Published on October 30, 2007
Slide1: Conclusions Concern over anthropogenic DIN input to estuaries is primarily related to the promotion of excess algal growth and anoxia or harmful algal blooms. Nutrient/phytoplankton relationships are more complicated than simple cause-and-effect scenarios (e.g. Sharp 2001). We have shown evidence and provide a mechanism in which persistently high [NH4] loading to estuaries may reduce phytoplankton biomass production. [NH4] higher than ca. 2-3µM reduces phytoplankton access to much of the DIN pool. (Fig. 4) Maximal phytoplankton VNH4 is significantly lower than VNO3 (Fig 5, Fig. 7). Maximal phytoplankton VC is achieved when linked with NO3 driven production (Fig. 6). As a result, bloom formation in SFE may only occur when NH4 concentrations are reduced to below inhibitory levels. This may be achieved through dilution with freshwater or by phytoplankton uptake during periods of stratification. Introduction The San Francisco Estuary (SFE) is characterized by relatively low primary production despite significant nutrient loading from both natural and anthropogenic sources. Declines in chl a and other parts of the food web have been documented over the past 20 years (Kimmerer & Orsi, 1996). Low production has been shown to be the result of light limitation over much of the estuary (Cloern, 1987) while declining chlorophyll a has been attributed mainly to the introduction of a benthic filter feeder. Changing nutrient management practices over the same period have led to shifts in inorganic nitrogen speciation in SFE from NO3 to NH4. We have investigated how these shifts in DIN composition may influence primary production and biomass accumulation in SFE. Preliminary data on SFE phytoplankton suggest a negative relationship between [NH4] and chl a. Enclosure experiments designed to trace phytoplankton production over 5 days show that initially high [NH4] conditions suppress bloom development relative to initial conditions of low NH4 and high NO3. The results appear to be due to relatively low specific C and NH4 uptake in high [NH4] systems. San Francisco Tiburon Pacific Ocean Central Bay Suisun Bay San Pablo Bay Study Site Figure 1: Water for enclosure experiments was collected in March, July and September, 2005 in Suisun (red), San Pablo (blue) and Central Bays (green). Methods Hypotheses Consistent patterns in DIC drawdown and chl a production occurred in March, July and September enclosure experiments (Fig 3). DIC drawdown in Suisun Bay was 17-20% of draw- down in San Pablo and Central Bays, respectively (Fig 3, top). Chl a increased in all enclosures. Final chl a was highest in San Pablo Bay enclosure (Fig 3, bottom, blue). Chl a concentrations in Central Bay enclosure increased through 62 hours, then declined as nutrients were exhausted (Fig 3, bottom, green). Chl a in Suisun Bay lagged Central and San Pablo Bays during the first 48 hours (Fig 3, bottom, red). Figure 3: (Top) Dissolved inorganic carbon (DIC) and (Bottom) chlorophyll a concentration time series in enclosure experiments. Note different scales for chl a concentrations. Contribution by larger phytoplankton (from size-fractionated chl a and flow cytometry) in three bays were similar both initially and at the end of the experiment (Table 1). Initially, 50-70% of chl a was found in >5.0µm size fraction in all bays. The >5.0µm size fraction represented 80-100% of chl a at 86 hours. Flow cytometry showed increases in the percentage of >5µm cells over the experiment. The percentage of cells 3-5µm decreased by ca. half in all bays. VNO3 vs. [NH4] (Fig 4) show clear evidence of NH4 inhibition of phytoplankton NO3 uptake in San Francisco Bay. This has been found in other systems (e.g. Dortch 1990). In SFE, [NH4] >2-3µM shuts down NO3 use. As phytoplankton cannot use NO3 when [NH4] is inhibiting, and NO3 constitutes a large fraction of DIN (ca. 80%) in SFE, DIN concentrations are not a reliable predictor of potential estuarine productivity. Specific C uptake (VC) supported by NH4 assimilation (inside yellow box) reached a maximal value of 0.02h-1. VC supported by NO3 assimilation reached maximal values of 0.060h-1. VC values of ca. 0.042h-1 represent 1 doubling per day. Phytoplankton growth based on NH4 assimilation was lower compared to rates when NO3 