Size-dependent changes in phytoplankton C and N uptake in the dynamic mixed layer of Lake Biwa

1. Short-term (days) hydrodynamic effects of wind-induced mixing on phytoplankton size structure, and C and N uptake characteristics, were studied in the surface mixed layer (epilimnion) of Lake Biwa (North Basin), before and during a period of high winds (typhoons). 2. The latter period was characterized by two major typhoon events associated with deepening of the seasonal thermocline, reduced water column stability, decreased underwater irradiance and increased dissolved reactive N and particulate P. 3. Nutrient concentrations, seston C/N ratios, and uptake rates indicated that phytoplankton biomass and production were limited by P and not N throughout the study. Higher C- and N-based productivity during the typhoon period than before reflected the increased phytoplankton biomass and higher specific uptake rates due to increased nutrient supply. 4. Changes in the size-structure of phytoplankton (< 2 and > 2 μm) were associated with variations in the stratification and mixing regime. When vertical stability was high (before the typhoons) concentrations of > 2 μm biomass (chlorophyll a, particulate organic C and N) were higher at the bottom of the mixed layer than at the surface whereas, when stability of the mixed layer was low (the typhoon period), the contribution of picoplankton (< 2 μm) to total Chl a increased at the surface and decreased at the bottom following the first high winds. 5. Photoadaptive adjustments of the phytoplankton provided further evidence of hydrodynamic control. The lower intracellular Chl a concentrations and C and N uptake efficiencies in the < 2 μm fraction suggest that they experienced, on average, higher irradiance than the larger cells because of their lower sinking rates. During the stability period, picoplankton exhibited higher photosynthetic efficiencies at the bottom of the mixed layer than at the surface. Such differences disappeared during the typhoon period indicating that the mixing rate was then probably higher than the photoacclimation rate in the small size fraction. 6. The present results stress the highly transient nature of biological homogeneity in the surface mixed layer of the lake.     

Size-dependent phytoplankton responses to atmospheric forcing in Lake Biwa

Size-dependent changes in chlorophyll a and uptake of inorganiccarbon (C) and nitrogen (N) by phytoplankton were measured inthe shallow South Basin of Lake Biwa, before and during a periodof typhoons (high winds). The latter period was characterizedby complete mixing of the water column, a major decline in underwaterirradiance, and a transient increase in dissolved reactive Nand phosphorus (P). Nutrient concentrations, seston N:P ratiosand uptake rates indicate that P and not N limited phytoplanktonover the whole study period. The typhoon-induced increase inphosphorus supply resulted in Blackman-type (increased C- andN-specific growth rates) and Liebig-type (increased biomassyield) responses by the phytoplankton. Picoplankton were dominantin the relatively stable and clear water column prior to thetyphoons, but were rapidly outgrown by larger cells during andafter wind-induced mixing. The slower response of picoplanktonindicates lower maximum intrinsic growth rates and photosyntheticefficiency. These observations are contrary to the view thatpicoplankton have higher light-harvesting abilities and growthrates than larger cells. Typhoon-induced mixing stimulated theshift to fast-growing, dim light-adapted larger cells. The resultsquestion the allometric paradigm of increasing growth ratesand light-capturing efficiency with decreasing cell size, butare consistent with the oceanographic view that large-celledphytoplankton control the major fluctuations in biomass andprimary productivity, while picoplankton account for a comparativelystable background productivity.     

The daily pattern of nitrogen uptake by phytoplankton in dynamic mixed layer environments

The transport and assimilation of the various forms of biologically available nitrogen by phytoplankton, and the subsequent biosynthesis of N-containing macromolecules, have the potential to respond in different ways during the daily growth cycle. This review examines five types of effect that may influence the daily pattern of nitrogen uptake and metabolism: light versus dark (the day/night cycle); changes in irradiance during the day (including the diurnal rise and fall in photon fluence rates); circadian rhythms (endogenous patterns of variation which may continue in the absence of external environmental forcing); periodic variations in exogenous nitrogen supply; and the 24-hour dynamics of stratification and mixing. The hydrodynamic effects operate through a variety of direct and indirect controls, and can substantially modify the diel rhythmicity of phytoplankton growth.     

