Dynamics of nutrient uptake strategies: lessons from the tortoise and the hare

Many autotrophs vary their allocation to nutrient uptake in response to environmental cues, yet the dynamics of this plasticity are largely unknown. Plasticity dynamics affect the extent of single versus multiple nutrient limitation and thus have implications for plant ecology and biogeochemical cycling. Here we use a model of two essential nutrients cycling through autotrophs and the environment to determine conditions under which different plastic or fixed nutrient uptake strategies are adaptive. Our model includes environment-independent costs of being plastic, environment-dependent costs proportional to the rate of plastic change, and costs of being mismatched to the environment, the last of which is experienced by both fixed and plastic types. In equilibrium environments, environment-independent costs of being plastic select for tortoise strategies—fixed or less plastic types—provided that they are sufficiently close to co-limitation. At intermediate levels of environmental fluctuation forced by periodic nutrient inputs, more hare-like plastic strategies prevail because they remain near co-limitation. However, the fastest is not necessarily the best. The most adaptive strategy is an intermediate level of plasticity that keeps pace with environmental fluctuations, but is not faster. At high levels of environmental fluctuation, the environment-dependent cost of changing rapidly to keep pace with the environment becomes prohibitive and tortoise strategies again dominate. The existence and location of these thresholds depend on plasticity costs and rate, which are largely unknown empirically. These results suggest that the expectations for single nutrient limitation versus co-limitation and therefore biogeochemical cycling and autotroph community dynamics depend on environmental heterogeneity and plasticity costs.     

Dangerous nutrients: Evolution of phytoplankton resource uptake subject to virus attack

Phytoplankton need multiple resources to grow and reproduce (such as nitrogen, phosphorus, and iron), but the receptors through which they acquire resources are, in many cases, the same channels through which viruses attack. Therefore, phytoplankton can face a bottom-up vs. top-down tradeoff in receptor allocation: Optimize resource uptake or minimize virus attack? We investigate this top-down vs. bottom-up tradeoff using an evolutionary ecology model of multiple essential resources, specialist viruses that attack through the resource receptors, and a phytoplankton population that can evolve to alter the fraction of receptors used for each resource/virus type. Without viruses present the singular continuously stable strategy is to allocate receptors such that resources are co-limiting, which also minimizes the equilibrium concentrations of both resources. Only one virus type can be present at equilibrium (because phytoplankton, in this model, are a single resource for viruses), and when a virus type is present, it controls the equilibrium phytoplankton population size. Despite this top-down control on equilibrium densities, bottom-up control determines the evolutionary outcome. Regardless of which virus type is present, the allocation strategy that yields co-limitation between the two resources is continuously stable. This is true even when the virus type attacking through the limiting resource channel is present, even though selection for co-limitation in this case decreases the equilibrium phytoplankton population and does not decrease the equilibrium concentration of the limiting resource. Therefore, although moving toward co-limitation and decreasing the equilibrium concentration of the limiting resource often co-occur in models, it is co-limitation, and not necessarily the lowest equilibrium concentration of the limiting resource, that is the result of selection. This result adds to the growing body of literature suggesting that co-limitation at equilibrium is a winning strategy.     

Opening the black box of plant nutrient uptake under warming predicts global patterns in community biomass and biological carbon storage

