Impacts of Fungal Disease on Algal Biofuel Systems: Using Life Cycle Assessment to Compare Control Strategies.

While climate change has incentivized attention on sustainable fuel sources, algae has positioned itself as a both promising and problematic biofuel feedstock. Diseases such as fungal pathogens cause costly algal feedstock crashes, but the life cycle assessments (LCAs) used to analyze the viability of algal feedstocks for biofuel have yet to consider the impact of disease on life cycle metrics. Here, we incorporate a disease model into a well-documented LCA for algal biorefineries to compare two sustainability metrics, energy return on investment (EROI) and global warming potential (GWP). We begin by showing that failure to consider disease leads to overly optimistic LCA metric outputs. Then, we compare two leading control strategies of disease─chemical and biological. Our analyses show that biological engineering of a multispecies consortium of algae has a greater positive impact on LCA metrics than chemical control of the fungal pathogen using a fungicide. We expand how and when bi-cultures might advantageously exhibit the "dilution effect" whereby differentially susceptible species exhibit compensatory dynamics that stabilize feedstock production. Our results emphasize the impact of disease and suggest that multispecies consortia of algae can be biologically engineered to reduce greenhouse gas emissions and improve the economic viability of biofuel.

Human pressure drives biodiversity-multifunctionality relationships in large Neotropical wetlands.

Many studies have shown that biodiversity regulates multiple ecological functions that are needed to maintain the productivity of a variety of ecosystem types. What is unknown is how human activities may alter the 'multifunctionality' of ecosystems through both direct impacts on ecosystems and indirect effects mediated by the loss of multifaceted biodiversity. Using an extensive database of 72 lakes spanning four large Neotropical wetlands in Brazil, we demonstrate that species richness and functional diversity across multiple larger (fish and macrophytes) and smaller (microcrustaceans, rotifers, protists and phytoplankton) groups of aquatic organisms are positively associated with ecosystem multifunctionality. Whereas the positive association between smaller organisms and multifunctionality broke down with increasing human pressure, this positive relationship was maintained for larger organisms despite the increase in human pressure. Human pressure impacted multifunctionality both directly and indirectly through reducing species richness and functional diversity of multiple organismal groups. These findings provide further empirical evidence about the importance of aquatic biodiversity for maintaining wetland multifunctionality. Despite the key role of biodiversity, human pressure reduces the diversity of multiple groups of aquatic organisms, eroding their positive impacts on a suite of ecological functions that sustain wetlands.

Biodiversity and disease risk in an algal biofuel system: An experimental test in outdoor ponds using a before-after-control-impact (BACI) design.

For outdoor cultivation of algal feedstocks to become a commercially viable and sustainable option for biofuel production, algal cultivation must maintain high yields and temporal stability in environmentally variable outdoor ponds. One of the main challenges is mitigating disease outbreaks that leads to culture crashes. Drawing on predictions from the 'dilution effect' hypothesis, in which increased biodiversity is thought to reduce disease risk in a community, a teste of whether algal polycultures would reduce disease risk and improve feedstock production efficiencies compared to monocultures was performed. While the positive benefits of biodiversity on disease risk have been demonstrated in various systems, to the best of our knowledge this is the first test in an algal biofuel system. Here, the results a before-after-control-impact (BACI) experimental design to compare mean monoculture (control) and polyculture (impact) yield, stability, and productivity before and after fungal infection when grown in 400-L outdoor raceway ponds are presented. It has been found that polycultures did not experience a reduction in disease risk compared to monocultures or differ in production efficiencies throughout the course of the 43-day experiment. These results show that polyculture feedstocks can maintain similar levels of productivity, stability, and disease resistance to that of a monoculture. Determining whether these results are generalizable or represent one case study requires additional outdoor experiments using a larger variety of host and pathogen species.

Impacts of detritivore diversity loss on instream decomposition are greatest in the tropics.

The relationship between detritivore diversity and decomposition can provide information on how biogeochemical cycles are affected by ongoing rates of extinction, but such evidence has come mostly from local studies and microcosm experiments. We conducted a globally distributed experiment (38 streams across 23 countries in 6 continents) using standardised methods to test the hypothesis that detritivore diversity enhances litter decomposition in streams, to establish the role of other characteristics of detritivore assemblages (abundance, biomass and body size), and to determine how patterns vary across realms, biomes and climates. We observed a positive relationship between diversity and decomposition, strongest in tropical areas, and a key role of abundance and biomass at higher latitudes. Our results suggest that litter decomposition might be altered by detritivore extinctions, particularly in tropical areas, where detritivore diversity is already relatively low and some environmental stressors particularly prevalent.

