Elena Litchman

Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton

Redfield noted the similarity between the average nitrogen-to-phosphorus ratio in plankton (N:P = 16 by atoms) and in deep oceanic waters (N:P = 15; refs 1, 2). He argued that this was neither a coincidence, nor the result of the plankton adapting to the oceanic stoichiometry, but rather that phytoplankton adjust the N:P stoichiometry of the ocean to meet their requirements through nitrogen fixation, an idea supported by recent modelling studies. But what determines the N:P requirements of phytoplankton? Here we use a stoichiometrically explicit model of phytoplankton physiology and resource competition to derive from first principles the optimal phytoplankton stoichiometry under diverse ecological scenarios. Competitive equilibrium favours greater allocation to P-poor resource-acquisition machinery and therefore a higher N:P ratio; exponential growth favours greater allocation to P-rich assembly machinery and therefore a lower N:P ratio. P-limited environments favour slightly less allocation to assembly than N-limited or light-limited environments. The model predicts that optimal N:P ratios will vary from 8.2 to 45.0, depending on the ecological conditions. Our results show that the canonical Redfield N:P ratio of 16 is not a universal biochemical optimum, but instead represents an average of species-specific N:P ratios.

A Global Pattern of Thermal Adaptation in Marine Phytoplankton

Local Optima for Plankton Recent ocean warming has changed the seasonality and composition of the marine phytoplankton. Thomas et al. (p. 1085, published online 25 October) investigated the direct effect of temperature on phytoplankton. By fitting published data to reaction temperature norms for 194 phytoplankton strains isolated from a wide latitudinal range, the resultant temperature-related traits (maximum growth rate, temperature optimum, and thermal niche width) reveal latitudinal trends in temperature optima and diversity. Biogeographical differences indicate an increased susceptibility of tropical strains to further warming, and modeling predicts poleward shifts of tropical strains and a loss of phytoplankton diversity in the tropics within the next hundred years. Optimal growth rates for phytoplankton correlate with local temperature and predict movement toward the poles with warming. Rising ocean temperatures will alter the productivity and composition of marine phytoplankton communities, thereby affecting global biogeochemical cycles. Predicting the effects of future ocean warming on biogeochemical cycles depends critically on understanding how existing global temperature variation affects phytoplankton. Here we show that variation in phytoplankton temperature optima over 150 degrees of latitude is well explained by a gradient in mean ocean temperature. An eco-evolutionary model predicts a similar relationship, suggesting that this pattern is the result of evolutionary adaptation. Using mechanistic species distribution models, we find that rising temperatures this century will cause poleward shifts in species’ thermal niches and a sharp decline in tropical phytoplankton diversity in the absence of an evolutionary response.

Marine phytoplankton temperature versus growth responses from polar to tropical waters – outcome of a scientific community-wide study

“It takes a village to finish (marine) science these days” Paraphrased from Curtis Huttenhower (the Human Microbiome project) The rapidity and complexity of climate change and its potential effects on ocean biota are challenging how ocean scientists conduct research. One way in which we can begin to better tackle these challenges is to conduct community-wide scientific studies. This study provides physiological datasets fundamental to understanding functional responses of phytoplankton growth rates to temperature. While physiological experiments are not new, our experiments were conducted in many laboratories using agreed upon protocols and 25 strains of eukaryotic and prokaryotic phytoplankton isolated across a wide range of marine environments from polar to tropical, and from nearshore waters to the open ocean. This community-wide approach provides both comprehensive and internally consistent datasets produced over considerably shorter time scales than conventional individual and often uncoordinated lab efforts. Such datasets can be used to parameterise global ocean model projections of environmental change and to provide initial insights into the magnitude of regional biogeographic change in ocean biota in the coming decades. Here, we compare our datasets with a compilation of literature data on phytoplankton growth responses to temperature. A comparison with prior published data suggests that the optimal temperatures of individual species and, to a lesser degree, thermal niches were similar across studies. However, a comparison of the maximum growth rate across studies revealed significant departures between this and previously collected datasets, which may be due to differences in the cultured isolates, temporal changes in the clonal isolates in cultures, and/or differences in culture conditions. Such methodological differences mean that using particular trait measurements from the prior literature might introduce unknown errors and bias into modelling projections. Using our community-wide approach we can reduce such protocol-driven variability in culture studies, and can begin to address more complex issues such as the effect of multiple environmental drivers on ocean biota.

