Climate change in size-structured ecosystems

One important aspect of climate change is the increase in average temperature, which will not only have direct physiological effects on all species but also indirectly modifies abundances, interaction strengths, food-web topologies, community stability and functioning. In this theme issue, we highlight a novel pathway through which warming indirectly affects ecological communities: by changing their size structure (i.e. the body-size distributions). Warming can shift these distributions towards dominance of small- over large-bodied species. The conceptual, theoretical and empirical research described in this issue, in sum, suggests that effects of temperature may be dominated by changes in size structure, with relatively weak direct effects. For example, temperature effects via size structure have implications for top-down and bottom-up control in ecosystems and may ultimately yield novel communities. Moreover, scaling up effects of temperature and body size from physiology to the levels of populations, communities and ecosystems may provide a crucially important mechanistic approach for forecasting future consequences of global warming.     

Climate change impacts in multispecies systems: drought alters food web size structure in a field experiment

Experimental data from intergenerational field manipulations of entire food webs are scarce, yet such approaches are essential for gauging impacts of environmental change in natural systems. We imposed 2 years of intermittent drought on stream channels in a replicated field trial, to measure food web responses to simulated climate change. Drought triggered widespread losses of species and links, with larger taxa and those that were rare for their size, many of which were predatory, being especially vulnerable. Many network properties, including size–scaling relationships within food chains, changed in response to drought. Other properties, such as connectance, were unaffected. These findings highlight the need for detailed experimental data from different organizational levels, from pairwise links to the entire food web. The loss of not only large species, but also those that were rare for their size, provides a newly refined way to gauge likely impacts that may be applied more generally to other systems and/or impacts.     

Climate change effects on macrofaunal litter decomposition: the interplay of temperature,body masses and stoichiometry

Macrofauna invertebrates of forest floors provide important functions in the decomposition process of soil organic matter, which is affected by the nutrient stoichiometry of the leaf litter. Climate change effects on forest ecosystems include warming and decreasing litter quality (e.g. higher C : nutrient ratios) induced by higher atmospheric CO₂ concentrations. While litter-bag experiments unravelled separate effects, a mechanistic understanding of how interactions between temperature and litter stoichiometry are driving decomposition rates is lacking. In a laboratory experiment, we filled this void by quantifying decomposer consumption rates analogous to predator–prey functional responses that include the mechanistic parameters handling time and attack rate. Systematically, we varied the body masses of isopods, the environmental temperature and the resource between poor (hornbeam) and good quality (ash). We found that attack rates increased and handling times decreased (i) with body masses and (ii) temperature. Interestingly, these relationships interacted with litter quality: small isopods possibly avoided the poorer resource, whereas large isopods exhibited increased, compensatory feeding of the poorer resource, which may be explained by their higher metabolic demands. The combination of metabolic theory and ecological stoichiometry provided critically important mechanistic insights into how warming and varying litter quality may modify macrofaunal decomposition rates.     

Climate change impacts on body size and food web structure on mountain ecosystems

The current distribution of climatic conditions will be rearranged on the globe. To survive, species will have to keep pace with climates as they move. Mountains are among the most affected regions owing to both climate and land-use change. Here, we explore the effects of climate change in the vertebrate food web of the Pyrenees. We investigate elevation range expansions between two time-periods illustrative of warming conditions, to assess: (i) the taxonomic composition of range expanders; (ii) changes in food web properties such as the distribution of links per species and community size-structure; and (iii) what are the specific traits of range expanders that set them apart from the other species in the community—in particular, body mass, diet generalism, vulnerability and trophic position within the food web. We found an upward expansion of species at all elevations, which was not even for all taxonomic groups and trophic positions. At low and intermediate elevations, predator : prey mass ratios were significantly reduced. Expanders were larger, had fewer predators and were, in general, more specialists. Our study shows that elevation range expansions as climate warms have important and predictable impacts on the structure and size distribution of food webs across space.     

