Pelagic Ecology of the Low Salinity San Francisco Estuary

Pelagic organisms spend all or part of their lives in the open water, where habitat isdefined not by edges but by physiological tolerance to salinity and temperature. The LowSalinity Zone (LSZ) of the San Francisco Estuary constitutes a habitat for a suite of organismsthat are specialized to survive in this unique confluence of terrestrial, freshwater, and marineinfluences. While there are many habitats with distinct ecologies that are part of the Estuary(including marine, freshwater, intertidal marsh and benthic mudflat systems) each is linked to theLSZ by export and import of freshwater, nutrients, carbon, and organisms Harv |Kimmerer|2004.

The distribution and abundance of organisms in the LSZ is dependent upon both abioticand biotic factors. Abiotic factors include the physical geography and hydrology of the Estuary,including nutrient inputs, sediment load, turbidity, environmental stochasticity, climate andanthropogenic influences (Kimmerer 2002). Abiotic factors tend to drive production in theestuarine environment, and are mediated by biotic factors.

Biotic factors include nutrient uptake and primary production, secondary production of
zooplankton, foodweb and trophic dynamics, energetic transfer, advection and dispersal in and out of the system, survivorship and mortality, predation, and competition from introducedspecies.

Physical geography

The San Francisco Bay is both a bay and an estuary. The former term refers to any inletor cove providing a physical refuge from the open ocean. An estuary is any physiographicfeature where freshwater meets an ocean or sea. The northern portion of the Bay is a brackish estuary, consisting of a number of physical embayments which are dominated by both marineand fresh water fluxes. These geographic entities are, moving from saline to fresh (or west toeast): San Pablo Bay, immediately north of the Central Bay; the Carquinez Strait, a narrow, deepchannel leading to Suisun Bay; and the Delta of the Sacramento and San Joaquin Rivers.

Until the 20th Century, the LSZ of the Estuary was fringed by tule-dominated freshwater
wetlands. Between 80-95% of these historic wetlands have been filled to facilitate land use anddevelopment around the Bay Area (Conomos 1979). Habitat loss at the edges of the pelagic zoneis thought to create a loss of native pelagic fish species, by increasing vulnerability to predation.

The intertidal and benthic Estuary is presently dominated by mudflats that are largely theresult of sedimentation derived from gold mining in the Sierras in the late 19th Century. Thetrend toward high sediment loads was reversed in the 1950’s with the advent of the CentralValley Water Project, locking up most sediment behind dams, and resulting in an annual net lossof sediments from the Estuary (Vayssieres 2006). Thus the mudflats appear to be slowlyreceding, although turbidity remains extremely high. The high turbidity of the water isresponsible for the unique condition that exists in the San Francisco Estuary wherein highnutrient availability does not lead to high phytoplankton production. Instead, most algaephotosynthetic organisms are light-limited (Jassby 2000).

The Delta has likewise experienced heavy alteration. Beginning in the 19th Century,naturally occurring levies were reinforced for permanency, to protect farmlands from regularflooding. Many of these farms were established on peat islands occurring in the middle of theDelta waterways. Intensive farming oxidized the high carbon content of the soil, causingconsiderable loss of soil mass. As a consequence, these islands have subsided, or sunk, to nearly6 meters below sea level (Deverel 1998). The Delta today consists of highly riprappedwaterways, punctuated by islands that appear like “floating bowls” with their basins far belowthe surface of the water (Philip 2007). These islands are at high risk for flooding due to levycollapse. The subsequent eastward shift in salinity is expected to dramatically alter the ecologyof the entire LSZ of the San Francisco Estuary (Lund 2007).

Hydrodynamics

The LSZ centers around 2 psu (practical salinity units, a measurement of salinity) andranges from about 6 psu down to 0.5 psu. The primary fresh water inputs to the Estuary derivefrom regional precipitation, the Sacramento River, and the San Joaquin River (Kimmerer 2002) .River inflow is largely controlled by upstream reservoir releases. A significant fraction of thisinflow is exported out of the Delta by the federal Central Valley Project and the State WaterProject to southern California for agricultural and urban use. These alterations have removedmuch of the variation in through-estuary outflow (i.e., freshwater that makes it out the GoldenGate), creating lower outflow in the winter and higher outflow in the summer than historicallyfound in the Estuary. Phytoplankton, zooplankton, and larval and adult fish can becomeentrained in the export pumps, causing a potentially significant but unknown impact on theabundance of these organisms. This may be particularly true of the endangered Delta smelt, asmall endemic fish; unexceptional except that is has been described as being tremendouslyabundant in historical accounts (Moyle 1992). The Delta smelt is believed to migrate and spawnupstream in the Delta during the early summer, placing its eggs and larvae at high risk forentrainment (Bennett 2006). Management for the smelt is currently the source of controversy asits ecology brings into collision course the disparate water needs of conservation, developmentand agriculture in California.

