Temporal dynamics of estuarine phytoplankton: A case study of San Francisco Bay

Detailed surveys throughout San Francisco Bay over an annual cycle (1980) show that seasonal variations of phytoplankton biomass, community composition, and productivity can differ markedly among estuarine habitat types. For example, in the river-dominated northern reach (Suisun Bay) phytoplankton seasonality is characterized by a prolonged summer bloom of netplanktonic diatoms that results from the accumulation of suspended particulates at the convergence of nontidal currents (i.e. where residence time is long). Here turbidity is persistently high such that phytoplankton growth and productivity are severely limited by light availability, the phytoplankton population turns over slowly, and biological processes appear to be less important mechanisms of temporal change than physical processes associated with freshwater inflow and turbulent mixing. The South Bay, in contrast, is a lagoon-type estuary less directly coupled to the influence of river discharge. Residence time is long (months) in this estuary, turbidity is lower and estimated rates of population growth are high (up to 1–2 doublings d^–1), but the rapid production of phytoplankton biomass is presumably balanced by grazing losses to benthic herbivores. Exceptions occur for brief intervals (days to weeks) during spring when the water column stratifies so that algae retained in the surface layer are uncoupled from benthic grazing, and phytoplankton blooms develop. The degree of stratification varies over the neap-spring tidal cycle, so the South Bay represents an estuary where (1) biological processes (growth, grazing) and a physical process (vertical mixing) interact to cause temporal variability of phytoplankton biomass, and (2) temporal variability is highly dynamic because of the short-term variability of tides. Other mechanisms of temporal variability in estuarine phytoplankton include: zooplankton grazing, exchanges of microalgae between the sediment and water column, and horizontal dispersion which transports phytoplankton from regions of high productivity (shallows) to regions of low productivity (deep channels).Multi-year records of phytoplankton biomass show that large deviations from the typical annual cycles observed in 1980 can occur, and that interannual variability is driven by variability of annual precipitation and river discharge. Here, too, the nature of this variability differs among estuary types. Blooms occur only in the northern reach when river discharge falls within a narrow range, and the summer biomass increase was absent during years of extreme drought (1977) or years of exceptionally high discharge (1982). In South Bay, however, there is a direct relationship between phytoplankton biomass and river discharge. As discharge increases so does the buoyancy input required for density stratification, and wet years are characterized by persistent and intense spring blooms.     

Projected evolution of California's San Francisco Bay-Delta-river system in a century of climate change

Background

Accumulating evidence shows that the planet is warming as a response to human emissions of greenhouse gases. Strategies of adaptation to climate change will require quantitative projections of how altered regional patterns of temperature, precipitation and sea level could cascade to provoke local impacts such as modified water supplies, increasing risks of coastal flooding, and growing challenges to sustainability of native species.

Methodology/Principal Findings

We linked a series of models to investigate responses of California''s San Francisco Estuary-Watershed (SFEW) system to two contrasting scenarios of climate change. Model outputs for scenarios of fast and moderate warming are presented as 2010–2099 projections of nine indicators of changing climate, hydrology and habitat quality. Trends of these indicators measure rates of: increasing air and water temperatures, salinity and sea level; decreasing precipitation, runoff, snowmelt contribution to runoff, and suspended sediment concentrations; and increasing frequency of extreme environmental conditions such as water temperatures and sea level beyond the ranges of historical observations.

Conclusions/Significance

Most of these environmental indicators change substantially over the 21^st century, and many would present challenges to natural and managed systems. Adaptations to these changes will require flexible planning to cope with growing risks to humans and the challenges of meeting demands for fresh water and sustaining native biota. Programs of ecosystem rehabilitation and biodiversity conservation in coastal landscapes will be most likely to meet their objectives if they are designed from considerations that include: (1) an integrated perspective that river-estuary systems are influenced by effects of climate change operating on both watersheds and oceans; (2) varying sensitivity among environmental indicators to the uncertainty of future climates; (3) inevitability of biological community changes as responses to cumulative effects of climate change and other drivers of habitat transformations; and (4) anticipation and adaptation to the growing probability of ecosystem regime shifts.     

