Anticipating responses to climate change and planning for resilience in California's freshwater ecosystems.

As human-caused climate changes accelerate, California will experience hydrologic and temperature conditions different than any encountered in recorded history. How will these changes affect the state's freshwater ecosystems? Rivers, lakes, and wetlands are managed as a water resource, but they also support a complex web of life, ranging from bacteria, fungi, and algae to macrophytes, woody plants, invertebrates, fish, amphibians, reptiles, birds, and mammals. In much of the state, native freshwater organisms already struggle to survive massive water diversions and dams, deteriorating water quality, extensive land cover modification for agriculture and urban development, and invasions of exotic species. In the face of climate change, we need to expand efforts to recover degraded ecosystems and to protect the resilience, health, and viability of existing ecosystems. For this, more process-based understanding of river, lake, and wetlands ecosystems is needed to forecast how systems will respond to future climate change and to our interventions. This will require 1) expanding our ability to model mechanistically how freshwater biota and ecosystems respond to environmental change; 2) hypothesis-driven monitoring and field studies; 3) education and training to build research, practitioner, stewardship, and policy capabilities; and 4) developing tools and policies for building resilient ecosystems. A goals-driven, hypothesis-informed collaboration among tribes, state (and federal) agencies, nongovernmental organizations, academicians, and consultants is needed to accomplish these goals and to advance the skills and knowledge of the future workforce of practitioners, regulators, and researchers who must live with the climate changes that are already upon us and will intensify.

Clades of huge phages from across Earth's ecosystems.

Bacteriophages typically have small genomes1 and depend on their bacterial hosts for replication2. Here we sequenced DNA from diverse ecosystems and found hundreds of phage genomes with lengths of more than 200 kilobases (kb), including a genome of 735 kb, which is-to our knowledge-the largest phage genome to be described to date. Thirty-five genomes were manually curated to completion (circular and no gaps). Expanded genetic repertoires include diverse and previously undescribed CRISPR-Cas systems, transfer RNAs (tRNAs), tRNA synthetases, tRNA-modification enzymes, translation-initiation and elongation factors, and ribosomal proteins. The CRISPR-Cas systems of phages have the capacity to silence host transcription factors and translational genes, potentially as part of a larger interaction network that intercepts translation to redirect biosynthesis to phage-encoded functions. In addition, some phages may repurpose bacterial CRISPR-Cas systems to eliminate competing phages. We phylogenetically define the major clades of huge phages from human and other animal microbiomes, as well as from oceans, lakes, sediments, soils and the built environment. We conclude that the large gene inventories of huge phages reflect a conserved biological strategy, and that the phages are distributed across a broad bacterial host range and across Earth's ecosystems.

Synthetic threads through the web of life.

CRISPR-Cas gene editing tools have brought us to an era of synthetic biology that will change the world. Excitement over the breakthroughs these tools have enabled in biology and medicine is balanced, justifiably, by concern over how their applications might go wrong in open environments. We do not know how genomic processes (including regulatory and epigenetic processes), evolutionary change, ecosystem interactions, and other higher order processes will affect traits, fitness, and impacts of edited organisms in nature. However, anticipating the spread, change, and impacts of edited traits or organisms in heterogeneous, changing environments is particularly important with "gene drives on the horizon." To anticipate how "synthetic threads" will affect the web of life on Earth, scientists must confront complex system interactions across many levels of biological organization. Currently, we lack plans, infrastructure, and funding for field science and scientists to track new synthetic organisms, with or without gene drives, as they move through open environments.

Microcoleus (Cyanobacteria) form watershed-wide populations without strong gradients in population structure.

