Temperature and CO2 interactively drive shifts in the compositional and functional structure of peatland protist communities.

Microbes affect the global carbon cycle that influences climate change and are in turn influenced by environmental change. Here, we use data from a long-term whole-ecosystem warming experiment at a boreal peatland to answer how temperature and CO2 jointly influence communities of abundant, diverse, yet poorly understood, non-fungi microbial Eukaryotes (protists). These microbes influence ecosystem function directly through photosynthesis and respiration, and indirectly, through predation on decomposers (bacteria and fungi). Using a combination of high-throughput fluid imaging and 18S amplicon sequencing, we report large climate-induced, community-wide shifts in the community functional composition of these microbes (size, shape, and metabolism) that could alter overall function in peatlands. Importantly, we demonstrate a taxonomic convergence but a functional divergence in response to warming and elevated CO2 with most environmental responses being contingent on organismal size: warming effects on functional composition are reversed by elevated CO2 and amplified in larger microbes but not smaller ones. These findings show how the interactive effects of warming and rising CO2 levels could alter the structure and function of peatland microbial food webs-a fragile ecosystem that stores upwards of 25% of all terrestrial carbon and is increasingly threatened by human exploitation.

Predator mass mortality events restructure food webs through trophic decoupling.

Predators have a key role in structuring ecosystems1-4. However, predator loss is accelerating globally4-6, and predator mass-mortality events7 (MMEs)-rapid large-scale die-offs-are now emblematic of the Anthropocene epoch6. Owing to their rare and unpredictable nature7, we lack an understanding of how MMEs immediately impact ecosystems. Past predator-removal studies2,3 may be insufficient to understand the ecological consequences of MMEs because, in nature, dead predators decompose in situ and generate a resource pulse8, which could alter ensuing ecosystem dynamics by temporarily enhancing productivity. Here we experimentally induce MMEs in tritrophic, freshwater lake food webs and report ecological dynamics that are distinct from predator losses2,3 or resource pulses9 alone, but that can be predicted from theory8. MMEs led to the proliferation of diverse consumer and producer communities resulting from weakened top-down predator control1-3 and stronger bottom-up effects through predator decomposition8. In contrast to predator removals alone, enhanced primary production after MMEs dampened the consumer community response. As a consequence, MMEs generated biomass dynamics that were most similar to those of undisturbed systems, indicating that they may be cryptic disturbances in nature. These biomass dynamics led to trophic decoupling, whereby the indirect beneficial effects of predators on primary producers are lost and later materialize as direct bottom-up effects that stimulate primary production amid intensified herbivory. These results reveal ecological signatures of MMEs and demonstrate the feasibility of forecasting novel ecological dynamics arising with intensifying global change.

Temperature and nutrients drive eco-phenotypic dynamics in a microbial food web.

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.

Viral infections likely mediate microbial controls on ecosystem responses to global warming.

Climate change is affecting how energy and matter flow through ecosystems, thereby altering global carbon and nutrient cycles. Microorganisms play a fundamental role in carbon and nutrient cycling and are thus an integral link between ecosystems and climate. Here, we highlight a major black box hindering our ability to anticipate ecosystem climate responses: viral infections within complex microbial food webs. We show how understanding and predicting ecosystem responses to warming could be challenging-if not impossible-without accounting for the direct and indirect effects of viral infections on different microbes (bacteria, archaea, fungi, protists) that together perform diverse ecosystem functions. Importantly, understanding how rising temperatures associated with climate change influence viruses and virus-host dynamics is crucial to this task, yet is severely understudied. In this perspective, we (i) synthesize existing knowledge about virus-microbe-temperature interactions and (ii) identify important gaps to guide future investigations regarding how climate change might alter microbial food web effects on ecosystem functioning. To provide real-world context, we consider how these processes may operate in peatlands-globally significant carbon sinks that are threatened by climate change. We stress that understanding how warming affects biogeochemical cycles in any ecosystem hinges on disentangling complex interactions and temperature responses within microbial food webs.

Rapid eco-phenotypic feedback and the temperature response of biomass dynamics.

