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Microbial plankton response to resource limitation: Insights from the community structure and seston stoichiometry in Florida Bay, USA
Abstract and Figures
Concentrations of dissolved and particulate nutrients, chlorophyll, and microorganisms (0.01 to 200 mu m) were simultaneously measured during a 1 d survey of 12 stations in Florida Bay, USA, to characterize the microbial plankton community with respect to resource limitation. Three distinct types of trophic conditions, reflected in seston elemental stoichiometry and community structure, were identified within the bay. The first type, characteristic of the isolated eastern region, had low nutrient concentrations, imbalanced stoichiometry, and small microbial biomass with a large proportion of bacteria. The microbial community in this region was characterized by weak relationships between microzooplankton and phytoplankton and the predominance of mixotrophic taxa and the autotrophic ciliate Mesodinium rubrum. The second type, found in the north-central region influenced by Taylor Slough inflow, had elevated nutrient concentrations, elemental stoichiometry skewed toward N, and high turbidity. Under these conditions, the picocyanobacterium Synechococcus formed a dense bloom and coincided with an abundant, multi-step microbial food web. Finally, at the boundary with the Gulf of Mexico, low concentrations of nutrients were balanced at approximately the Redfield ratio and supported nanophytoplankton that were tightly correlated with microzooplankton. These data are consistent with the notion of P Limitation in Florida Bay but also demonstrate that Si, Light, and N may be co-limiting to phytoplankton in the eastern, north-central, and western boundary regions, respectively. Our findings suggest that multiple resource gradients, in conjunction with microbial food web processes, are important factors determining the plankton community structure in Florida Bay and should be considered in studies on ecological disturbances.
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... Regions based on those described by Phlips et al. (1995) were employed for this study to segregate the bay into 5 regions, i.e. northeast, east, north central, south central, and west (Fig. 1A). The West Bay experiences nitrogen limitation, whereas the East Bay is phosphorus-limited (Lavrentyev et al. 1998, Boyer et al. 1999. The East Bay is starved of phosphorus primarily as a function of its calcium-carbonate-rich sediments (Zhang et al. 2004), which bind phosphorus and render it unavailable for organic assimilation. ...
... The diversity in the phytoplankton community of the eastern regions of the bay is believed to be driven by severe resource limitation (i.e. extreme phosphorus limitation), which promotes a variety of survival strategies (Lavrentyev et al. 1998). ...
Estuarine environments support dynamic phytoplankton blooms, especially in lowlatitude regions, where the effects of local drivers dominate. Identifying key bloom drivers from entangled ecological and anthropogenic influences is particularly challenging in stressed systems where several disturbances interact. Additionally, processes controlling bloom and non-bloom phytoplankton biomass dynamics can differ spatially, further confounding characterization of disturbance regimes that create bloom-favorable conditions. This study aims to explore the question of whether the shift from non-bloom to bloom conditions is matched by a shift in the relative importance of water quality drivers. Florida Bay (USA), a shallow subtropical inner shelf lagoon, was chosen as the study site due to its unique bloom dynamics and low-latitude location, as well as for the availability of long-term (16 yr) water quality data consisting of monthly measurements from 28 locations across the 2200 km2 bay. At each of the locations, we applied a novel thresholdbased quantile regression analysis to chlorophyll a data to define bloom conditions, separate data from non-bloom conditions, and evaluate phytoplankton biomass dynamics of each of the 2 states. The final suite of explanatory covariates revealed spatial trends and differences in the relative importance of water quality descriptors of phytoplankton between the 2 conditions. The effects of turbidity and salinity on phytoplankton biomass became pronounced during blooms, whereas non-bloom conditions were primarily explained by autoregressive phytoplankton biomass trends and nutrient dynamics. The proposed analytical approach is not limited to any particular aquatic system type, and can be used to produce practical spatiotemporal information to guide management, restoration, and conservation efforts.