Latitude dictates plant diversity effects on instream decomposition.

Running waters contribute substantially to global carbon fluxes through decomposition of terrestrial plant litter by aquatic microorganisms and detritivores. Diversity of this litter may influence instream decomposition globally in ways that are not yet understood. We investigated latitudinal differences in decomposition of litter mixtures of low and high functional diversity in 40 streams on 6 continents and spanning 113° of latitude. Despite important variability in our dataset, we found latitudinal differences in the effect of litter functional diversity on decomposition, which we explained as evolutionary adaptations of litter-consuming detritivores to resource availability. Specifically, a balanced diet effect appears to operate at lower latitudes versus a resource concentration effect at higher latitudes. The latitudinal pattern indicates that loss of plant functional diversity will have different consequences on carbon fluxes across the globe, with greater repercussions likely at low latitudes.

Why does the public support or oppose agricultural nutrient runoff regulations? The effects of political orientation, environmental worldview, and policy specific beliefs.

This research examines public acceptability of regulations to reduce agricultural nutrient runoff and curb Harmful Algal Blooms (HABs). We tested the effects of two novel policy specific beliefs including support for farmers' autonomy and support for external accountability. We also simultaneously tested the direct and indirect effects of political orientation and environmental worldview through a Direct Effect Model and a Mediation Model using structural equation modelling. Survey data were collected from 729 Ohio residents collected in November 2018. The specific regulatory policy measure we targeted is fines on excessive agricultural runoff. As hypothesized, autonomy beliefs negatively affect, and accountability positively affect support for fines. Both models revealed good fits. the direct effects of environmental worldviews political orientation were not supported. Instead, environmental worldviews indirectly increased support for fines through increased accountability beliefs and diminished autonomy beliefs. From the results, we suggest that when proposing suitable regulations for specific sites, policy makers and interest groups should be aware of differences in public support for farmer autonomy and external accountability, and that such differences are likely rooted in environmental worldviews. The study also suggests a need for coupled ecological and social studies that assess the likelihood of regional agricultural producers voluntarily adopting conservation practices and forecast the effectiveness of potential accountability measures.

Scaling up biodiversity-ecosystem function relationships across space and over time.

Understanding how to scale up effects of biological diversity on ecosystem functioning and services remains challenging. There is a general consensus that biodiversity loss alters ecosystem processes underpinning the goods and services upon which humanity depends. Yet most of that consensus stems from experiments performed at small spatial scales for short time frames, which limits transferability of conclusions to longer-term, landscape-scale conservation policies and management. Here we develop quantitative scaling relationships linking 374 experiments that tested plant diversity effects on biomass production across a range of scales. We show that biodiversity effects increase by factors of 1.68 and 1.10 for each 10-fold increase in experiment temporal and spatial scales, respectively. Contrary to prior studies, our analyses suggest that the time scale of experiments, rather than their spatial scale, is the primary source of variation in biodiversity effects. But consistent with earlier research, our analyses reveal that complementarity effects, rather than selection effects, drive the positive space-time interactions for plant diversity effects. Importantly, we also demonstrate complex space-time interactions and nonlinear responses that emphasize how simple extrapolations from small-scale experiments are likely to underestimate biodiversity effects in real-world ecosystems. Quantitative scaling relationships from this research are a crucial step towards bridging controlled experiments that identify biological mechanisms across a range of scales. Predictions from scaling relationships like these could then be compared with observations for fine-tuning the relationships and ultimately improving their capacities to predict consequences of biodiversity loss for ecosystem functioning and services over longer time frames across real-world landscapes.

Intra-guild predation (IGP) can increase or decrease prey density depending on the strength of IGP.

In consumer communities, intra-guild predation (IGP) is a commonly observed interaction that is widely believed to increase resource density. However, some recent theoretical work predicts that resource density should first decrease, and then increase as the strength of IGP increases. This occurs because weak to intermediate IGP increases the IG predator density more than it reduces the IG prey density, so that weak to intermediate IGP leads to the lowest resource density compared to weak or strong IGP. We test this prediction that basal resource density would first decrease and then increase as the strength of IGP increase. We used a well-studied system with two protozoa species engaged in IGP and three bacteria species as the basal resources. We experimentally manipulated the percentage of the IG prey population that was available to an IG predator as a proxy for IGP strength. We found that bacterial density first decreased (by ~25%) and then increased (by ~30%) as the strength of IGP increased. Using a modified version of a published IGP model, we were able to explain ~70% of the variation in protozoa and bacterial density. Agreement of the empirical results with model predictions suggests that IGP first increased the IG predator density by consuming a small proportion of the IG prey population, which in turn increased the summed consumer density and decreased the bacterial resource density. As IGP strength increased further, the IG predator became satiated by the IG prey, which then freed the bacterial resource from predation and thus increased bacterial density. Consequently, our work shows that IGP can indeed decrease or increase basal resource density depending on its strength. Consequently, the impacts of IGP on resource density is potentially more complex than previously thought.

