The nutrient-load hypothesis: patterns of resource limitation and community structure driven by competition for nutrients and light

Resource competition theory predicts that the outcome of competition for two nutrients depends on the ratio at which these nutrients are supplied. Yet there is considerable debate whether nutrient ratios or absolute nutrient loads determine the species composition of phytoplankton and plant communities. Here we extend the classical resource competition model for two nutrients by including light as additional resource. Our results suggest the nutrient-load hypothesis, which predicts that nutrient ratios determine the species composition in oligotrophic environments, whereas nutrient loads are decisive in eutrophic environments. The underlying mechanism is that nutrient enrichment shifts the species interactions from competition for nutrients to competition for light, which favors the dominance of superior light competitors overshadowing all other species. Intermediate nutrient loads can generate high biodiversity through a fine-grained patchwork of two-species and three-species coexistence equilibria. Depending on the species traits, however, competition for nutrients and light may also produce multiple alternative stable states, suppressing the predictability of the species composition. The nutrient-load hypothesis offers a solution for several discrepancies between classical resource competition theory and field observations, explains why eutrophication often leads to diversity loss, and provides a simple conceptual framework for patterns of biodiversity and community structure observed in nature.     

Stoichiometrically explicit competition between grazers: species replacement, coexistence, and priority effects along resource supply gradients

Assuming key trade-offs among interactors, several models (resource ratio, keystone predation, intraguild predation) predict changes in species composition over resource supply gradients. Ecological stoichiometry could also predict compositional shifts of grazers over gradients of nutrient and light supply through a mechanism involving (mis)matches between elemental body composition of grazers and plants. This hypothesis is explored here using a suite of two-grazer, one-plant models that incorporate three key components: plant production depends on light and nutrients, nutrient content of plants can vary, and homeostatic grazers can be carbon or nutrient limited. The results from this suite closely resemble the classical resource ratio model describing plant competition for two resources. Here, the models predict shifts of grazer composition along resource supply gradients if species trade off competitive abilities for plant carbon and nutrients. Given this trade-off, superior nutrient competitors should dominate low nutrient environments, and superior carbon competitors should dominate high nutrient environments. At intermediate nutrient supply, species can coexist at a stable equilibrium, or alternative stable states emerge, depending on how grazers impact their resources. These results depend on food web architecture, however. For instance, predators can alter or reduce possibilities for stoichiometry-mediated coexistence of grazers.     

Vertical distribution and composition of phytoplankton under the influence of an upper mixed layer

The vertical distribution of phytoplankton is of fundamental importance for the dynamics and structure of aquatic communities. Here, using an advection-reaction-diffusion model, we investigate the distribution and competition of phytoplankton species in a water column, in which inverse resource gradients of light and a nutrient can limit growth of the biomass. This problem poses a challenge for ecologists, as the location of a production layer is not fixed, but rather depends on many internal parameters and environmental factors. In particular, we study the influence of an upper mixed layer (UML) in this system and show that it leads to a variety of dynamic effects: (i) Our model predicts alternative density profiles with a maximum of biomass either within or below the UML, thereby the system may be bistable or the relaxation from an unstable state may require a long-lasting transition. (ii) Reduced mixing in the deep layer can induce oscillations of the biomass; we show that a UML can sustain these oscillations even if the diffusivity is less than the critical mixing for a sinking phytoplankton population. (iii) A UML can strongly modify the outcome of competition between different phytoplankton species, yielding bistability both in the spatial distribution and in the species composition. (iv) A light limited species can obtain a competitive advantage if the diffusivity in the deep layers is reduced below a critical value. This yields a subtle competitive exclusion effect, where the oscillatory states in the deep layers are displaced by steady solutions in the UML. Finally, we present a novel graphical approach for deducing the competition outcome and for the analysis of the role of a UML in aquatic systems.     

