A case for an active eukaryotic marine biosphere during the Proterozoic era.

The microfossil record demonstrates the presence of eukaryotic organisms in the marine ecosystem by about 1,700 million years ago (Ma). Despite this, steranes, a biomarker indicator of eukaryotic organisms, do not appear in the rock record until about 780 Ma in what is known as the "rise of algae." Before this, it is argued that eukaryotes were minor ecosystem members, with prokaryotes dominating both primary production and ecosystem dynamics. In this view, the rise of algae was possibly sparked by increased nutrient availability supplying the higher nutrient requirements of eukaryotic algae. Here, we challenge this view. We use a size-based ecosystem model to show that the size distribution of preserved eukaryotic microfossils from 1,700 Ma and onward required an active eukaryote ecosystem complete with phototrophy, osmotrophy, phagotrophy, and mixotrophy. Model results suggest that eukaryotes accounted for one-half or more of the living biomass, with eukaryotic algae contributing to about one-half of total marine primary production. These ecosystems lived with deep-water phosphate levels of at least 10% of modern levels. The general lack of steranes in the pre-780-Ma rock record could be a result of poor preservation.

Deriving Population Scaling Rules from Individual-Level Metabolism and Life History Traits.

AbstractIndividual metabolism generally scales with body mass with an exponent around 3/4. From dimensional arguments it follows that maximum population growth rate (rmax) scales with a -1/4 exponent. However, the dimensional argument implicitly assumes that offspring size is proportional to adult size. Here, we calculate rmax from metabolic scaling at the level of individuals within size-structured populations while explicitly accounting for offspring size. We identify four general patterns of how rmax scales with adult mass based on four empirical life history patterns employed by groups of species. These life history patterns are determined by how traits of somatic growth rate and/or offspring mass relate to adult mass. One life history pattern-constant adult-to-offspring mass ratio and somatic growth rate independent of adult mass-leads to the classic -1/4 scaling of rmax. The other three life history patterns either lead to nonmetabolic population growth scaling with adult mass or do not follow a power-law relationship at all. Using life history data on five marine taxa and terrestrial mammals, we identify species groups that belong to one of each case. We predict that elasmobranchs, copepods, and mammals follow standard -1/4 power-law scaling, whereas teleost fish and bivalves do not have a pure power-law scaling. Our work highlights how taxa may deviate from the classic -1/4 metabolic scaling pattern of maximum population growth. The approach is generic and can be applied to any taxa.

Co-adaptive behavior of interacting populations in a habitat selection game significantly impacts ecosystem functions.

Individuals of different interacting populations often adjust to prevailing conditions by changing their behavior simultaneously, with consequences for trophic relationships throughout the system. While we now have a good theoretical understanding of how individuals adjust their behavior, the population dynamical consequences of co-adaptive behaviors are rarely described. Further, mechanistic descriptions of ecosystem functions are based on population models that seldom take behavior into account. Here, we present a model that combines the population dynamics and adaptive behavior of organisms of two populations simultaneously. We explore how the Nash equilibrium of a system - i.e. the optimal behavior of its constituent organisms - can shape population dynamics, and conversely how population dynamics impact the Nash equilibrium of the system. We illustrate this for the case of diel vertical migration (DVM), the daily movement of marine organisms between food-depleted but safe dark depths and more risky nutrition-rich surface waters. DVM represents the archetypal example of populations choosing between a foraging arena (the upper sunlit ocean) and a refuge (the dark depths). We show that population sizes at equilibrium are significantly different if organisms can adapt their behavior, and that optimal DVM behaviors within the community vary significantly if population dynamics are considered. As a consequence, ecosystem function estimates such as trophic transfer efficiency and vertical carbon export differ greatly when fitness seeking behavior is included. Ignoring the role of behavior in multi-trophic population modeling can potentially lead to inaccurate predictions of population biomasses and ecosystem functions.

Spatial drivers of instability in marine size-spectrum ecosystems.

