Global investigation of lake habitat coupling by fishes.

Habitat coupling, where consumers acquire resources from different habitats, plays an important role in ecosystem functioning. In this study, we provide a global investigation of lake habitat coupling by freshwater fishes between littoral (nearshore) and pelagic (open water) zones and elucidate the extent to which magnitude of coupling varies according to environmental context and consumer traits. We consider the influence of lake factors (surface area, depth, shoreline complexity, and annual temperature), relative trophic position of consumers, fish community species richness, and fish morphological traits on habitat coupling by fishes. Using a worldwide dataset consisting of fish stable isotope values (δ13C and δ15N), we developed an index of habitat coupling, and used Bayesian hierarchical and non-hierarchical beta regressions to estimate the effects of environmental lake context and morphological traits on habitat coupling by fishes. Our results show high rates of habitat coupling among fishes globally with marked taxonomic differences in the magnitude and variation. Habitat coupling was higher in lower elevation lakes and in regions characterized by relatively colder climates, whereas other environmental context factors had little or no effects on habitat coupling. Furthermore, habitat coupling was associated with several locomotion and feeding traits, but independent from species maximum body length. Overall, we highlight the prevalence of multiple resources supporting fish populations and suggest future research identify implications to ecosystem functioning that may result from alterations to habitat coupling by fishes.

Delayed trophic response of a marine predator to ocean condition and prey availability during the past century.

Understanding the response of predators to ecological change at multiple temporal scales can elucidate critical predator-prey dynamics that would otherwise go unrecognized. We performed compound-specific nitrogen stable isotope analysis of amino acids on 153 harbor seal museum skull specimens to determine how trophic position of this marine predator has responded to ecosystem change over the past century. The relationships between harbor seal trophic position, ocean condition, and prey abundance, were analyzed using hierarchical modeling of a multi-amino-acid framework and applying 1, 2, and 3 years temporal lags. We identified delayed responses of harbor seal trophic position to both physical ocean conditions (upwelling, sea surface temperature, freshwater discharge) and prey availability (Pacific hake, Pacific herring, and Chinook salmon). However, the magnitude and direction of the trophic position response to ecological changes depended on the temporal delay. For example, harbor seal trophic position was negatively associated with summer upwelling but had a 1-year delayed response to summer sea surface temperature, indicating that some predator responses to ecosystem change are not immediately observable. These results highlight the importance of considering dynamic responses of predators to their environment as multiple ecological factors are often changing simultaneously and can take years to propagate up the food web.

Optimizing Amazonian dams for nature.

Algorithms assess opportunities, forgone benefits, and environmental trade-offs.

Stable isotope signatures in historic harbor seal bone link food web-assimilated carbon and nitrogen resources to a century of environmental change.

Anthropogenic climate change will impact nutrient cycles, primary production, and ecosystem structure in the world's oceans, although considerable uncertainty exists regarding the magnitude and spatial variability of these changes. Understanding how regional-scale ocean conditions control nutrient availability and ultimately nutrient assimilation into food webs will inform how marine resources will change in response to climate. To evaluate how ocean conditions influence the assimilation of nitrogen and carbon into coastal marine food webs, we applied a novel dimension reduction analysis to a century of newly acquired molecular isotope data derived from historic harbor seal bone specimens. By measuring bulk δ13 C and δ15 N values of source amino acids of these top predators from 1928 to 2014, we derive indices of primary production and nitrogen resources that are assimilated into food webs. We determined coastal food webs responded to climate regimes, coastal upwelling, and freshwater discharge, yet the strength of responses to individual drivers varied across the northeast Pacific. Indices of primary production and nitrogen availability in the Gulf of Alaska were dependent on regional climate indices (i.e., North Pacific Gyre Oscillation) and upwelling. In contrast, the coastal Washington and Salish Sea food webs were associated with local indices of freshwater discharge. For some regions (eastern Bering Sea, northern Gulf of Alaska) food web-assimilated production was coupled with nitrogen sources; however, other regions demonstrated no production-nitrogen coupling (Salish Sea). Temporal patterns of environmental indices and isotopic data from Washington state varied about the long-term mean with no directional trend. Data from the Gulf of Alaska, however, showed below average harbor seal δ13 C values and above average ocean conditions since 1975, indicating a change in primary production in recent decades. Altogether, these findings demonstrate stable isotope data can provide useful indices of nitrogen resources and phytoplankton dynamics specific to what is assimilated by food webs.