Biomass dynamics capture information on population dynamics and ecosystem-level processes (e.g., changes in production over time). Understanding how rising temperatures associated with global climate change influence biomass dynamics is thus a pressing issue in ecology. The total biomass of a species depends on its density and its average mass. Consequently, disentangling how biomass dynamics responds to increasingly warm and variable temperatures ultimately depends on understanding how temperature influences both density and mass dynamics. Here, we address this issue by keeping track of experimental microbial populations growing to carrying capacity for 15 days at two different temperatures, and in the presence and absence of temperature variability. We develop a simple mathematical expression to partition the contribution of changes in density and mass to changes in biomass and assess how temperature responses in either one influence biomass shifts. Moreover, we use time-series analysis (Convergent Cross Mapping) to address how temperature and temperature variability influence reciprocal effects of density on mass and vice versa. We show that temperature influences biomass through its effects on density and mass dynamics, which have opposite effects on biomass and can offset each other. We also show that temperature variability influences biomass, but that effect is independent of any effects on density or mass dynamics. Last, we show that reciprocal effects of density and mass shift significantly across temperature regimes, suggesting that rapid and environment-dependent eco-phenotypic dynamics underlie biomass responses. Overall, our results connect temperature effects on population and phenotypic dynamics to explain how biomass responds to temperature regimes, thus shedding light on processes at play in cosmopolitan and abundant microbes as the world experiences increasingly warm and variable temperatures.

Protist Predation Influences the Temperature Response of Bacterial Communities.

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.

Phylogenetic structure of specialization: A new approach that integrates partner availability and phylogenetic diversity to quantify biotic specialization in ecological networks.

Biotic specialization holds information about the assembly, evolution, and stability of biological communities. Partner availabilities can play an important role in enabling species interactions, where uneven partner availabilities can bias estimates of biotic specialization when using phylogenetic diversity indices. It is therefore important to account for partner availability when characterizing biotic specialization using phylogenies. We developed an index, phylogenetic structure of specialization (PSS), that avoids bias from uneven partner availabilities by uncoupling the null models for interaction frequency and phylogenetic distance. We incorporate the deviation between observed and random interaction frequencies as weights into the calculation of partner phylogenetic α-diversity. To calculate the PSS index, we then compare observed partner phylogenetic α-diversity to a null distribution generated by randomizing phylogenetic distances among the same number of partners. PSS quantifies the phylogenetic structure (i.e., clustered, overdispersed, or random) of the partners of a focal species. We show with simulations that the PSS index is not correlated with network properties, which allows comparisons across multiple systems. We also implemented PSS on empirical networks of host-parasite, avian seed-dispersal, lichenized fungi-cyanobacteria, and hummingbird pollination interactions. Across these systems, a large proportion of taxa interact with phylogenetically random partners according to PSS, sometimes to a larger extent than detected with an existing method that does not account for partner availability. We also found that many taxa interact with phylogenetically clustered partners, while taxa with overdispersed partners were rare. We argue that species with phylogenetically overdispersed partners have often been misinterpreted as generalists when they should be considered specialists. Our results highlight the important role of randomness in shaping interaction networks, even in highly intimate symbioses, and provide a much-needed quantitative framework to assess the role that evolutionary history and symbiotic specialization play in shaping patterns of biodiversity. PSS is available as an R package at https://github.com/cjpardodelahoz/pss.

Linking species traits and demography to explain complex temperature responses across levels of organization.

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.

Genetic and plastic rewiring of food webs under climate change.

Climate change is altering ecological and evolutionary processes across biological scales. These simultaneous effects of climate change pose a major challenge for predicting the future state of populations, communities and ecosystems. This challenge is further exacerbated by the current lack of integration of research focused on these different scales. We propose that integrating the fields of quantitative genetics and food web ecology will reveal new insights on how climate change may reorganize biodiversity across levels of organization. This is because quantitative genetics links the genotypes of individuals to population-level phenotypic variation due to genetic (G), environmental (E) and gene-by-environment (G × E) factors. Food web ecology, on the other hand, links population-level phenotypes to the structure and dynamics of communities and ecosystems. We synthesize data and theory across these fields and find evidence that genetic (G) and plastic (E and G × E) phenotypic variation within populations will change in magnitude under new climates in predictable ways. We then show how changes in these sources of phenotypic variation can rewire food webs by altering the number and strength of species interactions, with consequences for ecosystem resilience. We also find evidence suggesting there are predictable asymmetries in genetic and plastic trait variation across trophic levels, which set the pace for phenotypic change and food web responses to climate change. Advances in genomics now make it possible to partition G, E and G × E phenotypic variation in natural populations, allowing tests of the hypotheses we propose. By synthesizing advances in quantitative genetics and food web ecology, we provide testable predictions for how the structure and dynamics of biodiversity will respond to climate change.

