Foundation species stabilize an alternative eutrophic state in nutrient-disturbed ponds via selection on microbial community.

Eutrophication due to nutrient addition can result in major alterations in aquatic ecosystem productivity. Foundation species, individually and interactively, whether present as invasive species or as instruments of ecosystem management and restoration, can have unwanted effects like stabilizing turbid eutrophic states. In this study, we used whole-pond experimental manipulations to investigate the impacts of disturbance by nutrient additions in the presence and absence of two foundation species: Dreissena polymorpha (a freshwater mussel) and Myriophyllum spicatum (a macrophyte). We tracked how nutrient additions to ponds changed the prokaryotic and eukaryotic communities, using 16S, 18S, and COI amplicon sequencing. The nutrient disturbance and foundation species imposed strong selection on the prokaryotic communities, but not on the microbial eukaryotic communities. The prokaryotic communities changed increasingly over time as the nutrient disturbance intensified. Post-disturbance, the foundation species stabilized the prokaryotic communities as observed by the reduced rate of change in community composition. Our analysis suggests that prokaryotic community change contributed both directly and indirectly to major changes in ecosystem properties, including pH and dissolved oxygen. Our work shows that nutrient disturbance and foundation species strongly affect the prokaryotic community composition and stability, and that the presence of foundation species can, in some cases, promote the emergence and persistence of a turbid eutrophic ecosystem state.

Warming underpins community turnover in temperate freshwater and terrestrial communities.

Rising temperatures are leading to increased prevalence of warm-affinity species in ecosystems, known as thermophilisation. However, factors influencing variation in thermophilisation rates among taxa and ecosystems, particularly freshwater communities with high diversity and high population decline, remain unclear. We analysed compositional change over time in 7123 freshwater and 6201 terrestrial, mostly temperate communities from multiple taxonomic groups. Overall, temperature change was positively linked to thermophilisation in both realms. Extirpated species had lower thermal affinities in terrestrial communities but higher affinities in freshwater communities compared to those persisting over time. Temperature change's impact on thermophilisation varied with community body size, thermal niche breadth, species richness and baseline temperature; these interactive effects were idiosyncratic in the direction and magnitude of their impacts on thermophilisation, both across realms and taxonomic groups. While our findings emphasise the challenges in predicting the consequences of temperature change across communities, conservation strategies should consider these variable responses when attempting to mitigate climate-induced biodiversity loss.

Environmentally independent selection for hybrids between divergent freshwater stickleback lineages in semi-natural ponds.

Hybridization following secondary contact of genetically divergent populations can influence the range expansion of invasive species, though specific outcomes depend on the environmental dependence of hybrid fitness. Here, using two genetically and ecologically divergent threespine stickleback lineages that differ in their history of freshwater colonization, we estimate fitness variation of parental lineages and hybrids in semi-natural freshwater ponds with contrasting histories of nutrient loading. In our experiment, we found that fish from the older freshwater lineage (Lake Geneva) and hybrids outperformed fish from the younger freshwater lineage (Lake Constance) in terms of both growth and survival, regardless of the environmental context of our ponds. Across all ponds, hybrids exhibited the highest survival. Although wild-caught adult populations differed in their functional and defence morphology, it is unclear which of these traits underlie the fitness differences observed among juveniles in our experiment. Overall, our work suggests that when hybrid fitness is insensitive to environmental conditions, as observed here, introgression may promote population expansion into unoccupied habitats and accelerate invasion success.

Linking human impacts to community processes in terrestrial and freshwater ecosystems.

Human impacts such as habitat loss, climate change and biological invasions are radically altering biodiversity, with greater effects projected into the future. Evidence suggests human impacts may differ substantially between terrestrial and freshwater ecosystems, but the reasons for these differences are poorly understood. We propose an integrative approach to explain these differences by linking impacts to four fundamental processes that structure communities: dispersal, speciation, species-level selection and ecological drift. Our goal is to provide process-based insights into why human impacts, and responses to impacts, may differ across ecosystem types using a mechanistic, eco-evolutionary comparative framework. To enable these insights, we review and synthesise (i) how the four processes influence diversity and dynamics in terrestrial versus freshwater communities, specifically whether the relative importance of each process differs among ecosystems, and (ii) the pathways by which human impacts can produce divergent responses across ecosystems, due to differences in the strength of processes among ecosystems we identify. Finally, we highlight research gaps and next steps, and discuss how this approach can provide new insights for conservation. By focusing on the processes that shape diversity in communities, we aim to mechanistically link human impacts to ongoing and future changes in ecosystems.