The relative importance of separation by distance and by environment to population genetic diversity can be conveniently tested in river networks, where these two drivers are often independently distributed over space. To evaluate the importance of dispersal and environmental conditions in shaping microbial population structures, we performed genome-resolved metagenomic analyses of benthic Microcoleus-dominated cyanobacterial mats collected in the Eel and Russian River networks (California, USA). The 64 Microcoleus genomes were clustered into three species that shared >96.5% average nucleotide identity (ANI). Most mats were dominated by one strain, but minor alleles within mats were often shared, even over large spatial distances (>300 km). Within the most common Microcoleus species, the ANI between the dominant strains within mats decreased with increasing spatial separation. However, over shorter spatial distances (tens of kilometres), mats from different subwatersheds had lower ANI than mats from the same subwatershed, suggesting that at shorter spatial distances environmental differences between subwatersheds in factors like canopy cover, conductivity, and mean annual temperature decreases ANI. Since mats in smaller creeks had similar levels of nucleotide diversity (π) as mats in larger downstream subwatersheds, within-mat genetic diversity does not appear to depend on the downstream accumulation of upstream-derived strains. The four-gamete test and sequence length bias suggest recombination occurs between almost all strains within each species, even between populations separated by large distances or living in different habitats. Overall, our results show that, despite some isolation by distance and environmental conditions, sufficient gene-flow occurs among cyanobacterial strains to prevent either driver from producing distinctive population structures across the watershed.

Blue Waters, Green Bottoms: Benthic Filamentous Algal Blooms Are an Emerging Threat to Clear Lakes Worldwide.

Nearshore (littoral) habitats of clear lakes with high water quality are increasingly experiencing unexplained proliferations of filamentous algae that grow on submerged surfaces. These filamentous algal blooms (FABs) are sometimes associated with nutrient pollution in groundwater, but complex changes in climate, nutrient transport, lake hydrodynamics, and food web structure may also facilitate this emerging threat to clear lakes. A coordinated effort among members of the public, managers, and scientists is needed to document the occurrence of FABs, to standardize methods for measuring their severity, to adapt existing data collection networks to include nearshore habitats, and to mitigate and reverse this profound structural change in lake ecosystems. Current models of lake eutrophication do not explain this littoral greening. However, a cohesive response to it is essential for protecting some of the world's most valued lakes and the flora, fauna, and ecosystem services they sustain.

Effects of the hippopotamus on the chemistry and ecology of a changing watershed.

Cross-boundary transfers of nutrients can profoundly shape the ecology of recipient systems. The common hippopotamus, Hippopotamus amphibius, is a significant vector of such subsidies from terrestrial to river ecosystems. We compared river pools with high and low densities of H. amphibius to determine how H. amphibius subsidies shape the chemistry and ecology of aquatic communities. Our study watershed, like many in sub-Saharan Africa, has been severely impacted by anthropogenic water abstraction reducing dry-season flow to zero. We conducted observations for multiple years over wet and dry seasons to identify how hydrological variability influences the impacts of H. amphibius During the wet season, when the river was flowing, we detected no differences in water chemistry and nutrient parameters between pools with high and low densities of H. amphibius Likewise, the diversity and abundance of fish and aquatic insect communities were indistinguishable. During the dry season, however, high-density H. amphibius pools differed drastically in almost all measured attributes of water chemistry and exhibited depressed fish and insect diversity and fish abundance compared with low-density H. amphibius pools. Scaled up to the entire watershed, we estimate that H. amphibius in this hydrologically altered watershed reduces dry-season fish abundance and indices of gamma-level diversity by 41% and 16%, respectively, but appears to promote aquatic invertebrate diversity. Widespread human-driven shifts in hydrology appear to redefine the role of H. amphibius, altering their influence on ecosystem diversity and functioning in a fashion that may be more severe than presently appreciated.

Eighty years of food-web response to interannual variation in discharge recorded in river diatom frustules from an ocean sediment core.