Nitrogenous nutrient uptake by phytoplankton and ammonium regeneration by microbial assemblage in Lake Biwa

In situ rates of nitrate, ammoniwn and urea uptake by the phytoplanktonassemblage, and the regeneration rate of ammonium by the microbialassemblage, in Lake Biwa were measured using the nitrogen 15tracer method from 1985 to 1987. The rate of total nitrogen(sum of ammonium, nitrate and urea) uptake was in the rangeof 62–594 ng N^–1 r^–1 h^–1. The percentagecontribution of ammonium uptake was 41–92%, that of urea4–58% and that of nitrate <1–28% of total uptake.The annual mean new production which was supported by nitrateuptake was 18% of the total production in 1986. The phytoplanktonassemblage in Lake Biwa preferentially utilized regeneratednitrogen, such as ammonium and urea, whose concentration wasmuch lower than that of nitrate throughout the observation penodwithout in summer. The in situ nitrogen uptake rate was almostsufficient to meet the nitrogen requirement of the phytoplanktonassemblage, except in midsummer when the nitrate concentrationwas below the detection limit of 0.3 µg N r^–1. Inthe trophogemc layer, the rate of ammonium regeneration was66–272 ng N 1^–1 h^–1 Although the ambient ammoniumconcentration in the trophogenic layer was maintained at aroundthe half-saturation constant for ammonium uptake kinetics, theammomum uptake rates were always highly correlated with ammoniumregeneration rates. From the size fractionation experimentsand estimates from the literature, it was suggested that themicrobial assemblage <1 µm may have been the most importantagent responsible for the ammonium regeneration processes inthe trophogenic layer.     

Day-night changes in production of carbohydrate and protein by natural phytoplankton population from Lake Biwa, Japan

The ¹³C and gas chromatography-mass spectrometry (¹³C-GC-MS)method was applied to determine the day-night changes in thecomposition of photosynthetic products of the natural phytoplanktonpopulation from Lake Biwa, Japan. Glucose is the most abundantmonosaccharide in acid-hydrolyzable carbohydrate. The contributionof glucose was high in incubatesd samples in daytime and decreasedduring the night. Other monosaccharides (rhamnose, fucose, ribose,arabinose, xylose, mannose and galactose) and amino acids tendedto be produced throughout both day- and night-time. These resultssuggested that the carbon flows from glucose, which might constitutereserve glucan, to other monosaccharides and amino acids duringnight-time. The disproportionate production of glucose (reservedglucan) during daytime was thus partly cancelled out at night.     

Analysis of long-term variation in phytoplankton biovolume in the northern basin of Lake Biwa

The long-term variation in phytoplankton biovolume in the northern basin of Lake Biwa was analyzed using periodic phytoplankton census data from January 1979 to December 2009. Population densities obtained from census data were transformed into biovolumes, and phytoplankton species were categorized into three size fractions: net phytoplankton (≥4,000 μm³ cell^?1, ≥ca. 20 μm in diameter), large nanophytoplankton (100–4,000 μm³ cell^?1, ca. 6–20 μm in diameter), and small nanophytoplankton (<100 μm³ cell^?1, <ca. 6 μm in diameter). Although the annual total biovolume gradually decreased over time, the total biovolumes in winter and spring were found to increase. Furthermore, a decrease in the biovolume of net phytoplankton and an increase in that of small nanophytoplankton were observed. Because of succession in the phytoplankton community, the average cell volume of the phytoplankton community decreased from 269 μm³ cell^?1 in the 1980s to 56 μm³ cell^?1 in the 2000s. Lake warming accompanied with the intensification of thermal stratification and the augmentation of wind speed were observed at Lake Biwa over the study period. Serial analysis correcting for autocorrelation revealed that oligotrophication in the epilimnion, induced by lake warming and limitation of light available for phytoplankton growth by wind-induced water mixing, was a potential factor in the succession of the phytoplankton community.     

Spatial changes of phytoplanktonic size spectra in Lake Biwa

The degree of eutrophication in Lake Biwa was examined from the characteristics of spatial distribution in size spectra computed by a size spectra analyser with an optical fiber sensor. Two types of size spectra could be recognised: (1) size distribution only presenting a peak in a size less than about 20 m in equivalent diameter and (2) size distribution with two peaks in size spectra.The second pattern with two peaks was observed in the size spectra from the south basin, the sites near the central part and the southern part of the north basin, and seemed to be associated with advanced eutrophic conditions. In addition, the degree of eutrophication along the east side of the south basin was examined from changes in size spectra and from hydrological conditions. We inferred that the eutrophic condition around the central sites of the north basin is influenced by the water current from the gyre.     

