ABSTRACTGross primary production (GPP) is the largest flux in the carbon cycle, yet its response to global warming is highly uncertain. The temperature sensitivity 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 community structure and functional trait distributions. Here, we show that selection on photosynthetic traits within and across taxa dampen 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, rates of ecosystem-level GPP were independent of temperature, despite a 20 ºC thermal gradient. Our results suggest that thermal adaptation 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.

AbstractMarine phytoplankton are responsible for over 45% of annual global net primary production. Ocean warming is expected to drive massive reorganisation of phytoplankton communities, resulting in pole-ward range shifts and sharp declines in species diversity, particularly in the tropics. The impacts of warming on phytoplankton species depend critically on their physiological sensitivity to temperature change, characterised by thermal tolerance curves. Local extinctions arise when temperatures exceed species’ thermal tolerance limits. The mechanisms that determine the characteristics of thermal tolerance curves (e.g. optimal and maximal temperatures) and their variability among the broad physiological diversity of marine phytoplankton are however poorly understood. Here we show that differences in the temperature responses of photosynthesis and respiration establish physiological trade-offs that constrain the thermal tolerance of 18 species of marine phytoplankton, spanning cyanobacteria as well as the red and green super-families. Across all species we found that rates of respiration were more sensitive to increasing temperature and typically had higher optimal temperatures than photosynthesis. Consequently, the fraction of photosynthetic energy available for allocation to growth (carbon-use efficiency) declined exponentially with rising temperatures with a sensitivity that was invariant among the 18 species. Furthermore, the optimal temperature of growth was generally lower than that of photosynthesis and as a result, supra-optimal declines in growth rate were associated with temperature ranges where the carbon-use efficiency exhibited accelerated declines. These highly conserved patterns demonstrate that the limits of thermal tolerance in marine phytoplankton are underpinned by common metabolic constraints linked to the differential temperature responses of photosynthesis and respiration.Significance StatementThe impacts of warming on marine phytoplankton depend on their sensitivity to rising temperatures, yet there is currently limited understanding of the mechanisms that limit thermal tolerance among the diversity of marine phytoplankton. Using a comparative study on the dominant, ecologically important lineages of marine phytoplankton – Bacillariophyceae, Dinophyceae, Cyanophyceae, Prasinophyceae, Prymnesiophyceae – we show that rates of respiration are consistently more sensitive to increasing temperature than photosynthesis. Consequently, the fraction of photosynthetic energy available for growth declines with rising temperatures with a sensitivity that is invariant among species. Our results suggest that declines in phytoplankton performance at high temperatures are driven by universal metabolic constrains linked to rising respiratory costs eventually exceeding the supply of reduced carbon from photosynthesis.

Global warming is associated with an increase in sea surface temperature and its variability. The consequences of evolving in variable, fluctuating environments are explored by a large body of theory: when populations evolve in fluctuating environments the frequency of fluctuations determines the shapes of tolerance curves (indicative of habitats that organisms can inhabit) and trait reaction norms (the phenotypes that organisms display across these environments). Despite this well-established theoretical backbone, predicting how trait and tolerance curves will evolve in organisms at the foundation of marine ecosystems remains a challenge. Here, we used a globally distributed phytoplankton, Thalassiosira pseudonana, and show that fluctuations in temperature on scales of 3-4 generations rapidly selected for populations with enhanced trait plasticity and elevated thermal tolerance. Fluctuations spanning 30-40 generations selected for the formation of two stable, genetically and physiologically distinct populations, one evolving high trait plasticity and enhanced thermal tolerance, and the other, akin to samples evolved under constant warming, with lower trait plasticity and a smaller increase in thermal tolerance.

Net emissions of the potent GHG methane from ecosystems represent the balance between microbial methane production (methanogenesis) and oxidation (methanotrophy), each with different sensitivities to temperature. How this balance will be altered by long-term global warming, especially in freshwaters that are major methane sources, remains unknown. Here we show that the experimental warming of artificial ponds over 11 years drives a disproportionate increase in methanogenesis over methanotrophy that increases the warming potential of the gases they emit. The increased methane emissions far exceed temperature-based predictions, driven by shifts in the methanogen community under warming, while the methanotroph community was conserved. Our experimentally induced increase in methane emissions from artificial ponds is, in part, reflected globally as a disproportionate increase in the capacity of naturally warmer ecosystems to emit more methane. Our findings indicate that as Earth warms, natural ecosystems will emit disproportionately more methane in a positive feedback warming loop.

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.

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.

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.

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.

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).

