Interaction among Non-toxic Phytoplankton,Toxic Phytoplankton and Zooplankton: Inferences from Field Observations

We explore the mutual dependencies and interactions among different groups of species of the plankton population, based on an analysis of the long-term field observations carried out by our group in the North–West coast of the Bay of Bengal. The plankton community is structured into three groups of species, namely, non-toxic phytoplankton (NTP), toxic phytoplankton (TPP) and zooplankton. To find the pair-wise dependencies among the three groups of plankton, Pearson and partial correlation coefficients are calculated. To explore the simultaneous interaction among all the three groups, a time series analysis is performed. Following an Expectation Maximization (E-M) algorithm, those data points which are missing due to irregularities in sampling are estimated, and with the completed data set a Vector Auto-Regressive (VAR) model is analyzed. The overall analysis demonstrates that toxin-producing phytoplankton play two distinct roles: the inhibition on consumption of toxic substances reduces the abundance of zooplankton, and the toxic materials released by TPP significantly compensate for the competitive disadvantages among phytoplankton species. Our study suggests that the presence of TPP might be a possible cause for the generation of a complex interaction among the large number of phytoplankton and zooplankton species that might be responsible for the prolonged coexistence of the plankton species in a fluctuating biomass.     

Plankton blooms induced by turbulent flows

Plankton play an important role in the ecology of the ocean and the climate because of their participation in the global carbon cycle at the base of the food chain. However, damaging plankton blooms can sometimes occur and are initially characterized by sudden transient increases in the phytoplankton population. They are thought to be driven by several effects, such as seasonal variations in temperature and salinity, and nutrient mixing. Furthermore, phytoplankton and zooplankton have different buoyancy properties, leading to a differential response in turbulent environments. In this paper, we investigate this effect in a model of advected plankton dynamics. We find that, over a range of parameter values, flows of marine species subjected to inertial/viscous forces naturally lead to patchiness and, in turn, periodically sustained plankton blooms.     

How do sinking phytoplankton species manage to persist?

Phytoplankton require light for photosynthesis. Yet, most phytoplankton species are heavier than water and therefore sink. How can these sinking species persist? Somehow, the answer should lie in the turbulent motion that redisperses sinking phytoplankton over the vertical water column. Here, we show, using a reaction-advection-diffusion equation of light-limited phytoplankton, that there is a turbulence window sustaining sinking phytoplankton species in deep waters. If turbulent diffusion is too high, phytoplankton are mixed to great depths, and the depth-averaged light conditions are too low to allow net positive population growth. Conversely, if turbulent diffusion is too low, sinking phytoplankton populations end up at the ocean floor and succumb in the dark. At intermediate levels of turbulent diffusion, however, phytoplankton populations can outgrow both mixing rates and sinking rates. In this way, the reproducing population as a whole can maintain a position in the well-lit zone near the top of the water column, even if all individuals within the population have a tendency to sink. This theory unites earlier classic results by Sverdrup and Riley as well as our own recent findings and provides a new conceptual framework for the understanding of phytoplankton dynamics under the influence of mixing processes.     

Ammonia-oxidizing archaea release a suite of organic compounds potentially fueling prokaryotic heterotrophy in the ocean

Ammonia-oxidizing archaea (AOA) constitute a considerable fraction of microbial biomass in the global ocean, comprising 20%–40% of the ocean's prokaryotic plankton. However, it remains enigmatic to what extent these chemolithoautotrophic archaea release dissolved organic carbon (DOC). A combination of targeted and untargeted metabolomics was used to characterize the exometabolomes of three model AOA strains of the Nitrosopumilus genus. Our results indicate that marine AOA exude a suite of organic compounds with potentially varying reactivities, dominated by nitrogen-containing compounds. A significant fraction of the released dissolved organic matter (DOM) consists of labile compounds, which typically limit prokaryotic heterotrophic activity in open ocean waters, including amino acids, thymidine and B vitamins. Amino acid release rates corresponded with ammonia oxidation activity and the three Nitrosopumilus strains predominantly released hydrophobic amino acids, potentially as a result of passive diffusion. Despite the low contribution of DOC released by AOA (~0.08%–1.05%) to the heterotrophic prokaryotic carbon demand, the release of physiologically relevant metabolites could be crucial for microbes that are auxotrophic for some of these compounds, including members of the globally abundant and ubiquitous SAR11 clade.     

