Cell size trade-offs govern light exploitation strategies in marine phytoplankton

Marine phytoplankton show complex community structures and biogeographic distributions, the net results of physiological and ecological trade-offs of species responses to fluctuating, heterogeneous environments. We analysed photosynthesis, responses to variable light and macromolecular allocations across a size panel of marine centric diatoms. The diatoms have strong capacities to withstand and exploit fluctuating light, when compared with picophytoplankton. Within marine diatoms, small species show larger effective cross-sections for photochemistry, and fast metabolic repair of photosystem II after photoinactivation. In contrast, large diatoms show lower susceptibility to photoinactivation, and therefore incur lower costs to endure short-term exposures to high light, especially under conditions that limit metabolic rates. This size scaling of key photophysiological parameters thus helps explain the relative competitive advantages of larger versus smaller species under different environmental regimes, with implications for the function of the biogenic carbon pump. These results provide a mechanistic framework to explain and predict shifts in marine phytoplankton community size structure with changes in surface irradiance and mixed layer depth.     

闽南-台湾浅滩近岸上升流区浮游植物碳同化速率的研究

本文采用~(14)C同位素示踪法,测定了浮游植物光合作用速率,结合浮游植物细胞含碳量,计算了不同季节、不同深度下浮游植物碳同化速率常数,讨论了不同环境条件对浮游植物碳同化速率常数的影响。结果表明,闽南-台湾浅滩近岸上升流的形成,是该海域高生产力的主要原因,上升流期间浮游植物复制时间要比非上升流期间浮游植物复制时间缩短1.8倍。同时还表明,温度,光照强度、营养盐是控制浮游植物生长的主要因子。上升流期间营养盐始终保持在较高的水平。是上升流区具有较大的浮游植物碳同化速率常数(3.3d~(-1))的原因之一。适宜该海域浮游植物生长的光照强度在3 000—15 000lx之间,温度的影响可用Goldman和Carpenter模式近似表示。     

The photosynthetic response of C3 and C4 bioenergy grass species to fluctuating light

Bioenergy grass species are a renewable energy source, but their productivity has not been fully realized. Improving photosynthetic efficiency has been proposed as a mechanism to increase the productivity of bioenergy grass species. Fluctuating light, experienced by all field grown crops, is known to reduce photosynthetic efficiency. This experiment aimed to evaluate the photosynthetic performance of both C₃ and C₄ bioenergy grass species under steady state and fluctuating light conditions by examining leaf gas exchange. The fluctuating light regime used here decreased carbon assimilation across all species when compared to expected steady state values. Overall, C₄ species assimilated more carbon than C₃ species during the fluctuating light regime, with both photosynthetic types assimilating about 16% less carbon than expected based on steady state measurements. Little diversity was observed in response to fluctuating light among C₃ species, and photorespiration partially contributed to the rapid decreases in net photosynthetic rates during high to low light transitions. In C₄ species, differences among the four NADP-ME species were apparent. Diversity observed among C₄ species in this experiment provides evidence that photosynthetic efficiency in response to fluctuating light may be targeted to increase C₄ bioenergy grass productivity.     

An improved dynamic model of photosynthesis for estimation of carbon gain in sunfleck light regimes

A dynamic model of leaf photosynthesis for C₃ plants has been developed for examination of the role of the dynamic properties of the photosynthetic apparatus in regulating CO₂ assimilation in variable light regimes. The model is modified from the Farquhar-von Caemmerer-Berry model by explicitly including metabolite pools and the effects of light activation and deactivation of Calvin cycle enzymes. It is coupled to a dynamic stomatal conductance model, with the assimilation rate at any time being determined by the joint effects of the dynamic biochemical model and the stomatal conductance model on the intercellular CO₂ pressure. When parametrized for each species, the model was shown to exhibit responses to step changes in photon flux density that agreed closely with the observed responses for both the understory plant Alocasia macrorrhiza and the crop plant Glycine max. Comparisons of measured and simulated photosynthesis under simulated light regimes having natural patterns of lightfleck frequencies and durations showed that the simulated total for Alocasia was within ±4% of the measured total assimilation, but that both were 12–50% less than the predictions from a steady–state solution of the model. Agreement was within ±10% for Glycine max, and only small differences were apparent between the dynamic and steady–state predictions. The model may therefore be parametrized for quite different species, and is shown to reflect more accurately the dynamics of photosynthesis than earlier dynamic models.     