Predicting effects of multiple interacting global change drivers across trophic levels.

Global change encompasses many co-occurring anthropogenic drivers, which can act synergistically or antagonistically on ecological systems. Predicting how different global change drivers simultaneously contribute to observed biodiversity change is a key challenge for ecology and conservation. However, we lack the mechanistic understanding of how multiple global change drivers influence the vital rates of multiple interacting species. We propose that reaction norms, the relationships between a driver and vital rates like growth, mortality, and consumption, provide insights to the underlying mechanisms of community responses to multiple drivers. Understanding how multiple drivers interact to affect demographic rates using a reaction-norm perspective can improve our ability to make predictions of interactions at higher levels of organization-that is, community and food web. Building on the framework of consumer-resource interactions and widely studied thermal performance curves, we illustrate how joint driver impacts can be scaled up from the population to the community level. A simple proof-of-concept model demonstrates how reaction norms of vital rates predict the prevalence of driver interactions at the community level. A literature search suggests that our proposed approach is not yet used in multiple driver research. We outline how realistic response surfaces (i.e., multidimensional reaction norms) can be inferred by parametric and nonparametric approaches. Response surfaces have the potential to strengthen our understanding of how multiple drivers affect communities as well as improve our ability to predict when interactive effects emerge, two of the major challenges of ecology today.

Ecology and evolution of competitive trait variation in natural phytoplankton communities under selection.

Competition for limited resources is a major force in structuring ecological communities. Species minimum resource requirements (R*s) can predict competitive outcomes and evolve under selection in simple communities under controlled conditions. However, whether R*s predict competitive outcomes or demonstrate adaptive evolution in naturally complex communities is unknown. We subjected natural phytoplankton communities to three types of resource limitation (nitrogen, phosphorus, light) in outdoor mesocosms over 10 weeks. We examined the community composition weekly and isolated 21 phytoplankton strains from seven species to quantify responses to the selection of R* for these resources. We investigated the evolutionary change in R*s in the dominant species, Desmodesmus armatus. R*s were good predictors of species changes in relative abundance, though this was largely driven by the success of D. armatus across several treatments. This species also demonstrated an evolutionary change in R*s under resource limitation, supporting the potential for adaptive trait change to modify competitive outcomes in natural communities.

Regime shifts, trends, and variability of lake productivity at a global scale.

Lakes are often described as sentinels of global change. Phenomena like lake eutrophication, algal blooms, or reorganization in community composition belong to the most studied ecosystem regime shifts. However, although regime shifts have been well documented in several lakes, a global assessment of the prevalence of regime shifts is still missing, and, more in general, of the factors altering stability in lake status, is missing. Here, we provide a first global assessment of regime shifts and stability in the productivity of 1,015 lakes worldwide using trophic state index (TSI) time series derived from satellite imagery. We find that 12.8% of the lakes studied show regime shifts whose signatures are compatible with tipping points, while the number of detected regime shifts from low to high TSI has increased over time. Although our results suggest an overall stable picture for global lake dynamics, the limited instability signatures do not mean that lakes are insensitive to global change. Modeling the interaction between lake climatic, geophysical, and socioeconomic features and their stability properties, we find that the probability of a lake experiencing a tipping point increases with human population density in its catchment, while it decreases as the gross domestic product of that population increases. Our results show how quantifying lake productivity dynamics at a global scale highlights socioeconomic inequalities in conserving natural environments.

Non-additive effects of foundation species determine the response of aquatic ecosystems to nutrient perturbation.

Eutrophication is a persistent threat to aquatic ecosystems worldwide. Foundation species, namely those that play a central role in the structuring of communities and functioning of ecosystems, are likely important for the resilience of aquatic ecosystems in the face of disturbance. However, little is known about how interactions among such species influence ecosystem responses to nutrient perturbation. Here, using an array (N = 20) of outdoor experimental pond ecosystems (15,000 L), we manipulated the presence of two foundation species, the macrophyte Myriophyllum spicatum and the mussel Dreissena polymorpha, and quantified ecosystem responses to multiple nutrient disturbances, spread over two years. In the first year, we added five nutrient pulses, ramping up from 10 to 50 µg P/L over a 10-week period from mid-July to mid-October, and in the second year, we added a single large pulse of 50 µg P/L in mid-October. We used automated sondes to measure multiple ecosystems properties at high frequency (15-minute intervals), including phytoplankton and dissolved organic matter fluorescence, and to model whole-ecosystem metabolism. Overall, both foundation species strongly affected the ecosystem responses to nutrient perturbation, and, as expected, initially suppressed the increase in phytoplankton abundance following nutrient additions. However, when both species were present, phytoplankton biomass increased substantially relative to other treatment combinations: non-additivity was evident for multiple ecosystem metrics following the nutrient perturbations in both years but was diminished in the intervening months between our perturbations. Overall, these results demonstrate how interactions between foundation species can cause surprisingly strong deviations from the expected responses of aquatic ecosystems to perturbations such as nutrient additions.

