The role of ammonium and nitrate in spring bloom development in San Francisco Bay

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Abstract

The substantial inventory of nitrate (NO3) in San Francisco Bay (SFB) is unavailable to the resident phytoplankton most of the year due to the presence of ammonium (NH4) at inhibitory concentrations that prevents NO3 uptake. Low annual primary productivity in this turbid estuary is generally attributed to the poor irradiance conditions. However, this may not be the only cause; spring phytoplankton blooms occur irregularly in north SFB only when NH4 concentrations are low, <4 μmol L−1 and NO3 uptake by phytoplankton occurs. Field measurements and enclosure experiments confirm the NH4 inhibition process to be the cause of low NO3 utilization most of the year. Detailed analysis of spring blooms in three embayments of SFB over 3 years shows a consistent sequence of events that result in bursts of chlorophyll. The first requirement is improved irradiance conditions through stabilization of the water column by stratification or reduced tidal activity. Second, NH4 concentrations must be reduced to a critical range, 1 to 4 μmol L−1 through dilution by precipitation and by phytoplankton uptake. This enables rapid uptake of NO3 and subsequent increase in chlorophyll. The resulting bloom is due to both the initial uptake of NH4 and the subsequent uptake of NO3. The NO3 uptake step is crucial since it is the larger nitrogen source and uptake occurs at higher rates than that for NH4 at the concentrations that occur in SFB. Existing models of light-limited, non-nutrient limited productivity in SFB require modification to include the NH4 inhibition effect. From measured NH4 uptake rates and initial concentrations, calculations can be made to predict the length of time that favorable irradiance conditions are required for the phytoplankton population to reduce ambient NH4 concentrations to non-inhibiting concentrations and allow bloom formation to begin. For Suisun Bay, the time required is so long that blooms are unlikely in any season. For San Pablo and Central Bays, these times are too long in summer but sufficiently short in spring to allow bloom development, depending on the ambient NH4 concentration prior to the productivity season. NH4 sources to SFB are primarily anthropogenic, from agricultural drainage and sewage treatment plants, and if not sufficiently diluted by runoff and precipitation can prevent development of the spring phytoplankton bloom. Attention should be paid to the form of N making up dissolved inorganic nitrogen (DIN) in nutrient-rich estuaries.

Introduction

Turbid estuaries often exhibit low primary production that is usually attributed to the poor irradiance conditions and a shallow euphotic zone (Cloern, 1987). However, even in these estuaries, considerable variability in primary productivity may occur over a variety of time scales, from daily to interannual. The timing and number of productivity events that occur in any one season are likely to play important roles in the provisioning of the food chain. Especially important may be the disruption of normal ecosystem cycles. For example, zooplankton species evolved to depend on phytoplankton blooms in spring for food and egg production, may find the expected bloom to be absent or moved significantly in time from the normal seasonal cycle. Changes in turbidity cycles, e.g. changes in flow and wind patterns clearly have the potential for disrupting productivity cycles in turbid estuaries. However, other factors may be important as well in influencing timing and magnitude of primary production. Here, we consider the role of two different forms of inorganic nitrogen in modifying classical spring blooms of phytoplankton in San Francisco Bay (SFB), a turbid estuary impacted by anthropogenic inputs of nitrogenous nutrients (Schemel and Hager, 1986). Conventional wisdom suggests that NH4 and NO3 loadings to an estuary can be combined together as dissolved inorganic nitrogen (DIN) since phytoplankton have been shown in culture to grow equally well on both nitrogen sources (Syrett, 1981). Phytoplankton are also thought to prefer NH4 as a nitrogen source since the energetic costs of assimilating that species of nitrogen are less than that for NO3. By inference, an estuary whose phytoplankton are utilizing NH4 for growth should have the same primary productivity as if they were using NO3, or perhaps even higher productivity on NH4 compared to NO3.

The ability to separate out the use of NO3 and NH4 by phytoplankton in the marine environment was pioneered by Dugdale and Goering (1967) using the stable isotope 15N as a tracer. This has proved to be a powerful tool in studies of primary production in marine ecosystems. In productive oceanic ecosystems, the most abundant species of DIN is NO3 since NH4 is readily oxidized to NO3 and is the minor inorganic species (Codispoti, 1985). Although under some culture conditions algae use both forms of DIN simultaneously (Dortch, 1990), NO3 uptake is suppressed or inhibited by relatively low concentrations of NH4 as shown, for example, by Conway (1977) for the diatom Skeletonema costatum and by Cochlan and Harrison (1991) for the picoplankton species Micromonas pusilla. Field studies using 15N have confirmed the relationship between elevated NH4 concentrations and low NO3 uptake rates, e.g. in the Saronikos Gulf (Greece) due to the effects of sewage inputs (Dugdale and Hopkins, 1978); the Peru coastal upwelling system (Dugdale and MacIsaac, 1971); and more recently the upwelling center off Bodega Bay, California (Dugdale et al., 2006). In each of these studies, NO3 uptake was negatively correlated and reduced to low levels with ambient NH4 concentrations in the range of 1–2.5 μmol L−1. 15N studies in a series of upwelling sites, from Baja California to northwest Africa and Peru showed maximum specific NO3 uptake rates to always exceed maximum specific NH4 uptake rates with the conclusion “that the high biological productivity of the Peruvian upwelling system may be linked to the ability of the phytoplankton to take up and utilize NO3 at an extraordinary rate” (Codispoti et al., 1982). By analogy with these marine studies, estuaries could be expected to have higher primary productivity with phytoplankton growing on NO3 than when growing on NH4. However, if NH4 is at an inhibitory level, this form of DIN may not allow the high NO3-based productivity. San Francisco Bay, as an urban estuary impacted by anthropogenic inputs and with the likelihood of high NH4 concentrations, provided an ideal environment to investigate this scenario.

