class to one of three experimental conditions in which we exposed them to short videos that employed different messaging strategies: (a) an engaging science lecture, (b) consensus messaging, and (c) elite cues. We measured changes in student perceptions of climate change across five constructs (content knowledge, acceptance of scientific consensus, perceived risk, support for action, and climate identity) before and after viewing videos. Consensus messaging outperformed the other two conditions in increasing student acceptance of the scientific consensus, perceived risk of climate change, and climate identity, suggesting this may be an effective strategy for communicating the gravity of anthropogenic climate change. Elite cues outperformed the engaging science lecture condition in increasing student support for action on climate, with politically conservative students driving this relationship, suggesting that the messenger is more important than the message if changing opinions about the necessity of action on climate change is the desired outcome. Relative to the other conditions, the engaging science lecture did not support change in students' perceptions on climate, but appealing to student respect for authority produced positive results. Notably, we observed no decline in students' acceptance of climate science, indicating that none of the conditions induced a backfire effect.

Taxonomic and functional responses of macroinvertebrates to riparian forest conversion in tropical streams.

Land use change threatens the ecological integrity of tropical rivers and streams; however, few studies have simultaneously analyzed the taxonomic and functional responses of tropical macroinvertebrates to riparian forest conversion. Here, we used community structure, functional diversity, and stable isotope analyses to assess the impacts of riparian deforestation on macroinvertebrate communities of streams in southern Mexico. Monthly sampling during the dry season was conducted in streams with riparian forest (forest streams), and in streams with pasture dominating the riparian vegetation (pasture streams). Samples were collected for water quality (physical-chemical variables, nutrient concentrations, and total suspended solids), organic matter (leaf litter abundance and algal biomass), and macroinvertebrate abundance and diversity. Higher temperature, conductivity, suspended solids, and chlorophyll a were detected in pasture streams, while nitrate concentrations and leaf litter biomass were greater in forest streams. Macroinvertebrate density was higher in pasture sites, while no differences in taxonomic diversity and richness were found between land uses. Functional evenness was greater in forest streams, while richness and divergence were similar between land uses, despite differences in taxonomic composition. Environmental variables were associated with taxa distribution but not with functional traits, suggesting current conditions still promote redundancy in ecological function. Isotopic analyses indicated consumers in pasture streams were enriched in 13C and 15N relative to forest streams, potentially reflecting the higher algal biomass documented in pasture systems. Isotopic niches were broader and more overlapped in pasture streams, indicating more generalist feeding habits. No significant losses of taxonomic or functional diversity were detected in pasture streams. However, changes in trophic ecology suggest landscape-level processes are altering macroinvertebrate feeding habits in streams. The changes we observed in habitat, water quality, and macroinvertebrate community were related to the removal of the riparian vegetation, suggesting the structure and function of the focal systems would benefit from riparian restoration.

Assessing the Socio-Environmental Risk of Onsite Wastewater Treatment Systems to Inform Management Decisions.

Quantifying the risk that failing onsite waste treatment systems (OWTS), such as septic systems, present to human health and the environment is a key component in natural resource management. We integrated environmental and socio-demographic data to assess the potential environmental risk and environmental justice concerns related to septic infrastructure. We used this process to develop a framework that can be applied in other jurisdictions. We found only 8% of the registered OWTS presented potential environmental risk due to the topographic, hydrologic, or edaphic characteristics of their placement. In contrast, almost 70% of the OWTS presented potential environmental risk due to their age (25 years or older). Approximately 60% of the OWTS we estimated to be at risk from age or placement were found in census blocks with more than 30% of the population living below the poverty line, had a population that was more than 50% nonwhite, or was predominantly nonwhite and impoverished. Our work suggests that jurisdictions with limited information about septic infrastructure may be able to use geospatial data that they do have to predict the parcel-level locations of OWTS. These locations can then be used to inform environmental monitoring to proactively address environmental justice concerns.

Integration of ecosystem science into radioecology: A consensus perspective.