The effect of climate change on the amount of carbon stored in the different biological compartments of complex natural communities is relevant for a range of ecosystem functions and services. Temperature‐dependency of many physiological and ecological processes drives this storage capacity. As opposed to other physiological rates, the temperature‐dependence of nutrient uptake by plants has, to date, not been thoroughly investigated and therefore was not explicitly included in food web models. In a meta‐study, we extracted experimental data to establish the temperature‐dependence of the parameters determining plant nutrient uptake. Overall, we found an increase in the maximum uptake rate, as well as the half‐saturation density. As the respiration rates of plants (biomass loss) increase more strongly than the nutrient uptake rates (driving biomass gain under nutrient limitation), our results suggest that warming should decrease plant biomass. We applied these temperature‐dependent nutrient uptake rates by plants to a model of a three‐level food‐chain composed of two nutrients, a plant pool, and an herbivore pool. Having established plant nutrient uptake rates based on real data to replace the previously used assumption of logistic growth, we were able to use realistic natural nutrient deposition rates as the input variables in this model. This mechanistic model approach allowed us to show the quantitative responses of natural communities to realistic fertilization rates for the first time. We ran the model under realistic nutrient supply scenarios based on deposition data from the literature, adding a scenario of anthropogenic fertilization. We found decreases in overall community biomass with increasing temperature, but the intensity of this decrease varied strongly depending on the nutrient supply scenario. Our findings highlight the importance of including other global change drivers besides warming, as they can mediate the temperature impact on changes in global carbon storage and thus biomass‐related ecosystem services.     

Coupling of transcription termination to RNAi

Microbes require multiple essential elements that they acquire from the environment independently. Here we investigate how microbial stoichiometry and uptake rates depend on the conditions in which they grow. We modify a recent model of growth based on a multinutrient extension of the Droop model to allow a trade-off between ability to acquire two essential resources. In a static analysis, we show that the optimal allocation strategy is the one that results in co-limitation by both nutrients. We then add a dynamic equation to model the physiological acclimation uptake rates in changing conditions. This dynamic model predicts that the response of organismal stoichiometry to nutrient supply ratio can vary over time. The response of organismal stoichiometry and growth rate to a nutrient pulse depends on the speed at which cells adapt their uptake rates. In a variable environment, very fast or very slow acclimation may be better strategies than intermediate speed acclimation. We suggest experimental tests of the model and avenues for future model development.     

The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level

Trait-based approaches to community structure are increasingly used in terrestrial ecology. We show that such an approach, augmented by a mechanistic analysis of trade-offs among functional traits, can be successfully used to explain community composition of marine phytoplankton along environmental gradients. Our analysis of literature on major functional traits in phytoplankton, such as parameters of nutrient-dependent growth and uptake, reveals physiological trade-offs in species abilities to acquire and utilize resources. These trade-offs, arising from fundamental relations such as cellular scaling laws and enzyme kinetics, define contrasting ecological strategies of nutrient acquisition. Major groups of marine eukaryotic phytoplankton have adopted distinct strategies with associated traits. These diverse strategies of nutrient utilization can explain the distribution patterns of major functional groups and size classes along nutrient availability gradients.     

A cross-system synthesis of consumer and nutrient resource control on producer biomass

Nutrient availability and herbivory control the biomass of primary producer communities to varying degrees across ecosystems. Ecological theory, individual experiments in many different systems, and system-specific quantitative reviews have suggested that (i) bottom-up control is pervasive but top-down control is more influential in aquatic habitats relative to terrestrial systems and (ii) bottom-up and top-down forces are interdependent, with statistical interactions that synergize or dampen relative influences on producer biomass. We used simple dynamic models to review ecological mechanisms that generate independent vs. interactive responses of community-level biomass. We calibrated these mechanistic predictions with the metrics of factorial meta-analysis and tested their prevalence across freshwater, marine and terrestrial ecosystems with a comprehensive meta-analysis of 191 factorial manipulations of herbivores and nutrients. Our analysis showed that producer community biomass increased with fertilization across all systems, although increases were greatest in freshwater habitats. Herbivore removal generally increased producer biomass in both freshwater and marine systems, but effects were inconsistent on land. With the exception of marine temperate rocky reef systems that showed positive synergism of nutrient enrichment and herbivore removal, experimental studies showed limited support for statistical interactions between nutrient and herbivory treatments on producer biomass. Top-down control of herbivores, compensatory behaviour of multiple herbivore guilds, spatial and temporal heterogeneity of interactions, and herbivore-mediated nutrient recycling may lower the probability of consistent interactive effects on producer biomass. Continuing studies should expand the temporal and spatial scales of experiments, particularly in understudied terrestrial systems; broaden factorial designs to manipulate independently multiple producer resources (e.g. nitrogen, phosphorus, light), multiple herbivore taxa or guilds (e.g. vertebrates and invertebrates) and multiple trophic levels; and - in addition to measuring producer biomass - assess the responses of species diversity, community composition and nutrient status.     