Constraints and variation in food web link-species space.

Predicting food web structure in future climates is a pressing goal of ecology. These predictions may be impossible without a solid understanding of the factors that structure current food webs. The most fundamental aspect of food web structure-the relationship between the number of links and species-is still poorly understood. Some species interactions may be physically or physiologically 'forbidden'-like consumption by non-consumer species-with possible consequences for food web structure. We show that accounting for these 'forbidden interactions' constrains the feasible link-species space, in tight agreement with empirical data. Rather than following one particular scaling relationship, food webs are distributed throughout this space according to shared biotic and abiotic features. Our study provides new insights into the long-standing question of which factors determine this fundamental aspect of food web structure.

Increasing temperature weakens the positive effect of genetic diversity on population growth.

Genetic diversity and temperature increases associated with global climate change are known to independently influence population growth and extinction risk. Whether increasing temperature may influence the effect of genetic diversity on population growth, however, is not known. We address this issue in the model protist system Tetrahymena thermophila. We test the hypothesis that at temperatures closer to the species' thermal optimum (i.e., the temperature at which population growth is maximal, or T opt), genetic diversity should have a weaker effect on population growth compared to temperatures away from the thermal optimum. To do so, we grew populations of T. thermophila with varying levels of genetic diversity at increasingly warmer temperatures and quantified their intrinsic population growth rate, r. We found that genetic diversity increases population growth at cooler temperatures, but that as temperature increases, this effect weakens. We also show that a combination of changes in the amount of expressed genetic diversity (G) in r, plastic changes in population growth across temperatures (E), and strong G × E interactions underlie this temperature effect. Our results uncover important but largely overlooked temperature effects that have implications for the management of small populations with depauperate genetic stocks in an increasingly warming world.

Larger Area Facilitates Richness-Function Effects in Experimental Microcosms.

Species-area relationships (SAR) and biodiversity-ecosystem function (BEF) relationships are central patterns in community ecology. Although research on both patterns often invokes mechanisms of community assembly, both SARs and BEFs are generally treated as separate phenomena. Here we link the two by creating an experimental SAR in microcosm communities and show that greater species richness in larger areas is accompanied by greater ecosystem function. We then explore mechanisms of community assembly by determining whether rare, large, or high-biomass species are more likely to persist in the larger microcosms. Our results indicate that larger areas harbor more rare species of a wider range of body sizes and have higher functional diversity, implying that the addition of niche space that supports rare species underlies the effect of area on species richness and function. Our results suggest that the preservation of large areas is a potentially useful way of maximizing the provisioning of ecosystem services through the maintenance of biodiversity.

Temperature directly and indirectly influences food web structure.

Understanding whether and how environmental conditions may impact food web structure at a global scale is central to our ability to predict how food webs will respond to climate change. However, such an understanding is nascent. Using the best resolved available food webs to date, I address whether latitude, temperature, or both, explain the number of species and feeding interactions, the proportion of basal and top species, as well as the degree of omnivory, connectance and the number of trophic levels across food webs. I found that temperature is a more parsimonious predictor of food web structure than latitude. Temperature directly reduces the number of species, the proportion of basal species and the number of interactions while it indirectly increases omnivory levels, connectance and trophic level through its direct effects on the fraction and number of basal species. While direct impacts of temperature are routinely taken into account to predict how ecosystems may respond to global climate change, indirect effects have been largely overlooked. These results thus suggest that food webs may be affected by a combination of biotic and abiotic conditions, both directly and indirectly, in a changing world.

Eco-evolutionary dynamics, density-dependent dispersal and collective behaviour: implications for salmon metapopulation robustness.