Models of marine biogeochemistry capture the effects of temperature on phytoplankton growth via the monotonic, exponential Eppley coefficient, without considering the physiological or evolutionary processes that underpin this emergent, across-species temperature response. Here, we investigated both the within- and across-species temperature dependence of growth rate for 18 species of marine phytoplankton. We found that the temperature dependence of growth rate derived across species was lower than the average temperature response within species. This finding supports a “partial compensation” model of thermal adaptation and suggests that adaptation can partially compensate for the underlying thermodynamic effects of temperature on physiological rates observed within species. We also found that thermal tolerance traits (e.g. the optimum temperature for growth) systematically covaried with a host of key functional traits (e.g. cell size, elemental composition). Consequently, turnover in species composition in a warmer ocean, linked to interspecific variability in thermal tolerance traits, could be associated with major shifts in the functional trait composition of marine phytoplankton communities with far reaching implications for ecosystem functioning.

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.

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.

© 2018 John Wiley. &. Sons Ltd/CNRS. 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.

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.

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.

AbstractChloroplasts communicate information by signalling to nuclei during acclimation to fluctuating light. Several potential operating signals originating from chloroplasts have been proposed, but none have been shown to move to nuclei to modulate gene expression. One proposed signal is hydrogen peroxide (H2O2) produced by chloroplasts in a light-dependent manner. Using HyPer2, a genetically encoded fluorescent H2O2 sensor, we show that in photosynthetic Nicotiana benthamiana epidermal cells, exposure to high light increases H2O2 production in chloroplast stroma, cytosol and nuclei. Critically, over-expression of stromal ascorbate peroxidase (H2O2 scavenger) or treatment with DCMU (photosynthesis inhibitor) attenuates nuclear H2O2 accumulation and high light-responsive gene expression. Cytosolic ascorbate peroxidase over-expression has little effect on nuclear H2O2 accumulation and high light-responsive gene expression. This is because the H2O2 derives from a sub-population of chloroplasts closely associated with nuclei. Therefore, direct H2O2 transfer from chloroplasts to nuclei, avoiding the cytosol, enables photosynthetic control over gene expression.

In low-order forested streams, catchment-scale land-use modifications to vegetation can affect energy inputs into streams and trophic interactions within these donor-controlled food webs. We examined the effects of Pinus radiata plantations on the intercept and slope of the size spectrum (the relationship between log-mass and log-density) of macroinvertebrate communities in low-order forested streams. We compared three streams draining pine plantations with three draining native deciduous forests, all without significant differences in water physicochemical characteristics. While size spectrum intercept was similar between the two stream types, the slope of the size spectrum was shallower in pine than in deciduous streams based on a decline in the density of the smaller individuals. The shredder feeding guild showed the largest changes, with a significant reduction in their total density and, specifically, in the density of the smaller individuals from the deciduous to the pine streams. This alteration is explained by the change in very specialist shredders, such as plecopterans and trichopterans, but not in those with highly mobile crustaceans or more generalist dipterans. The effect detected for shredders might have scaled up to higher trophic levels as the density of invertebrate predators (small and big) was lower in streams under pine, suggesting a response to prey limitation. These results indicate that the change of in-stream resource quality arising from the replacement of deciduous vegetation by pine plantations can trigger size-specific responses of macroinvertebrates and target specialised feeding guilds such as shedders, and can elicit a bottom-up reaction in the organisation of food webs.

Understanding the mechanisms that determine how phytoplankton adapt to warming will substantially improve the realism of models describing ecological and biogeochemical effects of climate change. Here, we quantify the evolution of elevated thermal tolerance in the phytoplankton, Chlorella vulgaris. Initially, population growth was limited at higher temperatures because respiration was more sensitive to temperature than photosynthesis meaning less carbon was available for growth. Tolerance to high temperature evolved after ≈ 100 generations via greater down-regulation of respiration relative to photosynthesis. By down-regulating respiration, phytoplankton overcame the metabolic constraint imposed by the greater temperature sensitivity of respiration and more efficiently allocated fixed carbon to growth. Rapid evolution of carbon-use efficiency provides a potentially general mechanism for thermal adaptation in phytoplankton and implies that evolutionary responses in phytoplankton will modify biogeochemical cycles and hence food web structure and function under warming. Models of climate futures that ignore adaptation would usefully be revisited. Copyright