Human activities and climate variability drive fast‐paced change across the world's estuarine–coastal ecosystems

Time series of environmental measurements are essential for detecting, measuring and understanding changes in the Earth system and its biological communities. Observational series have accumulated over the past 2–5 decades from measurements across the world's estuaries, bays, lagoons, inland seas and shelf waters influenced by runoff. We synthesize information contained in these time series to develop a global view of changes occurring in marine systems influenced by connectivity to land. Our review is organized around four themes: (i) human activities as drivers of change; (ii) variability of the climate system as a driver of change; (iii) successes, disappointments and challenges of managing change at the sea‐land interface; and (iv) discoveries made from observations over time. Multidecadal time series reveal that many of the world's estuarine–coastal ecosystems are in a continuing state of change, and the pace of change is faster than we could have imagined a decade ago. Some have been transformed into novel ecosystems with habitats, biogeochemistry and biological communities outside the natural range of variability. Change takes many forms including linear and nonlinear trends, abrupt state changes and oscillations. The challenge of managing change is daunting in the coastal zone where diverse human pressures are concentrated and intersect with different responses to climate variability over land and over ocean basins. The pace of change in estuarine–coastal ecosystems will likely accelerate as the human population and economies continue to grow and as global climate change accelerates. Wise stewardship of the resources upon which we depend is critically dependent upon a continuing flow of information from observations to measure, understand and anticipate future changes along the world's coastlines.     

Estuary–ocean connectivity: fast physics,slow biology

Estuaries are connected to both land and ocean so their physical, chemical, and biological dynamics are influenced by climate patterns over watersheds and ocean basins. We explored climate‐driven oceanic variability as a source of estuarine variability by comparing monthly time series of temperature and chlorophyll‐a inside San Francisco Bay with those in adjacent shelf waters of the California Current System (CCS) that are strongly responsive to wind‐driven upwelling. Monthly temperature fluctuations inside and outside the Bay were synchronous, but their correlations weakened with distance from the ocean. These results illustrate how variability of coastal water temperature (and associated properties such as nitrate and oxygen) propagates into estuaries through fast water exchanges that dissipate along the estuary. Unexpectedly, there was no correlation between monthly chlorophyll‐a variability inside and outside the Bay. However, at the annual scale Bay chlorophyll‐a was significantly correlated with the Spring Transition Index (STI) that sets biological production supporting fish recruitment in the CCS. Wind forcing of the CCS shifted in the late 1990s when the STI advanced 40 days. This shift was followed, with lags of 1–3 years, by 3‐ to 19‐fold increased abundances of five ocean‐produced demersal fish and crustaceans and 2.5‐fold increase of summer chlorophyll‐a in the Bay. These changes reflect a slow biological process of estuary–ocean connectivity operating through the immigration of fish and crustaceans that prey on bivalves, reduce their grazing pressure, and allow phytoplankton biomass to build. We identified clear signals of climate‐mediated oceanic variability in this estuary and discovered that the response patterns vary with the process of connectivity and the timescale of ocean variability. This result has important implications for managing nutrient inputs to estuaries connected to upwelling systems, and for assessing their responses to changing patterns of upwelling timing and intensity as the planet continues to warm.     

EFFECTS OF LIGHT INTENSITY AND TEMPERATURE ON CRYPTOMONAS OVATA (CRYPTOPHYCEAE) GROWTH AND NUTRIENT UPTAKE RATES1

Specific growth rate of Cryptomonas ovata var. palustris Pringsheim was measured in batch culture at 14 light-temperature combinations. Both the maximum growth rate (μ_m) and optimum light intensity (I_opt) fit an empirical function that increases exponentially with temperature up to an optimum (T_opt), then declines rapidly as temperature exceeds T_opt. Incorporation of these functions into Steele's growth equation gives a good estimate of specific growth rate over a wide range of temperature and light intensity. Rates of phosphate, ammonium and nitrate uptake were measured separately at 16 combinations of irradiance and temperature and following a spike addition of all starved cells initially took up nutrient at a rapid rate. This transitory surge was followed by a period of steady, substrate-saturated uptake that persisted until external nutrient concentration fell. Substrate-saturated NO₃^?-uptake proceeded at very slow rates in the dark and was stimulated by both increased temperature and irradiance; NH₄⁺-uptake apparently proceeded at a basal rate at 8 and l4 C and was also stimulated by increased temperature and irradiance. Rates of NH₄^?-uptake were much higher than NO₃^?-uptake at all light-temperature combinations. Below 20 C, PO₄^?3-uptake was more rapid in dark than in light, but was light enhanced at 26 C.     

