The effect of elevated CO2 on growth and competition in experimental phytoplankton communities

We report an experiment designed to identify the effect of elevated CO₂ on species of phytoplankton in a simple laboratory system. Major taxa of phytoplankton differ in their ability to take up CO₂, which might lead to predictable changes in the growth rate of species and thereby shifts in the composition of phytoplankton communities in response to rising CO₂. Six species of phytoplankton belonging to three major taxa (cyanobacteria, diatoms and chlorophytes) were cultured in atmospheres whose CO₂ concentration was gradually increased from ambient levels to 1000 parts per million over about 100 generations and then maintained for a further 200 generations at elevated CO₂. The experimental design allowed us to trace a predictive sequence, from physiological features to the growth response of species to elevated CO₂ in pure culture, from the growth response in pure culture to competitive ability in pairwise mixtures and from pairwise competitive ability to shifts in the relative abundance of species in the full community of all six species. CO₂ altered the dynamics of growth in a fashion consistent with known differences among major taxa in their ability to take up and use CO₂. This pure‐culture response was partly successful in predicting the outcome of competition in pairwise mixtures, especially the enhanced competitive ability of chlorophytes relative to cyanobacteria, although generally statistical support was weak. The competitive response in pairwise mixtures was a good predictor of changes in competitive ability in the full community. Hence, there is a potential for forging a logical chain of inferences for predicting how phytoplankton communities will respond to elevated CO₂. Clearly further extensive experiments will be required to validate this approach in the greater complexity found in diverse communities and environments of natural systems.     

Temperature‐dependence of minimum resource requirements alters competitive hierarchies in phytoplankton

Resource competition theory is a conceptual framework that provides mechanistic insights into competition and community assembly of species with different resource requirements. However, there has been little exploration of how resource requirements depend on other environmental factors, including temperature. Changes in resource requirements as influenced by environmental temperature would imply that climate warming can alter the outcomes of competition and community assembly. We experimentally demonstrate that environmental temperature alters the minimum light and nitrogen requirements – as well as other growth parameters – of six widespread phytoplankton species from distinct taxonomic groups. We found that species require the most nitrogen at the highest temperatures while light requirements tend to be lowest at intermediate temperatures, although there are substantial interspecific differences in the exact shape of this relationship. We also experimentally parameterize two competition models, which we use to illustrate how temperature, through its effects on species’ traits, alters competitive hierarchies in multispecies assemblages, determining community dynamics. Developing a mechanistic understanding of how temperature influences the ability to compete for limiting resources is a critical step towards improving forecasts of community dynamics under climate warming.     

On a collision course: competition and dispersal differences create no-analogue communities and cause extinctions during climate change

Most climate change predictions omit species interactions and interspecific variation in dispersal. Here, we develop a model of multiple competing species along a warming climatic gradient that includes temperature-dependent competition, differences in niche breadth and interspecific differences in dispersal ability. Competition and dispersal differences decreased diversity and produced so-called 'no-analogue' communities, defined as a novel combination of species that does not currently co-occur. Climate change altered community richness the most when species had narrow niches, when mean community-wide dispersal rates were low and when species differed in dispersal abilities. With high interspecific dispersal variance, the best dispersers tracked climate change, out-competed slower dispersers and caused their extinction. Overall, competition slowed the advance of colonists into newly suitable habitats, creating lags in climate tracking. We predict that climate change will most threaten communities of species that have narrow niches (e.g. tropics), vary in dispersal (most communities) and compete strongly. Current forecasts probably underestimate climate change impacts on biodiversity by neglecting competition and dispersal differences.     

Asynchronous range shifts drive alpine plant–pollinator interactions and reduce plant fitness