Effects of Additions of DOC on Pelagic Biota in a Clearwater System: Results from a Whole Lake Experiment in Northern Sweden

An oligotrophic clearwater lake, initially characterized by a pronounced dominance of autotrophic phytoplankton and mostly by one species, the green alga Botryococcus, was subject to additions of dissolved organic carbon in the form of white sugar (sucrose) during two consecutive years. The hypothesis tested was that it is organic carbon per se, and not other possible effects of humic substances, that determines the differences in structure of the planktonic ecosystem between humic and clearwater lakes. The additions of DOC resulted in a significant increase in bacterial biomass and a decrease in the biomass of autotrophic phytoplankton. The biomass of mixotrophic and heterotrophic flagellates instead increased significantly, whereas no effects were found to propagate to higher trophic levels. As a result of the changes among biota, total planktonic biomass also decreased to a level typical of nearby humic lakes. We suggest that it is the carbon component of humic material and its utilization by bacterioplankton that determines the structure and function of the pelagic food web in humic lakes.     

The Absorption of Light in Lakes: Negative Impact of Dissolved Organic Carbon on Primary Productivity

Colored dissolved organic matter (CDOM) absorbs a substantial fraction of photosynthetically active radiation (PAR) in boreal lakes. However, few studies have systematically estimated how this light absorption influences pelagic primary productivity. In this study, 75 boreal lakes spanning wide and orthogonal gradients in dissolved organic carbon (DOC) and total phosphorus (TP) were sampled during a synoptic survey. We measured absorption spectra of phytoplankton pigments, CDOM, and non-algal particles to quantify the vertical fate of photons in the PAR region. Area-specific rates of gross primary productivity (PP_A) were estimated using a bio-optical approach based on phytoplankton in vivo light absorption and the light-dependent quantum yield of photochemistry in PSII measured by a PAM fluorometer. Subsequently, we calculated the effects of CDOM, DOC, and TP concentration on PP_A. CDOM absorbed the largest fraction of PAR in the majority of lakes (mean 56.3%, range 36.9–76.2%), phytoplankton pigments captured a comparatively minor fraction (mean 6.6%, range 2.2–28.2%). PP_A estimates spanned from 45 to 993 mg C m^?2 day^?1 (median 286 mg C m^?2 day^?1). We found contrasting effects of CDOM (negative) and TP (positive) on PP_A. The use of DOC or CDOM as predictors gave very similar results and the negative effect of these variables on PP_A can probably be attributed to shading. A future scenario of increased DOC, which is highly correlated with CDOM in these lakes, might impose negative effects on areal primary productivity in boreal lakes.     

Microplanktonic regeneration of ammonium and dissolved organic nitrogen in the upwelling area of the NW of Spain: relationships with dissolved organic carbon production and phytoplankton size-structure

Ammonium regeneration and dissolved organic nitrogen (DON) releasewere studied experimentally in the euphotic zone of shelf andoceanic waters of NW Spain in relation to coastal upwellingdynamics and the size-structure of phytoplankton communities.Incubations of plankton labelled with [¹⁵N]ammonium were madeduring four cruises, two of which also included size-fractionateddeterminations of chlorophyll a and primary production, andexperimental determinations of production rates of dissolvedorganic carbon (DOC) using ¹⁴C. Inorganic nitrogen concentrationswere mainly related to nitrate enrichment by upwelling pulses,while ammonium concentrations were generally low in all situations.Ammonium did not accumulate in the study area, suggesting adaily time scale coupling between regeneration and uptake. Incontrast, DON largely exceeded inorganic nitrogen in all situationsand generally increased from spring to autumn. Ammonium regenerationwas positively correlated with DON release and both rates showedthe largest variation in summer, with minimum values duringactive upwelling and maximum values when upwelling relaxed.Comparison of DON stocks and rates in different shelf areassuggests that DON release near the coast during summer was morepersistent in the water than DON release in off-shelf and oceanicareas. The carbon:nitrogen ratio of DOC and DON release rateswas highly variable, revealing a large excess of DOC comparedwith DON. This excess can be attributed to either an underestimateof total DON release (as only release from ammonium was measured)or to an enhanced production of carbon-rich organic substancesby diatoms in coastal areas. By considering a broad range oftrophic situations, this study reveals a fundamental differencebetween short term release of DOC and DON by plankton. Physiologicalprocesses (such as carbohydrate exudation by diatoms) seem tobe the cause of large DOC excess, whereas trophic processes(such as grazing) are more likely the cause of enhanced DONrelease.     