Biodiversity, ecosystem functioning and food webs in fresh waters: assembling the jigsaw puzzle

1. Dramatic advances have been made recently in the study of biodiversity–ecosystem functioning (B-EF) relations and food web ecology. These fields are now starting to converge, and this fusion has the potential to improve our understanding of how environmental stressors modulate ecosystem processes and the supply of 'goods and services'.
2. Food web structure and dynamics can exert particularly strong influences on B-EF relations in fresh waters, as consumer–resource interactions (e.g. trophic cascades) are often more important than horizontal interactions within trophic levels. For instance, many freshwater food webs are size structured, with large organisms tending to occupy the higher trophic levels and often exerting powerful effects on ecosystem processes. However, because they are also vulnerable to perturbations, non-random losses of these large taxa can alter both food web structure and ecosystem functioning profoundly.
3. Recently, the focus of food web research has shifted away from exploring patterns, towards developing an understanding of processes (e.g. quantifying fluxes of individuals, biomass, energy, nutrients) and how the two interact. Many of the best-characterized food webs are from fresh waters, and these ecosystems are now being used to address some of the shortcomings of earlier B-EF studies. I have identified several key gaps in our current knowledge and highlighted potentially fruitful avenues of future B-EF and food web research.
4. A major challenge for this newly emerging research is to place it within a unified theoretical framework. The application of metabolic theory and ecological stoichiometry may help to achieve this goal by considering biological systems within the constraints imposed upon them by physical and chemical laws.     

Warming alters the size spectrum and shifts the distribution of biomass in freshwater ecosystems

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.     

A cure for the plague of parameters: constraining models of complex population dynamics with allometries

A major goal of ecology is to discover how dynamics and structure of multi-trophic ecological communities are related. This is difficult, because whole-community data are limited and typically comprise only a snapshot of a community instead of a time series of dynamics, and mathematical models of complex system dynamics have a large number of unmeasured parameters and therefore have been only tenuously related to real systems. These are related problems, because long time-series, if they were commonly available, would enable inference of parameters. The resulting ‘plague of parameters’ means most studies of multi-species population dynamics have been very theoretical. Dynamical models parametrized using physiological allometries may offer a partial cure for the plague of parameters, and these models are increasingly used in theoretical studies. However, physiological allometries cannot determine all parameters, and the models have also rarely been directly tested against data. We confronted a model of community dynamics with data from a lake community. Many important empirical patterns were reproducible as outcomes of dynamics, and were not reproducible when parameters did not follow physiological allometries. Results validate the usefulness, when parameters follow physiological allometries, of classic differential-equation models for understanding whole-community dynamics and the structure–dynamics relationship.     

Warming alters the metabolic balance of ecosystems

The carbon cycle modulates climate change, via the regulation of atmospheric CO₂, 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 CO₂ 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 CO₂. 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.     

Linking genes to communities and ecosystems: Daphnia as an ecogenomic model

How do genetic variation and evolutionary change in critical species affect the composition and functioning of populations, communities and ecosystems? Illuminating the links in the causal chain from genes up to ecosystems is a particularly exciting prospect now that the feedbacks between ecological and evolutionary changes are known to be bidirectional. Yet to fully explore phenomena that span multiple levels of the biological hierarchy requires model organisms and systems that feature a comprehensive triad of strong ecological interactions in nature, experimental tractability in diverse contexts and accessibility to modern genomic tools. The water flea Daphnia satisfies these criteria, and genomic approaches capitalizing on the pivotal role Daphnia plays in the functioning of pelagic freshwater food webs will enable investigations of eco-evolutionary dynamics in unprecedented detail. Because its ecology is profoundly influenced by both genetic polymorphism and phenotypic plasticity, Daphnia represents a model system with tremendous potential for developing a mechanistic understanding of the relationship between traits at the genetic, organismal and population levels, and consequences for community and ecosystem dynamics. Here, we highlight the combination of traits and ecological interactions that make Daphnia a definitive model system, focusing on the additional power and capabilities enabled by recent molecular and genomic advances.     