Little is known about the importance of food-web processes as controls of river primary production due to the paucity of both long-term studies and of depositional environments which would allow retrospective fossil analysis. To investigate how freshwater algal production in the Eel River, northern California, varied over eight decades, we quantified siliceous shells (frustules) of freshwater diatoms from a well-dated undisturbed sediment core in a nearshore marine environment. Abundances of freshwater diatom frustules exported to Eel Canyon sediment from 1988 to 2001 were positively correlated with annual biomass of Cladophora surveyed over these years in upper portions of the Eel basin. Over 28 years of contemporary field research, peak algal biomass was generally higher in summers following bankfull, bed-scouring winter floods. Field surveys and experiments suggested that bed-mobilizing floods scour away overwintering grazers, releasing algae from spring and early summer grazing. During wet years, growth conditions for algae could also be enhanced by increased nutrient loading from the watershed, or by sustained summer base flows. Total annual rainfall and frustule densities in laminae over a longer 83-year record were weakly and negatively correlated, however, suggesting that positive effects of floods on annual algal production were primarily mediated by "top-down" (consumer release) rather than "bottom-up" (growth promoting) controls.

Diverse effects of the common hippopotamus on plant communities and soil chemistry.

The ecological importance of the common hippopotamus (Hippopotamus amphibius) in aquatic ecosystems is becoming increasingly well known. These unique megaherbivores are also likely to have a formative influence on the terrestrial ecosystems in which they forage. In this study, we employed a novel exclosure design to exclude H. amphibius from experimental plots on near-river grasslands. Our three-year implementation of this experiment revealed a substantial influence of H. amphibius removal on both plant communities and soil chemistry. H. amphibius significantly reduced grassland canopy height, increased the leafiness of common grasses, reduced woody plant abundance and size, and increased the concentrations of several soil elements. Many of the soil chemistry changes that we experimentally induced by exclusion of H. amphibius were mirrored in the soil chemistry differences between naturally occurring habitats of frequent (grazing lawns) and infrequent (shrub forest) use by H. amphibius and other grazing herbivores. In contrast to existing hypotheses regarding grazing species, we found that H. amphibius had little effect on local plant species richness. Simultaneous observations of exclosures designed to remove all large herbivores revealed that H. amphibius removal had ecologically significant impacts, but that the removal of all species of large herbivores generated more pronounced impacts than the removal of H. amphibius alone. In aggregate, our results suggest that H. amphibius have myriad effects on their terrestrial habitats that likely improve the quality of forage available for other herbivores. We suggest that ongoing losses of this vulnerable megaherbivore are likely to cause significant ecological change.

Integrating the invisible fabric of nature into fisheries management.

Overfishing and environmental change have triggered many severe and unexpected consequences. As existing communities have collapsed, new ones have become established, fundamentally transforming ecosystems to those that are often less productive for fisheries, more prone to cycles of booms and busts, and thus less manageable. We contend that the failure of fisheries science and management to anticipate these transformations results from a lack of appreciation for the nature, strength, complexity, and outcome of species interactions. Ecologists have come to understand that networks of interacting species exhibit nonlinear dynamics and feedback loops that can produce sudden and unexpected shifts. We argue that fisheries science and management must follow this lead by developing a sharper focus on species interactions and how disrupting these interactions can push ecosystems in which fisheries are embedded past their tipping points.

A keystone ecologist: Robert Treat Paine, 1933-2016.

Robert T. Paine, who passed away on 13 June 2016, is among the most influential people in the history of ecology. Paine was an experimentalist, a theoretician, a practitioner, and proponent of the "ecology of place," and a deep believer in the importance of natural history to ecological understanding. His scientific legacy grew from the discovery of a link between top-down forcing and species diversity, a breakthrough that led to the ideas of both keystone species and trophic cascades, and to our early understanding of the mosaic nature of biological communities, causes of zonation across physical gradients, and the intermediate-disturbance hypothesis of species diversity. Paine's influence as a mentor was equally important to the growth of ecological thinking, natural resource conservation, and policy. He served ecology as an Ecological Society of America president, an editor of the Society's journals, a member of and contributor to the National Academy of Sciences and the National Research Council, and an in-demand advisor to various state and federal agencies. Paine's broad interests, enthusiasm, charisma, and humor deeply affected our lives and the lives of so many others.

Mainstem-tributary linkages by mayfly migration help sustain salmonids in a warming river network.