Phytoplankton response to a changing climate

Phytoplankton are at the base of aquatic food webs and of global importance for ecosystem functioning and services. The dynamics of these photosynthetic cells are linked to annual fluctuations of temperature, water column mixing, resource availability, and consumption. Climate can modify these environmental factors and alter phytoplankton structure, seasonal dynamics, and taxonomic composition. Here, we review mechanistic links between climate alterations and factors limiting primary production, and highlight studies where climate change has had a clear impact on phytoplankton processes. Climate affects phytoplankton both directly through physiology and indirectly by changing water column stratification and resource availability, mainly nutrients and light, or intensified grazing by heterotrophs. These modifications affect various phytoplankton processes, and a widespread advance in phytoplankton spring bloom timing and changing bloom magnitudes have both been observed. Climate warming also affects phytoplankton species composition and size structure, and favors species traits best adapted to changing conditions associated with climate change. Shifts in phytoplankton can have far-reaching consequences for ecosystem structure and functioning. An improved understanding of the mechanistic links between climate and phytoplankton dynamics is important for predicting climate change impacts on aquatic ecosystems.     

The species composition of Antarctic phytoplankton interpreted in terms of Tilman's competition theory

Summary An attempt was made, to test for the impact of resource competition on Antarctic marine phytoplankton. According to theory, species composition near competitive equilibrium should be determined by the ratios of limiting resources. Enrichment bioassays identified silicon and nitrogen as limiting nutrients for some of the most important phytoplankton species during early austral summer in the region near the Antarctic Peninsula. Together with the generally acknowledged limiting resource light, this gave three meaningful ratios of essential resources (Si:N, Si:light, N:light) and one ratio of substitutable resources (NO₃:NH₄). Phytoplankton species assemblages were found to be well separated by the ratios of the essential resources and by mixing depth. Nine out of 12 individual species were found to be separated along at least one of the gradients of resource ratios. Where comparison with competition experiments was available, predicted and realized distributions of species were compatible.     

Temporal organization of phytoplankton communities linked to physical forcing

The performance of individual phytoplankton species is strongly governed by the thermal stratification’s impact on vertical mixing within the water column, which alters the position of phytoplankton relative to nutrients and light. The present study documents shifts in phytoplankton structure and vertical positioning that have accompanied intensified long-term stratification in a natural ecosystem. Ordination analysis is used to extract gradients in phytoplankton composition in Lake Tahoe, an extremely nutrient-poor lake, over a 23-year period of records. Community structure in the 1980s was associated most strongly with resource availability (low nitrogen to phosphorus ratios, deeper euphotic zone depth), while intensified stratification dominated the phytoplankton structure since the late 1990s. Within diatoms, small-sized cells increased with reduced mixing, suggesting that suppressed turbulence provides them with a competitive advantage over large-sized cells. Among the morphologically diverse chlorophytes, filamentous and coenobial forms were favored under intensified stratification. The selection for small-sized diatoms is accompanied by a shoaling trend in their vertical position in the water column. In contrast, the motile flagellates displayed a deeper vertical positioning in recent years, indicating that optimal growth conditions shifted likely due to reduced upwelling of nutrients. As the thermal stratification of lakes and oceans is strongly linked to climate variables, the present study confirms that climate warming will alter phytoplankton structure and dynamics largely through effects on nutrient availability and sinking velocities. Intensified stratification should favor the expansion of small-sized species and species with the capability of buoyancy regulation, which may alter primary productivity, nutrient recycling, and higher trophic productivity. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Resource storage and competition with spatial and temporal variation in resource availability

This study addresses interspecific competition for a nutrient resource that is stored within individuals in habitats with both temporal and spatial variation. In such environments, population structure is induced by the mixture at any location of individuals with different amounts of stored nutrient, acquired elsewhere in the habitat. Focusing on phytoplankton competing for phosphorus in a partially mixed water column, an individual-based Lagrangian model is used to represent this population structure, and partial differential equations that approximate competitive dynamics are constructed by averaging over this population structure. Although the approximation model overestimates the benefit of resource storage to competitive fitness, both approaches predict that species with high storage capacity are favored by periodic resource pulses that are short lived but large in magnitude. Such storage specialists can competitively exclude or coexist with species that have advantages in maximal nutrient uptake and population growth rates. For very infrequent resource pulses, competitive dynamics become close to neutral. Thus, persistence of diverse species that are differentiated in nutrient storage and uptake capabilities is favored by resource pulses occurring with periods that are many times the average generation time of competitors.     