Fluid-preserved fishes are one solution for assessing historical change in fish trophic level.

There are few resources available for assessing historical change in fish trophic dynamics, but specimens held in natural history collections could serve as this resource. In contemporary trophic ecology studies, trophic and source information can be obtained from compound-specific stable isotope analysis of amino acids of nitrogen (CSIA-AA-N).We subjected whole Sebastes ruberrimus and Clupea pallasii to formalin fixation and 70% ethanol preservation. We extracted tissue samples from each fish pre-fixation, after each chemical change, and then in doubling time for 32-64 days once placed in the final preservative. All samples were subjected to CSIA-AA-N, and their glutamic acid and phenylalanine profiles and associated trophic position were examined for differences over time by species.Glutamic acid and phenylalanine values were inconsistent in direction and magnitude, particularly during formalin fixation, but stabilized similarly (in 70% ethanol) among conspecifics. In some cases, the amino acid values of our final samples were significantly different than our initial pre-preservation samples. Nonetheless, significant differences in glutamic acid, phenylalanine, and estimated trophic position were not detected among samples that were in 70% ethanol for >24 hr.Our results suggest that the relative trophic position of fluid-preserved specimens can be estimated using CSIA-AA-N, and CSIA-AA-N estimates for fluid-preserved specimens should only be reported as relative differences. Timelines of trophic position change can be developed by comparing specimens collected at different points in time, revealing trophic information of the past and cryptic ecosystem responses.

Ocean acidification and warming effects on the physiology, skeletal properties, and microbiome of the purple-hinge rock scallop.

Ocean acidification and increased ocean temperature from elevated atmospheric carbon dioxide can significantly influence the physiology, growth and survival of marine organisms. Despite increasing research efforts, there are still many gaps in our knowledge of how these stressors interact to affect economically and ecologically important species. This project is the first to explore the physiological effects of high pCO2 and temperature on the acclimation potential of the purple-hinge rock scallop (Crassadoma gigantea), a widely distributed marine bivalve, important reef builder, and potential aquaculture product. Scallops were exposed to two pCO2 (365 and 1050 µatm) and temperature (14 and 21.5 °C) conditions in a two-factor experimental design. Simultaneous exposure to high temperature and high pCO2 reduced shell strength, decreased outer shell density and increased total lipid content. Despite identical diets, scallops exposed to high pCO2 had higher content of saturated fatty acids, and lower content of polyunsaturated fatty acids suggesting reorganization of fatty acid chains to sustain basic metabolic functions under high pCO2. Metagenomic sequencing of prokaryotes in scallop tissue revealed treatment differences in community composition between treatments and in the presence of genes associated with microbial cell regulation, signaling, and pigmentation. Results from this research highlight the complexity of physiological responses for calcifying species under global change related stress and provide the first insights for understanding the response of a bivalve's microbiome under multiple stressors.

Does lipid-correction introduce biases into isotopic mixing models? Implications for diet reconstruction studies.

Carbon isotopes are commonly used in trophic ecology to estimate consumer diet composition. This estimation is complicated by the fact that lipids exhibit a more depleted carbon signature (δ13C) than other macromolecules, and are often found at different concentrations among individual organisms. Some researchers argue that lipids bias diet reconstructions using stable isotopes and should be accounted for prior to analysis in food web mixing models, whereas others contend that removing lipids may result in erroneous interpretations of the trophic interactions under study. To highlight this disagreement on best practices for applying δ13C in food web studies, we sampled the recent literature to determine the frequency and method of lipid-correction. We then quantified the potential magnitude and source of bias in mixing model results from a theoretical example and case study of diet reconstruction. The literature was split nearly evenly as to whether lipid-correction was applied to δ13C data in mixing model estimates of diet composition. Comparative mixing model scenarios demonstrated that lipid-correction can substantially alter the estimated diet composition and interpretation of consumer foraging habits. Given the lack of consensus on whether or not to lipid-correct prey and/or consumers, and the associated variation in mixing model results, we call for the establishment of a unified framework that will guide diet reconstruction in stable isotope ecology. Uncertainty in the prevalence of direct routing versus de novo synthesis of lipids across ecosystems, taxa, and trophic levels must be resolved to better guide treatment of lipids in isotope studies using carbon.