Toxic phytoplankton-induced spatiotemporal patterns

Here we consider a reaction diffusion system of three plankton populations, a zooplankton feeding on two phytoplankton populations, in two different settings. Firstly, the two phytoplanktons are both non-toxic and both enhance the growth of the grazing zooplankton. Secondly, we assume that one of the phytoplankton releases toxin and thereby inhibits the growth of the zooplankton. Our analytic and numerical study shows that the spatiotemporal distribution of the plankton species is uniform when both phytoplankton populations are non-toxic. However, in the presence of toxin-producing phytoplankton, the biomass distribution of all the plankton populations becomes inhomogeneous.     

Nutrient availability as major driver of phytoplankton-derived dissolved organic matter transformation in coastal environment

Incubation experiments were performed to examine the processing of fresh autochthonous dissolved organic matter (DOM) produced by coastal plankton communities in spring and autumn. The major driver of observed DOM dynamics was the seasonally variable inorganic nutrient status and characteristics of the initial bulk DOM, whereas the characteristics of the phytoplankton community seemed to have a minor role. Net accumulation of dissolved organic carbon (DOC) during the 18-days experiments was 3.4 and 9.2 µmol l^?1 d^?1 in P-limited spring and N-limited autumn, respectively. Bacterial bioassays revealed that the phytoplankton-derived DOC had surprisingly low proportions of biologically labile DOC, 12.6% (spring) and 17.5% (autumn). The optical characteristics of the DOM changed throughout the experiments, demonstrating continuous heterotrophic processing of the DOM pool. However, these temporal changes in optical characteristics of the DOM pool were not the same between seasons, indicating seasonally variable environmental drivers. Nitrogen and phosphorus availability is likely the main driver of these seasonal differences, affecting both phytoplankton extracellular release of DOM and its heterotrophic degradation by bacteria. These findings underline the complexity of the DOM production and consumption by the natural planktonic community, and show the importance of the prevailing environmental conditions regulating the DOM pathways.     

The microbial loop in flowing waters

The microbial loop in flowing waters is dependent on allochthonous sources of carbon, which vary in quality. The proportion of dissolved organic carbon (DOC) that can be degraded ranges from <1 to over 50%, and the bioavailability of DOC (micrograms bacterial biomass produced per milligram DOC present) ranges over two orders of magnitude. Bioavailability of DOC is predictable from the ratio of H/C and O/C of the DOC, but further work is needed to develop simple predictors of bioavailability of DOC in a range of environments. Consumers of bacteria in streams range in size from protists to insect larvae, with highest rates of bacterial consumption found among the meiofauna and certain filter feeders and grazers. Because there appear to be fewer trophic transfers in the lotic microbial loop, it functions more as a link in flowing waters than it appears to do in the marine plankton.     

Life in transition: balancing inertial and viscous forces by planktonic copepods

Copepods (1-10 mm aquatic crustaceans moving at 1-1000 mm s(-1)) live at Reynolds numbers that vary over 5 orders of magnitude, from 10(-2) to 10(3). Hence, they live at the interface between laminar and turbulent regimes and are subject to the physical constraints imposed by both viscous and inertial realms. At large scales, the inertially driven system enforces the dominance of physically derived fluid motion; plankton, advected by currents, adjust their life histories to the changing oceanic environment. At Kolmogorov scales, a careful interplay of evenly matched forces of biology and physics occurs. Copepods conform or deform the local physical environment for their survival, using morphological and behavioral adaptations to shift the balance in their favor. Examples of these balances and transitions are observed when copepods engage in their various survival tasks of feeding, predator avoidance, mating, and signaling. Quantitative analyses of their behavior give measures of such physical properties of their fluid medium as energy dissipation rates, molecular diffusion rates, eddy size, and eddy packaging. Understanding the micromechanics of small-scale biological-physical-chemical interactions gives insight into factors influencing large-scale dynamics of copepod distribution, patchiness, and encounter probabilities in the sea.     