Fatty acid composition in photosynthetic products of natural phytoplankton population in Lake Biwa, Japan

Fatty acid composition of phytoplankton photosynthetic productswas determined by a ¹³C tracer and gas chromatography-mass spectrometry(¹³C-GC-MS) method from August 1985 to June 1986 in Lake Biwa,Japan. The total fatty acid production rate varied from 2.8to 10.9 µg C l^–1 day^–1 at the water surfaceand accounted for 9.1–30% of photosynthetic productionof particulate organic carbon. A high contribution of fattyacid to the particulate organic carbon production rate was noticedduring winter time, and an increase in the fatty acid contributionresulted in an increase in the C/N value in the photosyntheticproducts. The fatty acid composition varied throughout the year,mainly depending on the seasonal change in the dominant phytoplanktonspecies. The contribution of polyunsaturated fatty acids tototal fatty acids was low during the summer period, probablydue to nitrogen limitation of phytoplankton growth.     

Spatial distribution and seasonal changes of pesticides in Lake Biwa,Japan

The spatial distribution and seasonal variation in the concentrations in Lake Biwa of pesticides used in paddy fields were studied. Lake Biwa is the largest lake in Japan and is a recognized water resource for 14 million people in the Kinki district. Samples were collected nine times from April to December 2001 at ten sites within the lake and at the mouths of six influent rivers. Weekly sampling was also carried out at a single site on an effluent river. Among the 20 pesticides analyzed, the detection frequencies in surface water were almost 100% for simetryn, bromobutide, and isoprothiolane; around 75% for molinate and pyroquilon; around 30% for three herbicides and one fungicide; and almost zero for the remaining substances. The maximum concentrations of pesticides detected frequently in the lake were in the range 0.1–0.4µgl^–1. The occurrence of a few pesticides below the thermocline may be explained by thermal stratification and vertical circulation. Although the thermocline suppressed vertical diffusion in spring and summer during pesticide application periods, a few pesticides remaining at the surface of the lake in winter were transported to the hypolimnion by vertical circulation and remained there even after the reestablishment of the thermocline. The half-lives of pesticides in the lake were estimated to be more than a year for simetryn, half a year for bromobutide, 1.5 months for molinate, and 1 month for dimepiperate. The main cause of elimination for molinate and dimepiperate was estimated to be degradation, that for simetryn was outflow, and for bromobutide both degradation and outflow were significant.     

Estimation of N or C uptake rates by phytoplankton using 15N or 13C: revisiting the usual computation formulae

The uptake of N by phytoplankton is generally estimated usingthe ¹⁵N technique and, under some circumstances, the uptakeof C is estimated using ¹³C. Rigorous examination of formulaefor computing net transport rates leads to several interestingand even unexpected conclusions. These are that the ¹⁵N or ¹³Ctechnique formula for computing net transport rates () is identicalto that of the ¹⁴C technique, in spite of apparent dissimilaritieswhich reflect differences in equipment used for determiningnon-radioactive and radioactive isotopes; the so-called specificuptake rates (V) should not be used with natural samples, exceptas a step in the calculation of transport rates (); estimationof is unaffected by the presence/absence of non-phytoplanktonicpaniculate organic matter (POM) in the incubated sample; thepractice of adding the concentration of tracer to the denominatorof expression representing the concentration of tracer in thedissolved phase at the beginning of incubation should be discontinued;and the concentration of POM should be determined from the inoculatedsample at the end of incubation (or, alternatively, from a sampleincubated in parallel) and not from a water sample taken atthe beginning of the incubation.     

Photosynthetic organic carbon production and respiratory organic carbon consumption in the trophogenic layer of Lake Biwa

Measurement of the photosynthetic production rate in Lake Biwawas camed out from May 1985 to September 1987. In the light-saturatedlayer, the seasonal variation in the photosynthesis rate perchlorophyll a was regulated by water temperature. The depth-integratedphotosynthetic production rate was 0.21-1.48 g C m^–2 day^–1and the maximum value was observed in midsummer when the watertemperature of the mixed surface layer was highesL The criticalnutrient for photosynthesis may be dissolved reactive phosphorus,which was generally <1 µg P 1^–1 throughout theobservation period. In the trophogenic layer, respiratory organiccarbon consumption, estimated from measurement of respiratoiyelectron transport system activity, was 0.35-1.07 (mean 0.66)g C m^–1 day^–1 and corresponded, on average, to 79%of the photosynthetic carbon production rate. This implies thatthe major part of photosynthetic fixed organic matter mightbe recycled in the trophogenic layer. The estimated settlingorganic carbon flux at 20 m depth, from calculation of theseparameters and changes in the particulate organic carbon concentration,was 0.01 (-0.09 to 0.13) g C m^–1 day^–1 The meansettling organic carbon flux measured by sediment trap at 20m was 0.19 (0.09-0.31) g C m^–1 day^–1 higher thanthe estimated value. It seemed that organic matter collectedby sediment trap may contain allochthonous matter and resuspendedepilimnetic sediment matter.     