Response to Comment on "Designing river flows to improve food security futures in the Lower Mekong Basin".

Williams et al claim that the data used in Sabo et al were improperly scaled to account for fishing effort, thereby invalidating the analysis. Here, we reanalyze the data rescaled per Williams et al and following the methods in Sabo et al Our original conclusions are robust to rescaling, thereby invalidating the assertion that our original analysis is invalid.

Monitoring of tropical freshwater fish resources for sustainable use.

Tropical freshwater ecosystems are some of the world's most biodiverse and productive systems where determining what sustainable exploitation of inland fisheries looks like is particularly challenging. One of the greatest obstacles to sustainable management is collecting and using quality data on fish production and yield. The biodiversity and hydro-ecology of these systems often under open-access governance, add to the complexity of managing them. This paper describes an integrated citizen-science, earth observation, environmental DNA and independent survey approach to collecting fish and fisheries data, using the Cambodian Mekong as a case study.

Consumer trophic positions respond variably to seasonally fluctuating environments.

The effects of environmental seasonality on food web structure have been notoriously understudied in empirical ecology. Here, we focus on seasonal changes in one key attribute of a food web, consumer trophic position. We ask whether fishes inhabiting tropical river-floodplain ecosystems behave as seasonal omnivores, by shifting their trophic positions in relation to the annual flood pulse, or whether they feed at the same trophic position all year, as much empirical work implicitly assumes. Using dietary data from the Tonle Sap Lake, Cambodia, and a literature review, we find evidence that some fishes, especially small piscivores, increased consumption of invertebrates and/or plant material during the wet season, as predicted. However, nitrogen stable isotope (δ15 N) data for 26 Tonle Sap fishes, spanning a broader range of functional groups, uncovered high variation in seasonal trophic position responses among species (0 to ±0.52 trophic positions). Based on these findings, species respond to the flood pulse differently. Diverse behavioral responses to seasonality, underpinned by spatiotemporal variation at multiple scales, could be central for rerouting matter and energy flow in these dynamic ecosystems. Seasonally flexible foraging behaviors warrant further study given their potential influence on food web dynamics in a range of fluctuating environments.

An assessment of assumptions and uncertainty in deuterium-based estimates of terrestrial subsidies to aquatic consumers.

The deuterium ratio (2 H/1 H) in tissue is often used to estimate terrestrial subsidies to aquatic consumers because of strongly differentiated values between terrestrial and aquatic primary producers. However, quantitative deuterium-based analyses of terrestrial resource assimilation are highly dependent on several poorly defined assumptions. We explored the sensitivity of these estimates to assumptions regarding environmental water contributions to consumer deuterium content (ω) and algal photosynthetic hydrogen discrimination (εH ). We also tested whether 13 C/12 C and 2 H/1 H-based estimates of terrestrial resource assimilation give similar outcomes. The average of the 12 experiments that have directly estimated proportional contributions of environmental water to consumer tissue 2 H/1 H was 0.27 ± 0.11 (mean ± SD), with similar values for invertebrates and fish. Conversely, of the 28 field studies that have used 2 H/1 H to characterize aquatic food webs, all but one assume a value that is less than our current best estimate, usually substantially less. A reanalysis of the raw data from four recent case studies indicates the calculated terrestrial contribution to aquatic consumers is extremely sensitive to this assumption. When the authors' original assumptions were used (i.e., ω = 0.16 ± 0.05), the estimated proportional contribution of terrestrial resources to aquatic consumers (θT ) averaged 29 ± 17%, and when ω = 0.27 was used the average estimated assimilation of allochthonous resources was ≈0.00. A compilation of published photosynthetic hydrogen discrimination values for microalgae averaged εH  = -150 ± 27‰ (SD, n = 99), and a sensitivity analysis showed the outcomes of these calculations were also strongly influenced by uncertainty in εH . There was no statistical association between 13 C/12 C and 2 H/1 H-based estimates of terrestrial subsidies (r = -0.12, n = 274). This analysis indicates that the assumptions in deuterium-based estimates of terrestrial resource assimilation are highly influential but poorly constrained; therefore, the impact of these assumptions on calculated outputs must be carefully assessed and thoroughly reported. Due to the highly uncertain assumptions inherent in deuterium-based analyses, we urge much more caution when using this approach to estimate terrestrial subsidies to consumers in aquatic ecosystems.