Microbiomes Reduce Their Host's Sensitivity to Interspecific Interactions.

Bacteria associated with eukaryotic hosts can affect host fitness and trophic interactions between eukaryotes, but the extent to which bacteria influence the eukaryotic species interactions within trophic levels that modulate biodiversity and species coexistence is mostly unknown. Here, we used phytoplankton, which are a classic model for evaluating interactions between species, grown with and without associated bacteria to test whether the bacteria alter the strength and type of species interactions within a trophic level. We demonstrate that host-associated bacteria alter host growth rates and carrying capacity. This did not change the type but frequently changed the strength of host interspecific interactions by facilitating host growth in the presence of an established species. These findings indicate that microbiomes can regulate their host species' interspecific interactions. As between-species interaction strength impacts their ability to coexist, our findings show that microbiomes have the potential to modulate eukaryotic species diversity and community composition.IMPORTANCE Description of the Earth's microbiota has recently undergone a phenomenal expansion that has challenged basic assumptions in many areas of biology, including hominid evolution, human gastrointestinal and neurodevelopmental disorders, and plant adaptation to climate change. By using the classic model system of freshwater phytoplankton that has been drawn upon for numerous foundational theories in ecology, we show that microbiomes, by facilitating their host population, can also influence between-species interactions among their eukaryotic hosts. Between-species interactions, including competition for resources, has been a central tenet in the field of ecology because of its implications for the diversity and composition of communities and how this in turn shapes ecosystem functioning.

Biodiversity Improves Life Cycle Sustainability Metrics in Algal Biofuel Production.

Algal biofuel has yet to realize its potential as a commercial and sustainable bioenergy source, largely due to the challenge of maximizing and sustaining biomass production with respect to energetic and material inputs in large-scale cultivation. Experimental studies have shown that multispecies algal polycultures can be designed to enhance biomass production, stability, and nutrient recycling compared to monocultures. Yet, it remains unclear whether these impacts of biodiversity make polycultures more sustainable than monocultures. Here, we present results of a comparative life cycle assessment (LCA) for algal biorefineries to compare the sustainability metrics of monocultures and polycultures of six fresh-water algal species. Our results showed that when algae were grown in outdoor experimental ponds, certain bicultures improved the energy return on investment (EROI) and greenhouse gas emissions (GHGs) by 20% and 16%, respectively, compared to the best monoculture. Bicultures outperformed monocultures by performing multiple functions simultaneously (e.g., improved stability, nutrient efficiency, biocrude characteristics), which outweighed the higher productivity attainable by a monoculture. Our results demonstrate that algal polycultures with optimized multifunctionality lead to enhanced life cycle metrics, highlighting the significant potential of ecological engineering for enabling future environmentally sustainable algal biorefineries.

Aquatic macroinvertebrates stabilize gravel bed sediment: A test using silk net-spinning caddisflies in semi-natural river channels.

Organisms can have large effects on the physical properties of the habitats where they live. For example, measurements in laboratory stream microcosms have shown that the presence of silk net-spinning insect larvae (Trichoptera: Hydropsychidae) can increase the shear force required to initiate movement of riverbed sediments. Few studies, however, have moved beyond laboratory settings to quantify the engineering impacts of aquatic insects under more complex field conditions. To bridge the gap between small-scale laboratory experiments and natural stream ecosystems, we conducted experiments in large (50 m2) outdoor river channels where net-spinning aquatic insects were manipulated in sediment patches that were 5 to 25 times larger than in previous studies. We tested whether larvae of two caddisfly species (Arctopsyche californica and Ceratopsyche oslari) influenced the stability of gravel during simulated floods when alone in monoculture and together in polyculture. On average, populations of caddisflies increased the critical shear stress required to initiate sediment movement by 20% compared to treatments without caddisflies. Per capita effects of caddisflies on sediment stability were similar between previous laboratory studies and this field experiment, and Arctopsyche had a larger per capita effect than Ceratopsyche, perhaps because of its larger size and stronger silk. Contrary to prior laboratory flume results, the effects of the two species on critical shear stress when together were similar to the additive expectation of both species when alone, but effects of the two species together were higher than the additive expectation when we accounted for density. Comparisons of total population and per capita effects suggest that caddisfly density, identity, and coexisting species likely have effects on the magnitude of caddisfly impacts on critical shear stress. Our findings imply that consideration of both the abundances and traits of ecosystem engineers is needed to describe and model their effects on sediment mobility.

