Comparative experimental evolution reveals species-specific idiosyncrasies in marine phytoplankton adaptation to warming.

A number of experimental studies have demonstrated that phytoplankton can display rapid thermal adaptation in response to warmed environments. While these studies provide insight into the evolutionary responses of single species, they tend to employ different experimental techniques. Consequently, our ability to compare the potential for thermal adaptation across different, ecologically relevant, species remains limited. Here, we address this limitation by conducting simultaneous long-term warming experiments with the same experimental design on clonal isolates of three phylogenetically diverse species of marine phytoplankton; the cyanobacterium Synechococcus sp., the prasinophyte Ostreococcus tauri and the diatom Phaeodoactylum tricornutum. Over the same experimental time period, we observed differing levels of thermal adaptation in response to stressful supra-optimal temperatures. Synechococcus sp. displayed the greatest improvement in fitness (i.e., growth rate) and thermal tolerance (i.e., temperature limits of growth). Ostreococcus tauri was able to improve fitness and thermal tolerance, but to a lesser extent. Finally, Phaeodoactylum tricornutum showed no signs of adaptation. These findings could help us understand how the structure of phytoplankton communities may change in response to warming, and possible biogeochemical implications, as some species show relatively more rapid adaptive shifts in their thermal tolerance.

The temperature dependence of microbial community respiration is amplified by changes in species interactions.

Respiratory release of CO2 by microorganisms is one of the main components of the global carbon cycle. However, there are large uncertainties regarding the effects of climate warming on the respiration of microbial communities, owing to a lack of mechanistic, empirically tested theory that incorporates dynamic species interactions. We present a general mathematical model which predicts that thermal sensitivity of microbial community respiration increases as species interactions change from competition to facilitation (for example, commensalism, cooperation and mutualism). This is because facilitation disproportionately increases positive feedback between the thermal sensitivities of species-level metabolic and biomass accumulation rates at warmer temperatures. We experimentally validate our theoretical predictions in a community of eight bacterial taxa and show that a shift from competition to facilitation, after a month of co-adaptation, caused a 60% increase in the thermal sensitivity of respiration relative to de novo assembled communities that had not co-adapted. We propose that rapid changes in species interactions can substantially change the temperature dependence of microbial community respiration, which should be accounted for in future climate-carbon cycle models.

Thermal traits govern the response of microbial community dynamics and ecosystem functioning to warming.

Understanding the ecological processes that underpin the dynamics of community turnover in response to environmental change is critical to predicting how warming will influence ecosystem functioning. Here, we quantify the effect of changing temperature on community composition and ecosystem functioning via the action of ecological selection on population-level thermal traits. To achieve this, we use microbes isolated from a network of geothermal streams in Iceland where in situ temperatures span 8-38°C within a single catchment. We first quantified variability in thermal tolerance between taxa, and then assembled synthetic communities along a broad thermal gradient to explore how temperature-driven selection on thermal tolerance traits shaped the emergent community structures and functions. We found marked changes in community structure and composition with temperature, such that communities exposed to extreme temperatures (10, 35°C) had highly asymmetric biomass distributions and low taxonomic richness. Thermal optima were a good predictor of the presence and relative abundance of taxa in the high-temperature treatments. We also found that the evenness of the abundance distribution was related to ecosystem production, such that communities with more equitable abundance distribution were also the most productive. Our results highlight the utility of using a multi-level approach that links population-level traits with community structure and ecosystem functioning to better understand how ecological communities will respond to global warming.

Warming impairs trophic transfer efficiency in a long-term field experiment.

In ecosystems, the efficiency of energy transfer from resources to consumers determines the biomass structure of food webs. As a general rule, about 10% of the energy produced in one trophic level makes it up to the next1-3. Recent theory suggests that this energy transfer could be further constrained if rising temperatures increase metabolic growth costs4, although experimental confirmation in whole ecosystems is lacking. Here we quantify nitrogen transfer efficiency-a proxy for overall energy transfer-in freshwater plankton in artificial ponds that have been exposed to seven years of experimental warming. We provide direct experimental evidence that, relative to ambient conditions, 4 °C of warming can decrease trophic transfer efficiency by up to 56%. In addition, the biomass of both phytoplankton and zooplankton was lower in the warmed ponds, which indicates major shifts in energy uptake, transformation and transfer5,6. These findings reconcile observed warming-driven changes in individual-level growth costs and in carbon-use efficiency across diverse taxa4,7-10 with increases in the ratio of total respiration to gross primary production at the ecosystem level11-13. Our results imply that an increasing proportion of the carbon fixed by photosynthesis will be lost to the atmosphere as the planet warms, impairing energy flux through food chains, which will have negative implications for larger consumers and for the functioning of entire ecosystems.