A Fatty Acid Based Bayesian Approach for Inferring Diet in Aquatic Consumers.

We modified the stable isotope mixing model MixSIR to infer primary producer contributions to consumer diets based on their fatty acid composition. To parameterize the algorithm, we generated a 'consumer-resource library' of FA signatures of Daphnia fed different algal diets, using 34 feeding trials representing diverse phytoplankton lineages. This library corresponds to the resource or producer file in classic Bayesian mixing models such as MixSIR or SIAR. Because this library is based on the FA profiles of zooplankton consuming known diets, and not the FA profiles of algae directly, trophic modification of consumer lipids is directly accounted for. To test the model, we simulated hypothetical Daphnia comprised of 80% diatoms, 10% green algae, and 10% cryptophytes and compared the FA signatures of these known pseudo-mixtures to outputs generated by the mixing model. The algorithm inferred these simulated consumers were comprised of 82% (63-92%) [median (2.5th to 97.5th percentile credible interval)] diatoms, 11% (4-22%) green algae, and 6% (0-25%) cryptophytes. We used the same model with published phytoplankton stable isotope (SI) data for δ13C and δ15N to examine how a SI based approach resolved a similar scenario. With SI, the algorithm inferred that the simulated consumer assimilated 52% (4-91%) diatoms, 23% (1-78%) green algae, and 18% (1-73%) cyanobacteria. The accuracy and precision of SI based estimates was extremely sensitive to both resource and consumer uncertainty, as well as the trophic fractionation assumption. These results indicate that when using only two tracers with substantial uncertainty for the putative resources, as is often the case in this class of analyses, the underdetermined constraint in consumer-resource SI analyses may be intractable. The FA based approach alleviated the underdetermined constraint because many more FA biomarkers were utilized (n < 20), different primary producers (e.g., diatoms, green algae, and cryptophytes) have very characteristic FA compositions, and the FA profiles of many aquatic primary consumers are strongly influenced by their diets.

Patterns of ecosystem metabolism in the Tonle Sap Lake, Cambodia with links to capture fisheries.

The Tonle Sap Lake in Cambodia is a dynamic flood-pulsed ecosystem that annually increases its surface area from roughly 2,500 km(2) to over 12,500 km(2) driven by seasonal flooding from the Mekong River. This flooding is thought to structure many of the critical ecological processes, including aquatic primary and secondary productivity. The lake also has a large fishery that supports the livelihoods of nearly 2 million people. We used a state-space oxygen mass balance model and continuous dissolved oxygen measurements from four locations to provide the first estimates of gross primary productivity (GPP) and ecosystem respiration (ER) for the Tonle Sap. GPP averaged 4.1±2.3 g O2 m(-3) d(-1) with minimal differences among sites. There was a negative correlation between monthly GPP and lake level (r = 0.45) and positive correlation with turbidity (r = 0.65). ER averaged 24.9±20.0 g O2 m(-3) d(-1) but had greater than six-fold variation among sites and minimal seasonal change. Repeated hypoxia was observed at most sampling sites along with persistent net heterotrophy (GPP

Centennial-scale fluctuations and regional complexity characterize Pacific salmon population dynamics over the past five centuries.

Observational data from the past century have highlighted the importance of interdecadal modes of variability in fish population dynamics, but how these patterns of variation fit into a broader temporal and spatial context remains largely unknown. We analyzed time series of stable nitrogen isotopes from the sediments of 20 sockeye salmon nursery lakes across western Alaska to characterize temporal and spatial patterns in salmon abundance over the past ∼500 y. Although some stocks varied on interdecadal time scales (30- to 80-y cycles), centennial-scale variation, undetectable in modern-day catch records and survey data, has dominated salmon population dynamics over the past 500 y. Before 1900, variation in abundance was clearly not synchronous among stocks, and the only temporal signal common to lake sediment records from this region was the onset of commercial fishing in the late 1800s. Thus, historical changes in climate did not synchronize stock dynamics over centennial time scales, emphasizing that ecosystem complexity can produce a diversity of ecological responses to regional climate forcing. Our results show that marine fish populations may alternate between naturally driven periods of high and low abundance over time scales of decades to centuries and suggest that management models that assume time-invariant productivity or carrying capacity parameters may be poor representations of the biological reality in these systems.