The spatial dispersal of individuals plays an important role in the dynamics of populations, and is central to metapopulation theory. Dispersal provides connections within metapopulations, promoting demographic and evolutionary rescue, but may also introduce maladapted individuals, potentially lowering the fitness of recipient populations through introgression of heritable traits. To explore this dual nature of dispersal, we modify a well-established eco-evolutionary model of two locally adapted populations and their associated mean trait values, to examine recruiting salmon populations that are connected by density-dependent dispersal, consistent with collective migratory behaviour that promotes navigation. When the strength of collective behaviour is weak such that straying is effectively constant, we show that a low level of straying is associated with the highest gains in metapopulation robustness and that high straying serves to erode robustness. Moreover, we find that as the strength of collective behaviour increases, metapopulation robustness is enhanced, but this relationship depends on the rate at which individuals stray. Specifically, strong collective behaviour increases the presence of hidden low-density basins of attraction, which may serve to trap disturbed populations, and this is exacerbated by increased habitat heterogeneity. Taken as a whole, our findings suggest that density-dependent straying and collective migratory behaviour may help metapopulations, such as in salmon, thrive in dynamic landscapes. Given the pervasive eco-evolutionary impacts of dispersal on metapopulations, these findings have important ramifications for the conservation of salmon metapopulations facing both natural and anthropogenic contemporary disturbances.This article is part of the theme issue 'Collective movement ecology'.

Life history traits and functional processes generate multiple pathways to ecological stability.

Stability contributes to the persistence of ecological communities, yet the interactions among different stabilizing forces are poorly understood. We assembled mesocosms with an algal resource and one to eight different clones of the consumer Daphnia ambigua and tracked algal and Daphnia abundances through time. We then fitted coupled ordinary differential equations (ODEs) to the consumer-resource time series. We show that variation in different components of stability (local stability and the magnitude of population fluctuations) across mesocosms arises through variation in life history traits and the functional processes represented by ODE model parameters. Local stability was enhanced by increased algal growth rate and Daphnia mortality and foraging rate. Population fluctuations were dampened by high Daphnia conversion efficiency and lower interaction strengths, low algal growth rate, high Daphnia death rate, and low Daphnia foraging. These results indicate that (1) stability in consumer-resource systems may arise through the net effect of multiple related stabilizing pathways and (2) different aspects of stability can vary independently and may respond in opposite directions to the same forces.

Phenotypic variation explains food web structural patterns.

Food webs (i.e., networks of species and their feeding interactions) share multiple structural features across ecosystems. The factors explaining such similarities are still debated, and the role played by most organismal traits and their intraspecific variation is unknown. Here, we assess how variation in traits controlling predator-prey interactions (e.g., body size) affects food web structure. We show that larger phenotypic variation increases connectivity among predators and their prey as well as total food intake rate. For predators able to eat only a few species (i.e., specialists), low phenotypic variation maximizes intake rates, while the opposite is true for consumers with broader diets (i.e., generalists). We also show that variation sets predator trophic level by determining interaction strengths with prey at different trophic levels. Merging these results, we make two general predictions about the structure of food webs: (i) trophic level should increase with predator connectivity, and (ii) interaction strengths should decrease with prey trophic level. We confirm these predictions empirically using a global dataset of well-resolved food webs. Our results provide understanding of the processes structuring food webs that include functional traits and their naturally occurring variation.

The ecological consequences of environmentally induced phenotypic changes.

Population dynamics and species persistence are often mediated by species traits. Yet many important traits, like body size, can be set by resource availability and predation risk. Environmentally induced changes in resource levels or predation risk may thus have downstream ecological consequences. Here, we assess whether quantity and type of resources affect the phenotype, the population dynamics, and the susceptibility to predation of a mixotrophic protist through experiments and a model. We show that cell shape, but not size, changes with resource levels and type, and is linked to carrying capacity, thus affecting population dynamics. Also, these changes lead to differential susceptibility to predation, with direct consequences for predator-prey dynamics. We describe important links between environmental changes, traits, population dynamics and ecological interactions, that underscore the need to further understand how trait-mediated interactions may respond to environmental shifts in resource levels in an increasingly changing world.

Gillespie eco-evolutionary models (GEMs) reveal the role of heritable trait variation in eco-evolutionary dynamics.