... Florida Bay has experienced increasing occurrences of phytoplankton blooms (e.g., Lavrentyev et al. 1998, Boyer et al. 1999, Phlips et al. 1999, Boyer et al. 2006. These blooms consist primarily of picocyanobacteria from the genus Synechococcus and occur most frequently in the north-central region of Florida Bay (Phlips et al. 1999). ...
... Previous studies have suggested that primary production in Florida Bay is P-limited Robblee 1999, Cotner et al. 2000). However, N limitation or co-limitation also has been observed in some cases (e.g., Lavrentyev et al. 1998). In the present study, available P (as o-PO 4 3-) was low (≤ 0.12 µM; Table 1), but DIN concentrations also were low in most cases. ...
... Concentrations of PO 4 3values remained at or near the analytical limit of detection throughout the time course studied herein (Table 1). Whereas the eastern bay region is generally considered to be severely P-limited (Fourqurean et al. 1992;Hitchcock et al. 1998;Lavrentyev et al. 1998), the central bay generally has been thought to have sufficient total dissolved N and P (inorganic and organic) to support normal phytoplankton growth (Boyer et al. 1999;Fourqurean and Robblee 1999). Most of the P in the central to eastern bays is present in the sediments either in the solid phase as loosely bound oxy-hydroxides or as apatite (Koch et al. 2001). ...
The availability of dissolved inorganic and organic nutrients and their transformations along the fresh to marine continuum are being modified by various natural and anthropogenic activities and climate-related changes. Subtropical central and eastern Florida Bay, located at the southern end of the Florida peninsula, is classically considered to have inorganic nutrient conditions that are in higher-than-Redfield ratio proportions, and high levels of organic and chemically-reduced forms of nitrogen. However, salinity, pH and nutrients, both organic and inorganic, change with changes in freshwater flows to the bay. Here, using a time series of water quality and physico-chemical conditions from 2009 to 2019, the impacts of distinct changes in managed flow, drought, El Niño-related increases in precipitation, and intensive storms and hurricanes are explored with respect to changes in water quality and resulting ecosystem effects, with a focus on understanding why picocyanobacterial blooms formed when they did. Drought produced hyper-salinity conditions that were associated with a seagrass die-off. Years later, increases in precipitation resulting from intensive storms and a hurricane were associated with high loads of organic nutrients, and declines in pH, likely due to high organic acid input and decaying organic matter, collectively leading to physiologically favorable conditions for growth of the picocyanobacterium, Synechococcus spp. These conditions, including very high concentrations of NH 4 ⁺ , were likely inhibiting for seagrass recovery and for growth of competing phytoplankton or their grazers. Given projected future climate conditions, and anticipated cycles of drought and intensive storms, the likelihood of future seagrass die-offs and picocyanobacterial blooms is high.
... Management implications of changes in the nutrient quantity and quality with respect to changes due to the C-111 project are also considered, from the perspective of algal bloom control. It is generally accepted that P is the limiting nutrient for primary production in Florida Bay, whereas N and silicon are not (Fourqurean et al., 1993;Phlips and Badylak, 1996;Hitchcock et al., 1998;Lavrentyev et al., 1998;Price et al., 2006). These experiments demonstrated that P additions substantially elevated the overall phytoplankton biomass (Fig. 2a) and all studied phytoplankton groups, picocyanobacteria, cryptophytes, diatoms, and peridinin-containing dinoflagellates (Fig. 2b-e). ...
... therein, 69] and in natural phytoplankton communities to a lesser degree [2,9,[70][71][72]. The comparison of our PN:PP ratios with those from coastal [72][73][74][75][76][77][78], lotic and lentic ecosystems [79][80][81], that continuously or episodically experience elevated levels of nutrients, suggested that high DIN:PO 3− 4 ratios caused PN:PP ratios to deviate from 16:1 in the Cardak Lagoon. The extent of deviation in measured PN:PP ratios from the Redfield ratio was generally similar to those seen under severely P-limited algal cultures [68], in most nutrient-impoverished parts of the ocean [82,83] and in aquatic ecosystems with highly disturbed nutrient stoichiometry [84]. ...