A mechanistic model of photoinhibition

A mechanistic model was developed, to simulate the main facets of photoinhibition in phytoplankton. Photoinhibition is modelled as a time dependent decrease in the initial slope of a photosynthesis versus irradiance curve, related to D1 (photosystem II reaction centre protein) damage and non-photochemical quenching. The photoinhibition model was incorporated into an existing ammonium-nitrate nutrition interaction model capable of simulating photoacclimation and aspects of nitrogen uptake and utilization. Hence the current model can simulate the effects of irradiance on photosynthesis from sub-saturating to inhibitory photon flux densities, during growth on different nitrogen sources and under nutrient stress. Model output conforms well to experimental data, allowing the extent of photoinhibition to be predicted under a range of nutrient and light regimes. The ability of the model to recreate the afternoon depression of photosynthesis and the enhancement of photosynthesis during fluctuating light suggests that these two processes are related to photoinhibition. The model may be used to predict changes in biomass and/or carbon fixation under a wide range of oceanographic situations, and it may also help to explain the progression to dominance of certain algal species, and bloom formation under defined irradiance and nutrient conditions.     

THE INFLUENCE OF FLUCTUATING LIGHT ON DIVERSITY AND SPECIES NUMBER OF NUTRIENT‐LIMITED PHYTOPLANKTON1

The influence of fluctuating light on diversity and species number of a natural phytoplankton assemblage competing for nutrients was investigated for 48 days under semicontinuous culture conditions. Light conditions were either changed periodically from high (65 μmol photons·m^?2·s^?1) to low intensity (15 μmol photons·m^?2·s^?1) at intervals of 1, 3, 6, and 12 days or fixed at constant light conditions of intermediate intensity (40 μmol photons·m^?2·s^?1). Fluctuating light at intervals of 1–12 days significantly affected phytoplankton diversity. The development of phytoplankton communities differed in treatments with different light regimes. In treatments with long light intervals, species abundance oscillated with the light phases. Differences in the temporal development of phytoplankton communities resulted in hump‐shaped relations between the interval length of the light phases and both species number and diversity index and can be explained by the intermediate disturbance hypothesis. Fluctuating light tends to sustain phytoplankton diversity under nutrient limitation if the light regime changes in the order of several days. This indicates that temporal changes in weather regime are important in preventing competitive exclusion of phytoplankton species in nature.     

Light use efficiency of California redwood forest understory plants along a moisture gradient

We investigated photosynthesis of five plant species growing in the understory at three sites (1,170-, 1,600- and 2,100-mm annual moisture inputs), along the geographical range of coastal California redwood forest, to determine whether greater inputs of rain and fog at northern sites enhance photosynthetic utilization of fluctuating light. Measurements of understory light environment and gas exchange were carried out to determine steady state and dynamic photosynthetic responses to light. Leaf area index ranged from 4.84 at the 2,100-mm site to 5.98 at the 1,170-mm site. Maximum rates of net photosynthesis and stomatal conductance (g) did not vary appreciably within species across sites. Photosynthetic induction after a change from low to high light was significantly greater in plants growing in lower light conditions regardless of site. Photosynthetic induction also increased with the rate of g in diffuse light, prior to the increase to saturating light levels. Post-illumination CO₂ assimilation was the largest factor contributing to variation in C gain during simulated lightflecks. The duration of post-illumination photosynthetic activity, total CO₂ assimilation per light received, and light use efficiency during simulated lightflecks increased significantly with moisture inputs in four out of five species. Increasing leaf N concentration with increasing moisture inputs in three out of five species, coupled with changes in leaf N isotopic composition with the onset of the summer fog season suggest that natural N deposition increases with rain and fog inputs and contributes to greater utilization of fluctuating light availability in coastal California redwood forests.     