Integrating physiological, ecological and evolutionary change: a Price equation approach

We use a general quantitative framework – the Price equation – to partition phenotypic responses to environmental change into separate physiological, evolutionary and ecological components. We demonstrate how these responses, which potentially occur over different timescales and are usually studied in isolation, can be combined in an additive way; and we discuss the main advantages of doing this. We illustrate our approach using two worked examples, concerning the emergence of toxin resistance within microbial communities, and the estimation of carbon uptake by marine phytoplankton in high-CO₂ environments. We find that this approach allows us to exclude particular mechanistic hypotheses with regard to community-level transformations, and to identify specific instances where appropriate data are lacking. Thus Price's equation provides not only a powerful conceptual aid, but also a means for testing hypotheses and for directing empirical research programmes.     

Evolution of nutrient uptake reveals a trade-off in the ecological stoichiometry of plant-herbivore interactions

Nutrient limitation determines the primary production and species composition of many ecosystems. Here we apply an adaptive dynamics approach to investigate evolution of the ecological stoichiometry of primary producers and its implications for plant-herbivore interactions. The model predicts a trade-off between the competitive ability and grazing susceptibility of primary producers, driven by changes in their nutrient uptake rates. High nutrient uptake rates enhance the competitiveness of primary producers but also increase their nutritional quality for herbivores. This trade-off enables coexistence of nutrient exploiters and grazing avoiders. If herbivores are not selective, evolution favors runaway selection toward high nutrient uptake rates of the primary producers. However, if herbivores select nutritious food, the model predicts an evolutionarily stable strategy with lower nutrient uptake rates. When the model is parameterized for phytoplankton and zooplankton, the evolutionary dynamics result in plant-herbivore oscillations at ecological timescales, especially in environments with high nutrient availability and low selectivity of the herbivores. High herbivore selectivity stabilizes the community dynamics. These model predictions show that evolution permits nonequilibrium dynamics in plant-herbivore communities and shed new light on the evolutionary forces that shape the ecological stoichiometry of primary producers.     

Date of marine annulus formation in Atlantic salmon (Salmo salar) and implications for retrospective growth analyses using scales

Fish scales have increasingly been used to quantify annual and seasonal growth trends and in efforts to relate growth to environmental conditions. Understanding the timing of formation of an annulus (a group of narrowly spaced circuli) is critical when assessing the influence of marine ecosystem conditions on seasonal growth patterns of Atlantic salmon, yet the literature does not provide consistent answers regarding the timing or drivers of marine annulus formation. This study demonstrates a novel method for estimating stock-specific annulus formation timing based on marked individuals with known emigration and return/recovery dates. An equation was applied to estimate the date of annulus completion for Atlantic salmon (Salmo salar) using known dates, number of circuli after the most recent annulus and marine circulus deposition rate. Five marine circulus deposition rate scenarios were tested, some of which accounted for individual, seasonal and age-related variability and others which use previously published marine circulus deposition rates. Based on these results, an argument is presented to reconsider the practice of assigning annulus formation dates to winter solstice in favour of dates estimated by a scenario that accounts for individual, seasonal and age-related variation in circulus deposition. This scenario suggests that annulus formation occurs between mid-February and late March. In this case, the annulus would be formed during the coldest part of the year in the primary overwintering area for North American Atlantic salmon.     