Habitat connectivity and ecosystem productivity: implications from a simple model

The import of resources (food, nutrients) sustains biological production and food webs in resource-limited habitats. Resource export from donor habitats subsidizes production in recipient habitats, but the ecosystem-scale consequences of resource translocation are generally unknown. Here, I use a nutrient-phytoplankton-zooplankton model to show how dispersive connectivity between a shallow autotrophic habitat and a deep heterotrophic pelagic habitat can amplify overall system production in metazoan food webs. This result derives from the finite capacity of suspension feeders to capture and assimilate food particles: excess primary production in closed autotrophic habitats cannot be assimilated by consumers; however, if excess phytoplankton production is exported to food-limited heterotrophic habitats, it can be assimilated by zooplankton to support additional secondary production. Transport of regenerated nutrients from heterotrophic to autotrophic habitats sustains higher system primary production. These simulation results imply that the ecosystem-scale efficiency of nutrient transformation into metazoan biomass can be constrained by the rate of resource exchange across habitats and that it is optimized when the transport rate matches the growth rate of primary producers. Slower transport (i.e., reduced connectivity) leads to nutrient limitation of primary production in autotrophic habitats and food limitation of secondary production in heterotrophic habitats. Habitat fragmentation can therefore impose energetic constraints on the carrying capacity of aquatic ecosystems. The outcomes of ecosystem restoration through habitat creation will be determined by both functions provided by newly created aquatic habitats and the rates of hydraulic connectivity between them.     

Seasonal changes in the chemistry and biology of a meromictic lake (Big Soda Lake,Nevada, U.S.A.)

Big Soda Lake is an alkaline, saline lake with a permanent chemocline at 34.5 m and a mixolimnion that undergoes seasonal changes in temperature structure. During the period of thermal stratification, from summer through fall, the epilimnion has low concentrations of dissolved inorganic nutrients (N, Si) and CH₄, and low biomass of phytoplankton (chlorophyll a ca. 1 mgm ^-3). Dissolved oxygen disappears near the compensation depth for algal photosynthesis (ca. 20 m). Surface water is transparent so that light is present in the anoxic hypolimnion, and a dense plate of purple sulfur photosynthetic bacteria (Ectothiorhodospira vacuolata) is present just below 20 m (Bchl a ca. 200 mgm^-3). Concentrations of N H₄ ⁺, Si, and CH₄ are higher in the hypolimnion than in the epilimnion. As the mixolimnion becomes isothermal in winter, oxygen is mixed down to 28 m. Nutrients (NH₄ ⁺, Si) and CH₄ are released from the hypolimnion and mix to the surface, and a diatom bloom develops in the upper 20 m (chlorophyll a > 40 mgm^-3). The deeper mixing of oxygen and enhanced light attenuation by phytoplankton uncouple the anoxic zone and photic zone, and the plate of photosynthetic bacteria disappears (Bchl a ca.10mgm^-3). Hence, seasonal changes in temperature distribution and mixing create conditions such that the primary producer community is alternately dominated by phytoplankton and photosynthetic bacteria: the phytoplankton may be nutrient-limited during periods of stratification and the photosynthetic bacteria are light-limited during periods of mixing.     