Size-spectrum models are a recent class of models describing the dynamics of a whole community based on a description of individual organisms. The models are motivated by marine ecosystems where they cover the size range from multicellular plankton to the largest fish. We propose to extend the size-spectrum model with spatial components. The spatial dynamics is governed by a random motion and a directed movement in the direction of increased fitness, which we call 'fitness-taxis'. We use the model to explore whether spatial irregularities of marine communities can occur due to the internal dynamics of predator-prey interactions and spatial movements. This corresponds to a pattern-formation analysis generalized to an entire ecosystem but is not limited to one prey and one predator population. The analyses take the form of Fourier analysis and numerical experiments. Results show that diffusion always stabilizes the equilibrium but fitness-taxis destabilizes it, leading to non-stationary spatially inhomogeneous population densities, which are travelling in size. However, there is a strong asymmetry between fitness-induced destabilizing effects and diffusion-induced stabilizing effects with the latter dominating over the former. These findings reveal that fitness taxis acts as a possible mechanism behind pattern formations in ecosystems with high diversity of organism sizes, which can drive the emergence of spatial heterogeneity even in a spatially homogeneous environment.

Body Size, Light Intensity, and Nutrient Supply Determine Plankton Stoichiometry in Mixotrophic Plankton Food Webs.

Trophic strategy determines stoichiometry of plankton. In general, heterotrophic zooplankton have lower and more stable C∶N and C∶P ratios than photoautotrophic phytoplankton, whereas mixotrophic protists, which consume prey and photosynthesize, have stoichiometry between zooplankton and phytoplankton. As trophic strategies change with cell size, body size may be a key trait influencing eukaryotic plankton stoichiometry. However, the relationship between body size and stoichiometry remains unclear. Here we measured plankton size-fractionated C∶N ratios under different intensities of light and nutrient supply in subtropical freshwater and marine systems. We found a unimodal body size-C∶N ratio pattern, with a maximum C∶N ratio at ∼50 µm diameter in marine and freshwater systems. Moreover, the variation in C∶N ratios is explained mainly by body size, followed by light intensity and nutrient concentration. To investigate the mechanisms behind this unimodal pattern, we constructed a size-based plankton food web model in which the trophic strategy and C∶N ratio are an emerging result. Our model simulations reproduce the unimodal pattern with a C∶N ratio of photoautotrophs ≤50 µm increasing with body size due to increase of photosynthetic carbon, whereas C∶N ratios of organisms >50 µm decrease with size due to decreasing photoautotrophic but increasing heterotrophic uptake. Based on our field observations and simulation, we extend the classic "light-nutrient" theory that determines plankton C∶N ratio to include body size and trophic strategy dependency. We conclude that body size and size-dependent uptake of resources (light, nutrients, and prey) determine plankton stoichiometry at various light and nutrient supplies.

Trait-based food web model reveals the underlying mechanisms of biodiversity-ecosystem functioning relationships.

The concept of biodiversity-ecosystem functioning (BEF) has been studied over the last three decades using experiments, theoretical models and more recently observational data. While theoretical models revealed that species richness is the best metric summarizing ecosystem functioning, it is clear that ecosystem function is explained by other variables besides species richness. Additionally, theoretical models rarely focus on more than one ecosystem function, limiting ecosystem functioning to biomass or production. There is a lack of theoretical background to verify how other components of biodiversity and species interactions support ecosystem functioning. Here, using simulations from a food web model based on a community assembly process and a trait-based approach, we test how species biodiversity, food web structure and predator-prey interactions determine several ecosystem functions (biomass, metabolism, production and productivity). Our results demonstrate that the relationship between species richness and ecosystem functioning depends on the type of ecosystem function considered and the importance of diversity and food web structure differs across functions. Particularly, we show that dominance plays a major role in determining the level of biomass, and it is at least as important as the number of species. We find that dominance occurs in the food web when species do not experience strong predation. By manipulating the structure of the food web, we show that species using a wider trait space (generalist communities) result in more connected food webs and generally reach the same level of functioning with less species. The model shows the importance of generalist versus specialist communities on BEF relationships, and as such, empirical studies should focus on quantifying the importance of diet/habitat use on ecosystem functioning. Our study provides a better understanding of BEF underlying mechanisms and generates research hypotheses that can be considered and tested in observational studies. We recommend that studies investigating links between biodiversity and ecosystem functions should include metrics of dominance, species composition, trophic structure and possibly environmental trait space. We also advise that more effort should be made into calculating several ecosystem functions and properties with data from natural multitrophic systems.

