Anthony I. Dell

Systematic variation in the temperature dependence of physiological and ecological traits

To understand the effects of temperature on biological systems, we compile, organize, and analyze a database of 1,072 thermal responses for microbes, plants, and animals. The unprecedented diversity of traits (n = 112), species (n = 309), body sizes (15 orders of magnitude), and habitats (all major biomes) in our database allows us to quantify novel features of the temperature response of biological traits. In particular, analysis of the rising component of within-species (intraspecific) responses reveals that 87% are fit well by the Boltzmann–Arrhenius model. The mean activation energy for these rises is 0.66 ± 0.05 eV, similar to the reported across-species (interspecific) value of 0.65 eV. However, systematic variation in the distribution of rise activation energies is evident, including previously unrecognized right skewness around a median of 0.55 eV. This skewness exists across levels of organization, taxa, trophic groups, and habitats, and it is partially explained by prey having increased trait performance at lower temperatures relative to predators, suggesting a thermal version of the life-dinner principle—stronger selection on running for your life than running for your dinner. For unimodal responses, habitat (marine, freshwater, and terrestrial) largely explains the mean temperature at which trait values are optimal but not variation around the mean. The distribution of activation energies for trait falls has a mean of 1.15 ± 0.39 eV (significantly higher than rises) and is also right-skewed. Our results highlight generalities and deviations in the thermal response of biological traits and help to provide a basis to predict better how biological systems, from cells to communities, respond to temperature change.

Automated image-based tracking and its application in ecology

The behavior of individuals determines the strength and outcome of ecological interactions, which drive population, community, and ecosystem organization. Bio-logging, such as telemetry and animal-borne imaging, provides essential individual viewpoints, tracks, and life histories, but requires capture of individuals and is often impractical to scale. Recent developments in automated image-based tracking offers opportunities to remotely quantify and understand individual behavior at scales and resolutions not previously possible, providing an essential supplement to other tracking methodologies in ecology. Automated image-based tracking should continue to advance the field of ecology by enabling better understanding of the linkages between individual and higher-level ecological processes, via high-throughput quantitative analysis of complex ecological patterns and processes across scales, including analysis of environmental drivers.

Dimensionality of consumer search space drives trophic interaction strengths

Trophic interactions govern biomass fluxes in ecosystems, and stability in food webs. Knowledge of how trophic interaction strengths are affected by differences among habitats is crucial for understanding variation in ecological systems. Here we show how substantial variation in consumption-rate data, and hence trophic interaction strengths, arises because consumers tend to encounter resources more frequently in three dimensions (3D) (for example, arboreal and pelagic zones) than two dimensions (2D) (for example, terrestrial and benthic zones). By combining new theory with extensive data (376 species, with body masses ranging from 5.24 × 10−14 kg to 800 kg), we find that consumption rates scale sublinearly with consumer body mass (exponent of approximately 0.85) for 2D interactions, but superlinearly (exponent of approximately 1.06) for 3D interactions. These results contradict the currently widespread assumption of a single exponent (of approximately 0.75) in consumer–resource and food-web research. Further analysis of 2,929 consumer–resource interactions shows that dimensionality of consumer search space is probably a major driver of species coexistence, and the stability and abundance of populations.

A bioenergetic framework for the temperature dependence of trophic interactions

Changing temperature can substantially shift ecological communities by altering the strength and stability of trophic interactions. Because many ecological rates are constrained by temperature, new approaches are required to understand how simultaneous changes in multiple rates alter the relative performance of species and their trophic interactions. We develop an energetic approach to identify the relationship between biomass fluxes and standing biomass across trophic levels. Our approach links ecological rates and trophic dynamics to measure temperature-dependent changes to the strength of trophic interactions and determine how these changes alter food web stability. It accomplishes this by using biomass as a common energetic currency and isolating three temperature-dependent processes that are common to all consumer-resource interactions: biomass accumulation of the resource, resource consumption and consumer mortality. Using this framework, we clarify when and how temperature alters consumer to resource biomass ratios, equilibrium resilience, consumer variability, extinction risk and transient vs. equilibrium dynamics. Finally, we characterise key asymmetries in species responses to temperature that produce these distinct dynamic behaviours and identify when they are likely to emerge. Overall, our framework provides a mechanistic and more unified understanding of the temperature dependence of trophic dynamics in terms of ecological rates, biomass ratios and stability.