Seasonal cycles of zooplankton from San Francisco Bay

The two estuarine systems composing San Francisco Bay have distinct zooplankton communities and seasonal population dynamics. In the South Bay, a shallow lagoon-type estuary, the copepods Acartia spp. and Oithona davisae dominate. As in estuaries along the northeast coast of the U.S., there is a seasonal succession involving the replacement of a cold-season Acartia species (A. clausi s.l.) by a warm-season species (A. californiensis), presumably resulting from the differential production and hatching of dormant eggs. Oithona davisae is most abundant during the fall. Copepods of northern San Francisco Bay, a partially-mixed estuary of the Sacramento-San Joaquin Rivers, organize into discrete populations according to salinity distribution: Sinocalanus doerrii (a recently introduced species) at the riverine boundary, Eurytemora affinis in the oligohaline mixing zone, Acartia spp. in polyhaline waters (18–30\%), and neritic species (e.g., Paracalanus parvus) at the seaward boundary. Sinocalanus doerrii and E. affinis are present year-round. Acartia clausi s.l. is present almost year-round in the northern reach, and A. californiensis occurs only briefly there in summer-fall. The difference in succession of Acartia species between the two regions of San Francisco Bay may reflect differences in the seasonal temperature cycle (the South Bay warms earlier), and the perennial transport of A. clausi s.l. into the northern reach from the seaward boundary by nontidal advection.Large numbers (>10⁶ m^–3) of net microzooplankton (>64 µm), in cluding the rotifer Synchaeta sp. and three species of tintinnid ciliates, occur in the South Bay and in the seaward northern reach where salinity exceeds about 5–10 Maximum densities of these microzooplankton are associated with high concentrations of chlorophyll. Meroplankton (of gastropods, bivalves, barnacles, and polychaetes) constitute a large fraction of zooplankton biomass in the South Bay during winter-spring and in the northern reach during summer-fall.Seasonal cycles of zooplankton abundance appear to be constant among years (1978–1981) and are similar in the deep (>10 m) channels and lateral shoals (<3 m). The seasonal zooplankton community dynamics are discussed in relation to: (1) river discharge which alters salinity distribution and residence time of plankton; (2) temperature which induces production and hatching of dormant copepod eggs; (3) coastal hydrography which brings neritic copepods of different zoogeographic affinities into the bay; and (4) seasonal cycles of phytoplankton.     

The annual cycles of phytoplankton biomass

Terrestrial plants are powerful climate sentinels because their annual cycles of growth, reproduction and senescence are finely tuned to the annual climate cycle having a period of one year. Consistency in the seasonal phasing of terrestrial plant activity provides a relatively low-noise background from which phenological shifts can be detected and attributed to climate change. Here, we ask whether phytoplankton biomass also fluctuates over a consistent annual cycle in lake, estuarine–coastal and ocean ecosystems and whether there is a characteristic phenology of phytoplankton as a consistent phase and amplitude of variability. We compiled 125 time series of phytoplankton biomass (chlorophyll a concentration) from temperate and subtropical zones and used wavelet analysis to extract their dominant periods of variability and the recurrence strength at those periods. Fewer than half (48%) of the series had a dominant 12-month period of variability, commonly expressed as the canonical spring-bloom pattern. About 20 per cent had a dominant six-month period of variability, commonly expressed as the spring and autumn or winter and summer blooms of temperate lakes and oceans. These annual patterns varied in recurrence strength across sites, and did not persist over the full series duration at some sites. About a third of the series had no component of variability at either the six- or 12-month period, reflecting a series of irregular pulses of biomass. These findings show that there is high variability of annual phytoplankton cycles across ecosystems, and that climate-driven annual cycles can be obscured by other drivers of population variability, including human disturbance, aperiodic weather events and strong trophic coupling between phytoplankton and their consumers. Regulation of phytoplankton biomass by multiple processes operating at multiple time scales adds complexity to the challenge of detecting climate-driven trends in aquatic ecosystems where the noise to signal ratio is high.     

The relative importance of light and nutrient limitation of phytoplankton growth: a simple index of coastal ecosystem sensitivity to nutrient enrichment

Anthropogenic nutrient enrichment of the coastal zone is now a well-established fact. However, there is still uncertainty about the mechanisms through which nutrient enrichment can disrupt biological communities and ecosystem processes in the coastal zone. For example, while some estuaries exhibit classic symptoms of acute eutrophication, including enhanced production of algal biomass, other nutrient-rich estuaries maintain low algal biomass and primary production. This implies that large differences exist among coastal ecosystems in the rates and patterns of nutrient assimilation and cycling. Part of this variability comes from differences among ecosystems in the other resource that can limit algal growth and production – the light energy required for photosynthesis. Complete understanding of the eutrophication process requires consideration of the interacting effects of light and nutrients, including the role of light availability as a regulator of the expression of eutrophication. A simple index of the relative strength of light and nutrient limitation of algal growth can be derived from models that describe growth rate as a function of these resources. This index can then be used as one diagnostic to classify the sensitivity of coastal ecosystems to the harmful effects of eutrophication. Here I illustrate the application of this diagnostic with light and nutrient measurements made in three California estuaries and two Dutch estuaries.