The vertical distribution of phytoplankton in stratified water columns

What determines the vertical distribution of phytoplankton in different aquatic environments remains an open question. To address this question, we develop a model to explore how phytoplankton respond through growth and movement to opposing resource gradients and different mixing conditions. We assume stratification creates a well-mixed surface layer on top of a poorly mixed deep layer and nutrients are supplied from multiple depth-dependent sources. Intraspecific competition leads to a unique strategic equilibrium for phytoplankton, which allows us to classify the distinct vertical distributions that can exist. Biomass can occur as a benthic layer (BL), a deep chlorophyll maximum (DCM), or in the mixed layer (ML), or as a combination of BL+ML or DCM+ML. The ML biomass can be limited by nutrients, light, or both. We predict how the vertical distribution, relative resource limitation, and biomass of phytoplankton will change across environmental gradients. We parameterized our model to represent potentially light and phosphorus limited freshwater lakes, but the model is applicable to a broad range of vertically stratified systems. Increasing nutrient input from the sediments or to the mixed layer increases light limitation, shifts phytoplankton towards the surface, and increases total biomass. Increasing background light attenuation increases light limitation, shifts the phytoplankton towards the surface, and generally decreases total biomass. Increasing mixed layer depth increases, decreases, or has no effect on light limitation and total biomass. Our model is able to replicate the diverse vertical distributions observed in nature and explain what underlying mechanisms drive these distributions.     

Exotic grasses and feces deposition by an exotic herbivore combine to reduce the relative abundance of native forbs

Increased resource availability can facilitate establishment of exotic plant species, especially when coincident with propagule supply. Following establishment, increased resource availability may also facilitate the spread of exotic plant species if it enhances their competitive abilities relative to native species. Exotic Canada geese (Branta canadensis) introduce both exotic grass seed and nutrients to an endangered plant community on the Gulf Islands of southwestern British Columbia, Canada. I used greenhouse experiments to assess the competitive advantage of the exotic grasses relative to native and exotic forbs in this community and to test the impacts of nutrient addition from goose feces on competitive outcomes. I grew experimental communities varying in their proportion of forbs versus exotic grasses, and added goose feces as a nutrient source. I found that both native and exotic forbs produced significantly more biomass in competition with conspecifics than in competition with the grasses, and that the proportional abundance of two out of three native forbs was lowest in the combined presence of exotic grasses and nutrient addition. In a second experiment, I found that in monoculture all species of forbs and grasses showed equal growth responses to nutrients. The exotic species did not convert additional nutrients into additional biomass at a higher rate, but did germinate earlier and grow larger than the native species regardless of nutrient availability. This suggests that the exotic species may have achieved their competitive advantage partly by pre-empting resources in community mixtures. Small and late-germinating native forbs may be particularly vulnerable to competitive suppression from exotic grasses and forbs and may be at an even greater disadvantage if their competitors are benefiting from early access to additional nutrients. In combination, the input of exotic propagules and additional nutrients by nesting geese may compromise efforts to maintain native community composition in this system.     

Decoding Size Distribution Patterns in Marine and Transitional Water Phytoplankton: From Community to Species Level