Multiple resource limitation theory applied to herbivorous consumers: Liebig's minimum rule vs. interactive co-limitation

There is growing consensus that the growth of herbivorous consumers is frequently limited by more than one nutrient simultaneously. This understanding, however, is based primarily on theoretical considerations and the applicability of existing concepts of co-limitation has rarely been tested experimentally. Here, we assessed the suitability of two contrasting concepts of resource limitation, i.e. Liebig's minimum rule and the multiple limitation hypothesis, to describe nutrient-dependent growth responses of a freshwater herbivore (Daphnia magna) in a system with two potentially limiting nutrients (cholesterol and eicosapentaenoic acid). The results indicated that these essential nutrients interact, and do not strictly follow Liebig's minimum rule, which consistently overestimates growth at co-limiting conditions and thus is not applicable to describe multiple nutrient limitation of herbivorous consumers. We infer that the outcome of resource-based modelling approaches assessing herbivore population dynamics strongly depends on the applied concept of co-limitation.     

Thermal stratification, nutrient dynamics, and phytoplankton productivity during the onset of spring phytoplankton growth in Lake Baikal, Russia

Lake Baikal, Russian Siberia, was sampled in July 1990 during the period of spring mixing and initiation of thermal stratification. Vertical profiles of temperature, dissolved nutrients (nitrate and soluble reactive phosphorus), phytoplankton biomass, and primary productivity were determined in an eleven-station transect encompassing the entire 636 km length of the lake. Pronounced horizontal variability in hydrodynamic conditions was observed, with the southern region of the lake being strongly thermally stratified while the middle and north basins were largely isothermal through July. The extent of depletion of surface water nutrients, and the magnitude of phytoplankton biomass and productivity, were found to be strongly correlated with the degree of thermal stratification. Horizontal differences likely reflected the contribution of two important factors: variation in the timing of ice-out in different parts of the lake (driving large-scale patterns of thermal stratification and other limnological properties) and localized effects of river inflows that may contribute to the preliminary stabilization of the water column in the face of intense turbulent spring mixing (driving meso-scale patterns). Examination of the relationships between surface water inorganic N and P depletion suggested that during the spring and early summer, phytoplankton growth in unstratified portions of the lake was largely unconstrained by nutrient supplies. As summer progressed, the importance of co-limitation by both N and P became more apparent. Uptake and regeneration rates, measured directly using the stable isotope ¹⁵N, revealed that phytoplankton in stratified portions of the lake relied primarily on NH₄ as their N source. Rates of NH₄ regeneration were in approximate equilibrium with uptake; both processes were dominated by organisms <2 µm. This pattern is similar to that observed for oligotrophic marine systems. Our study underscores the importance of hydrodynamic conditions in influencing patterns of biological productivity and nutrient dynamics that occur in Lake Baikal during its brief growing season.     

Optimizing the complexity of phytoplankton functional group modeling: An allometric approach

Elucidating patterns and mechanisms that shape phytoplankton assemblages is a popular area of research for empirical and theoretical ecologists. Despite the daunting complexity of phytoplankton dynamics, much of our current understanding has been based on simple models describing food-web interactions with few differential equations. Skeptical views in the literature raise concerns about the increasing model complexity and advice to seek parsimony rather than simplicity. To address this controversy (simple versus complex models), we propose the introduction of an extra layer of causality into plankton models by connecting algal processes (maximum growth rates, nutrient kinetics, settling velocities, metabolic rates) with species-specific morphological features (cell volume, surface-to-volume ratio, shape). In this study, we demonstrate the capacity of a size-based plankton model to reproduce observed water quality patterns (phosphate, total phosphorus, nitrate, total ammonia, total nitrogen, chlorophyll a, and total zooplankton biomass) in the Hamilton Harbour, Ontario. Consistent with empirical evidence, our modeling analysis showed that small algal species have a distinct competitive advantage in summer epilimnetic environments across the range of cell volume and nutrient loading conditions examined; especially, when they are characterized by higher optimal temperature for growth. Strong top-down pressure mediated by high zooplankton abundance effectively controls the standing biomass of phytoplankton species that can otherwise realize high growth rates under the conditions typically prevailing in the end-of-summer epilimnetic environments (e.g., higher temperature optima, higher tolerance in low water clarity). Under high zooplankton control, the secondary variations of phytoplankton are modulated by the ambient phosphorus levels and the size-based strategies for resources procurement, such as the regulation of nutrient transport kinetics. By contrast, when the summer algal assemblage is released by the zooplankton grazing, the exceedance of critical phytoplankton biomass levels and the likelihood of harmful algal blooms are determined by the multitude of factors that shape inter-specific competition patterns (e.g., relative abundance of competing species, nutrient uptake kinetics). Our study evaluates the strengths and weaknesses of this approach and identifies future directions that would provide operational models founded upon concepts of allometry.     

