An ecosystem model of the phytoplankton competition in the East China Sea, as based on field experiments

An ecological dynamic model for the simulation of two pelagic phytoplankton groups is developed in this article. Model parameters were adjusted and validated based on the light-limited field culture experiments and the mesocosm experiments in the East China Sea (ECS). The calculation comparisons from the proposed model, along with field experiment observations, show that the model simulate the datasets very well, qualitatively and quantitatively. The parameters’ sensitivity analysis indicates that the competition between the diatoms and dinoflagellates is most sensitive to the photosynthetic process, followed by the exudation process of the phytoplankton, while the autolysis and respiration processes of phytoplankton and the grazing and exudation processes of zooplankton can also influence this competition to some extent. The sensitive parameters include: the photosynthetic optimal specific rate; the optimal irradiance and optimal temperature for phytoplankton growth; and the half-saturation constant for limiting nutrients, etc. Results of the sensitivity analysis also indicate that light, temperature and limiting nutrients are the controlling environmental factors for the competition between the diatoms and dinoflagellates in the ECS. In order to explore the effects of light and nutrients on the phytoplankton competition, simulations were carried out with varying light and nutrient conditions. Model simulations suggest that the diatoms favor higher irradiance, lower DIN/PO₄–P ratios, higher SiO₄–Si/DIN ratios and higher nutrient concentrations, as compared to the dinoflagellates. These results support the speculation that the increase in the DIN/PO₄−P ratio and the decrease in the SiO₄–Si/DIN ratio in the ECS may be responsible for the composition change in the functional Harmful Algal Bloom (HAB) groups from the diatom to the dinoflagellate communities over the last two decades. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users. Handling editor: L. Naselli-Flores     

Phytoplankton competition in deep biomass maximum

Resource competition in heterogeneous environments is still an unresolved problem of theoretical ecology. In this article, I analyze competition between two phytoplankton species in a deep water column, where the distributions of main resources (light and a limiting nutrient) have opposing gradients and co-limitation by both resources causes a deep biomass maximum. Assuming that the species have a trade-off in resource requirements and the water column is weakly mixed, I apply the invasion threshold analysis (Ryabov and Blasius, Ecol Lett 14:220–228, 2011) to determine relations between environmental conditions and phytoplankton composition. Although species deplete resources in the interior of the water column, the resource levels at the bottom and surface remain high. As a result, the slope of resources gradients becomes a new crucial factor which, rather than the local resource values, determines the outcome of competition. The value of resource gradients nonlinearly depend on the density of consumers. This leads to complex relationships between environmental parameters and species composition. In particular, it is shown that an increase of both the incident light intensity or bottom nutrient concentrations favors the best light competitors, while an increase of the turbulent mixing or background turbidity favors the best nutrient competitors. These results might be important for prediction of species composition in deep ocean.     

Silicate and the functional geometry of marine phytoplankton

The impact of nutrient supply ratios on the functional geometryof phytoplankton has been studied by means of competition experimentswith phytoplankton communities from the Arabian Sea. Cell lengthand deviation from spherical shape of dominant competitors increasedwith Si:N ratios.Surface:volume ratios were minimal at intermediateSi:N ratios. Grazing by the rotifer Brachionus plicatilis didnot lead to a qualitative shift in the response of geometricproperties to Si:N ratios; however, mean cell lengths increasedwhile surface:volume ratios decreased.     

Near surface nutrient and phytoplankton distribution in the Drake Passage during early December

Summary Nutrient concentrations and phytoplankton species composition in near surface samples were studied along a S-N gradient in the Drake Passage, in early December 1984. Nitrate concentrations were much lower than usually previously reported from circum-Antarctic waters. Comparison of dissolved nutrient concentrations with growth requirements of Antarctic plankton algae suggests potential limitation of at least some species by nitrate or silicate. The taxonomic composition of the phytoplankton in our samples seemed to be partially controlled by competition for limiting nutrients.     

