Microbial communities regulate ecosystem responses to climate change. However, predicting these responses is challenging because of complex interactions among processes at multiple levels of organization. Organismal traits that determine individual performance and ecological interactions are essential for scaling up environmental responses from individuals to ecosystems. We combine protist microcosm experiments and mathematical models to show that key traits—cell size, shape, and contents—each explain different aspects of species’ demographic responses to changes in temperature. These differences in species’ temperature responses have complex cascading effects across levels of organization—causing nonlinear shifts in total community respiration rates across temperatures via coordinated changes in community composition, equilibrium densities, and community–mean species mass in experimental protist communities that tightly match theoretical predictions. Our results suggest that traits explain variation in population growth, and together, these two factors scale up to influence community- and ecosystem-level processes across temperatures. Connecting the multilevel microbial processes that ultimately influence climate in this way will help refine predictions about complex ecosystem–climate feedbacks and the pace of climate change itself.

1. Body size is a fundamental trait linked to many ecological processes-from individuals to ecosystems. Although the effects of body size on metabolism are well-known, how body size influences, and is influenced by, population growth and density is less clear. Specifically, 1) whether body size, or population dynamics, more strongly influences the other, and, 2) whether observed changes in body size are due to plasticity or rapid evolutionary change, are not well understood. 2. Here, we address these two issues by experimentally tracking population density and mean body size in the protist Tetrahymena pyriformis as it grows from low density to carrying capacity. We then use state-of-the-art time-series analyses to infer the direction, magnitude, and causality of the link between body size and ecological dynamics. Last, we fit two alternative dynamical models to our empirical time series to assess whether plasticity or rapid evolution better explains changes in mean body size. 3. Our results clearly indicate that changes in body size precede and determine changes in population density, not the other way around. We also show that a model assuming that size changes via plasticity more parsimoniously explains these observed coupled phenotypic and ecological dynamics than one that assumes rapid evolution drives changes in size. 4. Together these results suggest that rapid, plastic phenotypic change not only occurs well within ecological timescales but may even precede -and causally influence- ecological dynamics. Furthermore, large individuals may be favored and fuel high population growth rates when population density is low, but smaller individuals may be favored once populations reach carrying capacity and resources become scarcer. Thus, rapid plastic changes in functional traits may play a fundamental and currently unrecognized role in familiar ecological processes like logistic population growth.

Temperature strongly influences microbial community structure and function, in turn contributing to global carbon cycling that can fuel further warming. Recent studies suggest that biotic interactions among microbes may play an important role in determining the temperature responses of these communities. However, how predation regulates these microbiomes under future climates is still poorly understood. Here, we assess whether predation by a key global bacterial consumer—protists—influences the temperature response of the community structure and function of a freshwater microbiome. To do so, we exposed microbial communities to two cosmopolitan protist species—Tetrahymena thermophila and Colpidium sp.—at two different temperatures, in a month-long microcosm experiment. While microbial biomass and respiration increased with temperature due to community shifts, these responses changed over time and in the presence of protists. Protists influenced microbial biomass and respiration rate through direct and indirect effects on bacterial community structure, and predator presence actually reduced microbial respiration at elevated temperature. Indicator species analyses showed that these predator effects were mostly determined by phylum-specific bacterial responses to protist density and cell size. Our study supports previous findings that temperature is an important driver of microbial communities but also demonstrates that the presence of a large predator can mediate these responses to warming.

1. Body size is a fundamental trait linked to many ecological processes-from individuals to ecosystems. Although the effects of body size on metabolism are well-known, the potential reciprocal effects of body size and density are less clear. Specifically, (a) whether changes in body size or density more strongly influence the other and (b) whether coupled rapid changes in body size and density are due to plasticity, rapid evolutionary change or a combination of both.2. Here, we address these two issues by experimentally tracking population density and mean body size in the protist Tetrahymena pyriformis as it grows from low density to carrying capacity. We then use Convergent Cross Mapping time series analyses to infer the direction, magnitude and causality of the link between body size and population dynamics. We confirm the results of our analysis by experimentally manipulating body size and density while keeping the other constant. Last, we fit mathematical models to our experimental time series that account for purely plastic change in body size, rapid evolution in size, or a combination of both, to gain insights into the processes that most likely explain the observed dynamics.3. Our results indicate that changes in body size more strongly influence changes in density than the other way around, but also show that there is reciprocity in this effect (i.e., a feedback). We show that a model that only accounts for purely plastic change in size most parsimoniously explains observed, coupled phenotypic and ecological dynamics.4. Together, these results suggest (a) that body size can shift dramatically through plasticity, well within ecological timescales, (b) that rapid changes in body size may have a larger effect on population dynamics than the reverse, but (c) phenotypic and population dynamics influence each other as populations grow.Overall, we show that rapid plastic changes in functional traits like body size may play a fundamental-but currently unrecognized-role in familiar ecological processes such as logistic population growth.

Anthropogenic increases in temperature and nutrient loads will likely impact food web structure and stability. Although their independent effects have been reasonably well studied, their joint effects—particularly on coupled ecological and phenotypic dynamics—remain poorly understood. Here we experimentally manipulated temperature and nutrient levels in microbial food webs and used time-series analysis to quantify the strength of reciprocal effects between ecological and phenotypic dynamics across trophic levels. We found that (1) joint—often interactive—effects of temperature and nutrients on ecological dynamics are more common at higher trophic levels, (2) temperature and nutrients interact to shift the relative strength of top-down versus bottom-up control, and (3) rapid phenotypic change mediates observed ecological responses to changes in temperature and nutrients. Our results uncover how feedback between ecological and phenotypic dynamics mediate food web responses to environmental change. This suggests important but previously unknown ways that temperature and nutrients might jointly control the rapid eco-phenotypic feedback that determine food web dynamics in a changing world.