13C and 15N in microarthropods reveal little response of Douglas-fir ecosystems to climate change

Understanding ecosystem carbon (C) and nitrogen (N) cycling under global change requires experiments maintaining natural interactions among soil structure, soil communities, nutrient availability, and plant growth. In model Douglas-fir ecosystems maintained for five growing seasons, elevated temperature and carbon dioxide (CO₂) increased photosynthesis and increased C storage belowground but not aboveground. We hypothesized that interactions between N cycling and C fluxes through two main groups of microbes, mycorrhizal fungi (symbiotic with plants) and saprotrophic fungi (free-living), mediated ecosystem C storage. To quantify proportions of mycorrhizal and saprotrophic fungi, we measured stable isotopes in fungivorous microarthropods that efficiently censused the fungal community. Fungivorous microarthropods consumed on average 35% mycorrhizal fungi and 65% saprotrophic fungi. Elevated temperature decreased C flux through mycorrhizal fungi by 7%, whereas elevated CO₂ increased it by 4%. The dietary proportion of mycorrhizal fungi correlated across treatments with total plant biomass (n= 4, r²= 0.96, P= 0.021), but not with root biomass. This suggests that belowground allocation increased with increasing plant biomass, but that mycorrhizal fungi were stronger sinks for recent photosynthate than roots. Low N content of needles (0.8–1.1%) and A horizon soil (0.11%) coupled with high C : N ratios of A horizon soil (25–26) and litter (36–48) indicated severe N limitation. Elevated temperature treatments increased the saprotrophic decomposition of litter and lowered litter C : N ratios. Because of low N availability of this litter, its decomposition presumably increased N immobilization belowground, thereby restricting soil N availability for both mycorrhizal fungi and plant growth. Although increased photosynthesis with elevated CO₂ increased allocation of C to ectomycorrhizal fungi, it did not benefit plant N status. Most N for plants and soil storage was derived from litter decomposition. N sequestration by mycorrhizal fungi and limited N release during litter decomposition by saprotrophic fungi restricted N supply to plants, thereby constraining plant growth response to the different treatments.     

Linking community size structure and ecosystem functioning using metabolic theory

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.     

Warming increases the proportion of primary production emitted as methane from freshwater mesocosms

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 0.85 eV. 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.     

Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels

Current predictions on species responses to climate change strongly rely on projecting altered environmental conditions on species distributions. However, it is increasingly acknowledged that climate change also influences species interactions. We review and synthesize literature information on biotic interactions and use it to argue that the abundance of species and the direction of selection during climate change vary depending on how their trophic interactions become disrupted. Plant abundance can be controlled by aboveground and belowground multitrophic level interactions with herbivores, pathogens, symbionts and their enemies. We discuss how these interactions may alter during climate change and the resulting species range shifts. We suggest conceptual analogies between species responses to climate warming and exotic species introduced in new ranges. There are also important differences: the herbivores, pathogens and mutualistic symbionts of range-expanding species and their enemies may co-migrate, and the continuous gene flow under climate warming can make adaptation in the expansion zone of range expanders different from that of cross-continental exotic species. We conclude that under climate change, results of altered species interactions may vary, ranging from species becoming rare to disproportionately abundant. Taking these possibilities into account will provide a new perspective on predicting species distribution under climate change.     

Temperature,predator–prey interaction strength and population stability

Warming could strongly stabilize or destabilize populations and food webs by changing the interaction strengths between predators and their prey. Predicting the consequences of warming requires understanding how temperature affects ingestion (energy gain) and metabolism (energy loss). Here, we studied the temperature dependence of metabolism and ingestion in laboratory experiments with terrestrial arthropods (beetles and spiders). From this data, we calculated ingestion efficiencies (ingestion/metabolism) and per capita interaction strengths in the short and long term. Additionally, we investigated if and how body mass changes these temperature dependencies. For both predator groups, warming increased metabolic rates substantially, whereas temperature effects on ingestion rates were weak. Accordingly, the ingestion efficiency (the ratio of ingestion to metabolism) decreased in all treatments. This result has two possible consequences: on the one hand, it suggests that warming of natural ecosystems could increase intrinsic population stability, meaning less fluctuations in population density; on the other hand, decreasing ingestion efficiencies may also lead to higher extinction risks because of starvation. Additionally, predicted long‐term per capita interaction strengths decreased with warming, which suggests an increase in perturbation stability of populations, i.e., a higher probability of returning to the same equilibrium density after a small perturbation. Together, these results suggest that warming has complex and potentially profound effects on predator–prey interactions and food‐web stability.     