In the Fall of 2016 a workshop was held which brought together over 50 scientists from the ecological and radiological fields to discuss feasibility and challenges of reintegrating ecosystem science into radioecology. There is a growing desire to incorporate attributes of ecosystem science into radiological risk assessment and radioecological research more generally, fueled by recent advances in quantification of emergent ecosystem attributes and the desire to accurately reflect impacts of radiological stressors upon ecosystem function. This paper is a synthesis of the discussions and consensus of the workshop participant's responses to three primary questions, which were: 1) How can ecosystem science support radiological risk assessment? 2) What ecosystem level endpoints potentially could be used for radiological risk assessment? and 3) What inference strategies and associated methods would be most appropriate to assess the effects of radionuclides on ecosystem structure and function? The consensus of the participants was that ecosystem science can and should support radiological risk assessment through the incorporation of quantitative metrics that reflect ecosystem functions which are sensitive to radiological contaminants. The participants also agreed that many such endpoints exit or are thought to exit and while many are used in ecological risk assessment currently, additional data need to be collected that link the causal mechanisms of radiological exposure to these endpoints. Finally, the participants agreed that radiological risk assessments must be designed and informed by rigorous statistical frameworks capable of revealing the causal inference tying radiological exposure to the endpoints selected for measurement.

Global patterns and drivers of ecosystem functioning in rivers and riparian zones.

River ecosystems receive and process vast quantities of terrestrial organic carbon, the fate of which depends strongly on microbial activity. Variation in and controls of processing rates, however, are poorly characterized at the global scale. In response, we used a peer-sourced research network and a highly standardized carbon processing assay to conduct a global-scale field experiment in greater than 1000 river and riparian sites. We found that Earth's biomes have distinct carbon processing signatures. Slow processing is evident across latitudes, whereas rapid rates are restricted to lower latitudes. Both the mean rate and variability decline with latitude, suggesting temperature constraints toward the poles and greater roles for other environmental drivers (e.g., nutrient loading) toward the equator. These results and data set the stage for unprecedented "next-generation biomonitoring" by establishing baselines to help quantify environmental impacts to the functioning of ecosystems at a global scale.

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.

A global database of nitrogen and phosphorus excretion rates of aquatic animals.

Animals can be important in modulating ecosystem-level nutrient cycling, although their importance varies greatly among species and ecosystems. Nutrient cycling rates of individual animals represent valuable data for testing the predictions of important frameworks such as the Metabolic Theory of Ecology (MTE) and ecological stoichiometry (ES). They also represent an important set of functional traits that may reflect both environmental and phylogenetic influences. Over the past two decades, studies of animal-mediated nutrient cycling have increased dramatically, especially in aquatic ecosystems. Here we present a global compilation of aquatic animal nutrient excretion rates. The dataset includes 10,534 observations from freshwater and marine animals of N and/or P excretion rates. These observations represent 491 species, including most aquatic phyla. Coverage varies greatly among phyla and other taxonomic levels. The dataset includes information on animal body size, ambient temperature, taxonomic affiliations, and animal body N:P. This data set was used to test predictions of MTE and ES, as described in Vanni and McIntyre (2016; Ecology DOI: 10.1002/ecy.1582).

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.

Stoichiometric implications of a biphasic life cycle.

Animals mediate flows of elements and energy in ecosystems through processes such as nutrient sequestration in body tissues, and mineralization through excretion. For taxa with biphasic life cycles, the dramatic shifts in anatomy and physiology that occur during ontogeny are expected to be accompanied by changes in body and excreta stoichiometry, but remain little-explored, especially in vertebrates. Here we tested stoichiometric hypotheses related to the bodies and excreta of the wood frog (Lithobates sylvaticus) across life stages and during larval development. Per-capita rates of nitrogen (N) and phosphorus (P) excretion varied widely during larval ontogeny, followed unimodal patterns, and peaked midway through development (Taylor-Kollros stages XV and XII, respectively). Larval mass did not increase steadily during development but peaked at stage XVII and declined until the termination of the experiment at stage XXII. Mass-specific N and P excretion rates of the larvae decreased exponentially during development. When coupled with population-biomass estimates, population-level excretion rates were greatest at stages VIII-X. Percent carbon (C), N, and C:N of body tissue showed weak trends across major life stages; body P and C:P, however, increased sixfold during development from egg to adult. Our results demonstrate that intraspecific ontogenic changes in nutrient contents of excretion and body tissues can be significant, and that N and P are not always excreted proportionally throughout life cycles. These results highlight the dynamic roles that species play in ecosystems, and how the morphological and physiological changes that accompany ontogeny can influence ecosystem-level processes.

