Using Food Webs and Metabolic Theory to Monitor, Model, and Manage Atlantic Salmon—A Keystone Species Under Threat

Populations of Atlantic salmon are crashing across most of its natural range: understanding the underlying causes and predicting these collapses in time to intervene effectively are urgent ecological and socioeconomic priorities. Current management techniques rely on phenomenological analyses of demographic population time-series and thus lack a mechanistic understanding of how and why populations may be declining. New multidisciplinary approaches are thus needed to capitalize on the long-term, large-scale population data that are currently scattered across various repositories in multiple countries, as well as marshaling additional data to understand the constraints on the life cycle and how salmon operate within the wider food web. Here, we explore how we might combine data and theory to develop the mechanistic models that we need to predict and manage responses to future change. Although we focus on Atlantic salmon—given the huge data resources that already exist for this species—the general principles developed here could be applied and extended to many other species and ecosystems.

Allometric scaling of RNA abundance from genes to communities

The metabolic theory of ecology (MTE) and growth rate hypothesis (GRH) help explain the mechanistic basis of size (allometry) and temperature dependence on growth rate and whole-body-RNA content in organisms. However, testing RNA allometric scaling with next-generation sequencing is yet to be done. Here, we validated the assumptions of GRH and MTE on messenger RNA and ribosome abundance using mock community metatranscriptome analysis. Our findings highlight that fast-growing smaller species harbor greater RNA abundance per mass of tissue compared with species having larger body sizes and slower growth rates, where allometric slopes for genomic and gene-level RNA abundance range from –⅓ to −1. We found that genome size and body size impose significant constraints in interspecific RNA abundance scaling, while the assumed temperature dependence appeared to be weak. Lastly, allometric scaling integration in community-level models may extend the use of metatranscriptomics as a reliable tool for estimating ecosystem processes.

Long-term experimental evolution decouples size and production costs in Escherichia coli

Body size covaries with population dynamics across lifes domains. Theory holds that metabolism imposes fundamental constraints on the coevolution of size and demography. However, studies of interspecific patterns are confounded by other factors that covary with size and demography, and experimental tests of the causal links remain elusive. Here we leverage a 60,000-generation experiment in which Escherichia coli populations evolved larger cells to examine intraspecific metabolic scaling and correlations with demographic parameters. Metabolic theory successfully predicted the relations among size, metabolism, and maximum population density, with strong support for Damuths law of energy equivalence in this experiment. In contrast, populations of larger cells grew faster than those of smaller cells, contradicting the fundamental assumption that costs of production should increase proportionately with size. The finding that the costs of production are substantially decoupled from size requires re-examining the evolutionary drivers and ecological consequences of biological size more generally.

PAPEL DOS PEIXES NA RECICLAGEM DE NUTRIENTES EM RIACHOS TROPICAIS

Fish can contribute directly and indirectly to nutrient recycling in aquatic environments, affecting community structure and ecosystem processes. Through the excretion of metabolic waste, fish make inorganic nutrients available in the environment that can be used by algae and bacteria. Nitrogen and phosphorus are often limiting nutrients in streams, so fish can be a relevant source of these nutrients. Many factors can influence excretion rates, including diet, body nutrient demand (for reproduction and growth), ontogeny, body size, temperature and other abiotic factors. Currently, two theories propose to explain which factors control excretion rates: 1) The Theory of Ecological Stoichiometry is based on mass balance models and uses the amount of nutrients in the diet and the fish nutrient demand as predictors of excretion rates; and 2) the Metabolic Theory of Ecology that uses body size and temperature as factors that regulate an organism metabolic rates and, thus, its excretion rates. The relative importance of fish as nutrient recyclers in streams varies depending on species intrinsic characteristics and environmental factors. This includes the magnitude of excretion rates from the entire fish community, the nutrient concentration and nutrient input into the stream, the stream nutrient demand and the period of activity and behavior of the fish. For example, species that are abundant in oligotrophic streams have the potential to represent an important source of nutrients. But other peculiarities, such as diet, specific nutrient demands, or migratory behaviors, can make them important sources or sinks of nutrients in a stream. This article reviews studies that address the role of fish as nutrient recyclers and explains the most common techniques used in this type of studies.

Universal allometry from empirical parameters

Allometric settings of population dynamics models are appealing due to their parsimonious nature and broad utility when studying system level effects. Here, we parameterise the size-scaled Rosenzweig-Macarthur ODEs to eliminate prey-mass dependency. We define the functional response term to match experiments, and examine situations where metabolic theory derivations and observation diverge. We produce dynamics consistent with observation. Our parameterisation of the Rosenzweig-Macarthur system is an accurate minimal model across 15+ orders of mass magnitude.

Life-history dynamics: damping time, demographic dispersion and generation time

Transient dynamics are crucial for understanding ecological and life-history dynamics. In this study, we analyze damping time, the time taken by a population to converge to a stable (st)age structure following a perturbation, for over 600 species of animals and plants. We expected damping time to be associated with both generation time Tc and demographic dispersion σ based on previous theoretical work. Surprisingly, we find that damping time (calculated from the population projection matrix) is approximately proportional to Tc across taxa on the log-log scale, regardless of σ. The result suggests that species at the slow end of fast-slow continuum (characterized with long generation time, late maturity, low fecundity) are more vulnerable to external disturbances as they take more time to recover compared to species with fast life-histories. The finding on damping time led us to next examine the relationship between generation time and demographic dispersion. Our result reveals that the two life-history variables are positively correlated on a log-log scale across taxa, implying long generation time promotes demographic dispersion in reproductive events. Finally, we discuss our results in the context of metabolic theory and contribute to existing allometric scaling relationships.

Functionally redundant herbivores: urchin and gastropod grazers respond differently to ocean warming and rising CO2

Future ocean CO2 and temperatures are predicted to increase primary productivity across tropical marine habitats, potentially driving a shift towards algal-dominated systems. However, increased consumption of algae by benthic grazers could potentially counter this shift. Yet, the response of different grazer species to future conditions will be moderated by their physiologies, meaning that they may not be functional equivalents. Here, we experimentally assessed the physiological response of key grazers—the sea urchin Heliocidaris crassispina and 2 gastropod species, Astralium haematragum and Trochus maculatus—to predicted CO2 concentrations (400, 700 and 1000 ppm) and temperature conditions (ambient, +3 and +5°C). In line with metabolic theory, we found that urchin metabolic rate increased at future temperatures regardless of CO2 conditions, with evidence of metabolic acclimation to higher temperatures. The metabolic rate of A. haematragum was depressed only by CO2, whereas T. maculatus initially had elevated metabolic rates at moderate CO2, which were depressed by the combination of the highest CO2 concentration and temperatures. Taxa showed differential survival, with no urchin mortality under any future conditions but substantial mortality of both gastropods under elevated temperatures regardless of CO2 concentration. Importantly, all species had substantially reduced algal consumption in response to elevated CO2, though the urchins only demonstrated an energetic mismatch under combined future CO2 and temperature. Therefore, despite sharing an ecological niche, these key grazers are likely to be differentially affected by future environmental conditions, potentially reducing the strength of ecological compensatory responses depending on the functional redundancy in this grazing community.