Nutrient affinity, half-saturation constants and the cost of toxin production in dinoflagellates.

The two parameters of the Michaelis-Menten model, the maximum uptake rate and the half-saturation constant, are not stochastically independent, and the half-saturation constant is not a measure of nutrient affinity, as commonly assumed. Failure to realise their interdependence and mechanistic interpretation may lead to the emergence of false trade-offs.

Trophic Strategies of Unicellular Plankton.

Unicellular plankton employ trophic strategies ranging from pure photoautotrophs over mixotrophy to obligate heterotrophs (phagotrophs), with cell sizes from 10-8 to 1 µg C. A full understanding of how trophic strategy and cell size depend on resource environment and predation is lacking. To this end, we develop and calibrate a trait-based model for unicellular planktonic organisms characterized by four traits: cell size and investments in phototrophy, nutrient uptake, and phagotrophy. We use the model to predict how optimal trophic strategies depend on cell size under various environmental conditions, including seasonal succession. We identify two mixotrophic strategies: generalist mixotrophs investing in all three investment traits and obligate mixotrophs investing only in phototrophy and phagotrophy. We formulate two conjectures: (1) most cells are limited by organic carbon; however, small unicellulars are colimited by organic carbon and nutrients, and only large photoautotrophs and smaller mixotrophs are nutrient limited; (2) trophic strategy is bottom-up selected by the environment, while optimal size is top-down selected by predation. The focus on cell size and trophic strategies facilitates general insights into the strategies of a broad class of organisms in the size range from micrometers to millimeters that dominate the primary and secondary production of the world's oceans.

Food-web dynamics under climate change.

Climate change affects ecological communities through its impact on the physiological performance of individuals. However, the population dynamic of species well inside their thermal niche is also determined by competitors, prey and predators, in addition to being influenced by temperature changes. We use a trait-based food-web model to examine how the interplay between the direct physiological effects from temperature and the indirect effects due to changing interactions between populations shapes the ecological consequences of climate change for populations and for entire communities. Our simulations illustrate how isolated communities deteriorate as populations go extinct when the environment moves outside the species' thermal niches. High-trophic-level species are most vulnerable, while the ecosystem function of lower trophic levels is less impacted. Open communities can compensate for the loss of ecosystem function by invasions of new species. Individual populations show complex responses largely uncorrelated with the direct impact of temperature change on physiology. Such complex responses are particularly evident during extinction and invasion events of other species, where climatically well-adapted species may be brought to extinction by the changed food-web topology. Our results highlight that the impact of climate change on specific populations is largely unpredictable, and apparently well-adapted species may be severely impacted.

Adult and offspring size in the ocean: a database of size metrics and conversion factors.

The purpose of this dataset was to compile adult and offspring size estimates for marine organisms. Adult and offspring size estimates of 408 species were compiled from the literature covering >17 orders of magnitude in body mass and including Cephalopoda (ink fish), Cnidaria ("jelly" fish), Crustaceans, Ctenophora (comb jellies), Elasmobranchii (cartilaginous fish), Mammalia (mammals), Sagittoidea (arrow worms) and Teleost (i.e., Actinopterygii, bony fish). Individual size estimates were converted to standardized size estimates (carbon weight, g) to allow for among-group comparisons. This required a number of size estimates to be converted and a compilation of conversion factors obtained from the literature are also presented.

Correction: Spectroscopic characteristics of the OSIRIS near-backscattering crystal analyser spectrometer on the ISIS pulsed neutron source.

Correction for 'Spectroscopic characteristics of the OSIRIS near-backscattering crystal analyser spectrometer on the ISIS pulsed neutron source' by Mark T. F. Telling et al., Phys. Chem. Chem. Phys., 2005, 7, 1255-1261.

Size structures sensory hierarchy in ocean life.

Survival in aquatic environments requires organisms to have effective means of collecting information from their surroundings through various sensing strategies. In this study, we explore how sensing mode and range depend on body size. We find a hierarchy of sensing modes determined by body size. With increasing body size, a larger battery of modes becomes available (chemosensing, mechanosensing, vision, hearing and echolocation, in that order) while the sensing range also increases. This size-dependent hierarchy and the transitions between primary sensory modes are explained on the grounds of limiting factors set by physiology and the physical laws governing signal generation, transmission and reception. We theoretically predict the body size limits for various sensory modes, which align well with size ranges found in literature. The treatise of all ocean life, from unicellular organisms to whales, demonstrates how body size determines available sensing modes, and thereby acts as a major structuring factor of aquatic life.