Climate change is driving species' range shifts, which are in turn disrupting species interactions due to species‐specific differences in their abilities to migrate in response to climate. We evaluated the consequences of asynchronous range shifts in an alpine plant–pollinator community by transplanting replicated alpine meadow turfs downslope along an elevational gradient thereby introducing them to warmer climates and novel plant and pollinator communities. We asked how these novel plant–pollinator interactions affect plant reproduction. We found that pollinator communities differed substantially across the elevation/temperature gradient, suggesting that these plants will likely interact with different pollinator communities with warming climate. Contrary to the expectation that floral visitation would increase monotonically with warmer temperatures at lower elevations, visitation rate to the transplanted communities peaked under intermediate warming at midelevation sites. In contrast, visitation rate generally increased with temperature for the local, lower elevation plant communities surrounding the experimental alpine turfs. For two of three focal plant species in the transplanted high‐elevation community, reproduction declined at warmer sites. For these species, reproduction appears to be dependent on pollinator identity such that reduced reproduction may be attributable to decreased visitation from key pollinator species, such as bumble bees, at warmer sites. Reproduction in the third focal species appears to be primarily driven by overall pollinator visitation rate, regardless of pollinator identity. Taken together, the results suggest climate warming can indirectly affect plant reproduction via changes in plant–pollinator interactions. More broadly, the experiment provides a case study for predicting the outcome of novel species interactions formed under changing climates.     

Trait response in communities to environmental change: effect of interspecific competition and trait covariance structure

The response of ecological communities to environmental disturbances depends not just on the number of species they contain but also on the functional diversity of the constituent species; greater variation in the tolerance of species to different environmental disturbances is generally thought to confer greater resistance to the community. Here, I investigate how the functional diversity of communities changes with environmental disturbances. Specifically, I assume that there is variation in traits among species that confer tolerance or sensitivity to environmental disturbances. When a disturbance occurs, variation in species tolerances causes changes in the relative abundances of species, which in turn changes the average tolerance of the community. For example, if tolerance to an environmental disturbance is conferred by large body size, then the environmental disturbance should be expected to increase the average body size of individuals in the community. Despite this expectation, ecological interactions among species can affect the average community response. For example, if larger species are also strong competitors with each other, then this might reduce the increase in average body size in the community, because interspecific competition limits the grow in population density of large bodied species. Similarly, when disturbances affect multiple traits, the covariance in the distribution of trait values among species may restrict the response of any one trait; if two traits provide tolerance to the same disturbance but negatively covary among species, then the response of one trait will limit the response of the other trait at the community level. Using a Lotka–Volterra model for competitive communities, I derive general formulae that generate explicit predictions about the changes in average trait values in a community subject to environmental disturbances. These formulae demonstrate that competition can impede the change in average community trait values. However, the impediment is not considerable in comparison to the predominant factors of trait variances and species selection effects when species with the most similar trait values also experience the greatest interspecific competition. Similarly, negative covariances among different traits that confer resistance to the same environmental disturbance will impede their responses. I illustrate these results using phytoplankton data from a whole-lake experiment in which manipulation to the zooplankton community created a disturbance to the phytoplankton that changed the selective consumption of large vs. small phytoplankton.     

Warming will affect phytoplankton differently: evidence through a mechanistic approach

Although the consequences of global warming in aquatic ecosystems are only beginning to be revealed, a key to forecasting the impact on aquatic communities is an understanding of individual species' vulnerability to increased temperature. Despite their microscopic size, phytoplankton support about half of the global primary production, drive essential biogeochemical cycles and represent the basis of the aquatic food web. At present, it is known that phytoplankton are important targets and, consequently, harbingers of climate change in aquatic systems. Therefore, investigating the capacity of phytoplankton to adapt to the predicted warming has become a relevant issue. However, considering the polyphyletic complexity of the phytoplankton community, different responses to increased temperature are expected. We experimentally tested the effects of warming on 12 species of phytoplankton isolated from a variety of environments by using a mechanistic approach able to assess evolutionary adaptation (the so-called ratchet technique). We found different degrees of tolerance to temperature rises and an interspecific capacity for genetic adaptation. The thermal resistance level reached by each species is discussed in relation to their respective original habitats. Our study additionally provides evidence on the most resistant phytoplankton groups in a future warming scenario.     

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.     

Theoretical predictions for how temperature affects the dynamics of interacting herbivores and plants

Concern about climate change has spurred experimental tests of how warming affects species' abundance and performance. As this body of research grows, interpretation and extrapolation to other species and systems have been limited by a lack of theory. To address the need for theory for how warming affects species interactions, we used consumer-prey models and the metabolic theory of ecology to develop quantitative predictions for how systematic differences between the temperature dependence of heterotrophic and autotrophic population growth lead to temperature-dependent herbivory. We found that herbivore and plant abundances change with temperature in proportion to the ratio of autotrophic to heterotrophic metabolic temperature dependences. This result is consistent across five different formulations of consumer-prey models and over varying resource supply rates. Two models predict that temperature-dependent herbivory causes primary producer abundance to be independent of temperature. This finding contradicts simpler extensions of metabolic theory to abundance that ignore trophic interactions, and is consistent with patterns in terrestrial ecosystems. When applied to experimental data, the model explained 77% and 66% of the variation in phytoplankton and zooplankton abundances, respectively. We suggest that metabolic theory provides a foundation for understanding the effects of temperature change on multitrophic ecological communities.     