Leaf trait variation is similar among genotypes of Eucalyptus camaldulensis from differing climates and arises in plastic responses to the seasons rather than water availability.

We used a widely distributed tree Eucalyptus camaldulensis subsp. camaldulensis to partition intraspecific variation in leaf functional traits to genotypic variation and phenotypic plasticity. We examined if genotypic variation is related to the climate of genotype provenance and whether phenotypic plasticity maintains performance in a changing environment. Ten genotypes from different climates were grown in a common garden under watering treatments reproducing the wettest and driest edges of the subspecies' distribution. We measured functional traits reflecting leaf metabolism and associated with growth (respiration rate, nitrogen and phosphorus concentrations, and leaf mass per area) and performance proxies (aboveground biomass and growth rate) each season over a year. Genotypic variation contributed substantially to the variation in aboveground biomass but much less in growth rate and leaf traits. Phenotypic plasticity was a large source of the variation in leaf traits and performance proxies and was greater among sampling dates than between watering treatments. The variation in leaf traits was weakly correlated to performance proxies, and both were unrelated to the climate of genotype provenance. Intraspecific variation in leaf traits arises similarly among genotypes in response to seasonal environmental variation, instead of long-term water availability or climate of genotype provenance.

Phytoplankton thermal responses adapt in the absence of hard thermodynamic constraints.

To better predict how populations and communities respond to climatic temperature variation, it is necessary to understand how the shape of the response of fitness-related rates to temperature evolves (the thermal performance curve). Currently, there is disagreement about the extent to which the evolution of thermal performance curves is constrained. One school of thought has argued for the prevalence of thermodynamic constraints through enzyme kinetics, whereas another argues that adaptation can-at least partly-overcome such constraints. To shed further light on this debate, we perform a phylogenetic meta-analysis of the thermal performance curves of growth rate of phytoplankton-a globally important functional group-controlling for environmental effects (habitat type and thermal regime). We find that thermodynamic constraints have a minor influence on the shape of the curve. In particular, we detect a very weak increase of maximum performance with the temperature at which the curve peaks, suggesting a weak "hotter-is-better" constraint. Also, instead of a constant thermal sensitivity of growth across species, as might be expected from strong constraints, we find that all aspects of the thermal performance curve evolve along the phylogeny. Our results suggest that phytoplankton thermal performance curves adapt to thermal environments largely in the absence of hard thermodynamic constraints.

Evolutionary temperature compensation of carbon fixation in marine phytoplankton.

The efficiency of carbon sequestration by the biological pump could decline in the coming decades because respiration tends to increase more with temperature than photosynthesis. Despite these differences in the short-term temperature sensitivities of photosynthesis and respiration, it remains unknown whether the long-term impacts of global warming on metabolic rates of phytoplankton can be modulated by evolutionary adaptation. We found that respiration was consistently more temperature dependent than photosynthesis across 18 diverse marine phytoplankton, resulting in universal declines in the rate of carbon fixation with short-term increases in temperature. Long-term experimental evolution under high temperature reversed the short-term stimulation of metabolic rates, resulting in increased rates of carbon fixation. Our findings suggest that thermal adaptation may therefore have an ameliorating impact on the efficiency of phytoplankton as primary mediators of the biological carbon pump.

Abrupt declines in marine phytoplankton production driven by warming and biodiversity loss in a microcosm experiment.

Rising sea surface temperatures are expected to lead to the loss of phytoplankton biodiversity. However, we currently understand very little about the interactions between warming, loss of phytoplankton diversity and its impact on the oceans' primary production. We experimentally manipulated the species richness of marine phytoplankton communities under a range of warming scenarios, and found that ecosystem production declined more abruptly with species loss in communities exposed to higher temperatures. Species contributing positively to ecosystem production in the warmed treatments were those that had the highest optimal temperatures for photosynthesis, implying that the synergistic impacts of warming and biodiversity loss on ecosystem functioning were mediated by thermal trait variability. As species were lost from the communities, the probability of taxa remaining that could tolerate warming diminished, resulting in abrupt declines in ecosystem production. Our results highlight the potential for synergistic effects of warming and biodiversity loss on marine primary production.

Community-level respiration of prokaryotic microbes may rise with global warming.