Temperature-associated population diversity in salmon confers benefits to mobile consumers.

Habitat heterogeneity can generate intraspecific diversity through local adaptation of populations. While it is becoming increasingly clear that population diversity can increase stability in species abundance, less is known about how population diversity can benefit consumers that can integrate across population diversity in their prey. Here we demonstrate cascading effects of thermal heterogeneity on trout-salmon interactions in streams where rainbow trout rely heavily on the seasonal availability of anadromous salmon eggs. Water temperature in an Alaskan stream varied spatially from 5 degrees C to 17.5 degrees C, and spawning sockeye salmon showed population differentiation associated with this thermal heterogeneity. Individuals that spawned early in cool regions of the 5 km long stream were genetically differentiated from those spawning in warmer regions later in the season. Sockeye salmon spawning generates a pulsed resource subsidy that supports the majority of seasonal growth in stream-dwelling rainbow trout. The spatial and temporal structuring of sockeye salmon spawn timing in our focal stream extended the duration of the pulsed subsidy compared to a thermally homogeneous stream with a single population of salmon. Further, rainbow trout adopted movement strategies that exploited the multiple pulses of egg subsidies in the thermally heterogeneous stream. Fish that moved to track the resource pulse grew at rates about 2.5 times higher than those that remained stationary or trout in the reference stream with a single seasonal pulse of eggs. Our results demonstrate that habitat heterogeneity can have important effects on the population diversity of dominant species, and in turn, influence their value to species that prey upon them. Therefore, habitat homogenization may have farther-reaching ecological effects than previously considered.

A coherent signature of anthropogenic nitrogen deposition to remote watersheds of the Northern Hemisphere.

Humans have more than doubled the amount of reactive nitrogen (Nr) added to the biosphere, yet most of what is known about its accumulation and ecological effects is derived from studies of heavily populated regions. Nitrogen (N) stable isotope ratios ((15)N:(14)N) in dated sediments from 25 remote Northern Hemisphere lakes show a coherent signal of an isotopically distinct source of N to ecosystems beginning in 1895 ± 10 years (±1 standard deviation). Initial shifts in N isotope composition recorded in lake sediments coincide with anthropogenic CO(2) emissions but accelerate with widespread industrial Nr production during the past half century. Although current atmospheric Nr deposition rates in remote regions are relatively low, anthropogenic N has probably influenced watershed N budgets across the Northern Hemisphere for over a century.

Marine-derived nutrients, bioturbation, and ecosystem metabolism: reconsidering the role of salmon in streams.

In coastal areas of the North Pacific Ocean, annual returns of spawning salmon provide a substantial influx of nutrients and organic matter to streams and are generally believed to enhance the productivity of recipient ecosystems. Loss of this subsidy from areas with diminished salmon runs has been hypothesized to limit ecosystem productivity in juvenile salmon rearing habitats (lakes and streams), thereby reinforcing population declines. Using five to seven years of data from an Alaskan stream supporting moderate salmon densities, we show that salmon predictably increased stream water nutrient concentrations, which were on average 190% (nitrogen) and 390% (phosphorus) pre-salmon values, and that primary producers incorporated some of these nutrients into tissues. However, benthic algal biomass declined by an order of magnitude despite increased nutrients. We also measured changes in stream ecosystem metabolic properties, including gross primary productivity (GPP) and ecosystem respiration (ER), from three salmon streams by analyzing diel measurements of oxygen concentrations and stable isotopic ratios (delta O-O2) within a Bayesian statistical model of oxygen dynamics. Our results do not support a shift toward higher primary productivity with the return of salmon, as is expected from a nutrient fertilization mechanism. Rather, net ecosystem metabolism switched from approximately net autotrophic (GPP > or = ER) to a strongly net heterotrophic state (GPP << ER) in response to bioturbation of benthic habitats by salmon. Following the seasonal arrival of salmon, GPP declined to <12% of pre-salmon rates, while ER increased by over threefold. Metabolism by live salmon could not account for the observed increase in ER early in the salmon run, suggesting salmon nutrients and disturbance enhanced in situ heterotrophic respiration. Salmon also changed the physical properties of the stream, increasing air-water gas exchange by nearly 10-fold during peak spawning. We suggest that management efforts to restore salmon ecosystems should consider effects on ecosystem metabolic properties and how salmon disturbance affects the incorporation of marine-derived nutrients into food webs.