Invasive aquarium fish transform ecosystem nutrient dynamics.

Trade of ornamental aquatic species is a multi-billion dollar industry responsible for the introduction of myriad fishes into novel ecosystems. Although aquarium invaders have the potential to alter ecosystem function, regulation of the trade is minimal and little is known about the ecosystem-level consequences of invasion for all but a small number of aquarium species. Here, we demonstrate how ecological stoichiometry can be used as a framework to identify aquarium invaders with the potential to modify ecosystem processes. We show that explosive growth of an introduced population of stoichiometrically unique, phosphorus (P)-rich catfish in a river in southern Mexico significantly transformed stream nutrient dynamics by altering nutrient storage and remineralization rates. Notably, changes varied between elements; the P-rich fish acted as net sinks of P and net remineralizers of nitrogen. Results from this study suggest species-specific stoichiometry may be insightful for understanding how invasive species modify nutrient dynamics when their population densities and elemental composition differ substantially from native organisms. Risk analysis for potential aquarium imports should consider species traits such as body stoichiometry, which may increase the likelihood that an invasion will alter the structure and function of ecosystems.

Invasive fishes generate biogeochemical hotspots in a nutrient-limited system.

Fishes can play important functional roles in the nutrient dynamics of freshwater systems. Aggregating fishes have the potential to generate areas of increased biogeochemical activity, or hotspots, in streams and rivers. Many of the studies documenting the functional role of fishes in nutrient dynamics have focused on native fish species; however, introduced fishes may restructure nutrient storage and cycling freshwater systems as they can attain high population densities in novel environments. The purpose of this study was to examine the impact of a non-native catfish (Loricariidae: Pterygoplichthys) on nitrogen and phosphorus remineralization and estimate whether large aggregations of these fish generate measurable biogeochemical hotspots within nutrient-limited ecosystems. Loricariids formed large aggregations during daylight hours and dispersed throughout the stream during evening hours to graze benthic habitats. Excretion rates of phosphorus were twice as great during nighttime hours when fishes were actively feeding; however, there was no diel pattern in nitrogen excretion rates. Our results indicate that spatially heterogeneous aggregations of loricariids can significantly elevate dissolved nutrient concentrations via excretion relative to ambient nitrogen and phosphorus concentrations during daylight hours, creating biogeochemical hotspots and potentially altering nutrient dynamics in invaded systems.

Nutrition or detoxification: why bats visit mineral licks of the Amazonian rainforest.

Many animals in the tropics of Africa, Asia and South America regularly visit so-called salt or mineral licks to consume clay or drink clay-saturated water. Whether this behavior is used to supplement diets with locally limited nutrients or to buffer the effects of toxic secondary plant compounds remains unclear. In the Amazonian rainforest, pregnant and lactating bats are frequently observed and captured at mineral licks. We measured the nitrogen isotope ratio in wing tissue of omnivorous short-tailed fruit bats, Carollia perspicillata, and in an obligate fruit-eating bat, Artibeus obscurus, captured at mineral licks and at control sites in the rainforest. Carollia perspicillata with a plant-dominated diet were more often captured at mineral licks than individuals with an insect-dominated diet, although insects were more mineral depleted than fruits. In contrast, nitrogen isotope ratios of A. obscurus did not differ between individuals captured at mineral lick versus control sites. We conclude that pregnant and lactating fruit-eating bats do not visit mineral licks principally for minerals, but instead to buffer the effects of secondary plant compounds that they ingest in large quantities during periods of high energy demand. These findings have potential implications for the role of mineral licks for mammals in general, including humans.