A new perspective on the spatial, environmental, and metacommunity controls of local biodiversity.

Influential ecological research in the 1980s, elucidating that local biodiversity (LB) is a function of local ecological factors and the size of the regional species pool (γ-diversity), has prompted numerous investigations on the local and regional origins of LB. These investigations, however, have been mostly limited to single scales and target groups and centered exclusively on γ-diversity. Here we developed a unified framework including scale, environmental factors (heterogeneity and ambient levels), and metacommunity properties (intraspecific spatial aggregation, regional evenness, and γ-diversity) as hierarchical predictors of LB. We tested this framework with variance partitioning and structural equation modeling using subcontinental data on stream diatoms, insects, and fish as well as local physicochemistry, climate, and land use. Pure aggregation + regional evenness outperformed pure γ-diversity in explaining LB across groups. The covariance of the environment with aggregation + regional evenness rather than with γ-diversity generally explained a much greater proportion of the variance in diatom and insect LB, especially at smaller scales. Thus, disregarding aggregation and regional evenness, as commonly done, may lead to gross underestimation of the pure metacommunity effects and the indirect environmental effects on LB. We examined the shape of the local-regional species richness relationship, which has been widely used to infer local vs. regional effects on LB. We showed that this shape has an ecological basis, but its interpretation is not straightforward. Therefore, we advocate that the variance partitioning analysis under the proposed framework is adopted instead. In diatoms, metacommunity properties had the greatest total effects on LB, while in insects and fish, it was the environment, suggesting that larger organisms are more strongly controlled by the environment. Broader use of our framework may lead to novel biogeographical insights into the drivers of LB and improved projections of its trends along current and future environmental gradients.

On the shape and origins of the freshwater species-area relationship.

The species-area relationship (SAR) has over a 150-year-long history in ecology, but how its shape and origins vary across scales and organisms remains incompletely understood. This is the first subcontinental freshwater study to examine both these properties of the SAR in a spatially explicit way across major organismal groups (diatoms, insects, and fish) that differ in body size and dispersal capacity. First, to describe the SAR shape, we evaluated the fit of three commonly used models, logarithmic, power, and Michaelis-Menten. Second, we proposed a hierarchical framework to explain the variability in the SAR shape, captured by the parameters of the SAR model. According to this framework, scale and species group were the top predictors of the SAR shape, climatic factors (heterogeneity and median conditions) represented the second predictor level, and metacommunity properties (intraspecific spatial aggregation, γ-diversity, and species abundance distribution) the third predictor level. We calculated the SAR as a sample-based rarefaction curve using 60 streams within landscape windows (scales) in the United States, ranging from 160,000 to 6,760,000 km2 . First, we found that all models provided good fits (R2 ≥ 0.93), but the frequency of the best-fitting model was strongly dependent on organism, scale, and metacommunity properties. The Michaelis-Menten model was most common in fish, at the largest scales, and at the highest levels of intraspecific spatial aggregation. The power model was most frequent in diatoms and insects, at smaller scales, and in metacommunities with the lowest evenness. The logarithmic model fit best exclusively at the smallest scales and in species-poor metacommunities, primarily fish. Second, we tested our framework with the parameters of the most broadly used SAR model, the log-log form of the power model, using a structural equation model. This model supported our framework and revealed that the SAR slope was best predicted by scale- and organism-dependent metacommunity properties, particularly spatial aggregation, whereas the intercept responded most strongly to species group and γ-diversity. Future research should investigate from the perspective of our framework how shifts in metacommunity properties due to climate change may alter the SAR.

Niche dimensionality and herbivory control stream algal biomass via shifts in guild composition, richness, and evenness.

We developed a framework for the hierarchical pathways of bottom-up (niche dimensionality) and top-down control (herbivory) on biomass of stream algae via changes in guild composition (relative abundance of low profile, high profile, and motile guilds), species richness, and evenness. We further tested (1) the contrasting predictions of resource competition theory vs. the benthic model of coexistence on how the number of added nutrients constrains species richness, (2) the relationship between species richness and evenness, and (3) the biodiversity-ecosystem-function paradigm. Implementing a combination of field and lab experiments that manipulated for the first time in benthic algae herbivory and/or niche dimensionality, i.e., the number of added nutrients (NAN), including nitrogen, phosphorus, iron, and manganese, we made the following discoveries. First, important predictors of guild composition were herbivory (field) and NAN (lab); of richness, NAN (field) and NAN and guild composition (lab); of evenness, guild composition (field and lab) and herbivory (field); and of biomass, guild composition, NAN, and richness + evenness (field and lab). Herbivory increased the proportions of the low profile and motile guilds but decreased the proportion of the high profile guild. In the absence of grazing, greater proportions of the high profile guild resulted in elevated richness and biomass but diminished evenness, whereas in the presence of grazing, these relationships generally disappeared. Second, both experiments confirmed the prediction of the benthic model that species richness increases with NAN, a pattern inconsistent with resource competition theory. Third, supplementation with manganese and/or iron increased algal richness, indicating that micronutrients, which have generally been overlooked in stream ecology, added dimensions to the algal niche. Fourth, the richness-evenness relationship, observed only in the absence of herbivory, depended on the size of the species pool. It was positive at richness lower than 49 species (lab), implying complementarity and facilitation, while at higher richness (field and lab), this relationship was negative, consistent with negative interspecific interactions. Finally, the greater dependence of biomass production on guild composition and NAN than on richness and evenness suggests that more comprehensive, environmentally explicit, and trait-based approaches are necessary for the study of the biodiversity-ecosystem-function paradigm.