Understanding the mechanisms that determine how phytoplankton adapt to warming will substantially improve the realism of models describing ecological and biogeochemical effects of climate change. Here, we quantify the evolution of elevated thermal tolerance in the phytoplankton, Chlorella vulgaris. Initially, population growth was limited at higher temperatures because respiration was more sensitive to temperature than photosynthesis meaning less carbon was available for growth. Tolerance to high temperature evolved after ≈ 100 generations via greater down-regulation of respiration relative to photosynthesis. By down-regulating respiration, phytoplankton overcame the metabolic constraint imposed by the greater temperature sensitivity of respiration and more efficiently allocated fixed carbon to growth. Rapid evolution of carbon-use efficiency provides a potentially general mechanism for thermal adaptation in phytoplankton and implies that evolutionary responses in phytoplankton will modify biogeochemical cycles and hence food web structure and function under warming. Models of climate futures that ignore adaptation would usefully be revisited.

Phytoplankton are key components of aquatic ecosystems, fixing CO2 from the atmosphere through photosynthesis and supporting secondary production, yet relatively little is known about how future global warming might alter their biodiversity and associated ecosystem functioning. Here, we explore how the structure, function, and biodiversity of a planktonic metacommunity was altered after five years of experimental warming. Our outdoor mesocosm experiment was open to natural dispersal from the regional species pool, allowing us to explore the effects of experimental warming in the context of metacommunity dynamics. Warming of 4°C led to a 67% increase in the species richness of the phytoplankton, more evenly-distributed abundance, and higher rates of gross primary productivity. Warming elevated productivity indirectly, by increasing the biodiversity and biomass of the local phytoplankton communities. Warming also systematically shifted the taxonomic and functional trait composition of the phytoplankton, favoring large, colonial, inedible phytoplankton taxa, suggesting stronger top-down control, mediated by zooplankton grazing played an important role. Overall, our findings suggest that temperature can modulate species coexistence, and through such mechanisms, global warming could, in some cases, increase the species richness and productivity of phytoplankton communities.

In low-order forested streams, catchment-scale land-use modifications to vegetation can affect energy inputs into streams and trophic interactions within these donor-controlled food webs. We examined the effects of Pinus radiata plantations on the intercept and slope of the size spectrum (the relationship between log-mass and log-density) of macroinvertebrate communities in low-order forested streams. We compared three streams draining pine plantations with three draining native deciduous forests, all without significant differences in water physicochemical characteristics. While size spectrum intercept was similar between the two stream types, the slope of the size spectrum was shallower in pine than in deciduous streams based on a decline in the density of the smaller individuals. The shredder feeding guild showed the largest changes, with a significant reduction in their total density and, specifically, in the density of the smaller individuals from the deciduous to the pine streams. This alteration is explained by the change in very specialist shredders, such as plecopterans and trichopterans, but not in those with highly mobile crustaceans or more generalist dipterans. The effect detected for shredders might have scaled up to higher trophic levels as the density of invertebrate predators (small and big) was lower in streams under pine, suggesting a response to prey limitation. These results indicate that the change of in-stream resource quality arising from the replacement of deciduous vegetation by pine plantations can trigger size-specific responses of macroinvertebrates and target specialised feeding guilds such as shedders, and can elicit a bottom-up reaction in the organisation of food webs.

Aim: the average carbon-to-nitrogen-to-phosphorus ratio (C:N:P) of marine algae is known to be tightly coupled to that of the inorganic pools of C, N and P in the ocean interior (i.e. the Redfield ratio), and therefore plays a key role in regulating the C and N cycles in the ocean. The C:N:P ratio of algae also varies substantially, both within and among taxa, in response to variation in the abiotic environment, raising the possibility that biogeochemical controls on the marine C and N cycles may shift as a result of climate change. However, the role of temperature in driving phenotypic variation in stoichiometry within algal taxa, as well as biogeographic variation in particulate C, N and P among oceanic regions, remains largely unresolved. Location: Global. Methods: to assess the extent to which temperature controls algal stoichiometry we performed two complementary meta-analyses. First, we characterized the global temperature dependence of algal stoichiometry by analysing field data that encompassed 767 estimates of C:N:P from 22 oceanic sites spanning over 130° of latitude. Second, we characterized the within-species acclimation responses of C:N:P stoichiometry to temperature by analysing data that encompassed 17 experiments, 9 species and 4 taxonomic classes. Results: the geographic analyses demonstrated that the N:P and C:P ratios of marine algae were best predicted by latitudinal variation in average sea-surface temperature, and that both ratios increased 2.6-fold from 0 to 30°C. These global-scale temperature responses, which largely reflect geographic variation in the species compositions of algal assemblages, were of similar magnitude to the average within-species response of the N:P and C:P ratios to experimental temperature manipulations. Main conclusions: the congruence between field and experimental observations suggests that temperature-dependent physiological mechanisms operating at the subcellular level play an important role in determining the stoichiometry of algae in the world's oceans.