Separating the influence of resource 'availability' from resource 'imbalance' on productivity–diversity relationships

One of the oldest and richest questions in biology is that of how species diversity is related to the availability of resources that limit the productivity of ecosystems. Researchers from a variety of disciplines have pursued this question from at least three different theoretical perspectives. Species energy theory has argued that the summed quantities of all resources influence species richness by controlling population sizes and the probability of stochastic extinction. Resource ratio theory has argued that the imbalance in the supply of two or more resources, relative to the stoichiometric needs of the competitors, can dictate the strength of competition and, in turn, the diversity of coexisting species. In contrast to these, the field of Biodiversity and Ecosystem Functioning has argued that species diversity acts as an independent variable that controls how efficiently limited resources are utilized and converted into new tissue. Here we propose that all three of these fields give necessary, but not sufficient, conditions to explain productivity–diversity relationships (PDR) in nature. However, when taken collectively, these three paradigms suggest that PDR can be explained by interactions among four distinct, non-interchangeable variables: (i) the overall quantity of limiting resources, (ii) the stoichiometric ratios of different limiting resources, (iii) the summed biomass produced by a group of potential competitors and (iv) the richness of co-occurring species in a local competitive community. We detail a new multivariate hypothesis that outlines one way in which these four variables are directly and indirectly related to one another. We show how the predictions of this model can be fit to patterns of covariation relating the richness and biomass of lake phytoplankton to three biologically essential resources (N, P and light) in a large number of Norwegian lakes.     

Effects of resource additions on species richness and ANPP in an alpine meadow community

Aims Theories based on resource additions indicate that plant species richness is mainly determined by the number of limiting resources. However, the individual effects of various limiting resources on species richness and aboveground net primary productivity (ANPP) are less well understood. Here, we analyzed potential linkages between additions of limiting resources, species loss and ANPP increase and further explored the underlying mechanisms.Methods Resources (N, P, K and water) were added in a completely randomized block design to alpine meadow plots in the Qinghai-Tibetan Plateau. Plant aboveground biomass, species composition, mean plant height and light availability were measured in each plot. Regression and analysis of variance were used to analyze the responses of these measures to the different resource-addition treatments.Important findings Species richness decreased with increasing number of added limiting resources, suggesting that plant diversity was apparently determined by the number of limiting resources. Nitrogen was the most important limiting resource affecting species richness, whereas P and K alone had negligible effects. The largest reduction in species richness occurred when all three elements were added in combination. Water played a different role compared with the other limiting resources. Species richness increased when water was added to the treatments with N and P or with N, P and K. The decreases in species richness after resource additions were paralleled by increases in ANPP and decreases in light penetration into the plant canopy, suggesting that increased light competition was responsible for the negative effects of resource additions on plant species richness.     

Increase in Si:N drawdown ratio due to resting spore formation by spring bloom-forming diatoms under Fe- and N-limited conditions in the Oyashio region

Resting spore formation and Si:N drawdown ratios were investigated under iron (Fe)- and nitrogen (N)-limited conditions using a unialgal culture of Thalassiosira nordenskioeldii and natural phytoplankton assemblages during the spring bloom in the Oyashio region. In the unialgal culture of T. nordenskioeldii, 20% and 100% of the cells formed resting spores under Fe- and N-limited conditions, respectively. The Si:N drawdown ratios were 2- and 14-fold higher in Fe- and N-limited conditions, respectively, compared to Fe- and N-sufficient conditions. At the start of the natural phytoplankton incubation, 18 among 47 identified diatom species were known resting spore-forming species. Approximately 15 common diatom species formed resting spores under Fe- and N-limited conditions. During the natural phytoplankton incubation, the percentage of the resting spores increased with time under both Fe- and N-limited conditions, reaching 25% and 40% of total diatom abundance, respectively. The Si:N drawdown ratios significantly increased with an increase in the contribution of resting spores in both the unialgal culture and natural phytoplankton incubations. These results suggest that if the bloom dominated by neritic, resting spore-forming diatom species decline by either Fe- or N-depletion, Si may be utilized preferentially to N in the upper mixed layer due to the formation of heavily silicified resting spores.     

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.     