Human impacts on carbon, nitrogen and phosphorus cycles have differentially increased the flux of C, N and P to the coastal zone creating an altered environment with respect to nutrient stoichiometry for production and transfer of organic matter. Such changes can be more pronounced in closed and semi-enclosed ecosystems. The spatio-temporal variability in chl a, phytoplankton C, N and P content and stoichiometry were measured along with nutrients to reveal relations between them in a coastal lagoon. High nitrate concentrations and low availability of phosphate produced skewed nutrient stoichiometry that reflected itself in the large deviations of PC:PN and PN:PP from their corresponding Redfield ratios while the dynamic nature of fluctuations in nutrient concentrations led to wide variations in phytoplankton C, N and P content and in their ratios. The findings of the study provide insights into the possible alterations in phytoplankton stoichiometry in similar ecosystems receiving high
inputs which is not balanced with phosphorus and/or where P-reduction is the mode of eutrophication control as both can produce skewed nutrient stoichiometry.
Link for full text:http://www.tandfonline.com/doi/full/10.1080/02757540.2017.1316492
... The microbial food web (MFW) includes heterotrophic, autotrophic, and mixotrophic prokaryotes and eukaryotes. Multiple cascading trophic interactions within the MFW can affect the biogeochemical N cycle and have feedback effects on trophic conditions in coastal waters (Lavrentyev et al., 1998). MFW structure also is an important factor regulating algal community dynamics in eutrophic, cyanobacteria-dominated systems (Elser, 1999). ...
Nitrogen dynamics and microbial food web structure were characterized in subtropical, eutrophic, large (2,338 km2), shallow (1.9 m mean depth), and polymictic Lake Taihu (China) in Sept–Oct 2002 during a cyanobacterial bloom. Population growth and industrialization are factors in trophic status deterioration in Lake Taihu. Sites for investigation were selected along a transect from the Liangxihe River discharge into Meiliang Bay to the main lake. Water column nitrogen and microbial food web measurements were combined with sediment-water interface incubations to characterize and identify important processes related to system nitrogen dynamics. Results indicate a gradient from strong phosphorus limitation at the river discharge to nitrogen limitation or co-limitation in the main lake. Denitrification in Meiliang Bay may drive main lake nitrogen limitation by removing excess nitrogen before physical transport to the main lake. Five times higher nutrient mineralization rates in the water column versus sediments indicate that sediment nutrient transformations were not as important as water column processes for fueling primary production. However, sediments provide a site for denitrification, which, along with nitrogen fixation and other processes, can determine available nutrient ratios. Dissimilatory nitrate reduction to ammonium (DNRA) was important, relative to denitrification, only at the river discharge site, and nitrogen fixation was observed only in the main lake. Reflecting nitrogen cycling patterns, microbial food web structure shifted from autotrophic (phytoplankton dominated) at the river discharge to heterotrophic (bacteria dominated) in and near the main lake.
Florida Bay nutrient budgets have shown that the majority of existing and influent nitrogen (N) is in organic forms. Consequently, local remineralization processes have been found to regulate the supply of dissolved inorganic nitrogen (DIN). Sponges have dominated benthic animal biomass in Florida Bay and are known to influence local DIN concentrations through remineralization organic matter, yet the role of these organisms in local N budgets is largely unaddressed. We quantified the role of sponges in N cycling in Florida Bay during 2012–2013 by constructing an N budget for a sponge‐rich basin. Surveys of sponge biomass conducted in Mystery Basin found sponges at 57 of the 59 assessed stations. Sponge population maxima reached 21 individuals m−2 and biomass contributions as high as 4.4 Lsponge m−2. We estimated an average areal DIN contribution from total sponge biomass of 0.59 ± 0.28 mmol N m−2 d−1. However, calculated fluxes from the 59 stations exhibited significant spatial variability associated with changes in the size and species composition of the sponge community; peak N fluxes reached 3.5 ± 0.9 mmol N m−2 d−1 in areas with large populations of high microbial abundance sponges. The average flux from the sponge community was the largest of the estimated sources of DIN to Mystery Basin, representing roughly half of the overall N sourcing. This N satisfied more than half of the demand by primary productivity. These results indicate that sponges are important sources of inorganic N to Florida Bay environments.