Biogeographical Patterns of Species Richness and Abundance Distribution in Stream Diatoms Are Driven by Climate and Water Chemistry.

In this intercontinental study of stream diatoms, we asked three important but still unresolved ecological questions: (1) What factors drive the biogeography of species richness and species abundance distribution (SAD)? (2) Are climate-related hypotheses, which have dominated the research on the latitudinal and altitudinal diversity gradients, adequate in explaining spatial biotic variability? and (3) Is the SAD response to the environment independent of richness? We tested a number of climatic theories and hypotheses (i.e., the species-energy theory, the metabolic theory, the energy variability hypothesis, and the climatic tolerance hypothesis) but found no support for any of these concepts, as the relationships of richness with explanatory variables were nonexistent, weak, or unexpected. Instead, we demonstrated that diatom richness and SAD evenness generally increased with temperature seasonality and at mid- to high total phosphorus concentrations. The spatial patterns of diatom richness and the SAD-mainly longitudinal in the United States but latitudinal in Finland-were defined primarily by the covariance of climate and water chemistry with space. The SAD was not entirely controlled by richness, emphasizing its utility for ecological research. Thus, we found support for the operation of both climate and water chemistry mechanisms in structuring diatom communities, which underscores their complex response to the environment and the necessity for novel predictive frameworks.

Iron limitation effects on nitrogen-fixing organisms with possible implications for cyanobacterial blooms.

Cyanobacteria-dominated harmful algal blooms are increasing in occurrence. Many of the taxa contributing to these blooms are capable of fixing atmospheric nitrogen and should be favored under conditions of low nitrogen availability. Yet, synthesizing nitrogenase, the enzyme responsible for nitrogen fixation, is energetically expensive and requires substantial concentrations of iron. Phosphorus addition to nitrogen poor streams should promote nitrogen fixation, but experimental results so far have been inconclusive, suggesting that other factors may be involved in controlling this process. With iron potentially limited in many streams, we examined the influence of phosphorus-iron colimitation on the community structure of nitrogen-fixing organisms. In stream microcosms, using microscopic and molecular sequence data, we observed: (i) the greatest abundance of heterocyst forming nitrogen-fixing cyanobacteria in low nitrogen treatments with high phosphorus and iron and (ii) greater abundance of non-photosynthetic nitrogen-fixing bacteria in treatments with nitrogen compared to those without it. We also found that comparisons between molecular results and those obtained from microscopic identification provided complementary information about cyanobacterial communities. Our investigation indicates the potential for phosphorus-iron colimitation of stream nitrogen-fixing organisms.

The number of limiting resources in the environment controls the temporal diversity patterns in the algal benthos.

The role of the number of limiting resources (NLR) on species richness has been the subject of much theoretical and experimental work. However, how the NLR controls temporal beta diversity and the processes of community assembly is not well understood. To address this knowledge gap, we initiated a series of laboratory microcosm experiments, exposing periphyton communities to a gradient of NLR from 0 to 3, generated by supplementation with nitrogen, phosphorus, iron, and all their combinations. We hypothesized that similarly to alpha diversity, shown to decrease with the NLR in benthic algae, temporal beta diversity would also decline due to filtering. Additionally, we predicted that the NLR would also affect turnover and community nestedness, which would show opposing responses. Indeed, as the NLR increased, temporal beta diversity decreased; turnover, indicative of competition, decreased; and nestedness, suggestive of complementarity, increased. Finally, the NLR determined the role of deterministic versus stochastic processes in community assembly, showing respectively an increasing and a decreasing trend. These results imply that the NLR has a much greater, yet still unappreciated influence on producer communities, constraining not only alpha diversity but also temporal dynamics and community assembly.

Iron supply constrains producer communities in stream ecosystems.

The current paradigm that stream producers are under exclusive macronutrient control was recently challenged by continental studies, demonstrating that iron supply constrained diatom biodiversity and energy flows. Using algal abundance and water chemistry data from the National Water-Quality Assessment Program, we determined for the first time community thresholds along iron gradients in non-acidic running waters, i.e. 30-79.5 µg L(-1) and 70-120 µg L(-1) in oligotrophic and eutrophic streams, respectively. Given that Fe concentrations fell below both thresholds in 50% of US streams, and below the eutrophic threshold in 75% of US streams, we suggest that Fe limitation is potentially widespread and attribute it to the restricted distribution of wetlands. We also report results from the first laboratory experiments on algal-iron interactions in streams, revealing that iron supplementation leads to significant biovolume and biodiversity increase in both nitrogen fixing and non-nitrogen fixing algae. Therefore, the progressive brownification of freshwaters due to rising dissolved organic carbon and iron levels can have a stimulating influence on microbial producers with cascading effects along the trophic hierarchy. Future research in running waters should focus on the role of iron in algal physiology and biofilm functions, including accumulation of biomass, fixing atmospheric nitrogen and improving water quality.