Aim: the average carbon-to-nitrogen-to-phosphorus ratio (C:N:P) of marine algae is known to be tightly coupled to that of the inorganic pools of C, N and P in the ocean interior (i.e. the Redfield ratio), and therefore plays a key role in regulating the C and N cycles in the ocean. The C:N:P ratio of algae also varies substantially, both within and among taxa, in response to variation in the abiotic environment, raising the possibility that biogeochemical controls on the marine C and N cycles may shift as a result of climate change. However, the role of temperature in driving phenotypic variation in stoichiometry within algal taxa, as well as biogeographic variation in particulate C, N and P among oceanic regions, remains largely unresolved. Location: Global. Methods: to assess the extent to which temperature controls algal stoichiometry we performed two complementary meta-analyses. First, we characterized the global temperature dependence of algal stoichiometry by analysing field data that encompassed 767 estimates of C:N:P from 22 oceanic sites spanning over 130° of latitude. Second, we characterized the within-species acclimation responses of C:N:P stoichiometry to temperature by analysing data that encompassed 17 experiments, 9 species and 4 taxonomic classes. Results: the geographic analyses demonstrated that the N:P and C:P ratios of marine algae were best predicted by latitudinal variation in average sea-surface temperature, and that both ratios increased 2.6-fold from 0 to 30°C. These global-scale temperature responses, which largely reflect geographic variation in the species compositions of algal assemblages, were of similar magnitude to the average within-species response of the N:P and C:P ratios to experimental temperature manipulations. Main conclusions: the congruence between field and experimental observations suggests that temperature-dependent physiological mechanisms operating at the subcellular level play an important role in determining the stoichiometry of algae in the world's oceans.

Temperature is a key driver of ecological processes and patterns. The ramifications of temperature for ecological communities include not only its direct effects on the physiology of individuals, but also how these effects play out in the context of other processes such as competition. Apparently idiosyncratic or difficult to predict effects of temperature on competitive outcomes are well represented in the literature. General theoretical understanding of how physiological influences of temperature filter through community dynamics to determine outcomes is limited. We present a theoretical framework for predicting the effects of temperature on competition among species, based on understanding the effects of temperature on the physiological and population parameters of the species. The approach helps unify formal resource competition theory with metabolic and physiological ecology. Phytoplankton and many other ectotherms are smaller at higher temperatures. This has been observed experimentally, across geographical gradients, and as change accompanying climate warming, but it has not been explained in terms of competition. As a case study, we apply our theoretical framework to competition for nutrients among differently sized phytoplankton. Based on this analysis, we hypothesize that the prevalence of smaller phytoplankton at higher temperatures is at least partly due to an accentuated competitive advantage of smaller cells at higher temperatures with respect to nutrient uptake and growth. We examine the scope for extending the approach to understand resource competition, generally, among ectotherms of different sizes. © 2013 British Ecological Society.

Methane (CH4) is an important greenhouse gas because it has 25 times the global warming potential of carbon dioxide (CO2) by mass over a century. Recent calculations suggest that atmospheric CH4 emissions have been responsible for approximately 20% of Earth's warming since pre-industrial times. Understanding how CH4 emissions from ecosystems will respond to expected increases in global temperature is therefore fundamental to predicting whether the carbon cycle will mitigate or accelerate climate change. Methanogenesis is the terminal step in the remineralization of organic matter and is carried out by strictly anaerobic Archaea. Like most other forms of metabolism, methanogenesis is temperature-dependent. However, it is not yet known how this physiological response combines with other biotic processes (for example, methanotrophy, substrate supply, microbial community composition) and abiotic processes (for example, water-table depth) to determine the temperature dependence of ecosystem-level CH4 emissions. It is also not known whether CH4 emissions at the ecosystem level have a fundamentally different temperature dependence than other key fluxes in the carbon cycle, such as photosynthesis and respiration. Here we use meta-analyses to show that seasonal variations in CH4 emissions from a wide range of ecosystems exhibit an average temperature dependence similar to that of CH4 production derived from pure cultures of methanogens and anaerobic microbial communities. This average temperature dependence (0.96 electron volts (eV)), which corresponds to a 57-fold increase between 0 and 30°C, is considerably higher than previously observed for respiration (approximately 0.65 eV) and photosynthesis (approximately 0.3 eV). As a result, we show that both the emission of CH4 and the ratio of CH4 to CO2 emissions increase markedly with seasonal increases in temperature. Our findings suggest that global warming may have a large impact on the relative contributions of CO2 and CH4 to total greenhouse gas emissions from aquatic ecosystems, terrestrial wetlands and rice paddies.