Contrasting size evolution in marine and freshwater diatoms

Diatoms are key players in the global carbon cycle and most aquatic ecosystems. Their cell sizes impact carbon sequestration and energy transfer to higher trophic levels. We report fundamental differences in size distributions of marine and freshwater diatoms, with marine diatoms significantly larger than freshwater species. An evolutionary game theoretical model with empirical allometries of growth and nutrient uptake shows that these differences can be explained by nitrogen versus phosphorus limitation, nutrient fluctuations and mixed layer depth differences. Constant and pulsed phosphorus supply select for small sizes, as does constant nitrogen supply. In contrast, intermediate frequency nitrogen pulses common in the ocean select for large sizes or the evolutionarily stable coexistence of large and small sizes. Size-dependent sinking interacts with mixed layer depth (MLD) to further modulate optimal sizes, with smaller sizes selected for by strong sinking and shallow MLD. In freshwaters, widespread phosphorus limitation, together with strong sinking and shallow MLD produce size distributions with smaller range, means and upper values, compared with the ocean. Shifting patterns of nutrient limitation and mixing may alter diatom size distributions, affecting global carbon cycle and the structure and functioning of aquatic ecosystems.

Competition of Phytoplankton under Fluctuating Light

Light is an essential resource for phytoplankton and fluctuates on a wide range of timescales. To understand how light fluctuations affect phytoplankton community structure and diversity, we have studied a set of simple models using a combination of analytical and numerical techniques. Light fluctuations can affect community structure when species exhibit the gleaner‐opportunist trade‐off between competitive ability and ability to reach carrying capacity quickly. Fast fluctuations can switch the competitive dominant from a gleaner to an opportunist; slow fluctuations can cause this switch and also lead to stable coexistence. Coexistence is easiest between species that are highly differentiated along the gleaner‐opportunist trade‐off. Our results remain qualitatively unchanged when more realistic light fluctuations such as daily and seasonal changes in irradiance and the presence of a spatial gradient in light are considered. Seasonal change in day length may be one of the factors driving the seasonal succession of phytoplankton, from opportunist species dominant under shorter day lengths (spring and autumn) to gleaner species dominant under longer day length (summer). These results illustrate how resource fluctuations can have an important role in structuring ecological communities.

Linking traits to species diversity and community structure in phytoplankton

In addition to answering Hutchinson’s question “Why are there so many species?”, we need to understand why certain species are found only under certain environmental conditions and not others. Trait-based approaches are being increasingly used in ecology to do just that: explain and predict species distributions along environmental gradients. These approaches can be successful in understanding the diversity and community structure of phytoplankton. Among major traits shaping phytoplankton distributions are resource utilization traits, morphological traits (with size being probably the most influential), grazer resistance traits, and temperature responses. We review these trait-based approaches and give examples of how trait data can explain species distributions in both freshwater and marine systems. We also outline new directions in trait-based approaches applied to phytoplankton such as looking simultaneously at trait and phylogenetic structure of phytoplankton communities and using adaptive dynamics models to predict trait evolution.

Invisible invaders: non‐pathogenic invasive microbes in aquatic and terrestrial ecosystems

Although the number of studies on invasive plants and animals has risen exponentially, little is known about invasive microbes, especially non-pathogenic ones. Microbial invasions by viruses, bacteria, fungi and protists occur worldwide but are much harder to detect than invasions by macroorganisms. Invasive microbes have the potential to significantly alter community structure and ecosystem functioning in diverse terrestrial and aquatic ecosystems. Consequently, increased attention is needed on non-pathogenic invasive microbes, both free-living and symbiotic, and their impacts on communities and ecosystems. Major unknowns include the characteristics that make microbes invasive and properties of the resident communities and the environment that facilitate invasions. A comparison of microbial invasions with invasions of macroorganisms should provide valuable insights into general principles that apply to invasions across all domains of life and to taxon-specific invasion patterns. Invasive microbes appear to possess traits thought to be common in many invasive macroorganisms: high growth rate and resource utilization efficiency, and superior competitive abilities. Invading microorganisms are often similar to native species, but with enhanced performance traits, and tend to spread in lower diversity communities. Global change can exacerbate microbial invasions; therefore, they will likely increase in the future.