Four types of interference competition and their impacts on the ecology and evolution of size-structured populations and communities.

We investigate how four types of interference competition - which alternatively affect foraging, metabolism, survival, and reproduction - impact the ecology and evolution of size-structured populations. Even though all four types of interference competition reduce population biomass, interference competition at intermediate intensity sometimes significantly increases the abundance of adult individuals and the population׳s reproduction rate. We find that foraging and metabolic interference evolutionarily favor smaller maturation size when interference is weak and larger maturation size when interference is strong. The evolutionary response to survival interference and reproductive interference is always larger maturation size. We also investigate how the four types of interference competition impact the evolutionary dynamics and resultant diversity and trophic structure of size-structured communities. Like other types of trait-mediated competition, all four types of interference competition can induce disruptive selection and thus promote initial diversification. Even though foraging interference and reproductive interference are more potent in promoting initial diversification, they catalyze the formation of diverse communities with complex trophic structure only at high levels of interference intensity. By contrast, survival interference does so already at intermediate levels, while reproductive interference can only support relatively smaller communities with simpler trophic structure. Taken together, our results show how the type and intensity of interference competition jointly affect coexistence patterns in structured population models.

Trade-offs between objectives for ecosystem management of fisheries.

The strategic objectives for fisheries, which are enshrined in international conventions, are to maintain or restore stocks to produce maximum sustainable yield (MSY) and to implement the ecosystem approach, requiring that interactions between species be taken into account and conservation constraints be respected. While the yield and conservation aims are, to some extent, compatible when a fishery for a single species is considered, species interactions entail that MSY for a species depends on the species with which it interacts, and the yield and conservation objectives therefore conflict when an ecosystem approach to fisheries management is required. We applied a conceptual size- and trait-based model to clarify and resolve these issues by determining the fishing pattern that maximizes the total yield of an entire fish community in terms of catch biomass or economic rent under acceptable conservation constraints. Our results indicate that the eradication of large, predatory fish species results in a potential maximum catch at least twice as high as if conservation constraints are imposed. However, such a large catch could only be achieved at a cost of forgone rent; maximum rent extracts less than half of the potential maximum catch mass. When a conservation constraint is applied, catch can be maximized at negligible cost in forgone rent, compared with maximizing rent. Maximization of rent is the objective that comes closest to respecting conservation concerns.

Capital versus income breeding in a seasonal environment.

The allocation of resources between growth, storage, and reproduction is a key trade-off in the life-history strategies of organisms. A central dichotomy is between capital breeders and income breeders. Capital breeders build reserves that allow them to spawn at a later time independently of food availability, while income breeders allocate ingested food directly to reproduction. Motivated by copepod studies, we use an analytical model to compare the fitness of income with capital breeding in a deterministic seasonal environment. We analyze how the fitness of breeding strategies depend on feeding season duration and size at maturity. Small capital breeders perform better in short feeding seasons but fall behind larger individuals when the length of the feeding season increases. Income breeding favors smaller individuals as their short generation time allows for multiple generations within a year and thereby achieve a high annual growth rate, outcompeting capital breeders in long feeding seasons. Therefore, we expect to find a dominance of small income breeders in temperate waters, while large capital breeders should dominate high latitudes where the spring is short and intense. This pattern is evident in nature, particularly in organisms with a generation time of a year or less.

The consequences of balanced harvesting of fish communities.

Balanced harvesting, where species or individuals are exploited in accordance with their productivity, has been proposed as a way to minimize the effects of fishing on marine fish communities and ecosystems. This calls for a thorough examination of the consequences balanced harvesting has on fish community structure and yield. We use a size- and trait-based model that resolves individual interactions through competition and predation to compare balanced harvesting with traditional selective harvesting, which protects juvenile fish from fishing. Four different exploitation patterns, generated by combining selective or unselective harvesting with balanced or unbalanced fishing, are compared. We find that unselective balanced fishing, where individuals are exploited in proportion to their productivity, produces a slightly larger total maximum sustainable yield than the other exploitation patterns and, for a given yield, the least change in the relative biomass composition of the fish community. Because fishing reduces competition, predation and cannibalism within the community, the total maximum sustainable yield is achieved at high exploitation rates. The yield from unselective balanced fishing is dominated by small individuals, whereas selective fishing produces a much higher proportion of large individuals in the yield. Although unselective balanced fishing is predicted to produce the highest total maximum sustainable yield and the lowest impact on trophic structure, it is effectively a fishery predominantly targeting small forage fish.