Ecosystem respiration is a primary component of the carbon cycle and understanding the mechanisms that determine its temperature dependence will be important for predicting how rates of carbon efflux might respond to global warming. We used a rare model system, comprising a network of geothermally heated streams ranging in temperature from 5 °C to 25 °C, to explore the nature of the relationship between respiration and temperature. Using this 'natural experiment', we tested whether the natal thermal regime of stream communities influenced the temperature dependence of respiration in the absence of other potentially confounding variables. An empirical survey of 13 streams across the thermal gradient revealed that the temperature dependence of whole-stream respiration was equivalent to the average activation energy of the respiratory complex (0.6-0.7 eV). This observation was also consistent for in-situ benthic respiration. Laboratory experiments, incubating biofilms from four streams across the thermal gradient at a range of temperatures, revealed that the activation energy and Q 10 of respiration were remarkably consistent across streams, despite marked differences in their thermal history and significant turnover in species composition. Furthermore, absolute rates of respiration at standardised temperature were also unrelated to ambient stream temperature, but strongly reflected differences in biofilm biomass. Together, our results suggest that the core biochemistry, which drives the kinetics of oxidative respiratory metabolism, may be well conserved among diverse taxa and environments, and that the intrinsic sensitivity of respiration to temperature is not influenced by ambient environmental temperature. © 2011 Blackwell Publishing Ltd.

Understanding how biogeochemical cycles relate to the structure of ecological communities is a central research question in ecology. Here we approach this problem by focusing on body size, which is an easily measured species trait that has a pervasive influence on multiple aspects of community structure and ecosystem functioning. We test the predictions of a model derived from metabolic theory using data on ecosystem metabolism and community size structure. These data were collected as part of an aquatic mesocosm experiment that was designed to simulate future environmental warming. Our analyses demonstrate significant linkages between community size structure and ecosystem functioning, and the effects of warming on these links. Specifically, we show that carbon fluxes were significantly influenced by seasonal variation in temperature, and yielded activation energies remarkably similar to those predicted based on the temperature dependencies of individual-level photosynthesis and respiration. We also show that community size structure significantly influenced fluxes of ecosystem respiration and gross primary production, particularly at the annual time-scale. Assessing size structure and the factors that control it, both empirically and theoretically, therefore promises to aid in understanding links between individual organisms and biogeochemical cycles, and in predicting the responses of key ecosystem functions to future environmental change.

Ecosystem respiration is the biotic conversion of organic carbon to carbon dioxide by all of the organisms in an ecosystem, including both consumers and primary producers. Respiration exhibits an exponential temperature dependence at the subcellular and individual levels, but at the ecosystem level respiration can be modified by many variables including community abundance and biomass, which vary substantially among ecosystems. Despite its importance for predicting the responses of the biosphere to climate change, it is as yet unknown whether the temperature dependence of ecosystem respiration varies systematically between aquatic and terrestrial environments. Here we use the largest database of respiratory measurements yet compiled to show that the sensitivity of ecosystem respiration to seasonal changes in temperature is remarkably similar for diverse environments encompassing lakes, rivers, estuaries, the open ocean and forested and non-forested terrestrial ecosystems, with an average activation energy similar to that of the respiratory complex (approximately 0.65 electronvolts (eV)). By contrast, annual ecosystem respiration shows a substantially greater temperature dependence across aquatic (approximately 0.65 eV) versus terrestrial ecosystems (approximately 0.32 eV) that span broad geographic gradients in temperature. Using a model derived from metabolic theory, these findings can be reconciled by similarities in the biochemical kinetics of metabolism at the subcellular level, and fundamental differences in the importance of other variables besides temperature-such as primary productivity and allochthonous carbon inputs-on the structure of aquatic and terrestrial biota at the community level. © 2012 Macmillan Publishers Limited. All rights reserved.