The biogeography of marine plankton traits

Changes in marine plankton communities driven by environmental variability impact the marine food web and global biogeochemical cycles of carbon and other elements. To predict and assess these community shifts and their consequences, ecologists are increasingly investigating how the functional traits of plankton determine their relative fitness along environmental and biological gradients. Laboratory, field and modelling studies are adopting this trait-based approach to map the biogeography of plankton traits that underlies variations in plankton communities. Here, we review progress towards understanding the regulatory roles of several key plankton functional traits, including cell size, N2 -fixation and mixotrophy among phytoplankton, and body size, ontogeny and feeding behaviour for zooplankton. The trait biogeographical approach sheds light on what structures plankton communities in the current ocean, as well as under climate change scenarios, and also allows for finer resolution of community function because community trait composition determines the rates of significant processes, including carbon export. Although understanding of trait biogeography is growing, uncertainties remain that stem, in part, from the paucity of observations describing plankton functional traits. Thus, in addition to recommending widespread adoption of the trait-based approach, we advocate for enhanced collection, standardisation and dissemination of plankton functional trait data.

Large-scale biodiversity patterns in freshwater phytoplankton

Our planet shows striking gradients in the species richness of plants and animals, from high biodiversity in the tropics to low biodiversity in polar and high-mountain regions. Recently, similar patterns have been described for some groups of microorganisms, but the large-scale biogeographical distribution of freshwater phytoplankton diversity is still largely unknown. We examined the species diversity of freshwater phytoplankton sampled from 540 lakes and reservoirs distributed across the continental United States and found strong latitudinal, longitudinal, and altitudinal gradients in phytoplankton biodiversity, demonstrating that microorganisms can show substantial geographic variation in biodiversity. Detailed analysis using structural equation models indicated that these large-scale biodiversity gradients in freshwater phytoplankton diversity were mainly driven by local environmental factors, although there were residual direct effects of latitude, longitude, and altitude as well. Specifically, we found that phytoplankton species richness was an increasing saturating function of lake chlorophyll a concentration, increased with lake surface area and possibly increased with water temperature, resembling effects of productivity, habitat area, and temperature on diversity patterns commonly observed for macroorganisms. In turn, these local environmental factors varied along latitudinal, longitudinal, and altitudinal gradients. These results imply that changes in land use or climate that affect these local environmental factors are likely to have major impacts on large-scale biodiversity patterns of freshwater phytoplankton.

Industrial‐strength ecology: trade‐offs and opportunities in algal biofuel production

Microalgae represent one of the most promising groups of candidate organisms for replacing fossil fuels with contemporary primary production as a renewable source of energy. Algae can produce many times more biomass per unit area than terrestrial crop plants, easing the competing demands for land with food crops and native ecosystems. However, several aspects of algal biology present unique challenges to the industrial-scale aquaculture of photosynthetic microorganisms. These include high susceptibility to invading aquatic consumers and weeds, as well as prodigious requirements for nutrients that may compete with the fertiliser demands of other crops. Most research on algal biofuel technologies approaches these problems from a cellular or genetic perspective, attempting either to engineer or select algal strains with particular traits. However, inherent functional trade-offs may limit the capacity of genetic selection or synthetic biology to simultaneously optimise multiple functional traits for biofuel productivity and resilience. We argue that a community engineering approach that manages microalgal diversity, species composition and environmental conditions may lead to more robust and productive biofuel ecosystems. We review evidence for trade-offs, challenges and opportunities in algal biofuel cultivation with a goal of guiding research towards intensifying bioenergy production using established principles of community and ecosystem ecology.