Photosynthesis in the fleeting shadows: an overlooked opportunity for increasing crop productivity?

Photosynthesis measurements are traditionally taken under steady‐state conditions; however, leaves in crop fields experience frequent fluctuations in light and take time to respond. This slow response reduces the efficiency of carbon assimilation. Transitions from low to high light require photosynthetic induction, including the activation of Rubisco and the opening of stomata, whereas transitions from high to low light require the relaxation of dissipative energy processes, collectively known as non‐photochemical quenching (NPQ). Previous attempts to assess the impact of these delays on net carbon assimilation have used simplified models of crop canopies, limiting the accuracy of predictions. Here, we use ray tracing to predict the spatial and temporal dynamics of lighting for a rendered mature Glycine max (soybean) canopy to review the relative importance of these delays on net cumulative assimilation over the course of both a sunny and a cloudy summer day. Combined limitations result in a 13% reduction in crop carbon assimilation on both sunny and cloudy days, with induction being more important on cloudy than on sunny days. Genetic variation in NPQ relaxation rates and photosynthetic induction in parental lines of a soybean nested association mapping (NAM) population was assessed. Short‐term NPQ relaxation (<30 min) showed little variation across the NAM lines, but substantial variation was found in the speeds of photosynthetic induction, attributable to Rubisco activation. Over the course of a sunny and an intermittently cloudy day these would translate to substantial differences in total crop carbon assimilation. These findings suggest an unexplored potential for breeding improved photosynthetic potential in our major crops.     

Sunlight Effects on the Osmotrophic Uptake of DMSP-Sulfur and Leucine by Polar Phytoplankton

Even though the uptake and assimilation of organic compounds by phytoplankton has been long recognized, very little is still known about its potential ecological role in natural marine communities and whether it varies depending on the light regimes the algae experience. We combined measurements of size-fractionated assimilation of trace additions of ³H-leucine and ³⁵S-dimethylsulfoniopropionate (DMSP) with microautoradiography to assess the extent and relevance of osmoheterotrophy in summer phytoplankton assemblages from Arctic and Antarctic waters, and the role of solar radiation on it was further investigated by exposing samples to different radiation spectra. Significant assimilation of both substrates occurred in the size fraction containing most phytoplankton (>5 µm), sunlight exposure generally increasing ³⁵S-DMSP-sulfur assimilation and decreasing ³H-leucine assimilation. Microautoradiography revealed that the capacity to take up both organic substrates seemed widespread among different polar algal phyla, particularly in pennate and centric diatoms, and photosynthetic dinoflagellates. Image analysis of the microautoradiograms showed for the first time interspecific variability in the uptakes of ³⁵S-DMSP and ³H-leucine by phytoplankton depending on the solar spectrum. Overall, these results suggest that the role of polar phytoplankton in the utilization of labile dissolved organic matter may be significant under certain conditions and further confirm the relevance of solar radiation in regulating heterotrophy in the pelagic ocean.     

Modelling photosynthesis in fluctuating light with inclusion of stomatal conductance, biochemical activation and pools of key photosynthetic intermediates