The movement of water out of the estuary is complex and dependent upon a number offactors. tidesTidal cycles cause water to move toward and away from the Golden Gate four times in a24 hour period. Using 2 psu as a marker for the Low Salinity Zone, the direction and magnitudeof fluctuations can be tracked as the distance in kilometers from the Golden Gate, or X2.Because the position of X2 relies upon a number of physical parameters including inflow, export,and tides, its position shifts over many kilometers on a daily and seasonal cycle; over the courseof a year, it can range from San Pablo Bay during high flow periods, up into the Delta during thesummer drought. The position of X2 is carefully monitored and maintained by releasing waterfrom upstream reservoirs in anticipation of export demand. This is mandated by in the VernalisSalinity Standard, which was legally established to maintain habitat quality in the Estuary forwildlife and to prevent salinity from encroaching upstream to the export pumps (Trott 2006).


Gravitational circulation causes stratified high salinity water at depth to flow landwardwhile low salinity water on top flows seaward (Monismith 1996). The effect of gravitationalcirculation may be most pronounced during periods of high fresh water flow, providing anegative feedback for maintaining the salt field and the distribution of pelagic organisms in theEstuary.

Mixing is important at the landward edge of gravitational circulation, often around X2,where the water column becomes less stratified (Burau 1998). A fixed mixing zone occurs at the“Benicia Bump” at the east end of the Carquinez Strait, where the deep channel becomesdramatically shallower as it enters Suisun Bay (Schoellhamer 2001). Mixing is critical inmaintaining salinity such that extremely large inputs of fresh water are required to move X2 ashort distance to the west. Mixing also assists pelagic organisms in maintaining position in theEstuary (Kimmerer 2004) slowing the advection of primary and secondary production out of thesystem.

Primary Production and Nutrient Uptake

Primary production by phytoplankton fixes energy and key nutrients into a biologicallyavailable form (ie, food), via photosynthesis. Phytoplankton production is largely structured byphysical parameters: nutrient availability, sunlight, turbidity, and temperature.

The San Francisco Estuary has a non-limiting source of nutrients that can be used forprimary production, derived largely from waste water treatment facilities, agricultural and urbandrainage, and the ocean (Smith 2002; Dugdale 2003). In spite of this, the Estuary is unique inthat it tends to have a relatively depressed rate of primary production (Jassby 2002). This isprobably due to two factors: large inputs of nitrogen in the form of ammonium, which suppressesnitrate uptake by phytoplankton, and high turbidity, which limits light for photosynthesis to thetop few centimeters of the water column (Dugdale 2003). This turbidity is a legacy of hydraulicgold mining in the Sierra Nevada Mountains in the 1850’s (Nichols 1986).

High residence time of water in the Estuary tends to allow phytoplankton biomass toaccumulate, increasing density, while low residence time removes phytoplankton from theEstuary (Kimmerer 2004). The latter is typical of the main channels of the Estuary duringperiods of high flow, when surface waters tend to advect particles and plankton downstream.


Herbivory also removes phytoplankton from the water column. While the pelagicfoodweb is based upon phytoplankton production, most of this production is diverted to thebenthos via predation by the introduced Amur River clam, Corbula amurensis. Levels ofphytoplankton biomass declined by an order of magnitude after the widespread introduction ofC. amurensis in the mid-1980’s, and have not rebounded (Kimmerer 1994).

econdary Production

Secondary production refers to organisms that feed on primary production and transferenergy to higher trophic levels of the estuarine foodweb. Historically, secondary production inthe San Francisco Estuary was dominated by mysid shrimp production (Modlin 1997; Kimmerer1998). However, the native mysid Neomysis mercedis has been largely replaced by theintroduced Acanthomysis bowmani, which persists at lower densities. The introduced amphipod
Gammurus daiberi may have taken over some of this niche, but it is largely restricted to freshwater.

Today, the main source of secondary production derives from copepods. The naturalizednative calanoid copepod Eurytemora affinis is believed to have been introduced near the end of19th Century (Lee 1999). It dominated the zooplankton of the low salinity zone until the 1980’swhen it was largely replaced by another introduced calanoid copepod, Pseudodiaptomus forbesi(Orsi 1991; Kimmerer 1996). P. forbesi persists by maintaining a source population infreshwater, high-residence regions of the Estuary, particularly in the Delta, outside the range ofsalinity tolerance of the Amur River clam (Durand 2006). Because the once-dominant E. affinislacks an upstream range, it is more vulnerable to predation by the clam, and suffers fromapparent competition with P. forbesi.