A Lagrangian model of phytoplankton photosynthetic response in the upper mixed layer

Figure 1: On the top plot, the left vertical axis label shouldread ‘Cumulative Inhibition’ instead of ‘InstantaneousInhibition’. Figures 2, 3 and 5: The horizontal time axis should begin at6 or 0600 hours instead of 18 or 1800 hours.     

A Lagrangian model of phytoplankton photosynthetic response in the upper mixed layer

A previously developed Lagrangian model considered the distributionand light exposure of individual phytoplankton cells in a weaklystratified upper ocean layer mixed by depth-dependent turbulence.This model is coupled with a phytoplankton photoresponse model,previously applied in a Eulerian context, that includes a temporallydecaying dependence on inhibitory light exposure. The combinedmodel output provides the trajectory, light experience and photoresponseof each individual, or the photoresponse central tendency andvariability of the population that occurs at a given depth ata given time. The time dependence of the photoresponse is themain variable considered and determines the shape of the verticalprofile of primary production. Shorter response times yielda strong photoinhibition event that is nearly synchronous withinhibiting incident radiation. Longer response times are characterizedby weaker photoinhibition events that outlive the occurrenceof the inhibiting incident radiation for an interval relatedto the imposed time constant. Under the depth-dependent turbulentmixing regime imposed, photoinhibition is detectable even atwind speeds up to 10 m s^–1. Modeling and technologicalapproaches that compare the bulk characteristics of populationsto the statistical characteristics of the individuals formingthose populations are both under active development. A fruitfulfeedback relationship is likely in the near future.     

An Eulerian model of phytoplankton photosynthetic response in the upper mixed layer

An Eulenan model of an upper mixed layer forced by dynamic andconvective processes is combined with a temporally responsivephotoadaptation model of photosynthesis. Incident radiationis divided into photosyntheticalJy active and inactive componentsto distinguish between biological and physical forcing. Thephysical model is initialized to simulate conditions in LakeTiticaca on August 12, 1982 Model output provides the time courseof water column temperature, phytoplankton photoinhibition andrelative phytoplankton carbon fixation as depth contours forcomparison with published observations. The predicted and observedtemperature profiles generally agree; diurnal changes in specifichumidity are required to more accurately specify heat loss.The predicted photoinhibition resembles the observed photosyntheticstate of the natural community based on fluorescence, but themodeled recovery from photoinhibition is too rapid. This discrepancyalso affects the comparison between predicted and observed bottledeterminations of carbon fixation. The basic formulations inthe model provide approximate fits to field observations. Ifmore complete information on physical and biological initializationsand on temporal forcing were available, the basic formulationscould be refined     

Diel changes of uptake of inorganic carbon and nitrogen by phytoplankton, and the relationship between inorganic carbon and nitrogen uptake in Lake Nakanuma, Japan

Diel changes of uptake of inorganic carbon and nitrogen wereexamined in a small freshwater lake, Lake Nakanuma, Japan, bythe ¹³C and ¹⁵N method. Experiments were earned out in spring,summer and autumn in 1984. Carbon and nitrogen uptake in thelight incubation showed maxima around noon at the three seasons.Carbon uptake ceased at night, but ammonium uptake was fairlylarge at night. In the dark incubation carbon uptake did notoccur. Ammonium uptake showed a maximum at dusk in the darkexperiments. Diel changes of nitrate uptake were less clearthan those of ammonium uptake. These results indicate that nitrogenuptake partly depended on the carbon uptake. Then, we triedto explain the diel changes of nitrogen uptake, assuming thatthe nitrogen uptake partly depends on stored carbohydrate. Thediel changes may be elucidated by the sum of three terms: oneis the term of decay of stored carbohydrate, the second is theterm which indicates cumulative increase of stored carbohydrateand the third is the term which directly depends on light.     

