Galley Proofs for

Galley Proofs for Cloern, J.E., P.L. Barnard, E. Beller, J.C. Callaway, J.L. Grenier, E.D. Grosholz, R. Grossinger, K. Hieb, J.T. Hollibaugh, N. Knowles, M. Sutula, S. Veloz, K. Wasson, A. Whipple. 2016. Life on the Edge – California’s Estuaries, in Ecosystems of California: A Source Book, edited by Harold Mooney and Erika Zavaleta, University of California Press, 359-‐387.

Nine teen

Estuaries Life on the Edge Jam es E . C loern, Patr ic k L . Barnard, Er in Beller , John C. Call away, J. Le titia Gren ier , Edwin D. Groshol z , Rob in Grossinger , K athryn H ieb, Jam es T. Hollibaugh, Noah Knowles, Martha Sutu l a , Sam uel Veloz , Kerstin Wasson, and Alison Whi pple

Introduction On May 14, 1769, Friar Juan Crespí described his happiness upon arriving at the “splendid Harbor of San Diego,” a vast bay “plentiful in very large sardines, rays, and many other fish, and a great many mussels” (Crespí and Brown 2001). Over the following months, Crespí traversed the California coastline, encountering an abundance and variety of estuaries. He observed “a great deal of glitter where salt must be collecting” in a seasonally dry lagoon, the sand-dammed Santa Ynez River where “the sea has been putting a height of sand in front of it,” and finally a bay so large “that all the navies of Spain could fit in it”—California’s largest estuary, the San Francisco Bay-Delta. Crespí’s journal is part of a rich collection of observations detailing the physical and ecological diversity of California’s estuaries before modern modifications, ranging from large tidal bays to intermittently closed lagoons at the mouths of small creeks (Grossinger et al. 2011).

In estuaries across this spectrum early records show heterogeneous mosaics of habitat types reflecting California’s geologic, topographic, and climatic diversity. This diversity can be illustrated by comparing two very different estuary types: California’s largest estuary and some of its smallest (Figure 19.1). The San Francisco Bay-Delta historically drained 40% of the state’s area, with flows coalescing in the Sacramento and San Joaquin Rivers and meeting the tides within the estuary’s inland delta. Consequently, a large portion of the estuary was tidal yet fresh: 66% of the estuary’s 2,240 square kilometers of wetlands occurred in the freshwater Delta (Whipple et al. 2012). Though portions of these wetlands appeared to be “covered with nothing but tule” (Abella and Cook 1960), the landscape was also composed of 2,600 kilometers of winding tidal channels, willow-fern communities (Atwater 1980), sand mounds, and riparian forests 359

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along major river channels. This heterogeneity contributed to the higher observed plant diversity in the Delta as compared to other regions of the Bay-Delta estuary (Atwater et al. 1979, Vasey et al. 2012). Downstream, the estuary opened into a series of large bays with extensive fringing tidal flats and marshes. Open-water habitats at the seaward end of the estuarine gradient were bordered by broad tidal flats and pickleweed-dominated salt marshes with a dense network of tidal channels. In contrast to the Bay-Delta, the Santa Clara River mouth and associated estuaries in southern California had only seasonal freshwater input (Beller et al. 2011), with more limited tidal influence because the river mouth was “blocked up by sandhills” during summer (Cooper 1887) and connected to the ocean only “after the rains of winter” (Johnson 1855). A series of backbarrier lagoons marked former river mouths, separated from the ocean by sand dunes that effectively blocked the tides (Reed 1871). Instead of the Delta’s tules and extensive forests, many of these small estuaries were dominated by shallow hypersaline open-water areas, pickleweed-dominated salt marsh, and extensive salt pannes (Bard 1869). However, local springs brought more freshwater to other, neighboring lagoons to maintain permanent open-water areas with a compressed salinity gradient and fringing stands of tules, creating very different conditions even among adjacent systems. These examples drawn from reconstructions of early 1800s conditions illustrate the substantial seasonal variability and diversity of forms, physical characteristics, and biological communities of these coastal ecosystems. In this chapter we describe the diversity of California’s estuaries today, the processes that generate the complex patterns of variability characteristic of estuaries, the biological communities they support, the services they provide, their fast-paced transformations by human actions, and how future transformations will be influenced by choices we make. We begin with descriptions of the geographic and climatic settings of coastal California to provide the physical context for understanding why its estuaries exhibit the diversity of forms first documented in the eighteenth century and still expressed to varying extent today.