Nutrient concentrations in seawater, and C, N, P, Si and chlorophyll-a content in different-sized particulates were measured in Jiaozhou Bay, and C, N, P, Si composition in different-sized fractions of phytoplankton and their ecological responses to nutrient structure of the seawater were studied. Microphytoplankton and nanophytoplankton were dominant in Jiaozhou Bay. High C (16.50–20.97 μmol L⁻¹), N (2.46–2.99 μmol L⁻¹), and low P (0.06–0.12 μmol L⁻¹), Si (0.18–0.57 μmol L⁻¹) content, and high N/P (24.7–64.6) and low Si/P (4.4–10.8) and Si/N (0.06–0.20) ratios were found in all sized groups of particulates. These values reflected the elemental compositions of different-sized fractions of phytoplankton as being an ecological response to the nutrients in the seawater. The ratios deviated significantly from the Redfield values. The nutrient composition of seawater and particulates and their relationship to chlorophyll-a showed that phytoplankton growth was possibly limited by Si. Si limitation appears favorable for controlling the ecological equilibrium of Jiaozhou Bay. Different-sized fractions of phytoplankton had different suitability to nutrient structures of the seawater. Among phytoplankton-sized groups, nanophytoplankton and microphytoplankton growths were more adaptable in eutrophic Jiaozhou Bay, and more competitive for assimilation of Si. This is consistent with their diatom-dominated composition, controlling the biomass and productivity of phytoplankton in Jiaozhou Bay.
Cyanophages infecting marine Synechococcus cells were frequently very abundant and were found in every seawater sample along a transect in the western Gulf of Mexico and during a 28-month period in Aransas Pass, Tex. In Aransas Pass their abundance varied seasonally, with the lowest concentrations coincident with cooler water and lower salinity. Along the transect, viruses infecting Synechococcus strains DC2 and SYN48 ranged in concentration from a few hundred per milliliter at 97 m deep and 83 km offshore to ca. 4 x 10 ml near the surface at stations within 18 km of the coast. The highest concentrations occurred at the surface, where salinity decreased from ca. 35.5 to 34 ppt and Synechococcus concentrations were greatest. Viruses infecting strains SNC1, SNC2, and 838BG were distributed in a similar manner but were much less abundant (<10 to >5 x 10 ml). When Synechococcus concentrations exceeded ca. 10 ml, cyanophage concentrations increased markedly (ca. 10 to > 10 ml), suggesting that a minimum host density was required for efficient viral propagation. Data on the decay rate of viral infectivity d (per day), as a function of solar irradiance I (millimoles of quanta per square meter per second), were used to develop a relationship (d = 0.2610I - 0.00718; r = 0.69) for conservatively estimating the destruction of infectious viruses in the mixed layer of two offshore stations. Assuming that virus production balances losses and that the burst size is 250, ca. 5 to 7% of Synechococcus cells would be infected daily by viruses. Calculations based on contact rates between Synechococcus cells and infectious viruses produce similar results (5 to 14%). Moreover, balancing estimates of viral production with contact rates for the farthest offshore station required that most Synechococcus cells be susceptible to infection, that most contacts result in infection, and that the burst size be about 324 viruses per lytic event. In contrast, in nearshore waters, where ca. 80% of Synechococcus cells would be contacted daily by infectious cyanophages, only ca. 1% of the contacts would have to result in infection to balance the estimated virus removal rates. These results indicate that cyanophages are an abundant and dynamic component of marine planktonic communities and are probably responsible for lysing a small but significant portion of the Synechococcus population on a daily basis.