Temperature‐dependence of minimum resource requirements alters competitive hierarchies in phytoplankton

Resource competition theory is a conceptual framework that provides mechanistic insights into competition and community assembly of species with different resource requirements. However, there has been little exploration of how resource requirements depend on other environmental factors, including temperature. Changes in resource requirements as influenced by environmental temperature would imply that climate warming can alter the outcomes of competition and community assembly. We experimentally demonstrate that environmental temperature alters the minimum light and nitrogen requirements – as well as other growth parameters – of six widespread phytoplankton species from distinct taxonomic groups. We found that species require the most nitrogen at the highest temperatures while light requirements tend to be lowest at intermediate temperatures, although there are substantial interspecific differences in the exact shape of this relationship. We also experimentally parameterize two competition models, which we use to illustrate how temperature, through its effects on species’ traits, alters competitive hierarchies in multispecies assemblages, determining community dynamics. Developing a mechanistic understanding of how temperature influences the ability to compete for limiting resources is a critical step towards improving forecasts of community dynamics under climate warming.     

Dynamics of biomass partitioning in two competing meadow plant species

The optimal allocation theory predicts that growth is allocated between the shoot and the roots so that the uptake of the most limiting resource is increased. Allocation is dynamic due to resource depletion, interaction with competitors, and the allometry of growth. We assessed the effects of intra- and inter-specific competition on growth and resource allocation of the meadow species Ranunculus acris and Agrostis capillaris, grown in environments with high (+) or low (−) availability of light (L) and nutrients (N). We took samples twice a week over the 7 weeks experiment, to follow the changes in root-to-shoot ratios in plants of different sizes, and carried out a larger scale harvest at the end of the experiment. Of all the tested factors, availability of nutrients had the largest effect on the growth rate and shoot-to-root allocation in both species, although both competition and light had significant effects as well. The highest root-to-shoot ratios were measured from the L+N− treatment, and the lowest from the L−N+ treatment, as predicted by the optimal allocation theory. Competition changed resource allocation, but not always toward acquiring the resource that is most limiting to growth. We thus conclude that the greatest variation in shoot-to-root allocation was due to the resource availability and the effects of competition were small, probably due to low density of plants in the experiment.     

Resource Ratios and Phytoplankton Species Composition in a Strongly Stratified Lake

The epilimnetic phytoplankton and its relations to nutrient content in Lake Verevi through the whole vegetation period in 2000 were studied. Lake Verevi (surface 12.6 ha, mean depth 3.6 m, maximum depth 11 m) is a hypertrophic hard-water lake, where the so-called spring meromixis occurs due to an extremely warm spring. Most dissolved nutrients in the epilimnion were low already in spring, and their concentrations were quite stable during the study period. The concentration of total silicon was very low in spring but increased rapidly in summer. Total phosphorus followed the pattern for stratified eutrophic lakes, and total nitrogen was quite high. The stoichiometric N:P ratio fluctuated between 25 and 81. The dynamics of phytoplankton biomass with a spring peak from April to May and a late summer peak from July to August is typical of Estonian eutrophic lakes. Green algae and chrysophytes occurred in the phytoplankton throughout the vegetation period. The spring peak was dominated by diatoms (Synedra ulna and Synedra acus var. angustissima) and the summer peak was caused by Aphanizomenon klebahnii and Ceratium hirundinella. The study showed that in physically stratified systems, the total concentration of limiting resources and plain physical factors (light and temperature) may be more important in the determination of phytoplankton dominants than different resource ratios. A combination of light and temperature optimum, along with nutrient utilization and transport capacity, effectively segregates phytoplankton species and can be used for the explanation of seasonal succession pattern.     

Do nutrient-competition models predict nutrient availabilities in limnetic ecosystems?

Recent theory on resource competition, predicated on the importance of hypothesized trade-offs between minimum requirements for nutrient resources, predicts that there should be negative correlations between the supply rate of major limiting nutrients and the availability of at least some secondary nutrients and/or among the availabilities of different limiting nutrients. However, an analysis of four data sets from large-scale surveys of lakes shows mostly positive correlations among the availabilities and supplies of nutrients. In contrast, a fifth data set, obtained in an area of high acidification, does show several important negative correlations that are consistent with the nutrient competition models. Further analyses suggest two possible explanations for the preponderance of positive correlation. Negative correlations between nutrients and light indicate that an important trade-off among species regulating phytoplankton may involve low light requirements versus low nutrient requirements. The existence of negative correlations in nutrient availabilities in acidic lakes (where herbivory appears less important than in buffered lakes) also suggests that another important trade-off may involve an ability to minimize loss rates (especially due to grazing) versus an overall ability to exploit nutrient resources. Received: 23 February 1996 / Accepted: 30 September 1996     