Photosynthetic carbon gain in rapidly fluctuating light is controlled by stomatal conductance, activation of ribulose-1,5-bisphosphate carboxylase-oxygenase, a fast induction step in the regeneration of ribulose-1,5-bisphosphate, and the build-up of pools of photosynthetic intermediates that allow post-illumination CO₂ fixation. Experimental work over recent years has identified and characterised these factors. A physiologically-based dynamic model is described here that incorporates these factors and allows the simulation of carbon gain in response to any arbitrary sequence of light levels. The model output is found to conform well to previously reported plant responses of Alocasia macrorrhiza (L.) G. Don. observed under widely differing conditions. The model shows (i) responses of net assimilation rate and stomatal conductance to constant light levels and different CO₂ concentrations that are consistent with experimental observations and predictions of a steady-state model; (ii) carbon gain to continue after the end of lightflecks, especially in uninduced leaves; (iii) carbon gain to be only marginally reduced during low-light periods of up to 2 s; (iv) a fast-inducing component in the regeneration of ribulose-1,5-bisphosphate to be limiting for up to 60 s after an increase in light in uninduced leaves: the duration of this limitation lengthens with increasing CO₂ concentration and is absent at low CO₂ concentration; (v) oxygen evolution to exceed CO₂ fixation during the first few seconds of a lightfleck, but CO₂ fixation to continue after the end of the lightfleck whereas oxygen evolution decreases to low-light rates immediately. The model is thus able to reproduce published responses of leaves to a variety of perturbations. This provides good evidence that the present formulation of the model includes the essential rate-determining factors of photosynthesis under fluctuating light conditions. Received: 27 January 1997 / Accepted: 15 April 1997     

Population and community responses of phytoplankton to fluctuating light

Light is a major resource in aquatic ecosystems and has a complex pattern of spatio-temporal variability, yet the effects of dynamic light regimes on communities of phytoplankton are largely unexplored. I examined whether and how fluctuating light supply affects the structure and dynamics of phytoplankton communities. The effect of light fluctuations was tested at two average irradiances: low, 25 μmol quanta m⁻² s⁻¹ and high, 100 μmol quanta m⁻² s⁻¹ in 2- and 18-species communities of freshwater phytoplankton. Species diversity, and abundances of individual species and higher taxa, depended significantly on both the absolute level and the degree of variability in light supply, while total density, total biomass, and species richness responded only to light level. In the two-species assemblage, fluctuations increased diversity at both low and high average irradiances and in the multispecies community fluctuations increased diversity at high irradiance but decreased diversity at low average irradiance. Species richness was higher under low average irradiance and was not affected by the presence or absence of fluctuations. Diatom abundance was increased by fluctuations, especially at low average irradiance, where they became the dominant group, while cyanobacteria and green algae dominated low constant light and all high light treatments. Within each taxonomic group, however, there was no uniform pattern in species responses to light fluctuations: both the magnitude and direction of response were species-specific. The temporal regime of light supply had a significant effect on the growth rates of individual species grown in monocultures. Species responses to the regime of light supply in monocultures qualitatively agreed with their abundances in the community experiments. The results indicate that the temporal regime of light supply may influence structure of phytoplankton communities by differentially affecting growth rates and mediating species competition. Received: 24 September 1997 / Accepted: 8 July 1998     

An experimental evolutionary study on adaptation to temporally fluctuating pH in Escherichia coli

In this study, we use the bacterium Escherichia coli to examine evolutionary responses to environmental acidity fluctuating temporally among pH 5.3, 6.3, 7.0, and 7.8 (5,000-15 nM [H(+)]). Two experimental protocols of temporal variation were used. One group (six replicate lines) of populations evolved for 2,000 generations during exposure to a cycled regime fluctuating daily between pH 5.3 and 7.8. The other group (also in six replicate lines) evolved during exposure for 2,000 generations to a randomly shifting regime fluctuating stochastically each day among pH 5.3, 6.3, 7.0, and 7.8. Adaptation to these fluctuating acidity regimes was measured as a change in fitness relative to the common ancestor by direct competition experiments in both constant and fluctuating pH regimes. For comparisons with constant pH evolution, a group evolved at a constant pH of 5.3 and another group evolved at pH 7.8 were also tested. This study initiated the first long-term laboratory natural selection experiment on adaptation to variable acidity and addressed key questions concerning patterns of adaptation (trade-offs, specialists, generalists, plasticity, transitions, and acclimation) in temporally fluctuating environments.     

