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.

Do grazers respond to or control food quality? Cross-scale analysis of algivorous fish in littoral Lake Tanganyika.

Food quality determines the growth rate of primary consumers and ecosystem trophic efficiencies, but it is not clear whether variation in primary consumer densities control, or is controlled by, variation in food quality. We quantified variation in the density and condition of an abundant algae-eating cichlid, Tropheus brichardi, with respect to the quality and productivity of algal biofilms within and across rocky coastal sites in Lake Tanganyika, East Africa. Adjacent land use and sediment deposition in the littoral zone varied widely among sites. Tropheus brichardi maximized both caloric and phosphorus intake at the local scale by aggregating in shallow habitats: algivore density decreased with depth, tracking attached algae productivity (rETRMAX) remarkably well (r2 = 0.84, P = 0.00033). In contrast, algivore density was unrelated to among-site variation in algal productivity. Rather, there was significant increase in algal quality (r2 = 0.44, P = 0.011) and decrease in algal biomass (r2 = 0.53, P = 0.0068) with T. brichardi density across sites, consistent with strong top-down control of primary producers. The amount of inorganic sediment on rock surfaces was the strongest predictor of among-site variation in algivore density (r2 = 0.69, P = 0.00096), and algivore gut length increased with sedimentation (r2 = 0.36, P = 0.034). These patterns indicate extrinsic and top-down forcing of algal food quality and quantity across coastal landscapes, combined with adaptive habitat selection by fish at the local scale. Factors that degrade food quality by decreasing algal nutrient content or diluting the resource with indigestible material are likely to depress grazer densities, potentially dampening top-down control in high-light, low-nutrient aquatic ecosystems.

Stable Isotopes Reveal Nitrogen Loading to Lake Tanganyika from Remote Shoreline Villages.

Access to safe water is an ongoing challenge in rural areas in Tanzania where communities often lack access to improved sanitation. Methods to detect contamination of surface water bodies, such as monitoring nutrient concentrations and bacterial counts, are time consuming and results can be highly variable in space and time. On the northeast shore of Lake Tanganyika, Tanzania, the low population density coupled with the high potential for dilution in the lake necessitates the development of a sensitive method for detecting contamination in order to avoid human health concerns. We investigated the potential use of nitrogen and carbon stable isotopes of snail tissues to detect anthropogenic nutrient loading along the northeast shore of Lake Tanganyika. δ15N of snails was positively related to human population size in the nearest village, but only for villages with >4000 inhabitants. The areal footprint of villages within their watershed was also significantly correlated with snail δ15N, while agricultural land use and natural vegetation were not. Dissolved nutrient concentrations were not significantly different between village and reference sites. Our results indicate that nitrogen isotopes provide a sensitive index of local nutrient loading that can be used to monitor contamination of oligotrophic aquatic environments with low surrounding population densities.

Benthic algae compensate for phytoplankton losses in large aquatic ecosystems.

Anthropogenic activities can induce major trophic shifts in aquatic systems, yet we have an incomplete understanding of the implication of such shifts on ecosystem function and on primary production (PP) in particular. In recent decades, phytoplankton biomass and production in the Laurentian Great Lakes have declined in response to reduced nutrient concentrations and invasive mussels. However, the increases in water clarity associated with declines in phytoplankton may have positive effects on benthic PP at the ecosystem scale. Have these lakes experienced oligotrophication (a reduction of algal production), or simply a shift in autotrophic structure with no net decline in PP? Benthic contributions to ecosystem PP are rarely measured in large aquatic systems, but our calculations based on productivity rates from the Great Lakes indicate that a significant proportion (up to one half, in Lake Huron) of their whole-lake production may be benthic. The large declines (5-45%) in phytoplankton production in the Great Lakes from the 1970s to 2000s may be substantially compensated by benthic PP, which increased by up to 190%. Thus, the autotrophic productive capacity of large aquatic ecosystems may be relatively resilient to shifts in trophic status, due to a redirection of production to the near-shore benthic zone, and large lakes may exhibit shifts in autotrophic structure analogous to the regime shifts seen in shallow lakes.

Benthic-planktonic coupling, regime shifts, and whole-lake primary production in shallow lakes.

Alternative stable states in shallow lakes are typically characterized by submerged macrophyte (clear-water state) or phytoplankton (turbid state) dominance. However, a clear-water state may occur in eutrophic lakes even when macrophytes are absent. To test whether sediment algae could cause a regime shift in the absence of macrophytes, we developed a model of benthic (periphyton) and planktonic (phytoplankton) primary production using parameters derived from a shallow macrophyte-free lake that shifted from a turbid to a clear-water state following fish removal (biomanipulation). The model includes a negative feedback effect of periphyton on phosphorus (P) release from sediments. This in turn induces a positive feedback between phytoplankton production and P release. Scenarios incorporating a gradient of external P loading rates revealed that (1) periphyton and phytoplankton both contributed substantially to whole-lake production over a broad range of external P loading in a clear-water state; (2) during the clear-water state, the loss of benthic production was gradually replaced by phytoplankton production, leaving whole-lake production largely unchanged; (3) the responses of lakes to biomanipulation and increased external P loading were both dependent on lake morphometry; and (4) the capacity of periphyton to buffer the effects of increased external P loading and maintain a clear-water state was highly sensitive to relationships between light availability at the sediment surface and the of P release. Our model suggests a mechanism for the persistence of alternative states in shallow macrophyte-free lakes and demonstrates that regime shifts may trigger profound changes in ecosystem structure and function.

