How to estimate community energy flux? A comparison of approaches reveals that size-abundance trade-offs alter the scaling of community energy flux.

Size and metabolism are highly correlated, so that community energy flux might be predicted from size distributions alone. However, the accuracy of predictions based on interspecific energy-size relationships relative to approaches not based on size distributions is unknown. We compare six approaches to predict energy flux in phytoplankton communities across succession: assuming a constant energy use among species (per cell or unit biomass), using energy-size interspecific scaling relationships and species-specific rates (both with or without accounting for density effects). Except for the per cell approach, all others explained some variation in energy flux but their accuracy varied considerably. Surprisingly, the best approach overall was based on mean biomass-specific rates, followed by the most complex (species-specific rates with density). We show that biomass-specific rates alone predict community energy flux because the allometric scaling of energy use with size measured for species in isolation does not reflect the isometric scaling of these species in communities. We also find energy equivalence throughout succession, even when communities are not at carrying capacity. Finally, we discuss that species assembly can alter energy-size relationships, and that metabolic suppression in response to density might drive the allometry of community energy flux as biomass accumulates.

Conspecific chemical cues drive density-dependent metabolic suppression independently of resource intake.

Within species, individuals of the same size can vary substantially in their metabolic rate. One source of variation in metabolism is conspecific density - individuals in denser populations may have lower metabolism than those in sparser populations. However, the mechanisms through which conspecifics drive metabolic suppression remain unclear. Although food competition is a potential driver, other density-mediated factors could act independently or in combination to drive metabolic suppression, but these drivers have rarely been investigated. We used sessile marine invertebrates to test how food availability interacts with oxygen availability, water flow and chemical cues to affect metabolism. We show that conspecific chemical cues induce metabolic suppression independently of food and this metabolic reduction is associated with the downregulation of physiological processes rather than feeding activity. Conspecific cues should be considered when predicting metabolic variation and competitive outcomes as they are an important, but underexplored, source of variation in metabolic traits.

Testing MacArthur's minimisation principle: do communities minimise energy wastage during succession?

Robert MacArthur developed a theory of community assembly based on competition. By incorporating energy flow, MacArthur's theory allows for predictions of community function. A key prediction is that communities minimise energy wastage over time, but this minimisation is a trade-off between two conflicting processes: exploiting food resources, and maintaining low metabolism and mortality. Despite its simplicity and elegance, MacArthur's principle has not been tested empirically despite having long fascinated theoreticians. We used a combination of field chronosequence experiments and laboratory assays to estimate how the energy wastage of a community changes during succession. We found that older successional stages wasted more energy in maintenance, but there was no clear pattern in how communities of different age exploited food resources. We identify several reasons for why MacArthur's original theory may need modification and new avenues to further explore community efficiency, an understudied component of ecosystem functioning.

Does energy flux predict density-dependence? An empirical field test.

Changes in population density alter the availability, acquisition, and expenditure of resources by individuals, and consequently their contribution to the flux of energy in a system. While both negative and positive density-dependence have been well studied in natural populations, we are yet to estimate the underlying energy flows that generate these patterns and the ambivalent effects of density make prediction difficult. Ultimately, density-dependence should emerge from the effects of conspecifics on rates of energy intake (feeding) and expenditure (metabolism) at the organismal level, thus determining the discretionary energy available for growth. Using a model system of colonial marine invertebrates, we measured feeding and metabolic rates across a range of population densities to calculate how discretionary energy per colony changes with density and test whether this energy predicts observed patterns in organismal size across densities. We found that both feeding and metabolic rates decline with density but that feeding declines faster, and that this discrepancy is the source of density-dependent reductions in individual growth. Importantly, we could predict the size of our focal organisms after eight weeks in the field based on our estimates of energy intake and expenditure. The effects of density on both energy intake and expenditure overwhelmed the effects of body size; even though higher density populations had smaller colonies (with higher mass-specific biological rates), density effects meant that these smaller colonies had lower mass-specific rates overall. Thus, to predict the contribution of organisms to the flux of energy in populations, it seems necessary not only to quantify how rates of energy intake and expenditure scale with body size, but also how they scale with density given that this ecological constraint can be a stronger driver of energy use than the physiological constraint of body size.