On biological evolution and environmental solutions.

Drawing insights from multiple disciplines is essential for finding integrative solutions that are required to tackle complex environmental problems. Human activities are causing unprecedented influence on global ecosystems, culminating in the loss of species and fundamental changes in the selective environments of organisms across the tree of life. Our collective understanding about biological evolution can help identify and mitigate many of the environmental problems in the Anthropocene. To this end, we propose a stronger integration of environmental sciences with evolutionary biology.

The evolution of competitive ability for essential resources.

Competition for limiting resources is among the most fundamental ecological interactions and has long been considered a key driver of species coexistence and biodiversity. Species' minimum resource requirements, their R*s, are key traits that link individual physiological demands to the outcome of competition. However, a major question remains unanswered-to what extent are species' competitive traits able to evolve in response to resource limitation? To address this knowledge gap, we performed an evolution experiment in which we exposed Chlamydomonas reinhardtii for approximately 285 generations to seven environments in chemostats that differed in resource supply ratios (including nitrogen, phosphorus and light limitation) and salt stress. We then grew the ancestors and descendants in a common garden and quantified their competitive abilities for essential resources. We investigated constraints on trait evolution by testing whether changes in resource requirements for different resources were correlated. Competitive abilities for phosphorus improved in all populations, while competitive abilities for nitrogen and light increased in some populations and decreased in others. In contrast to the common assumption that there are trade-offs between competitive abilities for different resources, we found that improvements in competitive ability for a resource came at no detectable cost. Instead, improvements in competitive ability for multiple resources were either positively correlated or not significantly correlated. Using resource competition theory, we then demonstrated that rapid adaptation in competitive traits altered the predicted outcomes of competition. These results highlight the need to incorporate contemporary evolutionary change into predictions of competitive community dynamics over environmental gradients. This article is part of the theme issue 'Conceptual challenges in microbial community ecology'.

Diversity and temperature indirectly reduce CO2 concentrations in experimental freshwater communities.

Biodiversity loss and climate warming are occurring in concert, with potentially profound impacts on ecosystem functioning. We currently know very little about the combined effects of these changes on the links between the community structure, dynamics and the resulting in situ CO2 concentrations in freshwater ecosystems. Here we aimed to determine both individual and combined effects of temperature and non-resource diversity (species inedible for a given consumer) on CO2 concentration. Our analysis further aimed to establish both direct effects on CO2 concentrations and potential indirect effects that occur via changes to the phytoplankton and zooplankton biomasses. Our results showed that there were no interactive effects of changes in temperature and diversity on CO2 concentration in the water. Instead, independent increases in either temperature or non-resource diversity resulted in a substantial reduction in CO2 concentrations, particularly at the highest non-resource diversity. The effects of non-resource diversity and warming on CO2 were indirect, resulting largely from the positive impacts on total biomass of primary producers. Our study is the first to experimentally partition the impacts of temperature and diversity on the consumer-resource dynamics and associated changes to CO2 concentrations. It provides new mechanistic insights into the role of diverse plankton communities for ecosystem functioning and their importance in regulating CO2 dynamics under ongoing climate warming.

Author Correction: Proteome evolution under non-substitutable resource limitation.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Interactive effects of foundation species on ecosystem functioning and stability in response to disturbance.