We initiated studies of nutrient and productivity processes in SFB in 1997 using the stable isotope tracer 15N and found that NH4 uptake by phytoplankton in Central SFB dominated DIN uptake and that NO3 uptake was a rare occurrence in spite of abundant ambient NO3 concentrations (Hogue et al., 2005). Similar observations were made for the Delaware Estuary (Pennock, 1987) where NH4 fuels productivity in a high NO3 setting. Most annual primary production in central SFB depended upon NH4 (Hogue et al., 2005) except during spring when ambient NH4 concentrations fell to low values and high levels of primary production based on NO3 occurred. Subsequent measurements in the northern estuary (Suisun, San Pablo and Central Bays) were carried out from 1999 to 2002 that described the seasonal variability in nutrients, nutrient uptake and phytoplankton abundance (Wilkerson et al., 2006). In fall, there were small occasional blooms fueled by NH4 uptake by small-sized phytoplankton but the major periods of high productivity and chlorophyll accumulation occurred in spring dominated by large-sized phytoplankton, mostly diatoms (Cloern and Dufford, 2005). During spring blooms, there were higher rates of NO3 uptake than NH4 uptake indicating higher growth rates on NO3 by the phytoplankton. Spring blooms were observed in all three bays in 2000, but only in San Pablo and Central Bays in 2001 and 2002. Interestingly, the bloom in Suisun Bay in spring 2000 had the greatest phytoplankton abundance observed reaching 30 μg L−1 chlorophyll. This occurred when there were very low salinity values and low NH4 concentrations, neither of which occurred there in 2001 or 2002 (Wilkerson et al., 2006), accompanied by high NO3 uptake rates. This suggested that NH4 played a role in bloom dynamics, by limiting phytoplankton access to the NO3 pool. The goal of this study was to analyze the data collected during the 1999–2002 study and to use experimental enclosures to determine the conditions and mechanisms required to give phytoplankton access to the ambient NO3 and accumulate chlorophyll during spring blooms. We evaluate the role of two components of the DIN pool (i.e. NH4 and NO3) and their interaction as modulators of the development and/or suppression of spring blooms in San Francisco Bay.

Section snippets

Field data

Cruises designed to sample San Francisco Bay (SFB) monthly and weekly during the spring months of March and April were conducted aboard the R/V Questuary from November 1999 to August 2003. Water was sampled at three locations: Suisun Bay (USGS Sampling Station 6, 38′ 3.9°N 122′ 2.1°W), San Pablo Bay (USGS Station 13, 38′ 1.7°N 121′ 22.2°W) and Central Bay (RTC Station XB-D, 37′ 53.83°N 122′ 25.5°W) using a Seabird SBE-19 CTD and 3-L Niskin bottles mounted on an SBE-33 carousel. Surface samples

Field data from Suisun, San Pablo, and Central Bays

To establish the role of DIN and interacting nutrient processes in occurrences and extent of SFB blooms, the time series data for concentrations of chlorophyll, NH4, and NO3 and uptake of 15NO3 in Suisun, San Pablo, and Central Bays, measured between late 1999 and 2003 are shown in Fig. 1a–d. Four spring peaks in chlorophyll (blooms) occur in San Pablo and Central Bays (Fig. 1a) that coincide with reduced NH4 concentrations, often near zero (Fig. 1b). In Suisun Bay, only one bloom was observed,

Overview

The conditions in SFB are what have been termed for estuaries as HNLC, high nutrient low chlorophyll (Cloern, 2001) or HNLG, high nutrient low growth (Sharp, 2001). Most of the year primary production is low, and nutrients are in excess of requirements and exported from the estuary. Control of primary production in SFB was summarized by Jassby et al. (1996) as a light-limited system with nutrients assumed to be replete and non-limiting. Our results show that in addition to irradiance

Conclusions

Low annual primary production in SFB is due primarily to turbid conditions but is also modulated by high NH4 inputs and concentrations that can suppress access to NO3 by phytoplankton and may reduce the occurrence of spring blooms and quantity of accumulated chlorophyll. Since the NH4 concentrations at the end of winter are diluted by precipitation and runoff, and because the seasonal precipitation and runoff are highly variable, the spring primary productivity is even more variable than if it

Acknowledgments

This research was supported by the USA Environmental Protection Agency (EPA) Science to Achieve Results (STAR) program award #827644-01-0 and the University of Southern California SeaGrant Program. We wish to thank the crew of the R/V Questuary for their help with the sampling program (Captain David Morgan and Jay Tustin). Special thanks to James Cloern, Jonathan Sharp, Alex Parker and Wim Kimmerer for helpful discussions.

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