Animal migrations can link ecosystems across space. We discovered an aquatic insect that migrates between a river mainstem and its tributaries, and provides an important trophic subsidy for tributary predators. A mayfly, Ephemerella maculata, rears in a warm, sunlit productive river mainstem, then migrates as adults to cool, shaded unproductive tributaries where they oviposit and die. This migration tripled insect flux into a tributary for 1 month in summer. A manipulative field experiment showed that this E. maculata subsidy nearly tripled the growth of the young of the year steelhead trout (Oncorhynchus mykiss) in the recipient tributary over the summer months, and was more important than terrestrial invertebrate subsidies, which have been considered the primary food source for predators in small, forested creeks. By delivering food subsidies from productive but warming river mainstems to cool but food-limited tributaries, aquatic insect migrations could enhance resilience to cool-water predators in warming river networks.

High Time for Conservation: Adding the Environment to the Debate on Marijuana Liberalization.

The liberalization of marijuana policies, including the legalization of medical and recreational marijuana, is sweeping the United States and other countries. Marijuana cultivation can have significant negative collateral effects on the environment that are often unknown or overlooked. Focusing on the state of California, where by some estimates 60%-70% of the marijuana consumed in the United States is grown, we argue that (a) the environmental harm caused by marijuana cultivation merits a direct policy response, (b) current approaches to governing the environmental effects are inadequate, and

Structural and functional loss in restored wetland ecosystems.

Wetlands are among the most productive and economically valuable ecosystems in the world. However, because of human activities, over half of the wetland ecosystems existing in North America, Europe, Australia, and China in the early 20th century have been lost. Ecological restoration to recover critical ecosystem services has been widely attempted, but the degree of actual recovery of ecosystem functioning and structure from these efforts remains uncertain. Our results from a meta-analysis of 621 wetland sites from throughout the world show that even a century after restoration efforts, biological structure (driven mostly by plant assemblages), and biogeochemical functioning (driven primarily by the storage of carbon in wetland soils), remained on average 26% and 23% lower, respectively, than in reference sites. Either recovery has been very slow, or postdisturbance systems have moved towards alternative states that differ from reference conditions. We also found significant effects of environmental settings on the rate and degree of recovery. Large wetland areas (>100 ha) and wetlands restored in warm (temperate and tropical) climates recovered more rapidly than smaller wetlands and wetlands restored in cold climates. Also, wetlands experiencing more (riverine and tidal) hydrologic exchange recovered more rapidly than depressional wetlands. Restoration performance is limited: current restoration practice fails to recover original levels of wetland ecosystem functions, even after many decades. If restoration as currently practiced is used to justify further degradation, global loss of wetland ecosystem function and structure will spread.

Variation in terrestrial and aquatic sources of methylmercury in stream predators as revealed by stable mercury isotopes.

Mercury (Hg) is widely distributed in the environment, and its organic form, methylmercury (MeHg), can extensively bioaccumulate and biomagnify in aquatic and terrestrial food webs. Concentrations of MeHg in organisms are highly variable, and the sources in natural food webs are often not well understood. This study examined stable isotope ratios of MeHg (mass-dependent fractionation, as δ(202)HgMeHg; and mass-independent fractionation, as Δ(199)HgMeHg) in benthic invertebrates, juvenile steelhead trout (Oncorhynchus mykiss), and water striders (Gerris remigis) along a stream productivity gradient, as well as carnivorous terrestrial invertebrates, in a forested watershed at the headwater of South Fork Eel River in northern California. Throughout the sampling sites, δ(202)HgMeHg (after correction due to the effect of MeHg photodegradation) was significantly different between benthic (median = -1.40‰; range, -2.34 to -0.78‰; total number of samples = 29) and terrestrial invertebrates (median = +0.51‰; range, -0.37 to +1.40‰; total number of samples = 9), but no major difference between these two groups was found for Δ(199)HgMeHg. Steelhead trout (52 individual fishes) have MeHg of predominantly aquatic origins, with a few exceptions at the upstream locations (e.g., 1 fish collected in a tributary had a purely terrestrial MeHg source and 4 fishes had mixed aquatic and terrestrial MeHg sources). Water striders (seven pooled samples) derive MeHg largely from terrestrial sources throughout headwater sections. These data suggest that direct terrestrial subsidy (e.g., terrestrial invertebrates falling into water) can be important for some stream predators in headwater streams and could represent an important means of transfer of terrestrially derived MeHg (e.g., in situ methylation within forests, atmospheric sources) to aquatic ecosystems. Moreover, these findings show that terrestrial subsidies can enhance MeHg bioaccumulation of consumers in headwater streams where aqueous MeHg levels are very low.