Competition, predation and species responses to environmental change

Despite much effort over the past decade on the ecological consequences of global warming, ecologists still have little understanding of the importance of interspecific interactions in species responses to environmental change. Models predict that predation should mitigate species responses to environmental change, and that interspecific competition should aggravate species responses to environmental change. To test this prediction, we studied how predation and competition affected the responses of two ciliates, Colpidium striatum and Paramecium tetraurelia , to temperature change in laboratory microcosms. We found that neither predation nor competition altered the responses of Colpidium striatum to temperature change, and that competition but not predation altered the responses of Paramecium tetraurelia to temperature change. Asymmetric interactions and temperature-dependent interactions may have contributed to the disparity between model predictions and experimental results. Our results suggest that models ignoring inherent complexities in ecological communities may be inadequate in forecasting species responses to environmental change.     

Towards a mechanistic understanding of temperature and enrichment effects on species interaction strength,omnivory and food‐web structure

Revealing the links between species functional traits, interaction strength and food‐web structure is of paramount importance for understanding and predicting the relationships between food‐web diversity and stability in a rapidly changing world. However, little is known about the interactive effects of environmental perturbations on individual species, trophic interactions and ecosystem functioning. Here, we combined modelling and laboratory experiments to investigate the effects of warming and enrichment on a terrestrial tritrophic system. We found that the food‐web structure is highly variable and switches between exploitative competition and omnivory depending on the effects of temperature and enrichment on foraging behaviour and species interaction strength. Our model contributes to identifying the mechanisms that explain how environmental effects cascade through the food web and influence its topology. We conclude that considering environmental factors and flexible food‐web structure is crucial to improve our ability to predict the impacts of global changes on ecosystem diversity and stability.     

Facilitation promotes invasions in plant‐associated microbial communities

While several studies have established a positive correlation between community diversity and invasion resistance, it is less clear how species interactions within resident communities shape this process. Here, we experimentally tested how antagonistic and facilitative pairwise interactions within resident model microbial communities predict invasion by the plant–pathogenic bacterium Ralstonia solanacearum. We found that facilitative resident community interactions promoted and antagonistic interactions suppressed invasions both in the lab and in the tomato plant rhizosphere. Crucially, pairwise interactions reliably explained observed invasion outcomes also in multispecies communities, and mechanistically, this was linked to direct inhibition of the invader by antagonistic communities (antibiosis), and to a lesser degree by resource competition between members of the resident community and the invader. Together, our findings suggest that the type and strength of pairwise interactions can reliably predict the outcome of invasions in more complex multispecies communities.     

Community complexity drives patterns of natural selection on a chemical defense of Brassica nigra

Plants interact with many different species throughout their life cycle. Recent work has shown that the ecological effects of multispecies interactions are often not predictable from studies of the component pairwise interactions. Little is known about how multispecies interactions affect the evolution of ecologically important traits. We tested the direct and interactive effects of inter- and intraspecific competition, as well as of two abundant herbivore species (a generalist folivore and a specialist aphid), on the selective value of a defensive chemical compound in Brassica nigra. We found that investment in chemical defense was favored in interspecific competition but disfavored in intraspecific competition and that this pattern of selection was dependent on the presence of both herbivores, suggesting that selection will depend on the rarity or commonness of these species. These results show that the selective value of ecologically important traits depends on the complicated web of interactions present in diverse natural communities and that fluctuations in community composition may maintain genetic variation in such traits.     