Habitat structure determines resource use by zooplankton in temperate lakes.

While the importance of terrestrial linkages to aquatic ecosystems is well appreciated, the degree of terrestrial support of aquatic consumers remains debated. Estimates of terrestrial contributions to lake zooplankton have omitted a key food source, phytoplankton produced below the mixed layer. We used carbon and nitrogen stable isotope data from 25 Pacific Northwest lakes to assess the relative importance of particulate organic matter (POM) from the mixed layer, below the mixed layer and terrestrial detritus to zooplankton. Zooplankton and deep POM were depleted in ¹³C relative to mixed layer POM in lakes that can support deep primary production. A Bayesian stable isotope mixing model estimated that terrestrial detritus contributed <5% to zooplankton production, and confirms the role of lake optical and thermal properties; deep POM accounted for up to 80% of zooplankton production in the clearest lakes. These results suggest terrestrial support of lake zooplankton production is trivial.

Bioaccumulation and transport of contaminants: migrating sockeye salmon as vectors of mercury.

Biological transport by migratory animals is increasingly recognized as important to the long-range dispersal of toxic contaminants. Mercury (Hg) contamination is a widespread environmental concern with serious health implications for humans and wildlife. Due to their unique life history, anadromous salmon may act as important vectors for this contaminant, transferring Hg between marine and freshwater ecosystems. Previous analyses have considered contaminant transport by salmon to be unidirectional. These studies have evaluated Hg import to freshwater by spawning adults, but have not quantitatively assessed export through the migration of juveniles to the ocean. To determine the total Hg burden to freshwater systems by sockeye salmon, we reconstructed the net transport of Hg to the Wood River System in Bristol Bay, Alaska accounting for fluxes in (via adults) and out (via juveniles) of the system. Hg concentrations were higher in juvenile than adult salmon. Hg export from freshwater systems by salmon ranged from 3 to 30% of total import. Proportional export by smolts may be higher for populations under heavy exploitation with strong density dependence in juvenile recruitment. Full consideration of contaminant loading by migratory species requires attention to the relative contaminant flux at all life history stages and the effects of density dependent growth and survival.

Biotic control of stream fluxes: spawning salmon drive nutrient and matter export.

Organisms can control movements of nutrients and matter by physically modifying habitat. We examined how an ecosystem engineer, sockeye salmon (Oncorhynchus nerka), influences seasonal fluxes of sediments, nitrogen (N), and phosphorus (P) in streams of southwestern Alaska. The purpose of this study was to investigate whether salmon act as net importers or net exporters of matter and nutrients from streams and how these roles change as a function of salmon population density. We measured discharge and concentrations of suspended sediments and total N and P every 7-14 days for up to four summers in 10 streams spanning a gradient in salmon densities. We statistically allocated whole-season fluxes to salmon activities, such as excretion and bioturbation, and to export by hydrologic discharge. In addition, we used counts of spawning salmon to estimate nutrient and matter imports by salmon to streams. Large seasonal pulses of suspended sediments, P, and N were associated with salmon spawning activities, often increasing export an order of magnitude higher than during pre-salmon levels. Years and streams with more salmon had significantly higher levels of export of sediments and nutrients. In addition, years with higher precipitation had higher background export of P and N. Salmon exported an average of the equivalent of 189%, 60%, and 55% of total matter, P, and N that salmon imported in their bodies. The relative magnitude of export varied; salmon exported more than their bodies imported in 80%, 20%, and 16% across all streams and years for sediments, P, and N, respectively. A bioassay experiment indicated that the P exported by salmon is directly available for use by primary producers in the downstream lake. These results demonstrate that salmon not only move nutrients upstream on large spatial scales via their migration from the ocean and subsequent death, but also redistribute matter and nutrients on finer spatial scales through their spawning activities.