Physical Features of the California Coast Estuaries are transitional ecosystems at the land-sea interface, and unlike terrestrial and freshwater ecosystems they are strongly influenced by connectivity to both land and ocean. The morphology (size, form) and dynamics of estuaries are shaped by physical features of the land-ocean transition. California’s 1,766-kilometer-long coast is situated along the active tectonic boundary between the North American and Pacific plates (dashed line in Figure 19.2). The geologic complexity and active uplift associated with this setting created a mountainous terrain with deeply incised stream channels intersecting a plunging coastline (shown as a narrow band between the +100 meter and –100 meter contour lines on Figure 19.2); exceptions are the coastal plains bordering Mon-

Image on previous page: Mt. Tamalpais from Napa Slough by William Marple. This 1869 painting of Napa Valley’s tidal marshlands provides a rare view of a California estuary before reclamation. A steamer winds through the tall tules on its way to the port of Napa; small islands covered in willows can be seen at right. Courtesy of the California Historical Society.

terey Bay and the Los Angeles Basin. Over 70% of the shoreline comprises sea cliffs, bluffs, and coastal mountains; and the high-relief cliffs, headlands, and points are most common in the northern half of the state, where more erosion-resistant rocks predominate (Griggs et al. 2005, Hapke et al. 2009). California’s coast is fronted by a narrow continental shelf. The rugged coastline, proximity of mountains to the ocean, irregular shoreline, and narrow continental shelf create a physical setting that distinguishes California’s estuaries from those situated in the coastal plains of the U.S. Atlantic coast. Many California estuaries form along the lower reaches of stream valleys fronted by small beaches and barrier spits adjacent to headlands or behind barrier beaches, and they are typically backed by a narrow coastal plain (San Francisco Bay and the smaller estuaries in the Los Angeles basin are notable exceptions). Those situated in narrow coastal plains (e.g., Noyo, see Figure 19.2) drain watersheds of only a few hundred square kilometers—much smaller than watersheds characteristic of East Coast estuaries. High relief along the coast also isolates California’s estuaries topographically, both alongshore and cross-shore, so they have a wide diversity of forms and sizes. Lastly, the narrow continental shelf implies that California’s estuaries are closely connected to a high-productivity coastal upwelling system that is a source of phytoplankton biomass; larval and juvenile stages of marine fish and invertebrates that rear in estuaries; and nutrient-rich, low-oxygen, low-pH, deep ocean water. Three other coastal features influence the morphology and seasonal dynamics of California’s estuaries: sediment transport, waves, and tides. Alongshore transport is important because it carries away sediment from coastal erosion or streams that can otherwise seal off the mouths of smaller estuaries when energy from streamflow, waves, or tides is not sufficient to keep the inlets open. Sediment transport is controlled by geologic features that constrain alongshore flows, including submarine canyons that incise the continental shelf and transport sediment to the deep-sea floor. Several of these canyons extend nearly to the shoreline (e.g., Mugu and Monterey Canyons) and define the boundaries of coastal sediment transport (“littoral cells”). Rocky headlands also define the limits of littoral cells as well as the alongshore extent of numerous small beaches and longer expanses of uninterrupted sandy beaches. Waves are an important source of energy that shapes estuaries through their influence on sediment erosion, suspension, and transport. Wave energy off the California coast is dominated by long-period, westerly ocean swell. Wave energy increases from south to north along the coast, with average wave heights in central California of approximately 2.5 meters and a few tens of centimeters lower and higher in southern and northern California, respectively. Variability in the strength of ocean swell is strongly seasonal, with the largest waves arriving from November through April. Annual wave height in deep water exceeds 6 meters and reaches up to about 9 meters during extreme events (Wingfield and Storlazzi 2007). However, depending on direction of the swell relative to the coastline and the degree of topographic sheltering, which is prevalent in southern California, nearshore wave heights can be a fraction of those in deep water (Adams et al. 2008). Waves interact with changes in sea level. Warmer coastal waters and lowered atmospheric pressure during El Niño winters raise sea level along the California coast up to 30 centimeters, with an additional 5–10 centimeters of