Heritable trait variation is a central and necessary ingredient of evolution. Trait variation also directly affects ecological processes, generating a clear link between evolutionary and ecological dynamics. Despite the changes in variation that occur through selection, drift, mutation, and recombination, current eco-evolutionary models usually fail to track how variation changes through time. Moreover, eco-evolutionary models assume fitness functions for each trait and each ecological context, which often do not have empirical validation. We introduce a new type of model, Gillespie eco-evolutionary models (GEMs), that resolves these concerns by tracking distributions of traits through time as eco-evolutionary dynamics progress. This is done by allowing change to be driven by the direct fitness consequences of model parameters within the context of the underlying ecological model, without having to assume a particular fitness function. GEMs work by adding a trait distribution component to the standard Gillespie algorithm - an approach that models stochastic systems in nature that are typically approximated through ordinary differential equations. We illustrate GEMs with the Rosenzweig-MacArthur consumer-resource model. We show not only how heritable trait variation fuels trait evolution and influences eco-evolutionary dynamics, but also how the erosion of variation through time may hinder eco-evolutionary dynamics in the long run. GEMs can be developed for any parameter in any ordinary differential equation model and, furthermore, can enable modeling of multiple interacting traits at the same time. We expect GEMs will open the door to a new direction in eco-evolutionary and evolutionary modeling by removing long-standing modeling barriers, simplifying the link between traits, fitness, and dynamics, and expanding eco-evolutionary treatment of a greater diversity of ecological interactions. These factors make GEMs much more than a modeling advance, but an important conceptual advance that bridges ecology and evolution through the central concept of heritable trait variation.

Nested species-rich networks of scavenging vertebrates support high levels of interspecific competition.

Disentangling the processes that shape the organization of ecological assemblages and its implications for species coexistence is one of the foremost challenges of ecology. Although insightful advances have recently related community composition and structure with species coexistence in mutualistic and antagonistic networks, little is known regarding other species assemblages, such as those of scavengers exploiting carrion. Here we studied seven assemblages of scavengers feeding on ungulate carcasses in mainland Spain. We used dynamical models to investigate if community composition, species richness and structure (nestedness) affect species coexistence at carcasses. Scavenging networks showed a nested pattern in sites where highly efficient, obligate scavengers (i.e., vultures) were present and a non-nested pattern everywhere else. Griffon Vulture (Gyps fulvus) and certain meso-facultative mammalian scavengers (i.e., red fox, Vulpes vulpes, and stone marten, Martes foina) were the main species contributing to nestedness. Assemblages with vultures were also the richest ones in species. Nested species-rich assemblages with vulture presence were associated with high carcass consumption rates, indicating higher interspecific competition at the local scale. However, the proportion of species stopping the consumption of carrion (as derived from the competitive dynamic model) stabilized at high richness and nestedness levels. This suggests that high species richness and nestedness may characterize scavenging networks that are robust to high levels of interspecific competition for carrion. Some facilitative interactions driven by vultures and major facultative scavengers could be behind these observations. Our findings are relevant for understanding species' coexistence in highly competitive systems.

Crossing regimes of temperature dependence in animal movement.

A pressing challenge in ecology is to understand the effects of changing global temperatures on food web structure and dynamics. The stability of these complex ecological networks largely depends on how predator-prey interactions may respond to temperature changes. Because predators and prey rely on their velocities to catch food or avoid being eaten, understanding how temperatures may affect animal movement is central to this quest. Despite our efforts, we still lack a mechanistic understanding of how the effect of temperature on metabolic processes scales up to animal movement and beyond. Here, we merge a biomechanical approach, the Metabolic Theory of Ecology and empirical data to show that animal movement displays multiple regimes of temperature dependence. We also show that crossing these regimes has important consequences for population dynamics and stability, which depend on the parameters controlling predator-prey interactions. We argue that this dependence upon interaction parameters may help explain why experimental work on the temperature dependence of interaction strengths has so far yielded conflicting results. More importantly, these changes in the temperature dependence of animal movement can have consequences that go well beyond ecological interactions and affect, for example, animal communication, mating, sensory detection, and any behavioral modality dependent on the movement of limbs. Finally, by not taking into account the changes in temperature dependence reported here we might not be able to properly forecast the impact of global warming on ecological processes and propose appropriate mitigation action when needed.