Dynamics of carbon assimilation by St Lawrence estuary phytoplankton at the end of summer

This study presents data of in situ measurements of inorganic carbon assimilation by phytoplankton communities of the St Lawrence estuary during the end of summer 1982. We used carboxylase activity measurements (ribulose-1,5-bisphosphate carboxylase, carboxylases) and the ¹³C/¹²C ratio of phytoplankton organic carbon, expressed as ¹³C, to study patterns of assimilation. Upper estuary phytoplankton communities showed a smaller turn-over rate in carbon assimilation than lower estuary phytoplankton communities. Carbon assimilation was limited by light intensity in the upper estuary and by CO₂ availability in the lower estuary. In the St Lawrence estuary, stable carbon isotope ratios of phytoplankton organic carbon seemed to be controlled by inorganic carbon availability rather than by phytoplankton metabolism.     

Association between temporal and spatial beta diversity in phytoplankton

The rates of temporal and spatial species turnover have been compared in different organisms and scales, revealing that both are not independent but, rather, associated. However, the knowledge is limited for the association between spatial turnover and temporal turnover. Here, we performed two investigations of the phytoplankton composition in the lakes of the Yangtze River catchment in China in the spring and summer of 2012, which covered regional spatial scale and two‐season temporal scale. We analysed the association between temporal and spatial species turnover in phytoplankton. The results showed that 1) the two‐season temporal turnover of phytoplankton varied based on the mean values and the coefficient of variance of environmental variables, and pH was the most important variable negatively affecting the temporal turnover; 2) the spatial beta diversity of phytoplankton in summer was higher than that in spring, and the distance decay pattern was significant in summer, but not in spring; 3) the variation in spatial turnover in spring and summer was attributed to the primary environmental variables (nitrogen, phosphorus and underwater available light) and broader‐scale spatial variables; 4) the proportion of jointly explained variation of spatial Bray–Curtis dissimilarity by the environment and space increased from ~38% (spring) to ~55% (summer), which was mainly due to the variation in spatially structured environmental variables during the two‐season temporal turnover, such as pH and ion concentrations; 5) the community compositions in summer were more similar between the lakes with similar two‐season temporal turnover. These results indicate that the spatial turnover of phytoplankton composition in summer was partially predetermined by the variation in environmental variables and phytoplankton composition during the process of two‐season temporal turnover, and highlight the understanding of temporal variations in spatial beta diversity as well as the underlying assembly mechanisms in phytoplankton.     

The kinetics of algal photoadaptation in the context of vertical mixing

The responses of phytoplankton to turbulent motions in the surfacemixed layer can be measured to estimate the rate of verticalmixing. If the time scale for the response (photoadaptation)is shorter than that for vertical mixing, phytoplankton willexhibit a vertical gradient associated with adaptation to ambientlight, whereas if mixing occurs with a time scale shorter thanthat of photoadaptation, the surface mixed layer will be uniformwith respect to the photoadaptive parameter. To examine thephysiological bases for a model of vertical mixing and photoadaptation,we grew the marine diatom Thalassiosira pseudonana (clone 3H)at three photon flux densities and subjected the cultures toreciprocal light shifts, measuring physiological and chemicalchanges over the following 10 h. Several parameters, easilymeasured in nature and attributable primarily to phytoplankton,responded to fluctuating light on different time scales. Aftercultures were exposed to relatively bright light, both the initialslope of the photosynthesis-irradiance curve and in vivo fluorescencewere depressed on a time scale of less than an hour. Photosyntheticcapacity was also reduced transiently, but recovered over manyhours to a high level characteristic of an adapted state. First-orderkinetics (the current model of choice for describing photoadaptation)reasonably described the rapid responses of phytoplankton tobright light, but other parameters (i.e. cellular chemical compositionand photosynthetic capacity) changed as a result of unbalancedgrowth and required much longer to adapt from low to high lightas compared to from high to low light. A logistic model of thisadaptation is presented. The model suggests that hysteresisof adaptation during vertical mixing may have important consequences.The vertical distributions of photoadaptive properties in mixedlayers not only reveal the rate of vertical mixing, but showhow phytoplankton integrate environmental fluctuations.     