Ranking stressor impacts on periphyton structure and function with mesocosm experiments and environmental-change forecasts.

Streams are being subjected to physical, chemical, and biological stresses stemming from both natural and anthropogenic changes to the planet. In the face of limited time and resources, scientists, resource managers, and policy makers need ways to rank stressors and their impacts so that we can prioritize them from the most to least important (i.e., perform 'ecological triage'). We report results from an experiment in which we established a periphyton community from the Huron River (Michigan, USA) in 84 experimental 'flumes' (stream mesocosms). We then dosed the flumes with gradients of six common stressors (increased temperature, taxa extinctions, sedimentation, nitrogen, phosphorus, and road salt) and monitored periphyton structure and function. A set of a priori deterministic functions were fit to each stressor-endpoint response and model averaging based on AICc weights was used to develop concentration-response best-fit predictions. Model predictions from different stressors were then compared to forecasts of future environmental change to rank stressors according to the potential magnitude of impacts. All of the stressors studied altered at least one characteristic of the periphyton; however, the extent (i.e., structural and functional changes) and magnitude of effects expected under future forecasts differed significantly among stressors. Elevated nitrogen concentrations are projected to have the greatest combined effect on stream periphyton structure and function. Extinction, sediment, and phosphorus all had similar but less substantial impact on the periphyton (e.g., affected only structure not function, smaller magnitude change). Elevated temperature and salt both had measurable effects on periphyton, but their overall impacts were much lower than any of the other stressors. For periphyton in the Huron River, our results suggest that, among the stressors examined, increased N pollution may have the greatest potential to alter the structure and function of the periphyton community, and managers should prioritize reducing anthropogenic sources of nitrogen. Our study demonstrates an experimental approach to ecological triage that can be used as an additional line of evidence to prioritize management decisions for specific ecosystems in the face of ecological change.

Interactions between large and small detritivores influence how biodiversity impacts litter decomposition.

Understanding how biodiversity loss influences plant litter decomposition-that is, the biologically mediated conversion of coarse to fine particulate organic matter-is crucial to predict changes in the functioning of many stream ecosystems, where detrital food webs are dominant. Rates of litter decomposition are influenced by detritivore diversity, but the mechanisms behind this relationship are uncertain. As differences in detritivore body size are a major determinant of interspecific interactions, they should be key for predicting effects of detritivore diversity on decomposition. To explore this question, we manipulated detritivore diversity and body size simultaneously in a microcosm experiment using two small (Leuctra geniculata and Lepidostoma hirtum) and two large detritivore species (Sericostoma pyrenaicum and Echinogammarus berilloni) in all possible 1-, 2- and 4-species combinations, and litter discs of Alnus glutinosa. We expected that larger species would facilitate smaller species through the production of smaller litter fragments, resulting in faster decomposition and greater growth of smaller species in polycultures containing species of different body size. To examine this hypothesis, we used a set of "diversity-interaction" models that explored how decomposition was affected by different interspecific interactions and the role of body size, and quantified the magnitude of such effect through ratios of decomposition rates and detritivore growth between polycultures and monocultures. We found a clear positive effect of detritivore diversity on decomposition, which was mainly explained by facilitation and niche partitioning. Facilitation of small animals by larger ones was evidenced by a 12% increase in decomposition rates in polycultures compared to monocultures and the higher growth (20%) of small species, which partly fed on fine particulate organic matter produced by larger animals. When the large species were together in polycultures, decomposition was enhanced by 19%, but there were no changes in growth; niche partitioning was a plausible mechanism behind the increase in decomposition rates, as both species fed on different parts of litter discs, only one species being able to eat less palatable parts. Our study demonstrates that interspecific differences in body size should be taken into account in diversity-decomposition studies. Future studies should also consider differences in species' vulnerability to extinction depending on body size and how this might affect ecosystem functioning in different scenarios of detritivore diversity and more complex food webs.

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.