Role of phytoplankton size distribution in lake ecosystems revealed by a comparison of whole plankton community structure between Lake Baikal and Lake Biwa

The influence of the size distribution of phytoplankton on changes in the planktonic food web structures with eutrophication was examined using natural planktonic communities in two world-famous lakes: Lake Baikal and Lake Biwa. The size distribution of phytoplankton and the ratio of heterotrophic to autotrophic biomass (H/A ratio), indicating the balance between primary production and its consumption, were investigated in the lakes of different trophic status. The results revealed that microphytoplankton (>20μm) in mesotrophic Lake Biwa, and picophytoplankton (<2μm) or nanophytoplankton (2–20μm) in oligotrophic Lake Baikal, comprised the highest proportion of the total phytoplankton biomass. The H/A ratio was lower in Lake Biwa (<1) than in Lake Baikal (>1). The low H/A ratio in Lake Biwa appeared to be the consequence of the lack of consumption of the more abundant microphytoplankton, which were inferior competitors in nutrient uptake under oligotrophic conditions but less vulnerable to grazing. As a result, unconsumed microphytoplankton accumulated in the water column, decreasing the H/A ratio in Lake Biwa. Our results showed that food web structure and energy flow in planktonic communities were greatly influenced by the size distribution of phytoplankton, in conjunction with bottom-up (nutrient uptake) and top-down (grazing) effects at the trophic level of primary producers.     

Growth and phosphorus uptake of summer phytoplankton in Lake Erken (Sweden)

The thermal stratification in Lake Erken was short and relativelyunstable in 1989. Changes in the species composition of thephytoplankton between early May and August followed the generalsuccession pattern outlined for other temperate lakes. Fast-growing,r-strategist cryptophytes, dominant in the early phase of succession,could be separated sufficiently by 12 µm membrane filtersfrom larger K-strategists like Ceratium hirundinella and Gloeotrichiaechinulata which dominated in July. Under more turbulent conditions,the biomass of diatoms increased, and these species were also>12 µm. Growth rates of the phytoplankton and thoseof the two size groups were sensitive to the species composition,but fitted reasonably to the Droop model. Long turnover timesof orthophosphate in the water, the Phosphorus Deficiency Indicatordefined here as the ratio of the light-saturated rate of photosynthesisand the conductivity coefficient of phosphate uptake, and relativegrowth rates generally indicated low P-deficiency. Moderatedeficiency was observed in late July, towards the end of thestratification period. Steady-state net P-uptake rates werecalculated from the Droop model and compared with instantaneousnet P-uptake rates estimated from ³²P uptake kinetics by thelinear force-flow relationship of Falkner et al. (Arch. Microbiol.,152, 353–361, 1989). The two data sets showed surprisinglysimilar seasonal trends. Depletion of epilimnetic soluble reactivephosphorus (SRP) resulted in enhanced utilization of intracellularlystored P. Such periods were, however, interrupted by elevatedSRP inputs to the epilimnion that led to luxury P uptake anda low incidence of P deficiency.     

Long-term variation in abundance of the non-native phytoplankton Micrasterias hardyi (Zygnematophyceae,Streptophyta) in Lake Biwa,Japan

Limnology - Alien species have invaded worldwide and altered native biodiversity and ecosystem functions. In Lake Biwa, Japan, Micrasterias hardyi—considered an endemic species in...     

Effects of zooplankton on nutrient availability and seston C : N : P stoichiometry in inshore waters of Lake Biwa, Japan

Forty-eight-hour experimental manipulations of zooplankton biomass were performed to examine the potential effects of zooplankton on nutrient availability and phytoplankton biomass (as measured by seston concentration) and C : N : P stoichiometry in eutrophic nearshore waters of Lake Biwa, Japan. Increasing zooplankton, both mixed-species communities and Daphnia alone, consistently reduced seston concentration, indicating that nearshore phytoplankton were generally edible. The zooplankton clearance rates of inshore phytoplankton were similar to rates measured previously for offshore phytoplankton. Increased zooplankton biomass led to increased concentrations of nutrients (NH₄-N, soluble reactive phosphorus [SRP]). Net release rates were higher than those found in previous measurements made offshore, reflecting the nutrient-rich nature of inshore seston. Zooplankton nutrient recycling consistently decreased TIN : SRP ratios (TIN = NH₄ + NO₃ + NO₂). This effect probably resulted from the low N : P ratios of nearshore seston, which were lower than those commonly found in crustacean zooplankton and thus resulted in low retention efficiency of P (relative to N) by the zooplankton. Thus, zooplankton grazing inshore may ameliorate algal blooms due to direct consumption but tends to create nutrient supply conditions with low N : P, potentially favoring cyanobacteria. In comparison with previous findings for offshore, it appears that potential zooplankton effects on phytoplankton and nutrient dynamics differ qualitatively in inshore and offshore regions of Lake Biwa. Received: September 4, 2000 / Accepted: January 23, 2001     

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.