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A A

B B

N N

10 miles miles 10

Beachƒ Beach†

Shallow water Shallow Water

Dune† Duneƒ Alkali AlkaliMeadow† meadowƒ

Marsh / Salt Flatflat MarshPanne panne / salt

10 10kilometers kilometers N N

DeepWater water Deep

Tidal TidalFlat* flat*

1/2 mile ½ mile 1/2 kilometer ½ kilometer

Riparian RiparianForest forest/ Scrub* / scrub*

Tidal Marsh* TidalFreshwater freshwater marsh* Non-Tidal Freshwater Marsh* Nontidal freshwater marsh* Salt Marsh Salt/ Brackish / brackish marsh

**San SanFrancisco FranciscoBay-Delta Bay-Deltaonly only

High HighMarsh marshTransition transitionZone† zoneƒ

†ƒ Ventura Ventura only only

C C

D D

San FranciscoBay Bay San Francisco & & Delta

Ventura Ventura

Figure 19.1 Reconstructions of early 1800s landscapes for California’s largest estuary and some of its smallest, illustrating the substantial physical complexity and biodiversity formerly exhibited by California estuaries. In the San Francisco Bay–Delta estuary’s 2,240 square kilometers of wetlands (top), a diversity of ecological communities existed along the estuarine gradient. These included willow-fern complexes and dense riparian forest within the tule-dominated freshwater wetlands of the Delta (A), with the subtidal bays, broad tidal flats, and pickleweed-dominated tidal marshes of San Francisco Bay (B) further downstream. In comparison, a series of small, backbarrier lagoons associated with relict mouths of the Santa Clara River in Ventura County (bottom) experienced extremely limited tidal influence and freshwater input. High sand dunes blocked tidal access, creating shallow, hypersaline open-water areas, seasonally flooded salt flats, and pickleweed plains (C). At some lagoons local springs created fresher conditions, supporting fringing tule (D). Historical mapping courtesy of the San Francisco Estuary Institute. Photo credits: (A) artist unknown n.d. [LB67-712-41], courtesy of the Haggin Museum, Stockton, California; (B) artist unknown 1916 [A-1005], courtesy of the San Francisco Public Utilities Commission; (C) photograph by John Peabody Harrington 1913 [neg. 91-30700], courtesy of the National Anthropological Archives, Smithsonian Institution; (D) Brewster ca. 1889, courtesy of the Museum of Ventura County.


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Figure 19.2 Topography of the California coast, including tectonic plate boundaries (dashed red line) and selected watersheds (names capitalized in black). Three common types of estuaries are highlighted: drowned river mouth (Russian River mouth), tectonic (Tomales Bay), and barrier spit (San Diego Bay). Not shown: Pajaro River watershed, located immediately east of the Salinas watershed. Source: Data from U.S. Geological Survey, National Hydrography Dataset (NHD). Map: Parker Welch, Center for Integrated Spatial Research (CISR).


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Table 19.1 Watersheds of California’s estuaries have diverse sizes, degrees of water management, and runoff This table summarizes data for estuaries shown in Figure 19.3.

Area (km2)

Reservoir storage (×106 m3)

1970–2010 mean average outflow (m3/s)

Runoff ratio

40,609

3,951

470

0.44

9,529

96

243

0.51

293

0

6

0.49

3,843

405

62

0.51

164,655

73,122

762

0.20

Pajaro

3,368

44

4

0.10

Salinas

11,084

897

13

0.07

Tijuana

4,490

286

5

0.04

Estuarine watershed Klamath Eel Noyo Russian San Francisco Bay

Sources: U.S. Army Corps of Engineers 2013, U.S. Geological Survey 2013, CDWR 2011, International Boundary and Water Commission 2013, Watershed Boundary Dataset 2013. Note: Outflow and runoff are based on water-year (WY, beginning October 1) statistics.

decadal variability possibly associated with the Pacific Decadal Oscillation (Bromirski et al. 2003). The narrow shelf and absence of hurricanes to generate extreme winds and low atmospheric pressure result in small surge elevations during severe storms along the Pacific coast compared to Atlantic and Gulf coast settings. Nevertheless, storm surges force water-level fluctuations as high as 70 centimeters in protected embayments of central California. In estuaries connected to large rivers, these water-level extremes are amplified further when the ocean surge coincides with high river inflow (Cayan et al. 2008). During extreme events waves are the dominant factor that elevates water levels along the exposed outer coast and are capable of increasing water levels by several meters. Therefore, overtopping and breaching of beaches and barrier spits that protect and/ or close off estuary mouths are often associated with large waves. Tides are important because they drive hourly changes in water level and currents that transport ocean water into estuaries and are the most important source of energy to vertically mix estuaries. Tides of the Pacific coast are mixed, with both diurnal and semidiurnal periods of oscillation. Similar to the gradient of wave energy, the range of the tides increases from south to north, with an average diurnal range of 1.6 meters along the open coast in San Diego and up to 2.1 meters in Crescent City. The tidal range inside estuaries can be damped or amplified, depending on bathymetry and basin configuration. For example, the tidal range in lower South San Francisco Bay exceeds the range at the entrance by about 1 meter. Tides also oscillate over the fortnightly neap-spring cycle; the energetic spring tidal ranges can exceed neap tidal ranges by 1 meter or more.