Understanding how the metabolic rates of prokaryotes respond to temperature is fundamental to our understanding of how ecosystem functioning will be altered by climate change, as these micro-organisms are major contributors to global carbon efflux. Ecological metabolic theory suggests that species living at higher temperatures evolve higher growth rates than those in cooler niches due to thermodynamic constraints. Here, using a global prokaryotic dataset, we find that maximal growth rate at thermal optimum increases with temperature for mesophiles (temperature optima [Formula: see text]C), but not thermophiles ([Formula: see text]C). Furthermore, short-term (within-day) thermal responses of prokaryotic metabolic rates are typically more sensitive to warming than those of eukaryotes. Because climatic warming will mostly impact ecosystems in the mesophilic temperature range, we conclude that as microbial communities adapt to higher temperatures, their metabolic rates and therefore, biomass-specific CO[Formula: see text] production, will inevitably rise. Using a mathematical model, we illustrate the potential global impacts of these findings.

Energetic equivalence underpins the size structure of tree and phytoplankton communities.

The size structure of autotroph communities - the relative abundance of small vs. large individuals - shapes the functioning of ecosystems. Whether common mechanisms underpin the size structure of unicellular and multicellular autotrophs is, however, unknown. Using a global data compilation, we show that individual body masses in tree and phytoplankton communities follow power-law distributions and that the average exponents of these individual size distributions (ISD) differ. Phytoplankton communities are characterized by an average ISD exponent consistent with three-quarter-power scaling of metabolism with body mass and equivalence in energy use among mass classes. Tree communities deviate from this pattern in a manner consistent with equivalence in energy use among diameter size classes. Our findings suggest that whilst universal metabolic constraints ultimately underlie the emergent size structure of autotroph communities, divergent aspects of body size (volumetric vs. linear dimensions) shape the ecological outcome of metabolic scaling in forest vs. pelagic ecosystems.

Modelling ecosystem adaptation and dangerous rates of global warming.

We are in a period of relatively rapid climate change. This poses challenges for individual species and threatens the ecosystem services that humanity relies upon. Temperature is a key stressor. In a warming climate, individual organisms may be able to shift their thermal optima through phenotypic plasticity. However, such plasticity is unlikely to be sufficient over the coming centuries. Resilience to warming will also depend on how fast the distribution of traits that define a species can adapt through other methods, in particular through redistribution of the abundance of variants within the population and through genetic evolution. In this paper, we use a simple theoretical 'trait diffusion' model to explore how the resilience of a given species to climate change depends on the initial trait diversity (biodiversity), the trait diffusion rate (mutation rate), and the lifetime of the organism. We estimate theoretical dangerous rates of continuous global warming that would exceed the ability of a species to adapt through trait diffusion, and therefore lead to a collapse in the overall productivity of the species. As the rate of adaptation through intraspecies competition and genetic evolution decreases with species lifetime, we find critical rates of change that also depend fundamentally on lifetime. Dangerous rates of warming vary from 1°C per lifetime (at low trait diffusion rate) to 8°C per lifetime (at high trait diffusion rate). We conclude that rapid climate change is liable to favour short-lived organisms (e.g. microbes) rather than longer-lived organisms (e.g. trees).

Biodiversity-function relationships in methanogenic communities.

Methanogenic communities play a crucial role in carbon cycling and biotechnology (anaerobic digestion), but our understanding of how their diversity, or composition in general, determines the rate of methane production is very limited. Studies to date have been correlational because of the difficulty in cultivating their constituent species in pure culture. Here, we investigate the causal link between methanogenesis and diversity in laboratory anaerobic digesters by experimentally manipulating the diversity of cultures by dilution and subsequent equilibration of biomass. This process necessarily leads to the loss of the rarer species from communities. We find a positive relationship between methane production and the number of taxa, with little evidence of functional saturation, suggesting that rare species play an important role in methane-producing communities. No correlations were found between the initial composition and methane production across natural communities, but a positive relationship between species richness and methane production emerged following ecological selection imposed by the laboratory conditions. Our data suggest methanogenic communities show little functional redundancy, and hence, any loss of diversity-both natural and resulting from changes in propagation conditions during anaerobic digestion-is likely to reduce methane production.

Changes in temperature alter the relationship between biodiversity and ecosystem functioning.