Ecosystem respiration is the biotic conversion of organic carbon to carbon dioxide by all of the organisms in an ecosystem, including both consumers and primary producers. Respiration exhibits an exponential temperature dependence at the subcellular and individual levels, but at the ecosystem level respiration can be modified by many variables including community abundance and biomass, which vary substantially among ecosystems. Despite its importance for predicting the responses of the biosphere to climate change, it is as yet unknown whether the temperature dependence of ecosystem respiration varies systematically between aquatic and terrestrial environments. Here we use the largest database of respiratory measurements yet compiled to show that the sensitivity of ecosystem respiration to seasonal changes in temperature is remarkably similar for diverse environments encompassing lakes, rivers, estuaries, the open ocean and forested and non-forested terrestrial ecosystems, with an average activation energy similar to that of the respiratory complex (approximately 0.65 electronvolts (eV)). By contrast, annual ecosystem respiration shows a substantially greater temperature dependence across aquatic (approximately 0.65 eV) versus terrestrial ecosystems (approximately 0.32 eV) that span broad geographic gradients in temperature. Using a model derived from metabolic theory, these findings can be reconciled by similarities in the biochemical kinetics of metabolism at the subcellular level, and fundamental differences in the importance of other variables besides temperature—such as primary productivity and allochthonous carbon inputs—on the structure of aquatic and terrestrial biota at the community level.

The significance of freshwaters as key players in the global budget of both carbon dioxide and methane has recently been highlighted. In particular, rivers clearly do not act simply as inert conduits merely piping carbon from catchment to coast, but, on the whole, their metabolic activity transforms a considerable fraction of the carbon that they convey. In addition, nitrogen is cycled, sometimes in tight unison with carbon, with appreciable amounts being 'denitrified' between catchment and coast. However, shortfalls in our knowledge about the significance of exchange and interaction between rivers and their catchments, particularly the significance of interactions mediated through hyporheic sediments, are still apparent. From humble beginnings of quantifying the consumption of oxygen by small samples of gravel, to an integrated measurement of reach scale transformations of carbon and nitrogen, our understanding of the cycling of these two macro elements in rivers has improved markedly in the past few decades. However, recent discoveries of novel metabolic pathways in both the nitrogen and carbon cycle across a spectrum of aquatic ecosystems, highlights the need for new directions and a truly multidisciplinary approach to quantifying the flux of carbon and nitrogen through rivers. © 2011.

The significance of freshwaters as key players in the global budget of both carbon dioxide and methane has recently been highlighted. In particular, rivers clearly do not act simply as inert conduits merely piping carbon from catchment to coast, but, on the whole, their metabolic activity transforms a considerable fraction of the carbon that they convey. In addition, nitrogen is cycled, sometimes in tight unison with carbon, with appreciable amounts being 'denitrified' between catchment and coast. However, shortfalls in our knowledge about the significance of exchange and interaction between rivers and their catchments, particularly the significance of interactions mediated through hyporheic sediments, are still apparent. From humble beginnings of quantifying the consumption of oxygen by small samples of gravel, to an integrated measurement of reach scale transformations of carbon and nitrogen, our understanding of the cycling of these two macro elements in rivers has improved markedly in the past few decades. However, recent discoveries of novel metabolic pathways in both the nitrogen and carbon cycle across a spectrum of aquatic ecosystems, highlights the need for new directions and a truly multidisciplinary approach to quantifying the flux of carbon and nitrogen through rivers.

Global warming can affect all levels of biological complexity, though we currently understand least about its potential impact on communities and ecosystems. At the ecosystem level, warming has the capacity to alter the structure of communities and the rates of key ecosystem processes they mediate. Here we assessed the effects of a 4°C rise in temperature on the size structure and taxonomic composition of benthic communities in aquatic mesocosms, and the rates of detrital decomposition they mediated. Warming had no effect on biodiversity, but altered community size structure in two ways. In spring, warmer systems exhibited steeper size spectra driven by declines in total community biomass and the proportion of large organisms. By contrast, in autumn, warmer systems had shallower size spectra driven by elevated total community biomass and a greater proportion of large organisms. Community-level shifts were mirrored by changes in decomposition rates. Temperature-corrected microbial and macrofaunal decomposition rates reflected the shifts in community structure and were strongly correlated with biomass across mesocosms. Our study demonstrates that the 4°C rise in temperature expected by the end of the century has the potential to alter the structure and functioning of aquatic ecosystems profoundly, as well as the intimate linkages between these levels of ecological organization.