A dynamic model of darkness tolerance for phytoplankton: model description

To analyze various effects of prolonged darkness on phytoplankton population dynamics, we developed a dynamic model of darkness tolerance for phytoplankton and investigated its characteristics. To construct the basic concepts of the model, we categorized various changes in abundance of phytoplankton both during prolonged darkness and after reillumination into several patterns, and then considered the physiological processes producing these patterns. The nature of darkness tolerance was considered to incorporate previously experienced light conditions, including darkness, as a physiological activity, and members of the same phytoplankton species exhibit different dynamics even in identical light conditions due to such career effects. Taking this into consideration, we developed a cell quota model in relation to darkness tolerance. State variables for abundance were indicated by cell numbers, and physiological condition by three intracellular carbon pools with different physiological functions. Using our model, we analyzed the various changes in abundance of phytoplankton in relation to exposure to prolonged darkness. Various responses in terms of phytoplankton abundance to prolonged darkness and after reillumination were successfully reproduced by the model that simply assumed that deterioration of physiological mechanics, such as photosynthetic functions, was due to a prolonged dark condition. On the basis of the results of calculation and assumptions for the model, we discuss the limitations, problems, and effectiveness of the model. Handling editor: Luigi Naselli-Flores     

Simulation of leaf photosynthesis of C3 plants under fluctuating light and different temperatures

An induction-dependent empirical model was developed to simulate the C₃ leaf photosynthesis under fluctuating light and different temperatures. The model also takes into account the stomatal conductance when the light intensity just exceeds the compensation point after a prolonged period of darkness (initial stomatal conductance, $ g_{{{\text{S}}_{\text{ini}} }} $ ). The model was parameterized for both Chrysanthemum morifolium and Spinacia oleracea by artificially changing the induction states of the leaves in the climate chamber. The model was tested under natural conditions that were including frequent light flecks due to partial cloud cover and varying temperatures. The temporal course of observed photosynthesis rate and the carbon gain was compared to the simulation. The ability of the current model to predict the carbon assimilation rate was assessed using different statistical indexes. The model predictions were accurate but the model slightly underestimated the actual overall carbon gain. The accuracy of the simulation was largely dependent on the parameters that were calculated for the particular plant species, of which the simulation is intended for. In particular, the rate of change of induction and the initial stomatal conductance were found to be highly important and these were species-specific parameters for the predictions. The model is suitable for estimating instantaneous leaf CO₂ assimilation for different herbaceous plant species under dynamic environmental conditions. It can be simply calibrated for other crops, by estimating the individual parameters.     

Effect of (a)synchronous light fluctuation on diversity,functional and structural stability of a marine phytoplankton metacommunity

Disentangling the mechanisms that maintain the stability of communities and ecosystem properties has become a major research focus in ecology in the face of anthropogenic environmental change. Dispersal plays a pivotal role in maintaining diversity in spatially subdivided communities, but only a few experiments have simultaneously investigated how dispersal and environmental fluctuation affect community dynamics and ecosystem stability. We performed an experimental study using marine phytoplankton species as model organisms to test these mechanisms in a metacommunity context. We established three levels of dispersal and exposed the phytoplankton to fluctuating light levels, where fluctuations were either spatially asynchronous or synchronous across patches of the metacommunity. Dispersal had no effect on diversity and ecosystem function (biomass), while light fluctuations affected both evenness and community biomass. The temporal variability of community biomass was reduced by fluctuating light and temporal beta diversity was influenced interactively by dispersal and fluctuation, whereas spatial variability in community biomass and beta diversity were barely affected by treatments. Along the establishing gradient of species richness and dominance, community biomass increased but temporal variability of biomass decreased, thus highest stability was associated with species-rich but highly uneven communities and less influenced by compensatory dynamics. In conclusion, both specific traits (dominance) and diversity (richness) affected the stability of metacommunities under fluctuating conditions.