The Climate System: Precipitation and Runoff As mixing zones between seawater and freshwater, estuaries are dynamic ecosystems where variability of hydrodynamics, water chemistry, sediment transport, habitats, and bio-

logical communities are strongly influenced by variability of freshwater inflows from upstream watersheds. Patterns of freshwater inflow to California’s estuaries are shaped by the state’s geographic and land-use diversity as well as its meteorological patterns. Differences across estuaries in watershed size, hydrologic response, reservoir storage, and level of development result in a wide range of flow characteristics. Here we use eight estuarine watersheds (summarized in Table 19.1 and shown in Figure 19.3) to illustrate this diversity, and in the following section we show how variability of flow generates complex patterns of chemical and biological variability within estuaries.

Mean Annual Patterns

Annual cycles of estuarine freshwater inflows are driven primarily by the seasonality of watershed outflows, which is determined largely by California’s climate of wet winters and prolonged summer dry seasons (see Figure 19.3a). The seasonal patterns of atmospheric variability over the eastern North Pacific that produce this seasonality of runoff also produce the annual cycle of wind-driven coastal upwelling that is strongest in summer and relaxes during autumn-winter. The timing and magnitude of freshwater inflows to California’s estuaries are also affected by human activities in the watersheds. Dams delay and reduce annual runoff to varying degrees depending on reservoir size and the ultimate uses of the captured water. Groundwater pumping and recharge and water transfers between watersheds also affect annual cycles of estuarine inflow. The combination of atmospheric forcing, human activities, and watershed hydrology produce a variety of estuarine inflow patterns throughout California. Rugged terrain generates intense precipitation over watersheds draining to rivers along the northern coast such as the Eel, Noyo, and Russian Rivers (see Figure 19.3b). These basins have relatively little artificial storage or in-basin losses (e.g., evapotranspiration), resulting in high runoff ratios (outflow/precipitaEstuar ies 363


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10

300

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-150

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σQ/σP

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mm day-1

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m3 s-1 100 m-1

SF Bay P,Q Eel P,Q Salinas P,Q Upwelling

Mean prcp. Mean flow Storage

4

150

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0.1 1975

1980

1985

1990

1995

2000

2005

2010

0

SFB

Year

KLA

EEL

NOY

RUS

PAJ

SAL

TIJ

Location

Figure 19.3 California’s estuaries have diverse patterns of climate-driven variability in their watersheds and in the adjacent coastal ocean. See Table 19.1 for additional data sources. The x-axis labels in panels B and D correspond to the watersheds listed in Table 19.1. A Mean annual cycles for water years (October–September) 1970–2 010; area-averaged daily precipitation (P) and outflow (Q, from watershed

to estuary) in three watersheds (Maurer et al. 2002) and of upwelling (black line, right y-axis) near the Central Coast (Pacific Fisheries Environmental Laboratory 2013). B Mean area-averaged precipitation, outflow, and reservoir storage in major California watersheds in 2000. SFB: San Francisco Bay; from

north to south: KLA: Klamath River; EEL: Eel River; NOY: Noyo River; RUS: Russian River; PAJ: Pajaro River; SAL: Salinas River; TIJ: Tijuana River. C Mean annual flow magnitude (solid lines) and timing (dashed lines, right y-axis). Timing is computed as the weighted average of dates in

a given water year, where each date is weighted by that day’s flow magnitude. An early (e.g., December 1) date indicates a concentration of flow early in the rainy season for that year and conversely for later dates. Watershed color-coding follows panel A. D Ratio of standard deviations (σ) of mean annual flow (Q) and precipitation (P). This ratio is a measure of the damping effect of watershed

processes on interannual precipitation variability. Abbreviations follow panel B.