A major challenge in ecology is to understand determinants of ecosystem functioning and stability in the face of disturbance. Some important species can strongly shape community structure and ecosystem functioning, but their impacts and interactions on ecosystem-level responses to disturbance are less well known. Shallow ponds provide a model system in which to study the effects of such species because some taxa mitigate transitions between alternative ecosystem states caused by eutrophication. We performed pond experiments to test how two foundation species (a macrophyte and a mussel) affected the biomass of planktonic primary producers and its stability in response to nutrient additions. Individually, each species reduced phytoplankton biomass and tended to increase rates of recovery from disturbance, but together the species reversed these effects, particularly with larger nutrient additions. This reversal was mediated by high cyanobacterial dominance of the community and a resulting loss of trait evenness. Effects of the foundation species on primary producer biomass were associated with effects on other ecosystem properties, including turbidity and dissolved oxygen. Our work highlights the important role of foundation species and their interactive effects in determining responses of ecosystem functioning to disturbance.

Detecting the macroevolutionary signal of species interactions.

Species interactions lie at the heart of many theories of macroevolution, from adaptive radiation to the Red Queen. Although some theories describe the imprint that interactions will have over long timescales, we are still missing a comprehensive understanding of the effects of interactions on macroevolution. Current research shows strong evidence for the impact of interactions on macroevolutionary patterns of trait evolution and diversification, yet many macroevolutionary studies have only a tenuous relationship to ecological studies of interactions over shorter timescales. We review current research in this area, highlighting approaches that explicitly model species interactions and connect them to broad-scale macroevolutionary patterns. We also suggest that progress has been made by taking an integrative interdisciplinary look at individual clades. We focus on African cichlids as a case study of how this approach can be fruitful. Overall, although the evidence for species interactions shaping macroevolution is strong, further work using integrative and model-based approaches is needed to spur progress towards understanding the complex dynamics that structure communities over time and space.

Proteome evolution under non-substitutable resource limitation.

Resource limitation is a major driver of the ecological and evolutionary dynamics of organisms. Short-term responses to resource limitation include plastic changes in molecular phenotypes including protein expression. Yet little is known about the evolution of the molecular phenotype under longer-term resource limitation. Here, we combine experimental evolution of the green alga Chlamydomonas reinhardtii under multiple different non-substitutable resource limitation regimes with proteomic measurements to investigate evolutionary adaptation of the molecular phenotype. We demonstrate convergent proteomic evolution of core metabolic functions, including the Calvin-Benson cycle and gluconeogenesis, across different resource limitation environments. We do not observe proteomic changes consistent with optimized uptake of particular limiting resources. Instead, we report that adaptation proceeds in similar directions under different types of non-substitutable resource limitation. This largely convergent evolution of the expression of core metabolic proteins is associated with an improvement in the resource assimilation efficiency of nitrogen and phosphorus into biomass.

Ecological Engineering Helps Maximize Function in Algal Oil Production.

Algal biofuels have the potential to curb the emissions of greenhouse gases from fossil fuels, but current growing methods fail to produce fuels that meet the multiple standards necessary for economical industrial use. For example, algae grown as monocultures for biofuel production have not simultaneously and economically achieved high yields of the high-quality lipid-rich biomass desired for the industrial-scale production of bio-oil. Decades of study in the field of ecology have demonstrated that simultaneous increases in multiple functions, such as the quantity and quality of biomass, can occur in natural ecosystems by increasing biological diversity. Here, we show that species consortia of algae can improve the production of bio-oil, which benefits from both a high biomass yield and a high quality of biomass rich in fatty acids. We explain the underlying causes of increased quantity and quality of algal biomass among species consortia by showing that, relative to monocultures, species consortia can differentially regulate lipid metabolism genes while growing to higher levels of biomass, in part due to a greater utilization of nutrient resources. We identify multiple genes involved in lipid biosynthesis that are frequently upregulated in bicultures and further show that these elevated levels of gene expression are highly predictive of the elevated levels in biculture relative to that in monoculture of multiple quality metrics of algal biomass. These results show that interactions between species can alter the expression of lipid metabolism genes and further demonstrate that our understanding of diversity-function relationships from natural ecosystems can be harnessed to improve the production of bio-oil.IMPORTANCE Algal biofuels are one of the more promising forms of renewable energy. In our study, we investigate whether ecological interactions between species of microalgae regulate two important factors in cultivation-the biomass of the crop produced and the quality of the biomass that is produced. We found that species interactions often improved production yields, especially the fatty acid content of the algal biomass, and that differentially expressed genes involved in fatty acid metabolism are predictive of improved quality metrics of bio-oil. Other studies have found that diversity often improves productivity and stability in agricultural and natural ecosystems. Our results provide further evidence that growing multispecies crops of microalgae may improve the production of high-quality biomass for bio-oil.