Functional trait differences and the outcome of community assembly: an experimental test with vernal pool annual plants

Functional trait‐based approaches have seen rapid development in community ecology and biogeography in recent years, as they promise to offer a better mechanistic and predictive understanding of community structure. However, several key challenges remain. First, while many studies have explored connections between functional traits and abiotic gradients, far fewer have directly tested the common assumption that functional trait differences influence interspecific interactions. Second, empirical studies often ignore intraspecific trait variation within communities, even though intraspecific variation has been known to have substantial impacts on community dynamics. Here we present an experiment designed to assess the role of functional trait differences in predicting the outcome of interspecific species interactions among a suite of California vernal pool annual plants. Eight species were grown in pairwise combinations in two levels of inundation in a greenhouse and functional traits were measured on all individuals. Nested models predicting focal plant performance were fit to the data. For seven of the eight species in the experiment, the best model included a functional trait difference term that was consistent with a competitive hierarchy, indicating that focal species tended to do better when they had larger leaf size, lower specific leaf area, and greater investment in lateral canopy spread than their neighbors. Models that included individually measured trait values generally performed better than models using species trait averages. We tested if the same trait measurements predicted tolerance of inundation (a feature of vernal pool habitats), and species depth distributions from extensive field surveys, though we did not find strong relationships. Our results suggest that functional traits can be used to make inferences about the outcome of interspecific interactions, and that greater predictive power can come from considering intraspecific variation in functional traits, particularly in low diversity communities.     

Predictable ecological response to rising CO2 of a community of marine phytoplankton

Rising atmospheric CO₂ and ocean acidification are fundamentally altering conditions for life of all marine organisms, including phytoplankton. Differences in CO₂ related physiology between major phytoplankton taxa lead to differences in their ability to take up and utilize CO₂. These differences may cause predictable shifts in the composition of marine phytoplankton communities in response to rising atmospheric CO₂. We report an experiment in which seven species of marine phytoplankton, belonging to four major taxonomic groups (cyanobacteria, chlorophytes, diatoms, and coccolithophores), were grown at both ambient (500 μatm) and future (1,000 μatm) CO₂ levels. These phytoplankton were grown as individual species, as cultures of pairs of species and as a community assemblage of all seven species in two culture regimes (high‐nitrogen batch cultures and lower‐nitrogen semicontinuous cultures, although not under nitrogen limitation). All phytoplankton species tested in this study increased their growth rates under elevated CO₂ independent of the culture regime. We also find that, despite species‐specific variation in growth response to high CO₂, the identity of major taxonomic groups provides a good prediction of changes in population growth and competitive ability under high CO₂. The CO₂‐induced growth response is a good predictor of CO₂‐induced changes in competition (R² > .93) and community composition (R² > .73). This study suggests that it may be possible to infer how marine phytoplankton communities respond to rising CO₂ levels from the knowledge of the physiology of major taxonomic groups, but that these predictions may require further characterization of these traits across a diversity of growth conditions. These findings must be validated in the context of limitation by other nutrients. Also, in natural communities of phytoplankton, numerous other factors that may all respond to changes in CO2, including nitrogen fixation, grazing, and variation in the limiting resource will likely complicate this prediction.     

Ecological emergence of thermal clines in body size

The unprecedented rate of global warming requires a better understanding of how ecosystems will respond. Organisms often have smaller body sizes under warmer climates (Bergmann's rule and the temperature‐size rule), and body size is a major determinant of life histories, demography, population size, nutrient turnover rate, and food‐web structure. Therefore, by altering body sizes in whole communities, current warming can potentially disrupt ecosystem function and services. However, the underlying drivers of warming‐induced body downsizing remain far from clear. Here, we show that thermal clines in body size are predicted from universal laws of ecology and metabolism, so that size‐dependent selection from competition (both intra and interspecific) and predation favors smaller individuals under warmer conditions. We validate this prediction using 4.1 × 10⁶ individual body size measurements from French river fish spanning 29 years and 52 species. Our results suggest that warming‐induced body downsizing is an emergent property of size‐structured food webs, and highlight the need to consider trophic interactions when predicting biosphere reorganizations under global warming.     

Predictions of response to temperature are contingent on model choice and data quality

The equations used to account for the temperature dependence of biological processes, including growth and metabolic rates, are the foundations of our predictions of how global biogeochemistry and biogeography change in response to global climate change. We review and test the use of 12 equations used to model the temperature dependence of biological processes across the full range of their temperature response, including supra‐ and suboptimal temperatures. We focus on fitting these equations to thermal response curves for phytoplankton growth but also tested the equations on a variety of traits across a wide diversity of organisms. We found that many of the surveyed equations have comparable abilities to fit data and equally high requirements for data quality (number of test temperatures and range of response captured) but lead to different estimates of cardinal temperatures and of the biological rates at these temperatures. When these rate estimates are used for biogeographic predictions, differences between the estimates of even the best‐fitting models can exceed the global biological change predicted for a decade of global warming. As a result, studies of the biological response to global changes in temperature must make careful consideration of model selection and of the quality of the data used for parametrizing these models.     