Global warming and the loss of biodiversity through human activities (e.g., land-use change, pollution, invasive species) are two of the most profound threats to the functional integrity of the Earth's ecosystems. These factors are, however, most frequently investigated separately, ignoring the potential for synergistic effects of biodiversity loss and environmental warming on ecosystem functioning. Here we use high-throughput experiments with microbial communities to investigate how changes in temperature affect the relationship between biodiversity and ecosystem functioning. We found that changes in temperature systematically altered the relationship between biodiversity and ecosystem functioning. As temperatures departed from ambient conditions the exponent of the diversity-functioning relationship increased, meaning that more species were required to maintain ecosystem functioning under thermal stress. This key result was driven by two processes linked to variability in the thermal tolerance curves of taxa. First, more diverse communities had a greater chance of including species with thermal traits that enabled them to maintain productivity as temperatures shifted from ambient conditions. Second, we found a pronounced increase in the contribution of complementarity to the net biodiversity effect at high and low temperatures, indicating that changes in species interactions played a critical role in mediating the impacts of temperature change on the relationship between biodiversity and ecosystem functioning. Our results highlight that if biodiversity loss occurs independently of species' thermal tolerance traits, then the additional impacts of environmental warming will result in sharp declines in ecosystem function.

Role of carbon allocation efficiency in the temperature dependence of autotroph growth rates.

Relating the temperature dependence of photosynthetic biomass production to underlying metabolic rates in autotrophs is crucial for predicting the effects of climatic temperature fluctuations on the carbon balance of ecosystems. We present a mathematical model that links thermal performance curves (TPCs) of photosynthesis, respiration, and carbon allocation efficiency to the exponential growth rate of a population of photosynthetic autotroph cells. Using experiments with the green alga, Chlorella vulgaris, we apply the model to show that the temperature dependence of carbon allocation efficiency is key to understanding responses of growth rates to warming at both ecological and longer-term evolutionary timescales. Finally, we assemble a dataset of multiple terrestrial and aquatic autotroph species to show that the effects of temperature-dependent carbon allocation efficiency on potential growth rate TPCs are expected to be consistent across taxa. In particular, both the thermal sensitivity and the optimal temperature of growth rates are expected to change significantly due to temperature dependence of carbon allocation efficiency alone. Our study provides a foundation for understanding how the temperature dependence of carbon allocation determines how population growth rates respond to temperature.

Linking phytoplankton community metabolism to the individual size distribution.

Quantifying variation in ecosystem metabolism is critical to predicting the impacts of environmental change on the carbon cycle. We used a metabolic scaling framework to investigate how body size and temperature influence phytoplankton community metabolism. We tested this framework using phytoplankton sampled from an outdoor mesocosm experiment, where communities had been either experimentally warmed (+ 4 °C) for 10 years or left at ambient temperature. Warmed and ambient phytoplankton communities differed substantially in their taxonomic composition and size structure. Despite this, the response of primary production and community respiration to long- and short-term warming could be estimated using a model that accounted for the size- and temperature dependence of individual metabolism, and the community abundance-body size distribution. This work demonstrates that the key metabolic fluxes that determine the carbon balance of planktonic ecosystems can be approximated using metabolic scaling theory, with knowledge of the individual size distribution and environmental temperature.

Metabolic traits predict the effects of warming on phytoplankton competition.

Understanding how changes in temperature affect interspecific competition is critical for predicting changes in ecological communities with global warming. Here, we develop a theoretical model that links interspecific differences in the temperature dependence of resource acquisition and growth to the outcome of pairwise competition in phytoplankton. We parameterised our model with these metabolic traits derived from six species of freshwater phytoplankton and tested its ability to predict the outcome of competition in all pairwise combinations of the species in a factorial experiment, manipulating temperature and nutrient availability. The model correctly predicted the outcome of competition in 72% of the pairwise experiments, with competitive advantage determined by difference in thermal sensitivity of growth rates of the two species. These results demonstrate that metabolic traits play a key role in determining how changes in temperature influence interspecific competition and lay the foundation for mechanistically predicting the effects of warming in complex, multi-species communities.

Temperature-driven selection on metabolic traits increases the strength of an algal-grazer interaction in naturally warmed streams.