tion, see Table 19.1). The larger watersheds of the Klamath River and San Francisco Bay-Delta have more diverse topography and include substantial areas of moderate-to-low precipitation and significant in-basin losses. The Bay-Delta watershed in particular has agricultural regions with high losses to evapotranspiration and a massive freshwater management infrastructure, so its runoff ratio is low as a result of human activities. Rivers draining watersheds of the central coast (Pajaro, Salinas) receive less precipitation, and although they have little artificial storage, most flows are used for groundwater recharge (California Department of Water Resources 2009), resulting in low runoff ratios. The Tijuana basin follows a similar pattern, though urban consumption in an arid climate is the main in-basin loss. Historically, wastewater has been a major component of inflow to the Tijuana estuary (Zedler et al. 1984).

Interannual Patterns

Annual estuarine inflows are highly correlated throughout the state (see Figure 19.3c), but the timing of runoff is more dependent on the effects of artificial and natural water storage within basins. Storage and in-basin losses also reduce flow variability relative to precipitation variability (see Figure 19.3d). In particular, in-basin agricultural and urban losses strongly reduce interannual variability in the central coast (e.g., Pajaro, Salinas basins) and Tijuana basins, and freshwater management in the watershed reduces variability of inflow to the San Francisco Bay-Delta. Interannual outflow variability in the less developed northern coastal basins (e.g. Klamath, Eel, Noyo, Russian basins) is only slightly less than precipitation variability. Even in the more highly managed basins, however, meteorological forcing (air temperature, pre-

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cipitation) remains the dominant mechanism of interannual variability in the timing and magnitude of outflow (Knowles 2002). Another aspect of interannual variability that impacts all estuaries is drought—a natural and recurring feature of California’s climate that leads to increased salinity intrusion and longer residence times (slower flushing). Recent examples include the 1976–1977 and 1987–1992 droughts (see Figure 19.3c) and the record drought of 2013–2015. El Niño and La Niña events are important drivers of California’s interannual climate variability associated with opposing patterns of sea surface temperature in the equatorial Pacific that cycle roughly every three to seven years (Diaz and Markgraf 1992) (see Chapter 2, “Climate”). El Niño events tend to dampen coastal upwelling (Schwing et al. 2005). They also tend to cause wet years in southern California with milder impacts in the rest of the state, although impacts vary greatly among El Niño years. La Niña events tend toward the opposite weather pattern across California but with more consistent impacts across different La Niña events (Redmond and Koch 1991, Cayan et al. 1999).

Multidecadal Patterns

The Pacific Decadal Oscillation (PDO) has a similar northsouth pattern of impacts on precipitation as the El Niño/La Niña cycle (Mantua et al. 1997, Cayan et al. 1998), but its cycles have a longer period of forty to sixty years. The PDO and, to a greater extent the North Pacific Gyre Oscillation (NPGO), modulate the annual cycle of coastal upwelling and its associated physical and biological impacts (Di Lorenzo et al. 2008). The NPGO in particular has important impacts on biological communities through its influence on populations of marine species that migrate into estuaries (Cloern et al. 2010). Finally, clear evidence from records contained in tree-rings (Stine 1994) and estuarine sediment cores (Ingram et al. 1996) indicates that California’s climate has included droughts lasting from decades to centuries. Multidecadal droughts must have restructured biological communities across all California ecosystems, including in its estuaries.

E xtreme Flows

Peak flow events associated with storms play a critical role, flushing contaminants and supplying sediment while perturbing or altering estuaries through processes such as bottom scouring and precipitous drops in salinity that lead to displacement or wholesale mortality of marine organisms. El Niño years can bring such high-flow events, especially in the southern California watersheds (Cayan et al. 1999). Recent discoveries have revealed that long streams of water vapor originating in the tropics, termed “atmospheric rivers” (AR), are responsible for most major precipitation events in the western U.S. (Dettinger and Ingram 2013) (see Chapter 2, “Climate”). Concentrated in an average of about ten days each year, ARs cause more than 80% of flooding in California rivers. Approximately every one hundred to two hundred years an AR persists for a month or longer. The last such “megaflood” occurred in 1862, when sustained extreme precipitation swelled rivers along the California coast, transformed San Francisco Bay into a freshwater lake, reversed coastal currents, and amplified an associated ocean surge that cut a new channel into San Diego Bay (Engstrom 1996).