Competitive and demographic leverage points of community shifts under climate warming

Accelerating rates of climate change and a paucity of whole-community studies of climate impacts limit our ability to forecast shifts in ecosystem structure and dynamics, particularly because climate change can lead to idiosyncratic responses via both demographic effects and altered species interactions. We used a multispecies model to predict which processes and species'' responses are likely to drive shifts in the composition of a space-limited benthic marine community. Our model was parametrized from experimental manipulations of the community. Model simulations indicated shifts in species dominance patterns as temperatures increase, with projected shifts in composition primarily owing to the temperature dependence of growth, mortality and competition for three critical species. By contrast, warming impacts on two other species (rendering them weaker competitors for space) and recruitment rates of all species were of lesser importance in determining projected community changes. Our analysis reveals the importance of temperature-dependent competitive interactions for predicting effects of changing climate on such communities. Furthermore, by identifying processes and species that could disproportionately leverage shifts in community composition, our results contribute to a mechanistic understanding of climate change impacts, thereby allowing more insightful predictions of future biodiversity patterns.     

Ocean cleaning stations under a changing climate: biological responses of tropical and temperate fish‐cleaner shrimp to global warming

Cleaning symbioses play an important role in the health of certain coastal marine communities. These interspecific associations often occur at specific sites (cleaning stations) where a cleaner organism (commonly a fish or shrimp) removes ectoparasites/damaged tissue from a ‘client’ (a larger cooperating fish). At present, the potential impact of climate change on the fitness of cleaner organisms remains unknown. This study investigated the physiological and biochemical responses of tropical (Lysmata amboinensis) and temperate (L. seticaudata) cleaner shrimp to global warming. Specifically, thermal limits (CTMax), metabolic rates, thermal sensitivity, heat shock response (HSR), lipid peroxidation [malondialdehyde (MDA) concentration], lactate levels, antioxidant (GST, SOD and catalase) and digestive enzyme activities (trypsin and alkaline phosphatase) at current and warming (+3 °C) temperature conditions. In contrast to the temperate species, CTMax values decreased significantly from current (24–27 °C) to warming temperature conditions (30 °C) for the tropical shrimp, where metabolic thermal sensitivity was affected and the HSR was significantly reduced. MDA levels in tropical shrimp increased dramatically, indicating extreme cellular lipid peroxidation, which was not observed in the temperate shrimp. Lactate levels, GST and SOD activities were significantly enhanced within the muscle tissue of the tropical species. Digestive enzyme activities in the hepatopancreas of both species were significantly decreased by warmer temperatures. Our data suggest that the tropical cleaner shrimp will be more vulnerable to global warming than the temperate Lysmata seticaudata; the latter evolved in a relatively unstable environment with seasonal thermal variations that may have conferred greater adaptive plasticity. Thus, tropical cleaning symbioses may be challenged at a greater degree by warming‐related anthropogenic forcing, with potential cascading effects on the health and structuring of tropical coastal communities (e.g. coral reefs).     

Demographic effects of warming,elevated soil nitrogen and thinning on the colonization of a perennial plant

Global change is causing significant modifications to native plant communities. These effects can be direct through changes in productivity, or indirect through the spread of invading species. Identifying vital traits important for individual species’ response to environmental variation could be useful for making predictions about how entire communities may respond to global change. I studied the effects of factors associated with global change on the demography of an experimentally introduced species, Pityopsis aspera. In a Florida old-field, I investigated how warming, increased soil nitrogen and thinning of the extant plant community affected survival, growth and reproduction of P. aspera using a life table response experiment. The estimated population growth rate (λ) of P. aspera was reduced by nitrogen addition, as a result of decreased fecundity. However, λ increased in response to the warming treatment, as a result of increased fecundity. In the presence of thinning, both warming and nitrogen served to increase λ as a result of an increase in the growth of young individuals. This experiment illustrates how different vital rates contribute to the population level responses of an experimentally introduced plant to warming, and nitrogen deposition. Results also show how these demographic responses may occur via indirect effects through established species. This work highlights the importance of studying interactions among temperature, soil nitrogen and demography across the entire life cycle in order to capture the complex and, often, non-additive relationships mediating global change effects.