A variety of approaches including enumeration of visibly infected microbes, removal of viral particles, decay of viral infectivity, and measurements of viral production rates have been used to infer the impact of viruses on microbial mortality. The results are surprisingly consistent and suggest that, on average, about 20% of marine heterotrophic bacteria are infected by viruses and 10-20% of the bacterial community is lysed daily by viruses. The effect of viruses on phytoplankton is less certain, but ca. 3% of Synechococcus biomass may be lysed daily. The fraction of primary productivity this represents depends upon the relative biomass and growth rate of Synechococcus. Virus enrichment experiments suggest that the productivity of eukaryotic phytoplankton would be ca. 2% higher in the absence of viruses. Overall, probably about 2-3% of primary productivity is lost to viral lysis. There is considerable variation about these estimates; however, they represent a starting point for incorporating viral-mediated processes into aquatic ecosystem models.
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The dynamics of carbon (C), nitrogen (N), and phosphorus (P), elemental ratios, and dark uptake/release of N and P in bacterial and phytoplankton size fractions were studied during summer 1992 in three lakes of contrasting food web structure and trophic status (L240, L110, L227). We wished to determine if phytoplankton and bacteria differed in their elemental characteristics and to evaluate whether the functional role of bacteria in nutrient cycling (i.e., as sink or source) depended on bacterial elemental characteristics. Bacterial contributions to total suspended particulate material and to fluxes of nutrients in the dark were substantial and varied for different elements. This indicated that some techniques for assaying phytoplankton physiological condition are compromised by bacterial contributions. C/N ratios were generally less variable than C/P and N/P ratios. Both elemental ratios and biomass-normalized N and P flux indicated that phytoplankton growth in each lake was predominantly P-limited, although in L227 these data reflect the dominance of N-fixing cyanobacteria, and N was likely limiting early in the sampling season. In L227, phytoplankton N/P ratio and biomass-normalized N flux were negatively correlated, indicating that flux data were likely a reasonable measure of the N status of the phytoplankton. However, for L227 phytoplankton, P-flux per unit biomass was a hyperbolic function of N/P, suggesting that the dominant L227 cyanobacteria have a limited uptake and storage capacity and that P-flux per unit biomass may not be a good gauge of the P-limitation status of phytoplankton in this situation. Examination of N-flux data in the bacterial size fraction relative to the N/P ratio of the bacteria revealed a threshold N/P ratio (∼22:1 N/P, by atoms), below which, bacteria took up and sequestered added N, and above which, N was released. Thus, the functional role of bacteria in N cycling in these ecosystems depended on their N/P stoichiometry.
Upon examining combinations of environmental conditions most likely to elicit nuisance blooms, commonalities and analog situations become more apparent among coastal marine (dinoflagellate-dominated), estuarine (dinoflagellate- and cyanobacteria-dominated), and freshwater (cyanobacteria-dominated) ecosystems. A combination of the following hydrological, chemical and biotic factors will most likely lead to bloom-sensitive waters: a horizontally distinct water mass; a vertically stratified water column; warm weather conditions, as typified by dry monsoon tropical climates and summer seasons in temperate zones; high incident photosynthetically active radiation (PAR); enhanced allochthonous organic matter loading (both as DOC and POC); enhanced allochthonous inorganic nutrient loading (N and/or P); adequate availability of essential metals, supplied by terrigenous inputs or upwelling; underlying sediments physically and nutritionally suitable as "seed beds' for resting cysts and akinetes; algal-bacterial synergism, which exhibits positive impacts on phycosphere nutrient cycling; algal-micrograzer (protists and rotifers) synergism, which also enhances nutrient cycling without consumption of filamentous and colonial nuisance taxa; and selective (for non-nuisance taxa) activities of macrograzers (crustacean zooplankton, larval fish). Nuisance bloom taxa share numerous additional physiological and ecological characteristics, including limited heterotrophic capabilities, high degrees of motility, and toxicity. -from Authors