Trophic interactions are important determinants of the structure and functioning of ecosystems. Because the metabolism and consumption rates of ectotherms increase sharply with temperature, there are major concerns that global warming will increase the strength of trophic interactions, destabilizing food webs, and altering ecosystem structure and function. We used geothermally warmed streams that span an 11°C temperature gradient to investigate the interplay between temperature-driven selection on traits related to metabolism and resource acquisition, and the interaction strength between the keystone gastropod grazer, Radix balthica, and a common algal resource. Populations from a warm stream (~28°C) had higher maximal metabolic rates and optimal temperatures than their counterparts from a cold stream (~17°C). We found that metabolic rates of the population originating from the warmer stream were higher across all measurement temperatures. A reciprocal transplant experiment demonstrated that the interaction strengths between the grazer and its algal resource were highest for both populations when transplanted into the warm stream. In line with the thermal dependence of respiration, interaction strengths involving grazers from the warm stream were always higher than those with grazers from the cold stream. These results imply that increases in metabolism and resource consumption mediated by the direct, thermodynamic effects of higher temperatures on physiological rates are not mitigated by metabolic compensation in the long term, and suggest that warming could increase the strength of algal-grazer interactions with likely knock-on effects for the biodiversity and productivity of aquatic ecosystems.

The Temperature Dependence of Phytoplankton Stoichiometry: Investigating the Roles of Species Sorting and Local Adaptation.

The elemental composition of phytoplankton (C:N:P stoichiometry) is a critical factor regulating nutrient cycling, primary production and energy transfer through planktonic food webs. Our understanding of the multiple direct and indirect mechanisms through which temperature controls phytoplankton stoichiometry is however incomplete, increasing uncertainty in the impacts of global warming on the biogeochemical functioning of aquatic ecosystems. Here, we use a decade-long warming experiment in outdoor freshwater ponds to investigate how temperature-driven turnover in species composition and shifts in stoichiometric traits within species through local thermal adaptation contribute to the effects of warming on seston stoichiometry. We found that experimental warming increased seston C:P and N:P ratios, while the C:N ratio was unaffected by warming. Temperature was also the dominant driver of seasonal variation in seston stoichiometry, correlating positively with both C:P and N:P ratios. The taxonomic composition of the phytoplankton community differed substantially between the warmed and ambient treatments indicating that warming resulted in differential sorting of species from the regional pool. Furthermore, taxonomic composition also changed markedly over the year within each of the warmed and ambient treatments, highlighting substantial temporal turnover in species. To investigate whether local adaptation also played an important role in shaping the effects of warming on seston stoichiometry, we isolated multiple strains of the cosmopolitan alga, Chlamydomonas reinhardtii from across the warmed and ambient mesocosms. We found that warmed isolates had higher C:P and N:P ratios, shifts that were comparable in direction and magnitude to the effects of warming on seston stoichiometry. Our results suggest that both species sorting and local adaptation are likely to play important roles in shaping the effects of warming on bulk phytoplankton stoichiometry and indicate that major shifts in aquatic biogeochemistry should be expected in a warmer world.

Metabolic compensation constrains the temperature dependence of gross primary production.

Gross primary production (GPP) is the largest flux in the carbon cycle, yet its response to global warming is highly uncertain. The temperature dependence of GPP is directly linked to photosynthetic physiology, but the response of GPP to warming over longer timescales could also be shaped by ecological and evolutionary processes that drive variation in community structure and functional trait distributions. Here, we show that selection on photosynthetic traits within and across taxa dampens the effects of temperature on GPP across a catchment of geothermally heated streams. Autotrophs from cold streams had higher photosynthetic rates and after accounting for differences in biomass among sites, biomass-specific GPP was independent of temperature in spite of a 20 °C thermal gradient. Our results suggest that temperature compensation of photosynthetic rates constrains the long-term temperature dependence of GPP, and highlights the importance of considering physiological, ecological and evolutionary mechanisms when predicting how ecosystem-level processes respond to warming.

Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis.

Phytoplankton photosynthesis is a critical flux in the carbon cycle, accounting for approximately 40% of the carbon dioxide fixed globally on an annual basis and fuelling the productivity of aquatic food webs. However, rapid evolutionary responses of phytoplankton to warming remain largely unexplored, particularly outside the laboratory, where multiple selection pressures can modify adaptation to environmental change. Here, we use a decade-long experiment in outdoor mesocosms to investigate mechanisms of adaptation to warming (+4 °C above ambient temperature) in the green alga Chlamydomonas reinhardtii, in naturally assembled communities. Isolates from warmed mesocosms had higher optimal growth temperatures than their counterparts from ambient treatments. Consequently, warm-adapted isolates were stronger competitors at elevated temperature and experienced a decline in competitive fitness in ambient conditions, indicating adaptation to local thermal regimes. Higher competitive fitness in the warmed isolates was linked to greater photosynthetic capacity and reduced susceptibility to photoinhibition. These findings suggest that adaptive responses to warming in phytoplankton could help to mitigate projected declines in aquatic net primary production by increasing rates of cellular net photosynthesis.