Biodiversity effects in the wild are common and as strong as key drivers of productivity.

More than 500 controlled experiments have collectively suggested that biodiversity loss reduces ecosystem productivity and stability. Yet the importance of biodiversity in sustaining the world's ecosystems remains controversial, largely because of the lack of validation in nature, where strong abiotic forcing and complex interactions are assumed to swamp biodiversity effects. Here we test this assumption by analysing 133 estimates reported in 67 field studies that statistically separated the effects of biodiversity on biomass production from those of abiotic forcing. Contrary to the prevailing opinion of the previous two decades that biodiversity would have rare or weak effects in nature, we show that biomass production increases with species richness in a wide range of wild taxa and ecosystems. In fact, after controlling for environmental covariates, increases in biomass with biodiversity are stronger in nature than has previously been documented in experiments and comparable to or stronger than the effects of other well-known drivers of productivity, including climate and nutrient availability. These results are consistent with the collective experimental evidence that species richness increases community biomass production, and suggest that the role of biodiversity in maintaining productive ecosystems should figure prominently in global change science and policy.

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%.

Demonstration of transgressive overyielding of algal mixed cultures in microdroplets.

Algae are ubiquitous in natural ecosystems and have been studied extensively for biofuel production due to their unique metabolic capabilities. Most studies to date have approached biofuel optimization through synthetic biology and process engineering with few industrial scale projects considering algal community interactions. Such interactions can potentially lead to increased productivity and reduced community invasability, both important characteristics for scalable algal biofuel production. It is estimated that over a million species of algae exist such that elucidating the interactions that might be beneficial for biofuel production remains extremely resource and time intensive. Here we describe a strategy for rapid, high-throughput screening of algal community combinations using a microfluidic platform to generate millions of parallel, nanoliter-scale algal mixed cultures for estimation of biomass accumulation. Model communities were first studied in a bench scale flask experiment and then examined using microfluidic droplets. These experiments showed consistent results for both positively interacting algal bicultures that increase biomass when together, and negatively interacting bicultures that decrease biomass. Specifically, these included enhanced performance of two bicultures, Ankistrodesmus falcatus and Chlorella sorokiniana, Chlorella sorokiniana and Selenastrum minutum, and reduced performance of a biculture consisting of Selenastrum capricornutum and Scenedesmus ecornis. While the ultimate techno-economic feasibility of algal bioproducts hinges on an amalgamation of scientific fields, rapid screening of algal communities will prove imperative for efficiently discovering community interactions.

The economic value of grassland species for carbon storage.

Carbon storage by ecosystems is valuable for climate protection. Biodiversity conservation may help increase carbon storage, but the value of this influence has been difficult to assess. We use plant, soil, and ecosystem carbon storage data from two grassland biodiversity experiments to show that greater species richness increases economic value: Increasing species richness from 1 to 10 had twice the economic value of increasing species richness from 1 to 2. The marginal value of each additional species declined as species accumulated, reflecting the nonlinear relationship between species richness and plant biomass production. Our demonstration of the economic value of biodiversity for enhancing carbon storage provides a foundation for assessing the value of biodiversity for decisions about land management. Combining carbon storage with other ecosystem services affected by biodiversity may well enhance the economic arguments for conservation even further.

Ecosystem services in the Great Lakes.

A comprehensive inventory of ecosystem services across the entire Great Lakes basin is currently lacking and is needed to make informed management decisions. A greater appreciation and understanding of ecosystem services, including both use and non-use services, may have avoided misguided resource management decisions in the past that have resulted in legacies inherited by future generations. Given the interest in ecosystem services and lack of a coherent approach to addressing this topic in the Great Lakes, a summit was convened involving 28 experts working on various aspects of ecosystem services in the Great Lakes. The invited attendees spanned a variety of social and natural sciences. Given the unique status of the Great Lakes as the world's largest collective repository of surface freshwater, and the numerous stressors threatening this valuable resource, timing was propitious to examine ecosystem services. Several themes and recommendations emerged from the summit. There was general consensus that 1) a comprehensive inventory of ecosystem services throughout the Great Lakes is a desirable goal but would require considerable resources; 2) more spatially and temporally intensive data are needed to overcome our data gaps, but the arrangement of data networks and observatories must be well-coordinated; 3) trade-offs must be considered as part of ecosystem services analyses; and 4) formation of a Great Lakes Institute for Ecosystem Services, to provide a hub for research, meetings, and training is desirable. Several challenges also emerged during the summit, which are discussed in the paper.