From mice to elephants: overturning the ‘one size fits all’ paradigm in marine plankton food chains

It is widely believed that consumer control is a weak regulator of marine phytoplankton communities. It remains unclear, however, why this should be the case when marine consumers routinely regulate their prey at higher trophic levels. One possibility is that the weak consumer control of phytoplankton communities results from the inability of field researchers to effectively account for consumer–prey trophic relationships operating at the scale of the plankton. We explored this issue by reviewing studies of trophic control in marine plankton. Experimental studies indicate that size is a critical determinant of feeding relationships among plankton. In sharp contrast, of the 51 field studies reviewed, 78% did not distinguish among the sizes or species of phytoplankton and their consumers, but instead assumed a general bulk phytoplankton–zooplankton trophic connection. Such an approach neglects the possibility that several trophic connections may separate the smallest phytoplankton (0.2 μm) from the larger zooplankton (~ 1000 μm), a remarkable size differential exceeding that between a mouse (~10 cm) and an elephant (~2500 cm). The size‐based approach we propose integrates theory, experiments and field observations and has the potential to greatly enhance our understanding of the causes and consequences of recently documented restructuring of plankton communities.     

Effect of the rate of phytoplankton growth on the spaced-time dynamics of plankton communities in an homogeneous environment

We use a conceptual mathematical reaction-diffusion model to investigate the mechanisms of spatial structure formation and complex temporal dynamics of plankton in a heterogeneous environment. We take into account basic trophic interactions, namely, "prey-predator" interactions between phytoplankton, zooplankton, and fish in upper layers of natural waters. We consider plankton as a passive contaminant in turbulent waters. We show that plankton structure formation can result from the difference in phytoplankton growth rate in neighboring habitats. Phytoplankton and zooplankton biomass is shown to undergo both regular and chaotic oscillations. The fish predation rate substantially affects the spatial and temporal dynamics of plankton in a heterogeneous environment.     

Light and nutrient control phytoplankton biomass responses to global change in northern lakes

Global change affects terrestrial loadings of colored dissolved organic carbon (DOC) and nutrients to northern lakes. Still, little is known about how phytoplankton respond to changes in light and nutrient availability across gradients in lake DOC. In this study, we used results from whole‐lake studies in northern Sweden to show that annual mean phytoplankton biomass expressed unimodal curved relationships across lake DOC gradients, peaking at threshold DOC levels of around 11 mg/L. Whole‐lake single nutrient enrichment in selected lakes caused elevated biomass, with most pronounced effect at the threshold DOC level. These patterns give support to the suggested dual control by DOC on phytoplankton via nutrient (positively) and light (negatively) availability and imply that the lakes' location along the DOC axis is critical in determining to what extent phytoplankton respond to changes in DOC and/or nutrient loadings. By using data from the large Swedish Lake Monitoring Survey, we further estimated that 80% of northern Swedish lakes are below the DOC threshold, potentially experiencing increased phytoplankton biomass with browning alone, and/or combined with nutrient enrichment. The results support the previous model results on effects of browning and eutrophication on lake phytoplankton, and provide important understanding of how northern lakes may respond to future global changes.     

Constant release of photosynthate from marine phytoplankton.

The release rate of dissolved organic carbon (DOC) by unialgal cultures and natural phytoplankton assemblages was constant over a wide range of dissolved inorganic carbon concentrations. DOC release was not proportional to the particulate organic carbon production rate. We postulate that intracellular DOC, fated for release, exists either as a separate pool from that leading to particulate organic carbon production or that there is active metabolic control on one portion of a common pool.     

Critical conditions for phytoplankton blooms

We motivate and analyse a reaction—advection—diffusion model for the dynamics of a phytoplankton species. The reproductive rate of the phytoplankton is determined by the local light intensity. The light intensity decreases with depth due to absorption by water and phytoplankton. Phytoplankton is transported by turbulent diffusion in a water column of given depth. Furthermore, it might be sinking or buoyant depending on its specific density. Dimensional analysis allows the reduction of the full problem to a problem with four dimensionless parameters that is fully explored. We prove that the critical parameter regime for which a stationary phytoplankton bloom ceases to exist, can be analysed by a reduced linearized equation with particular boundary conditions. This problem is mapped exactly to a Bessel function problem, which is evaluated both numerically and by asymptotic expansions. A final transformation from dimensionless parameters back to laboratory parameters results in a complete set of predictions for the conditions that allow phytoplankton bloom development. Our results show that the conditions for phytoplankton bloom development can be captured by a critical depth, a compensation depth, and zero, one or two critical values of the vertical turbulent diffusion coefficient. These experimentally testable predictions take the form of similarity laws: every plankton—water—light-system characterized by the same dimensionless parameters will show the same dynamics.     