Rates of species accumulation and taxonomic diversification during phototrophic biofilm development are controlled by both nutrient supply and current velocity.

The accumulation of new and taxonomically diverse species is a marked feature of community development, but the role of the environment in this process is not well understood. To address this problem, we subjected periphyton in laboratory streams to low (10-cm · s(-1)), high (30-cm · s(-1)), and variable (9- to 32-cm · s(-1)) current velocity and low- versus high-nutrient inputs. We examined how current velocity and resource supply constrained (i) the rates of species accumulation, a measure of temporal beta-diversity, and (ii) the rates of diversification of higher taxonomic categories, defined here as the rate of higher taxon richness increase with the increase of species richness. Temporal biofilm dynamics were controlled by a strong nutrient-current interaction. Nutrients accelerated the rates of accumulation of new species, when flow velocity was not too stressful. Species were more taxonomically diverse under variable than under low-flow conditions, indicating that flow heterogeneity increased the niche diversity in the high-nutrient treatments. Conversely, the lower diversification rates under high- than under low-nutrient conditions at low velocity are explained with finer resource partitioning among species, belonging to a limited number of related genera. The overall low rates of diversification in high-current treatments suggest that the ability to withstand current stress was conserved within closely related species. Temporal heterogeneity of disturbance has been shown to promote species richness, but here we further demonstrate that it also affects two other components of biodiversity, i.e., temporal beta-diversity and diversification rate. Therefore, management efforts for preserving the inherent temporal heterogeneity of natural ecosystems will have detectable positive effects on biodiversity.

Taxonomic and functional composition of the algal benthos exhibits similar successional trends in response to nutrient supply and current velocity.

In an effort to identify the causes and patterns of temporal change in periphytic communities, we examined biomass accumulation, taxonomic and functional composition, rate of species turnover, and pairwise species correlations in response to variability in current velocity and nutrient supply in artificial stream flumes. Divergent patterns in community growth and succession were observed between nutrient treatments and, to a lesser extent, between flow treatments best described by shifts in taxonomic and functional composition. Specifically, understory low profile species, tolerant to low resource supply, became dominant under low nutrients, while overstory high profile and motile species with higher nutrient demands dominated the high nutrient treatments. Increased resource supply or current velocity did not influence the species turnover rate, measured by a time-lag analysis. Interspecific interactions, especially competition, did not appear to be driving community dynamics, as the number of positive and negative pairwise species correlations ranged between low and extremely low, respectively. The overwhelming majority of correlations were not significant, indicating that species within the biofilm matrix were not perceptibly influencing one another. Thus, temporal trends in taxonomic and functional composition were largely environmentally driven, signifying that coexistence in biofilms is defined by the same mechanism along the hierarchy from species to functional groups.

Succession in stream biofilms is an environmentally driven gradient of stress tolerance.

The century-long research on succession has bestowed us with a number of theories, but little agreement on what causes species replacements through time. The majority of studies has explored the temporal trends of individual species in plant and much less so in microbial communities, arguing that interspecific interactions, especially competition, play a key role in community organization throughout succession. In this experimental investigation of periphytic succession in re-circulating laboratory streams, we examined the density and the relative abundance of diatoms and soft algae for 35 days across gradients of low to high nutrient supply (nitrogen + phosphorus) and low to intermediate current velocity (10 vs. 30 cm·s(-1)). All algal species were classified into trophic groups and morphological guilds, both of which responded more strongly to nutrient than current velocity manipulations, as shown by regression analyses. We concluded that within the manipulated environmental ranges: (1) Succession was a gradient of stress tolerance, driven primarily by nutrient supply and secondarily, by current velocity. Nutrient supply had a qualitative effect in determining whether the contribution of species tolerant vs. sensitive to nutrient limitation would increase through time, while current velocity had a quantitative influence and affected only the rate of this increase. (2) The mechanism of algal succession at a functional level was a neutral coexistence, whereby the tolerant low profile guild maintained high density when overgrown by sensitive species, while sensitive species, constituting mostly the motile and high profile guilds, were neither facilitated nor inhibited by tolerant species but controlled by the environment. It is suggested that the mechanism of succession may depend on the level of biological organization with interspecific interactions giving way to neutral coexistence along the hierarchy from species to functional groups. Considering that the functional makeup is strictly environmentally defined, while species composition reflects local and regional species pools that may exhibit substantial geographic variability, succession is deterministic at a functional level but stochastic at a species level.