Predicting and detecting reciprocity between indirect ecological interactions and evolution.

Living nature can be thought of as a tapestry, defined not only by its constituent parts but also by how these parts are woven together. The weaving of this tapestry is a metaphor for species interactions, which can be divided into three broad classes: competitive, mutualistic, and consumptive. Direct interactions link together as more complex networks, for example, the joining of consumptive interactions into food webs. Food web dynamics are driven, in turn, by changes in the abundances of web members, whose numbers or biomass respond to bottom-up (resource limitation) and top-down (consumer limitation) forcing. The relative strengths of top-down and bottom-up forcing on the abundance of a given web member depend on its ecological context, including its topological position within the food web. Top-down effects by diverse consumers are nearly ubiquitous, in many cases influencing the structure and operation of ecosystems. While the ecological effects of such interactions are well known, far less is known of their evolutionary consequences. In this essay, we describe sundry consequences of these interaction chains on species and ecosystem processes, explain several known or suspected evolutionary effects of consumer-induced interaction chains, and identify areas where reciprocity between ecology and evolution involving the indirect effects of consumer-prey interaction chains might be further explored.

Effects of flow regimes altered by dams on survival, population declines, and range-wide losses of California river-breeding frogs.

Widespread alteration of natural hydrologic patterns by large dams combined with peak demands for power and water delivery during summer months have resulted in frequent aseasonal flow pulses in rivers of western North America. Native species in these ecosystems have evolved with predictable annual flood-drought cycles; thus, their likelihood of persistence may decrease in response to disruption of the seasonal synchrony between stable low-flow conditions and reproduction. We evaluated whether altered flow regimes affected 2 native frogs in California and Oregon (U.S.A.) at 4 spatial and temporal extents. We examined changes in species distribution over approximately 50 years, current population density in 11 regulated and 16 unregulated rivers, temporal trends in abundance among populations occupying rivers with different hydrologic histories, and within-year patterns of survival relative to seasonal hydrology. The foothill yellow-legged frog (Rana boylii), which breeds only in flowing water, is more likely to be absent downstream of large dams than in free-flowing rivers, and breeding populations are on average 5 times smaller in regulated rivers than in unregulated rivers. Time series data (range = 8 - 19 years) from 5 populations of yellow-legged frogs and 2 populations of California red-legged frogs (R. draytonii) across a gradient of natural to highly artificial timing and magnitude of flooding indicate that variability of flows in spring and summer is strongly correlated with high mortality of early life stages and subsequent decreases in densities of adult females. Flow management that better mimics natural flow timing is likely to promote persistence of these species and others with similar phenology.

Priority effects in microbiome assembly.

Advances in next-generation sequencing have enabled the widespread measurement of microbiome composition across systems and over the course of microbiome assembly. Despite substantial progress in understanding the deterministic drivers of community composition, the role of historical contingency remains poorly understood. The establishment of new species in a community can depend on the order and/or timing of their arrival, a phenomenon known as a priority effect. Here, we review the mechanisms of priority effects and evidence for their importance in microbial communities inhabiting a range of environments, including the mammalian gut, the plant phyllosphere and rhizosphere, soil, freshwaters and oceans. We describe approaches for the direct testing and prediction of priority effects in complex microbial communities and illustrate these with re-analysis of publicly available plant and animal microbiome datasets. Finally, we discuss the shared principles that emerge across study systems, focusing on eco-evolutionary dynamics and the importance of scale. Overall, we argue that predicting when and how current community state impacts the success of newly arriving microbial taxa is crucial for the management of microbiomes to sustain ecological function and host health. We conclude by discussing outstanding conceptual and practical challenges that are faced when measuring priority effects in microbiomes.