Understanding the mechanisms of phytoplankton community assembly is a fundamental issue of aquatic ecology. Here, we use field data from transitional (e.g. coastal lagoons) and coastal water environments to decode patterns of phytoplankton size distribution into organization and adaptive mechanisms. Transitional waters are characterized by higher resource availability and shallower well-mixed water column than coastal marine environments. Differences in physico-chemical regime between the two environments have been hypothesized to exert contrasting selective pressures on phytoplankton cell morphology (size and shape). We tested the hypothesis focusing on resource availability (nutrients and light) and mixed layer depth as ecological axes that define ecological niches of phytoplankton. We report fundamental differences in size distributions of marine and freshwater diatoms, with transitional water phytoplankton significantly smaller and with higher surface to volume ratio than marine species. Here, we hypothesize that mixing condition affecting size-dependent sinking may drive phytoplankton size and shape distributions. The interplay between shallow mixed layer depth and frequent and complete mixing of transitional waters may likely increase the competitive advantage of small phytoplankton limiting large cell fitness. The nutrient regime appears to explain the size distribution within both marine and transitional water environments, while it seem does not explain the pattern observed across the two environments. In addition, difference in light availability across the two environments appear do not explain the occurrence of asymmetric size distribution at each hierarchical level. We hypothesize that such competitive equilibria and adaptive strategies in resource exploitation may drive by organism’s behavior which exploring patch resources in transitional and marine phytoplankton communities.     

A modelling investigation of the distribution of stratification and phytoplankton abundance in the Irish Sea

Thermal stratification and phytoplankton abundance are modelledon a 5 km grid covering the Irish Sea. The water column is approximatedby three layers. The top layer is uniformly mixed by wind stirringand the bottom by tidal energy, while linear gradients can occurin the middle layer. The model is forced with hourly meteorologicaldata and mean tidal energies. Primary production is representedby a model with a single nutrient and a single phytoplanktonpopulation. The results from the model show good agreement withdata collected on a Ministry of Agriculture, Fisheries and Food(MAFF) cruise in May 1992 and with historical data. When advectionis included, driven by depth-averaged currents, the surfacetemperature patterns are improved but bottom temperatures indeep water are raised and high concentrations of chlorophyllare carried offshore from coastal regions. This indicates alimitation of using depth-averaged currents and a need to accountfor differences in phytoplankton species composition in coastaland offshore waters. Calculations demonstrate the importanceof salinity variations to stratification and phytoplankton growth.Smoothing the wind mixing energy has the effect of delayingthe onset of the spring bloom in areas where wind mixing issignificant. Removing the diurnal cycle of solar heating alsodelays the spring bloom. The chlorophyll gradient in the middlelayer has a large impact on the response of the model to short-termvariability in the meteorological forcings.     

The influence of turbidity on net phytoplankton photosynthesis in some Irish lakes

SUMMARY. An important influence on gross photosynthetic rates per unit area is the success with which phytoplankton competes for the available light with non-algal suspended material and dissolved organic compounds. Using a range of Irish lakes, with euphotic zones varying between 0.7 and 20 m and with chlorophyll-α values between 1 and 860 mg m⁻³, the effect on gross rates of photosynthesis is analysed for changes in the balance between the factors contributing to light attenuation. Net values per unit area are also likely to be modified in well-mixed systems as the ratio of light to dark regions in the water column are altered with changes in light penetration. Depth gradients in dark respiration are reported for L. Neagh which vary according to previous light history and nutrient stress. Possible cases of restraint on phytoplankton growth are discussed for optically deep situations.     

Impact of resource availability on species composition and diversity in freshwater nematodes

This study investigates the long-term effects of resource availability in a freshwater nematode community. We carried out a mesocosm experiment where natural nematode communities were exposed to nutrient addition/depletion over 2 years. Compared to the nutrient-addition treatment, species richness and diversity were strongly reduced upon nutrient depletion. The functional group of bacterial feeders particularly suffered severely from nutrient depletion. The decrease in diversity of bacterial feeders was linked to reduced species richness and diversity of large omnivorous species, as predicted by trophic-dynamic models. Tilmans (1976) statement, that under low nutrient levels the best competitor dominates the system, was applicable in our system. Upon nutrient depletion, resource depletion led to a monoculture of 1 small bacterial feeder, but even after 2 years of resource depletion, up to 16 species still coexisted. Our results provide strong evidence that freshwater nematode systems can be regulated by nutrient competition.     