was assimilated. DIN drawdown was significantly lower in Suisun Bay despite higher initial DIN concentrations. PO4 concentrations were reduced to <0.05µM in San Pablo and Central Bay enclosures by 72 hours. Elemental drawdown ratios approached Redfield Ratio. Relatively low C:N for Suisun Bay (3.7) and high N:P for San Pablo and Central Bay (30 and 23, respectively). Differences in phytoplankton biomass observed in Suisun, San Pablo and Central Bays are due, in part, to nitrogen substrate (NH4 or NO3) used for primary production. NH4 inhibition of phytoplankton NO3 uptake is a feature of San Francisco phytoplankton ecology. NH4 inhibition of phytoplankton NO3 use limits phytoplankton access to a significant portion of the total DIN pool. When access to NO3 is possible, specific phytoplankton NO3 uptake rates (VNO3) are higher then rates of NH4 uptake in SFE. Increases in NH4 loading to SFE may have contributed to the observed decline in phytoplankton biomass since 1986. 3 replicate cubitainers for each bay were filled with surface water at mid channel (Fig. 1). Cubitainers were held in flowing ambient bay water, under 50% surface PAR for 5 days. Samples were collected daily from each cubitainer and analyzed for inorganic nutrients, dissolved inorganic carbon, size fractionated chlorophyll a, flow cytometry, and particulate organic carbon and nitrogen. Phytoplankton carbon and nitrogen assimilation was measured using C-13 and N-15 (NH4 and NO3) stable isotope tracer techniques. Figure 2: Experimental design for enclosure experiments. All values presented below represent the average of 3 enclosure replicates. Typical ambient NO3, NH4 and chlorophyll a concentrations for the 3 bays are provided. Figure 4: NH4 inhibition of NO3 uptake using all data from March and July 2005. Figure 5: NH4 and NO3 drawdown and NH4 and NO3 uptake (h-1) in enclosures from March 2005. Results and Discussion Acknowledgements The authors wish to thank K. Lew for flow cytometry, F. Koch and L. Barada for sample collection and the crew of the RV Questuary. This research is supported by a USC Sea Grant Award to R.C. Dugdale and F. Wilkerson. Cloern, J. E. (1987). "Turbidity as a control on phytoplankton biomass and productivity in estuaries." Continental Shelf Research 7(11/12): 1367-1381. Dortch, Q. (1990). "The interaction between ammonium and nitrate uptake in phytoplankton." Marine Ecology Progress Series 61: 183-201. Kimmerer, W. J. and J. J. Orsi (1996). “Causes of long-term declines in zooplankton in the San Francisco Bay estuary since 1987”. San Francisco Bay: The Ecosystem. J. T. Hollibaugh. San Francisco., American Association for the Advancement of Science. Sharp, J. H. (2001). “Marine and aquatic communities, stress from eutrophication”. Encyclopedia of Biodiversity, Academic Press. 4: 1-11. NH4 and NO3 drawdown (Fig 5, top) and specific uptake, V, of NH4 and NO3 (Fig 5, bottom) provide a mechanism for delayed biomass production observed in Suisun Bay. Inhibitory concentrations of NH4 were found in Suisun, San Pablo, and Central Bays. NH4 concentrations in San Pablo and Central Bays were reduced to below inhibitory concentrations within 24 hours. NH4 in Suisun enclosures remained above inhibitory concentrations beyond 72 hours (fig 5, top left). VNH4 reached maximal values at 24 hours in Central and San Pablo bays and then declined as NH4 concentrations decreased. VNH4 in Suisun bay peaked at 72 hours (fig. 5 bottom left). NO3 concentrations decreased within 24 hours in Central and San Pablo enclosures but did not decline in Suisun until hour 72 (fig. 5, top right). Maximal specific NO3 uptake was seen after 48 and 72 hours for San Pablo and Central Bays, respectively (fig 5, bottom right). Maximal VNO3 was nearly 2-fold higher than maximal VNH4. NO3 kinetic curves (Fig 7. top) Day1) NH4 inhibition of NO3 uptake. Day 3) Saturated NO3 curve. Day 5) Nutrient exhaustion may have limited Vmax. NH4 kinetic curves (Fig 7, bottom) Day 1) Low Vmax. Day 3) Vmax = 0.036 and Ks = 1.18. Day 5) Data unavailable Table 1: Chlorophyll a and flow cytometry data for March 2005. Figure. 6: Specific carbon uptake for 3 bays. Yellow box indicates carbon production supported by NH4 uptake. Figure 7: Kinetic curves for NO3 and NH4 during 5 day enclosure experiments in April 2005.