A Novel Thin-Film Technique to Improve Accuracy of Fluorescence-Based Estimates for Periphytic Biofilms.

Recent studies suggest that photophysiological parameters for intact substrates with depth (e.g., periphytic biofilms, microphytobenthos) are overestimated by pulse-amplitude modulated (PAM) fluorometry. This overestimation results from depth-integration effects, following the activation of deeper photosynthesizing layers by an attenuated light signal. To mitigate this error, we propose a novel slide-based thin-film technique in which fluorescence is measured on a vertically representative subsample of the biofilm, spread evenly on a microscope slide. We compared bias and precision for photosynthetic parameters estimated through conventional PAM fluorometry on intact biofilms and through our novel slide-based technique, both theoretically and empirically. Numerical simulations confirmed the consistent overestimation of key parameters for intact biofilms, with relative errors up to 145%, compared to, at most, 52% on thin films. Paired empirical observations likewise demonstrated that estimates based on intact biofilms were consistently higher (up to 248%, p < 0.001) than estimates from thin films. Numerical simulation suggested greater precision with the slide-based technique for homogeneous biofilms, but potentially less precision for heterogeneous biofilms with improper subsampling. Our empirical comparison, however, demonstrated some improvement in precision with the slide-based technique (e.g., the coefficient of variation for the maximum electron transport rate was reduced 30%, p = 0.009). We recommend the use of the slide-based technique, particularly for biofilms that are thick or have small light attenuation coefficients. Care should be taken, however, to obtain vertically representative subsamples of the biofilm for measurement.

Depth-discrete metagenomics reveals the roles of microbes in biogeochemical cycling in the tropical freshwater Lake Tanganyika.

Lake Tanganyika (LT) is the largest tropical freshwater lake, and the largest body of anoxic freshwater on Earth's surface. LT's mixed oxygenated surface waters float atop a permanently anoxic layer and host rich animal biodiversity. However, little is known about microorganisms inhabiting LT's 1470 meter deep water column and their contributions to nutrient cycling, which affect ecosystem-level function and productivity. Here, we applied genome-resolved metagenomics and environmental analyses to link specific taxa to key biogeochemical processes across a vertical depth gradient in LT. We reconstructed 523 unique metagenome-assembled genomes (MAGs) from 34 bacterial and archaeal phyla, including many rarely observed in freshwater lakes. We identified sharp contrasts in community composition and metabolic potential with an abundance of typical freshwater taxa in oxygenated mixed upper layers, and Archaea and uncultured Candidate Phyla in deep anoxic waters. Genomic capacity for nitrogen and sulfur cycling was abundant in MAGs recovered from anoxic waters, highlighting microbial contributions to the productive surface layers via recycling of upwelled nutrients, and greenhouse gases such as nitrous oxide. Overall, our study provides a blueprint for incorporation of aquatic microbial genomics in the representation of tropical freshwater lakes, especially in the context of ongoing climate change, which is predicted to bring increased stratification and anoxia to freshwater lakes.

Toxic benthic freshwater cyanobacterial proliferations: Challenges and solutions for enhancing knowledge and improving monitoring and mitigation.

1. This review summarises knowledge on the ecology, toxin production, and impacts of toxic freshwater benthic cyanobacterial proliferations. It documents monitoring, management, and sampling strategies, and explores mitigation options. 2. Toxic proliferations of freshwater benthic cyanobacteria (taxa that grow attached to substrates) occur in streams, rivers, lakes, and thermal and meltwater ponds, and have been reported in 19 countries. Anatoxin- and microcystin-containing mats are most commonly reported (eight and 10 countries, respectively). 3. Studies exploring factors that promote toxic benthic cyanobacterial proliferations are limited to a few species and habitats. There is a hierarchy of importance in environmental and biological factors that regulate proliferations with variables such as flow (rivers), fine sediment deposition, nutrients, associated microbes, and grazing identified as key drivers. Regulating factors differ among colonisation, expansion, and dispersal phases. 4. New -omics-based approaches are providing novel insights into the physiological attributes of benthic cyanobacteria and the role of associated microorganisms in facilitating their proliferation. 5. Proliferations are commonly comprised of both toxic and non-toxic strains, and the relative proportion of these is the key factor contributing to the overall toxin content of each mat. 6. While these events are becoming more commonly reported globally, we currently lack standardised approaches to detect, monitor, and manage this emerging health issue. To solve these critical gaps, global collaborations are needed to facilitate the rapid transfer of knowledge and promote the development of standardised techniques that can be applied to diverse habitats and species, and ultimately lead to improved management.

Benthic algal production across lake size gradients: interactions among morphometry, nutrients, and light.