Climate-driven disparities among ecological interactions threaten kelp forest persistence.

The combination of ocean warming and acidification brings an uncertain future to kelp forests that occupy the warmest parts of their range. These forests are not only subject to the direct negative effects of ocean climate change, but also to a combination of unknown indirect effects associated with changing ecological landscapes. Here, we used mesocosm experiments to test the direct effects of ocean warming and acidification on kelp biomass and photosynthetic health, as well as climate-driven disparities in indirect effects involving key consumers (urchins and rock lobsters) and competitors (algal turf). Elevated water temperature directly reduced kelp biomass, while their turf-forming competitors expanded in response to ocean acidification and declining kelp canopy. Elevated temperatures also increased growth of urchins and, concurrently, the rate at which they thinned kelp canopy. Rock lobsters, which are renowned for keeping urchin populations in check, indirectly intensified negative pressures on kelp by reducing their consumption of urchins in response to elevated temperature. Overall, these results suggest that kelp forests situated towards the low-latitude margins of their distribution will need to adapt to ocean warming in order to persist in the future. What is less certain is how such adaptation in kelps can occur in the face of intensifying consumptive (via ocean warming) and competitive (via ocean acidification) pressures that affect key ecological interactions associated with their persistence. If such indirect effects counter adaptation to changing climate, they may erode the stability of kelp forests and increase the probability of regime shifts from complex habitat-forming species to more simple habitats dominated by algal turfs.

Organismal homeostasis buffers the effects of abiotic change on community dynamics.

The problem of linking fine-scale processes to broad-scale patterns remains a central challenge of ecology. As rates of abiotic change intensify, there is a critical need to understand how individual responses aggregate to generate compensatory dynamics that stabilize community processes. Notably, while local and global resource enhancement (e.g., nutrient and CO2 release) can reverse dominance relationship between key species (e.g., shifts from naturally kelp-dominated to turf-dominated systems), herbivores can counter these shifts by consuming the additional productivity of competing species (e.g., turfs). Here, we test whether consumer plasticity in energy intake to maintain growth in varying environments can underpin changes in consumption that buffer varying levels of productivity. In response to carbon and nutrient enrichment, herbivores increased consumption of higher-quality food, which acted as a buffer against enhanced production, while maintaining organismal processes across varying abiotic conditions (i.e., growth). These results not only suggest plasticity in feeding behavior, but also in energy acquisition and utilization to maintain organismal processes. Such plasticity may not only underpin organismal homeostasis, but also compensatory dynamics that emerge from the aggregate of these responses to buffer change in community processes.

Trophic compensation reinforces resistance: herbivory absorbs the increasing effects of multiple disturbances.

Disturbance often results in small changes in community structure, but the probability of transitioning to contrasting states increases when multiple disturbances combine. Nevertheless, we have limited insights into the mechanisms that stabilise communities, particularly how perturbations can be absorbed without restructuring (i.e. resistance). Here, we expand the concept of compensatory dynamics to include countervailing mechanisms that absorb disturbances through trophic interactions. By definition, 'compensation' occurs if a specific disturbance stimulates a proportional countervailing response that eliminates its otherwise unchecked effect. We show that the compounding effects of disturbances from local to global scales (i.e. local canopy-loss, eutrophication, ocean acidification) increasingly promote the expansion of weedy species, but that this response is countered by a proportional increase in grazing. Finally, we explore the relatively unrecognised role of compensatory effects, which are likely to maintain the resistance of communities to disturbance more deeply than current thinking allows.

Metabolic evolution in response to interspecific competition in a eukaryote.