A metacommunity perspective on source­sink dynamics and management: the Baltic Sea as a case study.

The degree to which metapopulation processes influence fish stock dynamics is a largely unresolved issue in marine science and management, especially for highly mobile species such as Atlantic cod (Gadus morhua) and herring (Clupea harengus). The Baltic Sea comprises a heterogeneous oceanographic environment that structures the spatial and temporal distribution of the dominant species cod, herring, and sprat (Sprattus sprattus). Despite local differences, the stocks are traditionally managed as homogeneous units. Here, we present a metacommunity-perspective on source­sink dynamics of Baltic Sea fish stocks by using a spatially disaggregated statistical food web model. The model is fitted to area-specific time series of multiple abiotic and biotic variables using state-space methods. Our analysis reveals pronounced net fluxes between areas, indicative of source­sink dynamics, as well as area-specific differences in species interactions (i.e., density dependence, competition, and predator­prey) and the degree of fishing and climate impact on survival and recruitment. Furthermore, model simulations show that decreasing exploitation pressure in the source area for cod (without reallocating fishing effort) produces an increase in neighboring sink habitats, but a decline of prey species in response to increased predation. Our approach provides valuable insight concerning metacommunity-structuring of marine fish and may serve as an important tool for implementing sustainable management strategies under the ecosystem approach to marine and fisheries management.

Impact of increased fishing on long-term sequestration of carbon by cephalopods.

Fish and other metazoans play a major role in long-term sequestration of carbon in the oceans through the biological carbon pump1. Recent studies estimate that fish can release about 1,200 to 1,500 million metric tons of carbon per year (MtC year-1) in the oceans through feces production, respiration, and deadfalls, with mesopelagic fish playing a major role1,2. This carbon remains sequestered (stored) in the ocean for a period that largely depends on the depth at which it is released. Cephalopods (squid, octopus, and cuttlefish) have the potential to sequester carbon more effectively than fish because they grow on average five times faster than fish3,4 and they die after reproducing at an early age4,5 (usually 1-2 years), after which their carcasses sink rapidly to the sea floor6. Deadfall of carcasses is particularly important for long-term sequestration because it rapidly transports carbon to depths where residence times are longest1,6. We estimate that cephalopod carcasses transfer 11-22 MtC to the seafloor globally. While cephalopods represent less than 5% of global fisheries catch7, fishing extirpates about 0.36 MtC year-1 of cephalopod carbon that could otherwise have sunk to the seafloor, about half as much as that of fishing large fish8.

Mixoplankton and mixotrophy: future research priorities.

Phago-mixotrophy, the combination of photoautotrophy and phagotrophy in mixoplankton, organisms that can combine both trophic strategies, have gained increasing attention over the past decade. It is now recognized that a substantial number of protistan plankton species engage in phago-mixotrophy to obtain nutrients for growth and reproduction under a range of environmental conditions. Unfortunately, our current understanding of mixoplankton in aquatic systems significantly lags behind our understanding of zooplankton and phytoplankton, limiting our ability to fully comprehend the role of mixoplankton (and phago-mixotrophy) in the plankton food web and biogeochemical cycling. Here, we put forward five research directions that we believe will lead to major advancement in the field: (i) evolution: understanding mixotrophy in the context of the evolutionary transition from phagotrophy to photoautotrophy; (ii) traits and trade-offs: identifying the key traits and trade-offs constraining mixotrophic metabolisms; (iii) biogeography: large-scale patterns of mixoplankton distribution; (iv) biogeochemistry and trophic transfer: understanding mixoplankton as conduits of nutrients and energy; and (v) in situ methods: improving the identification of in situ mixoplankton and their phago-mixotrophic activity.