Understanding how ecological communities are structured and how this may vary between different types of ecosystems is a fundamental question in ecology. We develop a general framework for quantifying size-structure within and among different ecosystem types (e.g. terrestrial, freshwater or marine), via the use of a suite of bivariate relationships between organismal size and properties of individuals, populations, assemblages, pair-wise interactions, and network topology. Each of these relationships can be considered a dimension of size-structure, along which real communities lie on a continuous scale. For example, the strength, slope, or elevation of the body mass-versus-abundance or predator size-versus-prey size relationships may vary systematically among ecosystem types. We draw on examples from the literature and suggest new ways to use allometries for comparing among ecosystem types, which we illustrate by applying them to published data. Finally, we discuss how dimensions of size-structure are interconnected and how we could approach this complex hierarchy systematically. We conclude: (1) there are multiple dimensions of size-structure; (2) communities may be size-structured in some of these dimensions, but not necessarily in others; (3) across-system comparisons via rigorous quantitative statistical methods are possible, and (4) insufficient data are currently available to illuminate thoroughly the full extent and nature of differences in size-structure among ecosystem types. © 2011 the Authors.

Organism size is one of the key determinants of community structure, and its relationship with abundance can describe how biomass is partitioned among the biota within an ecosystem. An outdoor freshwater mesocosm experiment was used to determine how warming of~4°C would affect the size, biomass and taxonomic structure of planktonic communities. Warming increased the steepness of the community size spectrum by increasing the prevalence of small organisms, primarily within the phytoplankton assemblage and it also reduced the mean and maximum size of phytoplankton by approximately one order of magnitude. The observed shifts in phytoplankton size structure were reflected in changes in phytoplankton community composition, though zooplankton taxonomic composition was unaffected by warming. Furthermore, warming reduced community biomass and total phytoplankton biomass, although zooplankton biomass was unaffected. This resulted in an increase in the zooplankton to phytoplankton biomass ratio in the warmed mesocosms, which could be explained by faster turnover within the phytoplankton assemblages. Overall, warming shifted the distribution of phytoplankton size towards smaller individuals with rapid turnover and low standing biomass, resulting in a reorganization of the biomass structure of the food webs. These results indicate future environmental warming may have profound effects on the structure and functioning of aquatic communities and ecosystems. © 2010 Blackwell Publishing Ltd.

Methane (CH4) and carbon dioxide (CO2) are the dominant gaseous end products of the remineralization of organic carbon and also the two largest contributors to the anthropogenic greenhouse effect. We investigated whether warming altered the balance of CH4 efflux relative to gross primary production (GPP) and ecosystem respiration (ER) in a freshwater mesocosm experiment. Whole ecosystem CH4 efflux was strongly related to temperature with an apparent activation energy of 0.85eV. Furthermore, CH4 efflux increased faster than ER or GPP with temperature, with all three processes having sequentially lower activation energies. Warming of 4°C increased the fraction of GPP effluxing as CH4 by 20% and the fraction of ER as CH4 by 9%, in line with the offset in their respective activation energies. Because CH4 is 21 times more potent as a greenhouse gas, relative to CO2, these results suggest freshwater ecosystems could drive a previously unknown positive feedback between warming and the carbon cycle. © 2010 Blackwell Publishing Ltd.

Attempts to gauge the biological impacts of climate change have typically focussed on the lower levels of organization (individuals to populations), rather than considering more complex multi-species systems, such as entire ecological networks (food webs, mutualistic and host-parasitoid networks). We evaluate the possibility that a few principal drivers underpin network-level responses to climate change, and that these drivers can be studied to develop a more coherent theoretical framework than is currently provided by phenomenological approaches. For instance, warming will elevate individual ectotherm metabolic rates, and direct and indirect effects of changes in atmospheric conditions are expected to alter the stoichiometry of interactions between primary consumers and basal resources; these effects are general and pervasive, and will permeate through the entire networks that they affect. In addition, changes in the density and viscosity of aqueous media could alter interactions among very small organisms and disrupt the pycnoclines that currently compartmentalize many aquatic networks in time and space. We identify a range of approaches and potential model systems that are particularly well suited to network-level studies within the context of climate change. We also highlight potentially fruitful areas of research with a view to improving our predictive power regarding climate change impacts on networks. We focus throughout on mechanistic approaches rooted in first principles that demonstrate potential for application across a wide range of taxa and systems. © 2010 Elsevier Ltd.

Riverine habitats are vulnerable to a host of environmental stressors, many of which are increasing in frequency and intensity across the globe. Climate change is arguably the greatest threat on the horizon, with serious implications for freshwater food webs via alterations in thermal regimes, resource quality and availability, and hydrology. This will induce radical restructuring of many food webs, by altering the identity of nodes, the strength and patterning of interactions and consequently the dynamics and architecture of the trophic network as a whole. Although such effects are likely to be apparent globally, they are predicted to be especially rapid and dramatic in high altitude and latitude ecosystems, which represent 'sentinel systems'. The complex and subtle connections between members of a food web and potential synergistic interactions with other environmental stressors can lead to seemingly counterintuitive responses to perturbations that cannot be predicted from the traditional focus of studying individual species in isolation. In this review, we highlight the need for developing new network-based approaches to understand and predict the consequences of global change in running waters. © 2010 Springer Science+Business Media B.V.