Competition drives rapid evolution, which, in turn, alters the trajectory of ecological communities. These eco-evolutionary dynamics are increasingly well-appreciated, but we lack a mechanistic framework for identifying the types of traits that will evolve and their trajectories. Metabolic theory offers explicit predictions for how competition should shape the (co)evolution of metabolism and size, but these are untested, particularly in eukaryotes. We use experimental evolution of a eukaryotic microalga to examine how metabolism, size, and demography coevolve under inter- and intraspecific competition. We find that the focal species evolves in accordance with the predictions of metabolic theory, reducing metabolic costs and maximizing population carrying capacity via changes in cell size. The smaller-evolved cells initially had lower population growth rates, as expected from their hyper-allometric metabolic scaling, but longer-term evolution yielded important departures from theory: we observed improvements in both population growth rate and carrying capacity. The evasion of this trade-off arose due to the rapid evolution of metabolic plasticity. Lineages exposed to competition evolved more labile metabolisms that tracked resource availability more effectively than lineages that were competition-free. That metabolic evolution can occur is unsurprising, but our finding that metabolic plasticity also co-evolves rapidly is new. Metabolic theory provides a powerful theoretical basis for predicting the eco-evolutionary responses to changing resource regimes driven by global change. Metabolic theory needs also to be updated to incorporate the effects of metabolic plasticity on the link between metabolism and demography, as this likely plays an underappreciated role in mediating eco-evolutionary dynamics of competition.

Genome Size Affects Fitness in the Eukaryotic Alga Dunaliella tertiolecta.

Genome size is tightly coupled to morphology, ecology, and evolution among species [1-5], with one of the best-known patterns being the relationship between cell size and genome size [6, 7]. Classic theories, such as the "selfish DNA hypothesis," posit that accumulating redundant DNA has fitness costs but that larger cells can tolerate larger genomes, leading to a positive relationship between cell size and genome size [8, 9]. Yet the evidence for fitness costs associated with relatively larger genomes remains circumstantial. Here, we estimated the relationships between genome size, cell size, energy fluxes, and fitness across 72 independent lineages in a eukaryotic phytoplankton. Lineages with relatively smaller genomes had higher fitness, in terms of both maximum growth rate and total biovolume reached at carrying capacity, but paradoxically, they also had lower energy fluxes than lineages with relative larger genomes. We then explored the evolutionary trajectories of absolute genome size over 100 generations and across a 10-fold change in cell size. Despite consistent directional selection across all lineages, genome size decreased by 11% in lineages with absolutely larger genomes but showed little evolution in lineages with absolutely smaller genomes, implying a lower absolute limit in genome size. Our results suggest that the positive relationship between cell size and genome size in nature may be the product of conflicting evolutionary pressures, on the one hand, to minimize redundant DNA and maximize performance-as theory predicts-but also to maintain a minimum level of essential function. VIDEO ABSTRACT.

Community efficiency during succession: a test of MacArthur's minimization principle in phytoplankton communities.

Robert MacArthur's niche theory makes explicit predictions on how community function should change over time in a competitive community. A key prediction is that succession progressively minimizes the energy wasted by a community, but this minimization is a trade-off between energy losses from unutilised resources and costs of maintenance. By predicting how competition determines community efficiency over time MacArthur's theory may inform on the impacts of disturbance on community function and invasion risk. We provide a rare test of this theory using phytoplankton communities, and find that older communities wasted less energy than younger ones but that the reduction in energy wastage was not monotonic over time. While community structure followed consistent and clear trajectories, community function was more idiosyncratic among adjoining successional stages and driven by total community biomass rather than species composition. Our results suggest that subtle shifts in successional sequence can alter community efficiency and these effects determine community function independently of individual species membership. We conclude that, at least in phytoplankton communities, general trends in community function are predictable over time accordingly to MacArthur's theory. Tests of MacArthur's minimization principle across very different systems should be a priority given the potential of this theory to inform on the functional properties of communities.

Resisting regime-shifts: the stabilising effect of compensatory processes.

Ecologists seem predisposed to studying change because we are intuitively interested in dynamic systems, including their vulnerability to human disturbance. We contrast this disposition with the value of studying processes that work against change. Although powerful, processes that counter disturbance often go unexplored because they yield no observable community change. This stability results from compensatory processes which are initiated by disturbance; these adjust in proportion to the strength of the disturbance to prevent community change. By recognising such buffering processes, we might also learn to recognise the early warning signals of community shifts which are notoriously difficult to predict because communities often show little to no change before their tipping point is reached.