Effects of nutrient supply and nutrient ratio on diversity–productivity relationships of phytoplankton in the Cau Hai lagoon,Vietnam

Diversity and productivity of primary producers are known to be influenced simultaneously by resource availability and resource ratio, but the relative importance of these two factors differed among studies and so far only entire phytoplankton communities were investigated which might ignore specific nutrient requirements and stoichiometric plasticity of different functional groups. We measured nutrient availability (DIN, total N [TN], total P [TP]), nutrient imbalance (TN:TP, DIN:TP, N:P_seston), species richness, and abundance of the whole phytoplankton community, as well as those specific for cyanobacteria, diatoms, and dinoflagellates in Cau Hai lagoon in Vietnam. We determined the correlation among these variables, using structural equation modeling. The models applied to the whole phytoplankton community indicated that the nutrient availability (particularly TP and DIN) drove variation in phytoplankton abundance and richness, and that abundance also depended on species richness. The models applied to different functional groups differed considerably from the entire community and among each other, and only a part of the models was significant. The relationship between nutrient availability (mainly TP) and abundance was driven by cyanobacteria, and the relationship between nutrient imbalance (only with N:P_seston) and species richness was driven by diatoms. Remarkably, the positive relationship between species richness and abundance, as consistently observed for the whole phytoplankton community, was only observed for one of the three functional groups (diatoms), indicating that resource complementarity occurs particularly among species of different functional groups. Our results emphasized that nutrient availability (TP and to a lesser extent DIN) as well as nutrient imbalance (albeit only with N:P_seston as proxy) were driving factors for the phytoplankton community in the Cau Hai lagoon and hence alterations in both of these factors leading to a shift in phytoplankton species composition and productivity.     

Changes in alkaline phosphatase activity and phosphate uptake in P-limited phytoplankton,induced by light intensity and spectral quality

Alkaline phosphatase activity and P uptake were determined in P-limited Dunaliella tertiolecta, Thalassiosira pseudonana, Phaeodactylum tricornumtum, and Prymnesium parvum grown under different light intensities and colors. Both intracellular and extracellular enzyme activities varied with the intensity and quality of light in a species-specific manner. The spectral composition of the light also affected P uptake kinetics. No correlation was found between enzyme activity and V_max both within a species and for pooled data for all four species, indicating that the change in uptake kinetics and enzyme activity was not related to P limitation, but induced by the light conditions. Changes in the optimum N:P ratio induced by light were also not related to P uptake kinetics or enzyme activity. These data suggest that light conditions may in themselves have profound effects on species competition for limiting nutrients. Furthermore, since both alkaline phosphatase activity and P uptake were influenced by the prevailing light conditions we suggest that these parameters be used cautiously when determining the P nutritional status of phytoplankton in nature.Address for reprint requests     

Effects of nitrogen enrichment on zooplankton biomass and N:P recycling ratios across a DOC gradient in northern-latitude lakes

We used data from whole-lake studies to assess how changes in food quantity (phytoplankton biomass) and quality (phytoplankton community composition, seston C:P and N:P) with N fertilization affect zooplankton biomass, community composition and C:N:P stoichiometry, and their N:P recycling ratio along a gradient in lake DOC concentrations. We found that despite major differences in phytoplankton biomass with DOC (unimodal distributions, especially with N fertilization), no major differences in zooplankton biomass were detectable. Instead, phytoplankton to zooplankton biomass ratios were high, especially at intermediate DOC and after N fertilization, implying low trophic transfer efficiencies. An explanation for the observed low phytoplankton resource use, and biomass responses in zooplankton, was dominance of colony forming chlorophytes of reduced edibility at intermediate lake DOC, combined with reduced phytoplankton mineral quality (enhanced seston N:P) with N fertilization. N fertilization, however, increased zooplankton N:P recycling ratios, with largest impact at low DOC where phytoplankton benefitted from light sufficiently to cause enhanced seston N:P. Our results suggest that although N enrichment and increased phytoplankton biomass do not necessarily increase zooplankton biomass, bottom-up effects may still impact zooplankton and their N:P recycling ratio through promotion of phytoplankton species of low edibility and altered mineral quality.

     

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.     