Attached algae play a minor role in conceptual and empirical models of lake ecosystem function but paradoxically form the energetic base of food webs that support a wide variety of fishes. To explore the apparent mismatch between perceived limits on contributions of periphyton to whole-lake primary production and its importance to consumers, we modeled the contribution of periphyton to whole-ecosystem primary production across lake size, shape, and nutrient gradients. The distribution of available benthic habitat for periphyton is influenced by the ratio of mean depth to maximum depth (DR = z/ z(max)). We modeled total phytoplankton production from water-column nutrient availability, z, and light. Periphyton production was a function of light-saturated photosynthesis (BPmax) and light availability at depth. The model demonstrated that depth ratio (DR) and light attenuation strongly determined the maximum possible contribution of benthic algae to lake production, and the benthic proportion of whole-lake primary production (BPf) declined with increasing nutrients. Shallow lakes (z < or =5 m) were insensitive to DR and were dominated by either benthic or pelagic primary productivity depending on trophic status. Moderately deep oligotrophic lakes had substantial contributions by benthic primary productivity at low depth ratios and when maximum benthic photosynthesis was moderate or high. Extremely large, deep lakes always had low fractional contributions of benthic primary production. An analysis of the world's largest lakes showed that the shapes of natural lakes shift increasingly toward lower depth ratios with increasing depth, maximizing the potential importance of littoral primary production in large-lake food webs. The repeatedly demonstrated importance of periphyton to lake food webs may reflect the combination of low depth ratios and high light penetration characteristic of large, oligotrophic lakes that in turn lead to substantial contributions of periphyton to autochthonous production.

Century-Long Warming Trends in the Upper Water Column of Lake Tanganyika.

Lake Tanganyika, the deepest and most voluminous lake in Africa, has warmed over the last century in response to climate change. Separate analyses of surface warming rates estimated from in situ instruments, satellites, and a paleolimnological temperature proxy (TEX86) disagree, leaving uncertainty about the thermal sensitivity of Lake Tanganyika to climate change. Here, we use a comprehensive database of in situ temperature data from the top 100 meters of the water column that span the lake's seasonal range and lateral extent to demonstrate that long-term temperature trends in Lake Tanganyika depend strongly on depth, season, and latitude. The observed spatiotemporal variation in surface warming rates accounts for small differences between warming rate estimates from in situ instruments and satellite data. However, after accounting for spatiotemporal variation in temperature and warming rates, the TEX86 paleolimnological proxy yields lower surface temperatures (1.46 °C lower on average) and faster warming rates (by a factor of three) than in situ measurements. Based on the ecology of Thaumarchaeota (the microbes whose biomolecules are involved with generating the TEX86 proxy), we offer a reinterpretation of the TEX86 data from Lake Tanganyika as the temperature of the low-oxygen zone, rather than of the lake surface temperature as has been suggested previously. Our analyses provide a thorough accounting of spatiotemporal variation in warming rates, offering strong evidence that thermal and ecological shifts observed in this massive tropical lake over the last century are robust and in step with global climate change.

Periphyton function in lake ecosystems.

Periphyton communities have received relatively little attention in lake ecosystems. However, evidence is increasing that they play a key role in primary productivity, nutrient cycling, and food web interactions. This review summarizes those findings and places them in a conceptual framework to evaluate the functional importance of periphyton in lakes. The role of periphyton is conceptualized based on a spatial hierarchy. At the coarsest scale, landscape properties such as lake morphometry, influence the amount of available habitat for periphyton growth. Watershed-related properties, such as loading of dissolved organic matter, nutrients, and sediments influence light availability and hence periphyton productivity. At the finer scale of within the lake, both habitat availability and habitat type affect periphyton growth and abundance. In addition, periphyton and phytoplankton compete for available resources at the within-lake scale. Our review indicates that periphyton plays an important functional role in lake nutrient cycles and food webs, especially under such conditions as relatively shallow depths, nutrient-poor conditions, or high water-column transparency. We recommend more studies assessing periphyton function across a spectrum of lake morphometry and trophic conditions.

Primary consumer stable nitrogen isotopes as indicators of nutrient source.

Non-point source loading of nitrogen and phosphorus is a primary cause of eutrophication of inland waters, although the diffuse and variable nature of nutrient inputs makes it difficult to trace and identify nutrient pathways. Stable nitrogen isotope values (delta15N) in aquatic biota are thought to reflect anthropogenic nutrient inputs, and they may be a promising tool fortracing nutrient sources in watersheds. We measured delta15N of aquatic consumers from a suite of 27 Danish lakes spanning a range of trophic states (oligotrophic to eutrophic) and land uses (forest, urban, agriculture). Primary consumer delta15N values (PCdelta15N) varied more than 14% among lakes. Models of PCdelta15N were developed from limnological, nitrogen loading, and nitrogen source variables using an information-theoretic approach (Akaike's Information Criteria, AIC). Models based on land use/ land cover performed best, indicating that elevated delta15N is not only associated with high nitrogen loading, but is also reflective of nitrogen source. Urban and agricultural land use in the watershed, and particularly within the riparian buffer areas, was quantitatively linked to elevated biotic delta15N.