The Body Size Dependence of Trophic Cascades

Trophic cascades are indirect positive effects of predators on resources via control of intermediate consumers. Larger-bodied predators appear to induce stronger trophic cascades (a greater rebound of resource density toward carrying capacity), but how this happens is unknown because we lack a clear depiction of how the strength of trophic cascades is determined. Using consumer resource models, we first show that the strength of a trophic cascade has an upper limit set by the interaction strength between the basal trophic group and its consumer and that this limit is approached as the interaction strength between the consumer and its predator increases. We then express the strength of a trophic cascade explicitly in terms of predator body size and use two independent parameter sets to calculate how the strength of a trophic cascade depends on predator size. Both parameter sets predict a positive effect of predator size on the strength of a trophic cascade, driven mostly by the body size dependence of the interaction strength between the first two trophic levels. Our results support previous empirical findings and suggest that the loss of larger predators will have greater consequences on trophic control and biomass structure in food webs than the loss of smaller predators.

Metabolic theory predicts whole-ecosystem properties

Significance A theory is presented which shows how the metabolism of individual organisms controls the flow of carbon through ecosystems. The theory synthesizes top-down, ecosystem-level and bottom-up, organism-level approaches to ecological energetics and material cycles. The theory predicts a very simple straight-line relationship between residence time of carbon molecules and the ratio of whole-ecosystem biomass to primary productivity. This and additional predictions for total throughfow and recycling are supported by numerical models and data from real ecosystems. The theory provides a powerful way to understand the roles of organisms in ecosystem processes at scales from local habitats to the biosphere. Such an understanding is important for addressing the impacts of human-caused changes in climate, land use, and biodiversity. Understanding the effects of individual organisms on material cycles and energy fluxes within ecosystems is central to predicting the impacts of human-caused changes on climate, land use, and biodiversity. Here we present a theory that integrates metabolic (organism-based bottom-up) and systems (ecosystem-based top-down) approaches to characterize how the metabolism of individuals affects the flows and stores of materials and energy in ecosystems. The theory predicts how the average residence time of carbon molecules, total system throughflow (TST), and amount of recycling vary with the body size and temperature of the organisms and with trophic organization. We evaluate the theory by comparing theoretical predictions with outputs of numerical models designed to simulate diverse ecosystem types and with empirical data for real ecosystems. Although residence times within different ecosystems vary by orders of magnitude—from weeks in warm pelagic oceans with minute phytoplankton producers to centuries in cold forests with large tree producers—as predicted, all ecosystems fall along a single line: residence time increases linearly with slope = 1.0 with the ratio of whole-ecosystem biomass to primary productivity (B/P). TST was affected predominantly by primary productivity and recycling by the transfer of energy from microbial decomposers to animal consumers. The theory provides a robust basis for estimating the flux and storage of energy, carbon, and other materials in terrestrial, marine, and freshwater ecosystems and for quantifying the roles of different kinds of organisms and environments at scales from local ecosystems to the biosphere.

Real versus Artificial Variation in the Thermal Sensitivity of Biological Traits.

Whether the thermal sensitivity of an organism’s traits follows the simple Boltzmann-Arrhenius model remains a contentious issue that centers around consideration of its operational temperature range and whether the sensitivity corresponds to one or a few underlying rate-limiting enzymes. Resolving this issue is crucial, because mechanistic models for temperature dependence of traits are required to predict the biological effects of climate change. Here, by combining theory with data on 1,085 thermal responses from a wide range of traits and organisms, we show that substantial variation in thermal sensitivity (activation energy) estimates can arise simply because of variation in the range of measured temperatures. Furthermore, when thermal responses deviate systematically from the Boltzmann-Arrhenius model, variation in measured temperature ranges across studies can bias estimated activation energy distributions toward higher mean, median, variance, and skewness. Remarkably, this bias alone can yield activation energies that encompass the range expected from biochemical reactions (from ∼0.2 to 1.2 eV), making it difficult to establish whether a single activation energy appropriately captures thermal sensitivity. We provide guidelines and a simple equation for partially correcting for such artifacts. Our results have important implications for understanding the mechanistic basis of thermal responses of biological traits and for accurately modeling effects of variation in thermal sensitivity on responses of individuals, populations, and ecological communities to changing climatic temperatures.