The carbon cycle modulates climate change via the regulation of atmospheric CO2, and represents one of the most important ecosystem services of value to humans. However, considerable uncertainties remain concerning potential feedbacks between the biota and the climate. We developed theoretical models derived from the metabolic theory of ecology (MTE), and tested them in an ecosystem-level manipulative experiment in freshwater mesocosms. The year-long experiment simulated a warming scenario (A1B; [IPCC, 2007]) expected by the end of the century. The key components of the carbon cycle - that is gross primary production (GPP), ecosystem respiration (ER) and CH4 efflux (ME) - measured in our experiment were all strongly related to temperature. Their temperature dependence was typically constrained by the average activation energy of their particular metabolic pathway, and as predicted by our models, this increased progressively for GPP, ER and ME. Warming of 4 C decreased the sequestration of CO2 by 13%, increased the fraction of primary production effluxing as methane by 20% and the fraction of ER as methane by 9%, in line with the offset in their respective activation energies. Because methane has 21 times the greenhouse gas radiative potential of CO2, these results suggest aquatic ecosystems could drive a previously unknown positive feedback between warming and the carbon cycle. We then used a series of global data compilations of measurements of rates of primary production and respiration to better understand the temperature dependence of the carbon cycle in other aquatic ecosystems and to compare them with data from terrestrial systems. Our experimental results were mirrored by our global data compilations, with the effective activation energy for marine and freshwater primary production identical to GPP measured in our experiment. Similarly, the temperature dependences of respiration in estuaries, lakes and the ocean were indistinguishable from that of ER in our experiment. Finally, our study suggests that the temperature dependence of primary production and respiration in aquatic ecosystems might differ from those in terrestrial ecosystems, and this could be crucial in predicting the future response of the carbon cycle in these different systems to global warming. © 2010 Elsevier Ltd.

The carbon cycle modulates climate change, via the regulation of atmospheric CO(2), and it represents one of the most important services provided by ecosystems. However, considerable uncertainties remain concerning potential feedback between the biota and the climate. In particular, it is unclear how global warming will affect the metabolic balance between the photosynthetic fixation and respiratory release of CO(2) at the ecosystem scale. Here, we present a combination of experimental field data from freshwater mesocosms, and theoretical predictions derived from the metabolic theory of ecology to investigate whether warming will alter the capacity of ecosystems to absorb CO(2). Our manipulative experiment simulated the temperature increases predicted for the end of the century and revealed that ecosystem respiration increased at a faster rate than primary production, reducing carbon sequestration by 13 per cent. These results confirmed our theoretical predictions based on the differential activation energies of these two processes. Using only the activation energies for whole ecosystem photosynthesis and respiration we provide a theoretical prediction that accurately quantified the precise magnitude of the reduction in carbon sequestration observed experimentally. We suggest the combination of whole-ecosystem manipulative experiments and ecological theory is one of the most promising and fruitful research areas to predict the impacts of climate change on key ecosystem services.

The integration of detailed information on feeding interactions with measures of abundance and body mass of individuals provides a powerful platform for understanding ecosystem organisation. Metabolism and, by proxy, body mass constrain the flux, turnover and storage of energy and biomass in food webs. Here, we present the first food web data for Lough Hyne, a species rich Irish Sea Lough. Through the application of individual-and size-based analysis of the abundance-body mass relationship, we tested predictions derived from the metabolic theory of ecology. We found that individual body mass constrained the flux of biomass and determined its distribution within the food web. Body mass was also an important determinant of diet width and niche overlap, and predator diets were nested hierarchically, such that diet width increased with body mass. We applied a novel measure of predator-prey biomass flux which revealed that most interactions in Lough Hyne were weak, whereas only a few were strong. Further, the patterning of interaction strength between prey sharing a common predator revealed that strong interactions were nearly always coupled with weak interactions. Our findings illustrate that important insights into the organisation, structure and stability of ecosystems can be achieved through the theoretical exploration of detailed empirical data. © 2008 Versita Warsaw and Springer-Verlag Berlin Heidelberg.

Is it possible to untangle the 'entangled bank'--Darwin's metaphor for the complexity and connectedness of species in the natural world? Studies on webs of species interactions suggest so, but a major question remains unanswered: how specialized are different ecological networks? By considering how strongly species interact with each other, information theory may give the answer.