Other calanoid copepods that may be of significance are the recently introduced
Sinocalanus doerri and Acartiella sinensis. Little is known about the life histories of theseorganisms, although based upon their morphology, they may prey on other copepods. Theyappear in irregular cycles of abundance, during which they may dominate the zooplankton (Orsi1999).Yet another invasive copepod, the very small cyclopoid Limnoithona tetraspina,appeared in the Low Salinity Zone in the 1990’s. Since then, L. tetraspina has become thenumerically dominant copepod, reaching densities on the order of 10,000/m3. It relies on the microbial loop as its food source, feeding upon bacteria,ciliates and rotifers (Bouley P. 2006). In addition, it seems invulnerable to predation by the AmurRiver clam, for reasons that are unknown. Because of its small size, L. tetraspina is generally notavailable for consumption by larger predators, particularly fish, making it an energetic dead end.

Foodweb

It is difficult to characterize the historic foodweb of the San Francisco Estuary because ofthe dramatic changes in geography, hydrology, and species composition that have occurred in thepast century. However, monitoring begun in the 1970’s gives some information about thehistoric dynamics of the foodweb. Prior to the 1980’s the LSZ was dominated by aphytoplankton-driven foodweb, a stable mesoplankton population dominated by E. affinis, andlarge macrozooplankton typified by San Francisco bay shrimp and mysids (Orsi 1986). Theseprovided nutrition and energy to native filter feeders such as the northern anchovy, Engraulismordax, and planktivores such as Delta smelt and juvenile salmon.

Foodweb change has been driven historically by increased turbidity, and more recentlyby introduced species, as described in the sections on primary and secondary production.Notably, the high clearance rate of the introduced Amur River clam population has produced aten-fold decline in plankton density, resulting in a carbon trap in the benthos and an assumedincrease in waste detrital production (Kimmerer 1996). This waste is hypothesized to fuel themicrobial loop, resulting in an increase in microzooplankton such as L. tetraspina, which utilize
rotifers and ciliates.

These changes are one cause for declining fish stocks. For example, the northernanchovy, Engraulis mordax, was until the 1980’s quite abundant in the Low Salinity Zone, untilits range in the Estuary became restricted to the Central and South Bays (Kimmerer 2006). Thisis probably due to a behavioral response following the introduction of the Amur River clam andthe subsequent decline in plankton availability.

More recently, a general Pelagic Organism Decline (POD) was described, and this hasbeen the source of much concern within the scientific, managerial, and political communities.Several key species, including Delta smelt, longfin smelt, striped bass, and threadfin shad havebeen declared “species of interest” because of a stepwise decline in abundance beginning in 2001(Taugher 2005) This was attended by a similar decline in secondary productivity and is currentlythe source of much research. A number of hypotheses have been proposed to explain the POD,including foodweb decline, water exports from the Delta, and toxics from urban, industrial, oragricultural sources.

Introduced species

Species introductions have been increasing since at least the 19th Century as a function ofincreasing trade and traffic. Introductions include numerous taxa, including copepods, shrimp,
amphipods, bivalves, fish and both rooted and floating plants. Many pelagic species have beenintroduced most recently through ballast water releases from large ships directly into the Estuary(Carlton 1996). As a result, many of these introduced species originate from estuaries around thePacific Rim, particularly copepods such as P. forbesi and L. tetraspina. The Amur River clamoriginates from Asia, and has created significant and drastic changes to the ecology of the LSZ,primarily by diverting pelagic food to the benthos and into an accelerated microbial loop (Cole1992).

Species have also been introduced via attachment to sporting boats which are traileredbetween regions (Carlton 1996). This is the probable source of a number of low salinity plantslike Egeria densa and water hyacinth (Eichhornia crassipes). These plants have createdprofound changes in the Delta by disrupting water flow, shading phytoplankton, and providinghabitat for piscivorous fish like the striped bass, Morone saxatilis, itself intentionally introducedin the late 1800’s from the Chesapeake Bay (Radovich 1963; Carlton 1996). The freshwater
quagga mussel, originally from Europe, is expected to be introduced by boaters within the nexttwo to ten years, in spite of precautionary measures (Dey 2007).

Future Ecology

The ecology of the Low Salinity Zone of the San Francisco Estuary is difficult tocharacterize because it is the result of a complex synergy of both abiotic and biotic factors. Inaddition, it continues to undergo rapid change resulting from newly introduced species, directanthropogenic influences and climate change. Future ecological changes will be driven on anecosystem wide scale, particularly as sea level rise, tectonic instability and infrastructure declinecause levy failure in the Delta (Epstein 2006). The resulting back-surge in water flow is expectedto force X2 into the Delta, jeopardizing spatially oriented habitat (like freshwater marshes),channelizing the low salinity zone, and threatening southern California’s water supply, withunknown and unforeseeable consequences for the natural and human ecology of the West coast’slargest estuary.

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