Potential consequences of climate change for primary production and fish production in large marine ecosystems

Existing methods to predict the effects of climate change on the biomass and production of marine communities are predicated on modelling the interactions and dynamics of individual species, a very challenging approach when interactions and distributions are changing and little is known about the ecological mechanisms driving the responses of many species. An informative parallel approach is to develop size-based methods. These capture the properties of food webs that describe energy flux and production at a particular size, independent of species'' ecology. We couple a physical–biogeochemical model with a dynamic, size-based food web model to predict the future effects of climate change on fish biomass and production in 11 large regional shelf seas, with and without fishing effects. Changes in potential fish production are shown to most strongly mirror changes in phytoplankton production. We project declines of 30–60% in potential fish production across some important areas of tropical shelf and upwelling seas, most notably in the eastern Indo-Pacific, the northern Humboldt and the North Canary Current. Conversely, in some areas of the high latitude shelf seas, the production of pelagic predators was projected to increase by 28–89%.     

From genes to ecosystems: a synthesis of the effects of plant genetic factors across levels of organization

Using two genetic approaches and seven different plant systems, we present findings from a meta-analysis examining the strength of the effects of plant genetic introgression and genotypic diversity across individual, community and ecosystem levels with the goal of synthesizing the patterns to date. We found that (i) the strength of plant genetic effects can be quite high; however, the overall strength of genetic effects on most response variables declined as the levels of organization increased. (ii) Plant genetic effects varied such that introgression had a greater impact on individual phenotypes than extended effects on arthropods or microbes/fungi. By contrast, the greatest effects of genotypic diversity were on arthropods. (iii) Plant genetic effects were greater on above-ground versus below-ground processes, but there was no difference between terrestrial and aquatic environments. (iv) The strength of the effects of intraspecific genotypic diversity tended to be weaker than interspecific genetic introgression. (v) Although genetic effects generally decline across levels of organization, in some cases they do not, suggesting that specific organisms and/or processes may respond more than others to underlying genetic variation. Because patterns in the overall impacts of introgression and genotypic diversity were generally consistent across diverse study systems and consistent with theoretical expectations, these results provide generality for understanding the extended consequences of plant genetic variation across levels of organization, with evolutionary implications.     

Predicting impacts of Arctic climate change: Past lessons and future challenges

General circulation models predict increases in temperature and precipitation in the Arctic as the result of increases in atmospheric carbon dioxide concentrations. Arctic ecosystems are strongly constrained by temperature, and may be expected to be markedly influenced by climate change. Perturbation experiments have been used to predict how Arctic ecosystems will respond to global climatic change, but these have often simulated individual perturbations (e.g. temperature alone) and have largely been confined to the short Arctic summer. The importance of interactions between global change variables (e.g. CO₂, temperature, precipitation) has rarely been examined, and much experimentation has been short-term. Similarly, very little experimentation has occurred in the winter when General circulation models predict the largest changes in climate will take place. Recent studies have clearly demonstrated that Arctic ecosystems are not dormant during the winter and thus much greater emphasis on experimentation during this period is essential to improve our understanding of how these ecosystems will respond to global change. This, combined with more long-term experimentation, direct observation of natural vegetation change (e.g. at the tundra/taiga boundary) and improvements in model predictions is necessary if we are to understand the future nature and extent of Arctic ecosystems in a changing climate.     

Persistence of high diversity in non-equilibrium ecological communities: implications for modern and fossil ecosystems

Explaining the origin and maintenance of biodiversity is critical for understanding the potential consequences of present-day environmental change on ecological communities, as well as the evolutionary history of ecosystems in the Earth's past. Much effort in theoretical ecology has focused on identifying mechanisms that promote stable coexistence of species at equilibrium. However, in a consumer-resource model of competition along an environmental gradient, high-diversity assemblages have the potential to persist in non-equilibrium states for millions of generations with very little species loss. Species' populations in such competitively accommodated communities show slow drift; if disrupted, they rapidly reorganize into alternative persistent states. Fossil examples of prolonged ecological stability lasting 1-5 Myr punctuated by rapid reorganization (e.g. brachiopods from the Permian Reef of west Texas) suggest that some palaeocommunities represent a record of periodically disrupted transient states rather than stable equilibria. The similarity between the theoretical results reported here and palaeontological data suggests that the maintenance of high-diversity communities, both in the past and present, may reflect long-duration, non-equilibrium transient dynamics. If so, this has implications for the response of such communities to present-day environmental change, as well as for the evolution of lineages in such systems.