Species Diversity Across Nutrient Gradients: An Analysis of Resource Competition in Model Ecosystems

The capture and efficient use of limiting resources influence the competitive success of individual plant species as well as species diversity across resource gradients. In simulations, efficient nutrient acquisition or nutrient retention by species were key predictors of success when nutrients were limiting. Increased nutrient supply favored species with characteristics that improved light interception or light use. Ecological theory suggests that low diversity on fertile sites may be a consequence of competitive exclusion by one or a few species with superior light-interception characteristics. On infertile sites, competitive exclusion may be a function of superior nutrient-acquisition characteristics in species. At intermediate fertility, a shift from single-resource specialization to a balanced effort in the acquisition of multiple resources should allow for greater species diversity. Thus, a unimodal relationship between diversity and nutrient supply, vegetation biomass, or productivity is predicted. However, simulations demonstrated alternate relationships depending on the ecosystem characteristic to which diversity was compared. Diversity was greatest at intermediate total biomass but increased monotonically with net primary production and nitrogen (N) supply. The highest diversity occurred midrange on a scale of community-level leaf area to fine-root length ratios, which in the context of the model indicates that the vegetation as a whole was simultaneously limited by both N and light and that effort toward the acquisition of both resources is distributed in such a way that both resources are equally exploited. Diversity was lowered by the presence of species with a superior ability to sequester resources.     

THE Si:C:N RATIO OF MARINE DIATOMS: INTERSPECIFIC VARIABILITY AND THE EFFECT OF SOME ENVIRONMENTAL VARIABLES1

The variability of marine diatom Si:C and Si:N composition ratios was examined to assess their utility as ecological conversion factors. Twenty-seven diatom species grown under an 18:6 h LD cycle and sampled at the end of the light period gave mean ratios, by atoms, of 0.13 ± 0.04 and 1.12 ± 0.33 for Si:C and Si:N ratios, respectively (95% C.I. reported). The mean ratios for 18 species grown under continuous illumination were 0.12 ± 0.03 for Si:C and 0.95 ± 0.23 for Si:N. The mean ratios of the clones grown under constant light were not statistically different from those calculated for the same species grown under an 18:6 h LD photoperiod. The overall mean Si:C and Si:N ratios for the 18:6 h LD and continuous light experiments taken together, weighted by the number of species in each experiment, are 0.13 and 1.05, respectively. The average ratios for the nine nanoplankton species (<20 μm) examined were 0.09 ± 0.03 for Si:C and 0.80 ± 0.35 for Si:N. The eighteen netplankton species (>20 μm) had higher mean ratios, Si:C = 0.15 ± 0.04 and Si:N = 1.20 ± 0.37. Time course sampling throughout a 24 h period revealed twofold variations in both ratios for individual species grown on a 14:10 h LD cycle. Changes in irradiance can also produce factor of two variations, both ratios being higher under low light. Comparisons of these data with those from the literature regarding the effects of temperature and nutrient limitation on diatom elemental composition suggest that use of these ratios to convert field estimates of biogenic silica into nitrogen or carbon units, or to estimate silica production from ¹⁴C data, should yield results accurate to within a factor of three under most circumstances.     

GROWTH RATE VARIATION IN THE N:P REQUIREMENT RATIO OF PHYTOPLANKTON1

Theoretical considerations predict that the cell N:P ratio at transition from nitrogen limitation to phosphorus limitation of phytoplankton growth (critical ratio, R_c) varies, as a function of population growth rate. This prediction is confirmed by experimental, data from the literature along with new experimental data for the marine, prymnesiophyte Pavlova lutheri (Droop) Green. R_c passes through a maximum at intermediate growth rates for the three phytoplankton species for which data, are available, but there is significant interspecific variability in its value. There is no theoretical or experimental evidence to support the idea that the ratio of subsistence N and P cell quotas is equal to R_c over the range of growth rates, or that the subsistence quota ratio equals the ratio of the N and P cell quotas minus a storage fraction. Examination of N:P composition ratios can be used to determine which nutrient is limiting, but cannot be used to determine relative growth rates or competitive advantage between species limited by the same nutrient. Growth rates are determined by environmental conditions and by the cell quota of the limiting nutrient, without reference to the cell quota of the non-limiting nutrient.     

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.