Predator‐induced changes in dissolved organic carbon dynamics

The fate of dissolved organic carbon (DOC) is partly determined by its availability to microbial degradation. Organisms at upper trophic levels could influence the bioavailability of DOC via cascading effects on primary producers and bacteria. Here we experimentally tested whether the presence of fish in aquatic food webs can indirectly affect the composition of the DOC pool. We found that fish had strong positive effects on phytoplankton biomass that affected the dynamics of DOC composition. Specifically, fish increased protein‐like, algae‐derived DOC mid‐experiment, concurrent with the strongest fish‐induced increase in phytoplankton biomass. Fish also increased bacterial abundance, altered the community composition and diversity of bacteria, and temporarily increased DOC compounds with fluorescence properties indicative of microbially‐reprocessed organic matter. Overall, our experiment revealed that fish can positively influence the substrate (algae‐produced DOC) and the key players (bacteria) of the microbial carbon pump. Consequently, fish could contribute to carbon sequestration by stimulating both the production of bioavailable DOC and the microbial degradation of bioavailable to persistent DOC. We propose this as a novel mechanism whereby the loss of predators from global ecosystems could alter carbon cycling.     

Primary production and phytoplankton composition in relation to DOC input and bacterioplankton production in humic Lake Örträsket

1. The biomass and production of picophytoplankton, large phytoplankton and heterotrophic bacterioplankton were measured in humic Lake Örträsket, northern Sweden during four consecutive summers.
2. High flow episodes, carrying fresh dissolved organic carbon (DOC) into the lake, always stimulated heterotrophic bacterial production at the expense of primary production. Primary production never exceeded bacterial production for approximately 20 days after such an episode had replenished epilimnial DOC. We suggest that allochthonous DOC is an energy source that stimulates bacterioplankton that, because of their efficient uptake of inorganic nutrients, are then able to outcompete phytoplankton. After the exhaustion of readily available DOC, phytoplankton were able to dominate epilimnion production in Lake Örträsket.
3. Biomass production was higher when dominated by phytoplankton than by bacterioplankton, despite a similar utilization of nutrients in the epilimnion throughout the summer. We propose that different C : N : P ratios of bacterioplankton and phytoplankton permit the latter to produce more carbon (C) biomass per unit of available inorganic nutrients than bacterioplankton.     

Sources of dissolved and particulate organic material in Loch Vale Watershed,Rocky Mountain National Park,Colorado, USA

The sources of both dissolved organic carbon (DOC) and particulate organic carbon (POC) to an alpine (Sky Pond) and a subalpine lake (The Loch) in Rocky Mountain National Park were explored for four years. The importance of both autochthonous and allochthonous sources of organic matter differ, not only between alpine and subalpine locations, but also seasonally. Overall, autochthonous sources dominate the organic carbon of the alpine lake, while allochthonous sources are a more significant source of organic carbon to the subalpine lake. In the alpine lake, Sky Pond, POC makes up greater than one third of the total organic matter content of the water column, and is related to phytoplankton abundance. Dissolved organic carbon is a product of within-lake activity in Sky Pond except during spring snowmelt and early summer (May–July), when stable carbon isotope ratios suggest a terrestrial source. In the subalpine lake, The Loch, DOC is a much more important constituent of water column organic material than POC, comprising greater than 90% of the spring snowmelt organic matter, and greater than 75% of the organic matter over the rest of the year. Stable carbon isotope ratios and a very strong relation of DOC with soluble Al_(tot) indicate DOC concentrations are almost entirely related to flushing of soil water from the surrounding watershed during spring snowmelt. Stable carbon isotope ratios indicate that, for both lakes, phytoplankton is an important source of DOC in the winter, while terrestrial material of plant or microbial origin contributes DOC during snowmelt and summer.