Competition, traits and resource depletion in plant communities

Although of primary importance to explain plant community structure, general relationships between plant traits, resource depletion and competitive outcomes remain to be quantified across species. Here, we used a comparative approach to test whether instantaneous measurements of plant traits can capture both the amount of resources depleted under plant cover over time (competitive effect) and the way competitors perceived this resource depletion (competitive response). We performed a large competition experiment in which phytometers from a single grass species were transplanted within 18 different monocultures grown in a common-garden experiment, with a time-integrative quantification of light and water depletion over the phytometers’ growing season. Resource-capturing traits were measured on both phytometers (competitive response traits) and monocultures (competitive effect traits). The total amounts of depleted light and water availabilities over the season strongly differed among monocultures; they were best estimated by instantaneous measurements of height and rooting depth, respectively, performed when either light or water became limiting. Specific leaf area and leaf water potential, two competitive response traits measured at the leaf level, were good predictors of changes in phytometer performance under competition, and reflected the amount of light and water, respectively, perceived by plants throughout their lifespan. Our results demonstrated the relevance of instantaneous measures of plant traits as indicators of resource depletion over time, validating the trait-based approach for competition ecology. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Harmful algal blooms of allelopathic microalgal species: The role of eutrophication

The ability of certain harmful algal species to produce and release chemicals that inhibit the growth of co-occurring phytoplankton species, here considered as allelopathy, is closely associated with competition for limiting nutrient resources. Many phytoplankton cells are known to release elevated amounts of organic compounds under nutrient limitation. Eutrophication alters the nitrogen-to-phosphorus balance and, when nutrient availability is unbalanced, nutrient limitation may result. Algal species that can compete successfully for available growth-limiting nutrient(s) have the potential to become dominant and form blooms. The stress conditions imposed by the shifted nutrient supply ratios can, in some algae, stimulate production of allelochemicals that inhibit potential competitors. Thus, under cultural eutrophication, altered nutrient (N, P) ratios and limiting nutrient supplies can stimulate increased production of allelochemicals, including toxins, by some algal species and accentuate the adverse effects of these substances on other algae. Future investigation on the characterization of the chemical compounds involved in the allelopathic process are needed to advance the study of the mode of action of phytoplankton allelochemicals.     

Field and experimental evidence for competition's role in phenotypic divergence

Resource competition has long been viewed as a major cause of phenotypic divergence within and between species. Theory predicts that divergence arises because natural selection favors individuals that are phenotypically dissimilar from their competitors. Yet, there are few conclusive tests of this key prediction. Drawing on data from both natural populations and a controlled experiment, this paper presents such a test in tadpoles of two species of spadefoot toads (Spea bombifrons and S. multiplicata). These two species show exaggerated divergence in trophic morphology where they are found together (mixed-species ponds) but not where each is found alone (pure-species ponds), suggesting that they have undergone ecological character displacement. Moreover, in pure-species ponds, both species exhibit resource polymorphism. Using body size as a proxy for fitness, we found that in pure-species ponds disruptive selection favors extreme trophic phenotypes in both species, suggesting that intraspecific competition for food promotes resource polymorphism. In mixed-species ponds, by contrast, we found that trophic morphology was subject to stabilizing selection in S. multiplicata and directional selection in S. bombifrons. A controlled experiment revealed that the more similar an S. multiplicata was to its S. bombifrons tankmate in resource use, the worse was its performance. These results indicate that S. multiplicata individuals that differ from S. bombifrons would be selectively favored in competition. Our data therefore demonstrate how resource competition between phenotypically similar individuals can drive divergence between them. Moreover, our results indicate that how competition contributes to such divergence may be influenced not only by the degree to which competitors overlap in resource use, but also by the abundance and quality of resources. Finally, our finding that competitively mediated disruptive selection may promote resource polymorphism has potentially important implications for understanding how populations evolve in response to heterospecific competitors. In particular, once a population evolves resource polymorphism, it may be more prone to undergo ecological character displacement.     

