Mridul K. Thomas

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.

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.

Toward an integration of evolutionary biology and ecosystem science

At present, the disciplines of evolutionary biology and ecosystem science are weakly integrated. As a result, we have a poor understanding of how the ecological and evolutionary processes that create, maintain, and change biological diversity affect the flux of energy and materials in global biogeochemical cycles. The goal of this article was to review several research fields at the interfaces between ecosystem science, community ecology and evolutionary biology, and suggest new ways to integrate evolutionary biology and ecosystem science. In particular, we focus on how phenotypic evolution by natural selection can influence ecosystem functions by affecting processes at the environmental, population and community scale of ecosystem organization. We develop an eco-evolutionary model to illustrate linkages between evolutionary change (e.g. phenotypic evolution of producer), ecological interactions (e.g. consumer grazing) and ecosystem processes (e.g. nutrient cycling). We conclude by proposing experiments to test the ecosystem consequences of evolutionary changes.

Global biogeochemical impacts of phytoplankton: a trait‐based perspective

Summary Phytoplankton are key players in the global carbon cycle, contributing about half of global primary productivity. Within the phytoplankton, functional groups (characterized by distinct traits) have impacts on other major biogeochemical cycles, such as nitrogen, phosphorus and silica. Changes in phytoplankton community structure, resulting from the unique environmental sensitivities of these groups, may significantly alter elemental cycling from local to global scales. We review key traits that distinguish major phytoplankton functional groups, how they affect biogeochemistry and how the links between community structure and biogeochemical cycles are modelled. Finally, we explore how global environmental change will affect phytoplankton communities, from the traits of individual species to the relative abundance of functional groups, and how that, in turn, may alter biogeochemical cycles. Synthesis. We can increase our mechanistic understanding of the links between the community structure of primary producers and biogeochemistry by focusing on traits determining functional group responses to the environment (response traits) and their biogeochemical functions (effect traits). Identifying trade-offs including allometric and phylogenetic constraints among traits will help parameterize predictive biogeochemical models, enhancing our ability to anticipate the consequences of global change.

Effects of temperature and nitrogen availability on the growth of invasive and native cyanobacteria

Rising temperatures are expected to favour the growth of bloom-forming cyanobacteria in temperate lakes, but may also change the composition of cyanobacterial communities. To predict future community and bloom dynamics, it is therefore important to understand how bloom-forming species respond to temperature. Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju is an invasive, toxin-producing, nitrogen-fixer that may benefit from warming. To understand how changing temperatures will influence its ability to compete against native North American bloom-formers, we characterized the thermal reaction norms and temperature traits of three C. raciborskii strains, four strains of Microcystis aeruginosa (Kützing) Kützing and one strain of Anabaena flos-aquae (Lyng.) Brèb. C. raciborskii strains had higher optimum temperatures and survived higher temperatures than toxic M. aeruginosa strains, but had no apparent advantage over the non-toxic M. aeruginosa strain or A. flos-aquae. M. aeruginosa strains and A. flos-aquae tolerated lower temperatures than C. raciborskii, suggesting that fitness differences at low temperature may be important in limiting the latter’s spread. Furthermore, we found that nutrient availability strongly influenced thermal reaction norm shape: nitrogen deprivation lowered growth rates and decreased both low- and high-temperature tolerance, but did not affect the optimum temperature in C. raciborskii.

Swift thermal reaction norm evolution in a key marine phytoplankton species

Temperature has a profound effect on the species composition and physiology of marine phytoplankton, a polyphyletic group of microbes responsible for half of global primary production. Here, we ask whether and how thermal reaction norms in a key calcifying species, the coccolithophore Emiliania huxleyi, change as a result of 2.5 years of experimental evolution to a temperature ≈2°C below its upper thermal limit. Replicate experimental populations derived from a single genotype isolated from Norwegian coastal waters were grown at two temperatures for 2.5 years before assessing thermal responses at 6 temperatures ranging from 15 to 26°C, with pCO2 (400/1100/2200 μatm) as a fully factorial additional factor. The two selection temperatures (15°/26.3°C) led to a marked divergence of thermal reaction norms. Optimal growth temperatures were 0.7°C higher in experimental populations selected at 26.3°C than those selected at 15.0°C. An additional negative effect of high pCO2 on maximal growth rate (8% decrease relative to lowest level) was observed. Finally, the maximum persistence temperature (Tmax) differed by 1–3°C between experimental treatments, as a result of an interaction between pCO2 and the temperature selection. Taken together, we demonstrate that several attributes of thermal reaction norms in phytoplankton may change faster than the predicted progression of ocean warming.

Individual-level trait diversity predicts phytoplankton community properties better than species richness or evenness

Understanding how microbial diversity influences ecosystem properties is of paramount importance. Cellular traits—which determine responses to the abiotic and biotic environment—may help us rigorously link them. However, our capacity to measure traits in natural communities has thus far been limited. Here we compared the predictive power of trait richness (trait space coverage), evenness (regularity in trait distribution) and divergence (prevalence of extreme phenotypes) derived from individual-based measurements with two species-level metrics (taxonomic richness and evenness) when modelling the productivity of natural phytoplankton communities. Using phytoplankton data obtained from 28 lakes sampled at different spatial and temporal scales, we found that the diversity in individual-level morphophysiological traits strongly improved our ability to predict community resource-use and biomass yield. Trait evenness—the regularity in distribution of individual cells/colonies within the trait space—was the strongest predictor, exhibiting a robust negative relationship across scales. Our study suggests that quantifying individual microbial phenotypes in trait space may help us understand how to link physiology to ecosystem-scale processes. Elucidating the mechanisms scaling individual-level trait variation to microbial community dynamics could there improve our ability to forecast changes in ecosystem properties across environmental gradients.

Water-borne pharmaceuticals reduce phenotypic diversity and response capacity of natural phytoplankton communities

Chemical micropollutants occur worldwide in the environment at low concentrations and in complex mixtures, and how they affect the ecology of natural systems is still uncertain. Dynamics of natural communities are driven by the interaction between individual organisms and their growth environment, which is mediated by the organisms’ expressed phenotypic traits. We tested whether exposure to a mixture of 12 pharmaceuticals and personal care products (PPCP) influences phenotypic trait diversity in lake phytoplankton communities and their ability to regulate biomass production to fit environmental changes (response capacity). We exposed natural phytoplankton assemblages to three mixture levels in permeable microcosms maintained at three depths in a eutrophic lake for one week, during which the environmental conditions were fluctuating. We studied individual-level traits, phenotypic diversity and community biomass. PPCP reduced individual-level trait variance and overall community phenotypic diversity, but maintained higher standing phytoplankton biomass compared to untreated controls. Estimated effect sizes of PPCP on traits and community properties were very large (partial Eta-squared > 0.15). The PPCP mixture antagonistically interacted with the natural environmental gradient in habitats offered by different depths and, at concentrations comparable to those in waste-water effluents, prevented communities from converging to the same phenotypic structure and total biomass of unexposed controls. We show that micropollutants can alter individual-level trait diversity of lake phytoplankton communities and therefore their capacity to respond to natural environmental gradients, potentially affecting aquatic ecosystem processes.