Light-mediated thresholds in stream-water nutrient composition in a river network.

The elemental composition of solutes transported by rivers reflects combined influences of surrounding watersheds and transformations within stream networks, yet comparatively little is known about downstream changes in effects of watershed loading vs. in-channel processes. In the forested watershed of a river under a mediterranean hydrologic regime, we examined the influence of longitudinal changes in environmental conditions on water-column nutrient composition during summer base flow across a network of sites ranging from strongly heterotrophic headwater streams to larger, more autotrophic sites downstream. Small streams (0.1-10 km2 watershed area) had longitudinally similar nutrient concentration and composition with low (approximately 2) dissolved nitrogen (N) to phosphorus (P) ratios. Abrupt deviations from this pattern were observed in larger streams with watershed areas > 100 km2 where insolation and algal abundance and production rapidly increased. Downstream, phosphorus and silica concentrations decreased by > 50% compared to headwater streams, and dissolved organic carbon and nitrogen increased by approximately 3-6 times. Decreasing dissolved P and increasing dissolved N raised stream-water N:P to 46 at the most downstream sites, suggesting a transition from N limitation in headwaters to potential P limitation in larger channels. We hypothesize that these changes were mediated by increasing algal photosynthesis and N fixation by benthic algal assemblages, which, in response to increasing light availability, strongly altered stream-water nutrient concentration and stoichiometry in larger streams and rivers.

The Functional Significance of Bacterial Predators.

Predation structures food webs, influences energy flow, and alters rates and pathways of nutrient cycling through ecosystems, effects that are well documented for macroscopic predators. In the microbial world, predatory bacteria are common, yet little is known about their rates of growth and roles in energy flows through microbial food webs, in part because these are difficult to quantify. Here, we show that growth and carbon uptake were higher in predatory bacteria compared to nonpredatory bacteria, a finding across 15 sites, synthesizing 82 experiments and over 100,000 taxon-specific measurements of element flow into newly synthesized bacterial DNA. Obligate predatory bacteria grew 36% faster and assimilated carbon at rates 211% higher than nonpredatory bacteria. These differences were less pronounced for facultative predators (6% higher growth rates, 17% higher carbon assimilation rates), though high growth and carbon assimilation rates were observed for some facultative predators, such as members of the genera Lysobacter and Cytophaga, both capable of gliding motility and wolf-pack hunting behavior. Added carbon substrates disproportionately stimulated growth of obligate predators, with responses 63% higher than those of nonpredators for the Bdellovibrionales and 81% higher for the Vampirovibrionales, whereas responses of facultative predators to substrate addition were no different from those of nonpredators. This finding supports the ecological theory that higher productivity increases predator control of lower trophic levels. These findings also indicate that the functional significance of bacterial predators increases with energy flow and that predatory bacteria influence element flow through microbial food webs.IMPORTANCE The word "predator" may conjure images of leopards killing and eating impala on the African savannah or of great white sharks attacking elephant seals off the coast of California. But microorganisms are also predators, including bacteria that kill and eat other bacteria. While predatory bacteria have been found in many environments, it has been challenging to document their importance in nature. This study quantified the growth of predatory and nonpredatory bacteria in soils (and one stream) by tracking isotopically labeled substrates into newly synthesized DNA. Predatory bacteria were more active than nonpredators, and obligate predators, such as Bdellovibrionales and Vampirovibrionales, increased in growth rate in response to added substrates at the base of the food chain, strong evidence of trophic control. This work provides quantitative measures of predator activity and suggests that predatory bacteria-along with protists, nematodes, and phages-are active and important in microbial food webs.