Integrating community assembly and biodiversity to better understand ecosystem function: the Community Assembly and the Functioning of Ecosystems (CAFE) approach.

The research of a generation of ecologists was catalysed by the recognition that the number and identity of species in communities influences the functioning of ecosystems. The relationship between biodiversity and ecosystem functioning (BEF) is most often examined by controlling species richness and randomising community composition. In natural systems, biodiversity changes are often part of a bigger community assembly dynamic. Therefore, focusing on community assembly and the functioning of ecosystems (CAFE), by integrating both species richness and composition through species gains, losses and changes in abundance, will better reveal how community changes affect ecosystem function. We synthesise the BEF and CAFE perspectives using an ecological application of the Price equation, which partitions the contributions of richness and composition to function. Using empirical examples, we show how the CAFE approach reveals important contributions of composition to function. These examples show how changes in species richness and composition driven by environmental perturbations can work in concert or antagonistically to influence ecosystem function. Considering how communities change in an integrative fashion, rather than focusing on one axis of community structure at a time, will improve our ability to anticipate and predict changes in ecosystem function.

Evolution as an ecosystem process: insights from genomics.

Evolution is a fundamental ecosystem process. The study of genomic variation of organisms can not only improve our understanding of evolutionary processes, but also of contemporary and future ecosystem dynamics. We argue that integrative research between the fields of genomics and ecosystem ecology could generate new insights. Specifically, studies of biodiversity and ecosystem functioning, evolutionary rescue, and eco-evolutionary dynamics could all benefit from information about variation in genome structure and the genetic architecture of traits, whereas genomic studies could benefit from information about the ecological context of evolutionary dynamics. We propose new ways to help link research on functional genomic diversity with (reciprocal) interactions between phenotypic evolution and ecosystem change. Despite numerous challenges, we anticipate that the wealth of genomic data being collected on natural populations will improve our understanding of ecosystems.

Ecological Stoichiometry Meets Ecological Engineering: Using Polycultures to Enhance the Multifunctionality of Algal Biocrude Systems.

For algal biofuels to be economically sustainable and avoid exacerbating nutrient pollution, algal cultivation and processing must maximize rates of biofuel production while simultaneously minimizing the consumption of nitrogen (N) and phosphorus (P) fertilizers. We experimentally tested whether algal polycultures could be engineered to improve N and P nutrient-use efficiency compared to monocultures by balancing trade-offs in nutrient-use efficiency and biocrude production. We analyzed the flows of N and P through the processes of cultivation, biocrude production through hydrothermal liquefaction, and nutrient recycling in a laboratory-scale system. None of the six species we examined exhibited high N efficiency, P efficiency, and biocrude production simultaneously; each had poor performance in at least one function (i.e., <25th percentile). Polycultures of two to six species did not outperform the best species in any single function, but some polycultures exhibited more balanced performance and maintained all three functions at higher levels simultaneously than any of the monocultures (i.e., >67th percentile). Moreover, certain polycultures came closer to optimizing all three functions than any of the monocultures. By balancing trade-offs between N and P efficiency and biocrude production, polycultures could be used to simultaneously reduce the demand for both N and P fertilizers by up to 85%.

Single-cell mass spectrometry reveals the importance of genetic diversity and plasticity for phenotypic variation in nitrogen-limited Chlamydomonas.

Phenotypic variation is vital for microbial populations to survive environmental perturbations. Both genetic and non-genetic factors contribute to an organism's phenotypic variation and therefore its fitness. To investigate the correlation between genetic diversity and phenotypic variation, we applied our recently developed mass spectrometry method that allows for the simultaneous measurement of more than 25 different lipids and pigments with high throughput in the unicellular microalga Chlamydomonas reinhardtii. We monitored the impact of nitrogen limitation on a genetically diverse wild-type strain CC-1690 and two isoclonal isolates from CC-1690 named ANC3 and ANC5. Measuring molecular composition of thousands of single cells at different time points of the experiment allowed us to capture a dynamic picture of the phenotypic composition and adaptation of the populations over time. Although the genetically diverse population maintained phenotypic variation over the whole time course of the experiment, the isoclonal cultures showed higher synchronicity in their phenotypic response. Furthermore, the genetically diverse population showed equal or greater phenotypic variation over the whole time range in multidimensional trait space compared with isoclonal populations. However, along individual trait axes non-genetic variance was higher in isoclonal populations.