The use of outdoor phytoplankton continuous cultures to analyse factors influencing species selection

Natural phytoplankton populations have been grown in outdoor continuous cultures at three dilution rates (D = 0.5, 0.25, and 0.1 · day^?1) under nitrogen (N) or silicon (Si) limitation and two light intensities. At a high specific nutrient flux (high dilution rate) under N limitation an assemblage of primarily small, fast growing centric diatoms such as Skeletonema costatum (Grev.) Cleve and Chaetoceros spp. dominated with a low percentage of flagellates. At a low specific nutrient flux, a mixture of larger, slower growing centric diatoms, small flagellates, and pennate diatoms was obtained. Similar trends were observed under silicate limitation. Decreasing the light intensity at the lowest dilution rate selected for an assemblage similar to that observed at the high dilution rate and high light intensity.The results of these competition experiments suggest that specific nutrient flux (dilution rate) is an important factor in determining between group dominance (e.g., centric and pennate diatoms and small flagellates). Successful competitors representing broad phytoplankton groups can be arranged along a resource gradient of specific nutrient flux (dilution rate), with groups such as centric and pennate diatoms, represented as high and medium flux species, respectively.     

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.     

Competition intensity at local versus regional spatial scales

Studies of competition intensity over natural (i.e. topographic) gradients often contradict the results from studies where artificial (i.e. fertilizer) gradients have been used. Why should the type of gradient matter? To explore the possibilities, we performed experiments to measure competition intensity experienced by tree seedlings from grass competitors across a natural resource gradient, and simultaneously across artificial soil nutrient (fertiliser) gradients. We measured various functional traits (i.e. specific leaf area, leaf area, leaf nitrogen content, δ¹⁵N, δ¹³C, RGR) to gain mechanistic insight into the nature of competition across these gradients. Competition intensity increased with increasing resource availability, unequivocally at the local scale (i.e. with fertilizer application) but not at the regional scale (i.e. across the natural productivity gradient). Our measurements of plant traits were generally consistent with measurements of competition intensity, and demonstrate that competition occurs even when resource levels are low. Competition mainly acted to reduce the growth of Eucalyptus seedlings. Functional (physiological) traits in the Eucalyptus seedlings were not strongly affected by competitors, with the possible exception of δ¹⁵N, which may effectively integrate information on soil nutrient, moisture and leaf processes.     

Phytoplankton dynamics in relation to connectivity,flow dynamics and resource availability—the case of a large,lowland river,the Hungarian Tisza

Large lowland rivers with sufficient hydrological storage capacity are capable of supporting primary production, but the dynamics of the advecting phytoplankton is poorly understood. Our study aimed at exploring how longitudinal versus lateral connectivity, flow dynamics versus resource availability and continuous versus discontinuous environmental gradients shaped the species composition of phytoplankton. Samples were taken from February to October 2000 along the Hungarian Tisza River (HTR) and in its main tributaries. Longitudinal and seasonal patterns were related to resources (light and nutrients) availability and flow dynamics derived from a 1D hydrodynamic model. The HTR was autotrophic during the study period, but tributary input considerably exceeded net autochtonous production. The Szamos River was the major source of both phytoplankton and nutrients in the HTR. Chryso- and euglenophytes were flushed into the main river from floodplain oxbows during high discharge. Imported algae experienced discontinuity in environmental gradients when entering the main river. The merged impact areas of two dams (IAD) that separate the two large meandering patches of the HTR disrupted the longitudinal profiles of both physico-chemical variables and attributes of algal assemblages (biomass, species composition, richness, similarity between adjacent sampling sites). Hydraulic storage along the IAD selectively favoured the recruitment of cryptophytes that, however, could not compensate for the enhanced sedimentation of diatoms in terms of biomass. Although the meandering patches presented several small-scale differences in major environmental gradients, both patches supported the growth of planktonic diatoms. Changes in algal biomass were decoupled from nutrient availability. We conclude that various measures must be applied in various lowland rivers within the same catchment to control their trophic status as a component of the ‘good ecological status’ defined in the Water Framework Directive.