Modelling zinc uptake by rice crop using a Barber-Cushman approach

The Barber-Cushman mechanistic nutrient uptake model which has been utilized extensively to describe and predict nutrient uptake by crop plants at different stages of crop growth was evaluated for its ability to predict the Zn uptake by rice seedlings. Uptake of the nutrient is, therefore, determined by the rate of nutrient supply to the root surface by mass flow and diffusion. Inter root competition and time dependent root density are accounted for by soil volume that delivers nutrients. The radii of these cylinders decline with increasing density. Since mass flow and diffusion each supply zinc to the root, the process can be described mathematically using the model of Barber-Cushman (1984). The 11 parameters of the model for the uptake by rice cultivars were measured by established experimental techniques. Zinc uptake at different growth stages predicted by the model was compared to measured zinc uptake by rice cultivars grown on sandy loam soil in a green house. Predicted zinc uptake was significantly correlated with observed uptake r ²=0.99^**. Sensitivity analysis was also used to investigate the impact of changes in soil nutrient supply, root morphological and root uptake kinetic parameters on simulated nutrient uptake. Overall results of sensitivity analysis indicate that the half distance between root axes, rate of root growth and water flux affect the uptake of zinc particularly at their higher values rather than at lower values and DaZn is the most sensitive parameter for zinc uptake at its lower values.     

Temperature–nutrient interactions exacerbate sensitivity to warming in phytoplankton

Temperature and nutrients are fundamental, highly nonlinear drivers of biological processes, but we know little about how they interact to influence growth. This has hampered attempts to model population growth and competition in dynamic environments, which is critical in forecasting species distributions, as well as the diversity and productivity of communities. To address this, we propose a model of population growth that includes a new formulation of the temperature–nutrient interaction and test a novel prediction: that a species’ optimum temperature for growth, T_opt, is a saturating function of nutrient concentration. We find strong support for this prediction in experiments with a marine diatom, Thalassiosira pseudonana: T_opt decreases by 3–6 °C at low nitrogen and phosphorus concentrations. This interaction implies that species are more vulnerable to hot, low‐nutrient conditions than previous models accounted for. Consequently the interaction dramatically alters species’ range limits in the ocean, projected based on current temperature and nitrate levels as well as those forecast for the future. Ranges are smaller not only than projections based on the individual variables, but also than those using a simpler model of temperature–nutrient interactions. Nutrient deprivation is therefore likely to exacerbate environmental warming's effects on communities.     

Effects of multiple timescales of resource supply on the maintenance of species and functional diversity

It is well known that variable resource supply can allow competitors to coexist on a single limiting resource, and this is one mechanism that may explain the maintenance of diversity in paradoxically speciose communities. Ecosystems experience fluctuations in resource supply on a range of timescales, but we have a poor understanding of how multiple frequencies of resource supply affect the maintenance of diversity and community structure. Here we explore this question using a model of phytoplankton competition for a limiting nutrient, parameterized using empirical tradeoffs between rapid growth, nutrient storage capacity and nutrient uptake affinity. Compared to a single frequency of nutrient supply, we find that multiple frequencies of nutrient supply increase functional diversity, by permitting the coexistence of strategies adapted to different frequencies of supply. Species richness is also promoted by multiple modes of nutrient supply, but not as consistently as functional diversity. Although this model is parameterized for phytoplankton, the fundamental dynamics and tradeoffs likely occur in a variety of ecosystems. Our results suggest that the spectrum of temporal variation driving communities should be further investigated in the context of the maintenance of diversity and the functional composition of communities under different environmental regimes.     