From Metabolic Constraints on Individuals to the Dynamics of Ecosystems

A major challenge in biology is to predict eco-evolutionary dynamics—coupled changes in the ecological dynamics of population density and the evolution of phenotypic (functional trait) variation within and between species—of entire communities and ecosystems. Although mathematical and computational tools allow eco-evolutionary dynamics to be simulated, it is difficult to isolate underlying mechanisms and therefore establish if simulated dynamics are relevant to the real world where the physical environment changes constantly over space and time. We argue that this problem can be resolved, or at least simplified, by first quantifying biomechanical and metabolic constraints on individual organisms, and then scaling these constraints up though ecological interactions to communities. This approach is logical also because environmental fluctuations affect ecosystems through their direct impacts on the fitness of individual organisms. We highlight recent theoretical and empirical advances toward the development of a mechanistic and metabolic-based understanding of trophic interactions and their eco-evolutionary consequences. In particular, we show how a metabolic theory of species interactions can naturally capture the ubiquitous effects of environmental temperature and body size constraints on community dynamics. Nevertheless, this theory is very much a work in progress, and we identify a number of important hurdles that stand in the way of a general, mechanistic understanding of the eco-evolutionary dynamics of aquatic ecosystems.

Intermittent pool beds are permanent cyclic habitats with distinct wet, moist and dry phases.

Recognition that intermittent pools are a single habitat phase of an intermittent pool bed that cycles between aquatic and terrestrial habitat greatly enhances their usefulness for addressing general questions in ecology. The aquatic phase has served as a model system in many ecological studies, because it has distinct habitat boundaries in space and time and is an excellent experimental system, but the aquatic to terrestrial transition and terrestrial phase remain largely unstudied. We conducted a field experiment within six replicate natural intermittent pool beds to explore macroinvertebrate community dynamics during the transition from aquatic to terrestrial habitat and during the terrestrial phase. We monitored and compared macroinvertebrate communities within leaf packs that i) remained wet, ii) underwent drying (i.e., started wet and then dried), and iii) remained dry. Our results show that i) a diverse macroinvertebrate community inhabits all phases of intermittent pool beds, ii) pool drying involves colonization by an assemblage of macroinvertebrates not recorded in permanently terrestrial leaf packs, iii) the community within dried leaf packs remains distinct from that of permanently terrestrial leaf packs for an extended period following drying (possibly until subsequent refilling), and iv) there are likely to be strong spatial and temporal resource linkages between the aquatic and terrestrial communities. The unique environmental characteristics of intermittent pool beds, which repeatedly cycle from aquatic to terrestrial habitat, should continue to make them valuable study systems.

Pawar et al . reply

replying to H. C. Giacomini, B. Shuter, D. T. de Kerckhove & P. A. Abrams 493, 10.1038/nature11829 (2012)Current studies assume that per-capita consumption rates always scale with body mass to an exponent of 0.75. We showed that, contrary to this assumption, consumption rates scale sublinearly (exponent of approximately 0.85) when organisms forage in two dimensions (2D), and superlinearly (exponent of approximately 1.06) when they forage in 3D. Giacomini et al. argue that the superlinear scaling in 3D interactions we observed cannot be reconciled with life-history theory for maximal body size. Consequently, they search for biases in our study that might cause this superlinear scaling. However, their comments do not challenge our central result that consumption rates scale superlinearly in 3D, and significantly more steeply than in 2D. We propose instead that life-history theory may need revision to include interaction dimensionality.