Nitrogen Limitation of Pond Ecosystems on the Plains of Eastern Colorado

Primary production in freshwater ecosystems is often limited by the availability of phosphorus (P), nitrogen (N), or a combination of both (NP co-limitation). While N fixation via heterocystous cyanobacteria can supply additional N, no comparable mechanism for P exists; hence P is commonly considered to be the predominant and ultimate limiting nutrient in freshwater ecosystems. However, N limitation can be maintained if P is supplied in stoichiometric excess of N (including N fixation). The main objective of this study was to examine patterns in nutrient limitation across a series of 21 vernal ponds in Eastern Colorado where high P fluxes are common. Across all ponds, water column dissolved inorganic N steadily decreased throughout the growth season due to biological demand while total dissolved P remained stable. The water column dissolved inorganic N to total dissolved P ratios suggested a transition from NP co-limitation to N limitation across the growth season. Periphyton and phytoplankton %C was strongly correlated with %N while %P was assimilated in excess of %N and %C in many ponds. Similarly, in nutrient addition bottle assays algae responded more strongly to N additions (11 out of 18 water bodies) than P additions (2 out of 18 water bodies) and responded most strongly when N and P were added in concert (12 out of 18 water bodies). Of the ponds that responded to nutrient addition, 92% exhibited some sort of N limitation while less than 8% were limited by P alone. Despite multiple lines of evidence for N limitation or NP co-limitation, N fixation rates were uniformly low across most ponds, most likely due to inhibition by water column nitrate. Within this set of 18 water bodies, N limitation or NP co-limitation is widespread due to the combination high anthropogenic P inputs and constrained N fixation rates.     

Differential niche dynamics among major marine invertebrate clades

The degree to which organisms retain their environmental preferences is of utmost importance in predicting their fate in a world of rapid climate change. Notably, marine invertebrates frequently show strong affinities for either carbonate or terrigenous clastic environments. This affinity is due to characteristics of the sediments as well as correlated environmental factors. We assessed the conservatism of substrate affinities of marine invertebrates over geological timescales, and found that niche conservatism is prevalent in the oceans, and largely determined by the strength of initial habitat preference. There is substantial variation in niche conservatism among major clades with corals and sponges being among the most conservative. Time‐series analysis suggests that niche conservatism is enhanced during times of elevated nutrient flux, whereas niche evolution tends to occur after mass extinctions. Niche evolution is not necessarily elevated in genera exhibiting higher turnover in species composition.     

Modeling magnesium,phosphorus and potassium uptake by loblolly pine seedlings using a Barber-Cushman approach

The Barber-Cushman mechanistic nutrient uptake model, which has been utilized extensively to describe and predict nutrient uptake by crop plants, was evaluated for its ability to predict K, Mg, and P uptake by loblolly pine (Pinus taeda L.) seedlings. Sensitivity analyses were also used to investigate the impact of changes in soil nutrient supply, root morphological, and root uptake kinetics parameters on simulated nutrient uptake. Established experimental techniques were utilized to define the 11 parameters needed to model uptake by 1-0 seedlings of K, Mg, and P from a modified A horizon soil (Lilly series). Model predictions of K and P uptake over a 180-d growth period were underestimated by 6 and 11%, respectively. Estimates of Mg uptake were underestimated by 62%. While the level of agreement between predicted and observed K and P values was quite acceptable, analysis of parameter values and results of sensitivity analyses both indicated that the model underestimation of Mg uptake was the result of applying an I_max value developed under relatively low Mg concentration to a situation in which the functional I_max would be much higher due to the dominance of passive versus active uptake. Overall results of sensitivity analyses indicate that under the circumstances investigated, I_max, was the primary variable controlling plant uptake of K, Mg, and P. The dominance of this term over others was due to the relatively high C_li values for all three nutrients. Reducing (-50%) or increasing (+ 100%) other soil supply, root morphological, and remaining root uptake kinetics values did not substantially alter model estimates of nutrient uptake.