The Diversity of California Estuaries California’s coastline has over four hundred bays, lagoons, and river mouths that we collectively refer to as estuaries. Based on their positions within the gradients of coastal geomorphology, runoff, and oceanography described earlier, California estuaries can be classified into three broad (and overlapping) classes.

Classic E stuaries

The classic estuary has adequate freshwater inflow and tidal exchange to maintain a broad salinity gradient year-round (Pritchard 1967). The only estuarine system in California with these properties is northern San Francisco Bay, although others—such as Humboldt, Tomales, and San Diego Bays—f unction as classic estuaries during the wet season. A key feature of this estuary type is estuarine circulation, where fresher water at the surface flows out of the estuary and saltier coastal water flows into the estuary along the bottom. Strong spring tides disrupt this circulation pattern by causing rapid vertical mixing. Thus, rather than being persistently layered with lower salinity near the surface and higher salinity near the bottom (characteristic of East Coast estuaries such as Chesapeake Bay), the salinity gradient in California estuaries tends to appear as a series of increasingly saltier cells from land to sea.

L agoons

Lagoonal estuaries are marine-dominated most of the year, have an open connection to the ocean, and thus are tidally influenced; a related type occurs at stream mouths (see next in chapter). They are often formed by the development of a sand spit that encloses a coastal embayment in the lee of an island or headland. By this definition lagoons are not formed directly in stream channels, so their relief is flat enough to support extensive tidal marshes and mudflats or sandflats. Examples of these lagoonal systems are Bodega Harbor, Bolinas Lagoon, and Morro and San Diego Bays. South San Francisco and Tomales Bays are lagoons formed primarily by tectonic processes. During summer or when lagoons are closed, freshwater inflow is less than evaporative water loss so salinity increases, in some cases above seawater salinity. Some lagoonal estuaries become extremely hypersaline when they are isolated from tidal exchange with the coastal ocean after formation of a sand barrier. Examples are Agua Hediondia and Batiquitos Lagoons in southern California and the Estero de Americano in central California. With increased freshwater inflow during winter, these estuaries freshen dramatically until the sand barrier breaches and tidal exchange of water is restored. Some of California’s shallow lagoons flush completely every tidal cycle and tend to be fully marine year-round (e.g., Bodega Harbor, Bolinas Lagoon, Morro Bay). Larger lagoonal estuaries are deeper and have longer water residence times. Warming of lagoon water during summer compensates for the increased density caused by high salinity. These opposing factors slow the density-driven estuarine circulation, so during summer lagoons such as Tomales Bay, South San Francisco Bay, and San Diego Bay retain water trapped at their head with an essentially infinite residence time. Long water retention isolates estuarine populations and alters water chemistry as the Estuar ies 365


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A

B

C

D

E

F

Figure 19.4 Typical habitat types in California estuaries. Photos: (A, C, D, E, F) Kerstin Wasson, (B) John Callaway A Brackish marsh, with a mix of freshwater and salt-tolerant vegetation. B Salt marsh, which dominates in the high intertidal of saline portions of estuaries. C Mudflat habitat dominates the intertidal zone below mean high water. D Oyster beds provide structured habitat on low intertidal or shallow subtidal mudflats. E Eelgrass beds provide structured habitat on low intertidal or shallow subtidal mudflats. F Open water provides water column habitat; below that, the subtidal bottom habitat is dominated

by soft sediments.

effects of biogeochemical processes, such as denitrification (Smith et al. 1996), accumulate during the dry season. Cooling and freshwater inflow during the wet season trigger rapid exchange of estuarine water with the ocean, leading to redistributions of salinity, organisms, and chemical constituents.

River Mouth E stuaries

These are the most common estuarine type in California, ranging from rivers and streams large enough to maintain freshwater inflow in midsummer to those with no summer inflow. The estuary is confined to a river channel, which is often steep-sided and supports only limited areas of intertidal mudflats or salt marshes. A critical factor in the hydrodynamics and ecology of these systems is whether they remain

open to tidal exchange year-round. Although saline during summer, river-dominated systems in northern California do not become hypersaline and they may become completely fresh following high runoff events. Some of these estuaries, such as the Russian, Gualala, Noyo, and Navarro Rivers, are important migratory corridors for anadromous fishes such as salmon and steelhead. Stream mouth estuaries that drain smaller watersheds or watersheds receiving little rainfall (typical of southern California) have little or no freshwater inflow by midsummer and can become hypersaline, particularly if ocean exchange is limited by formation of a sand barrier across the mouth. Winter runoff retained behind the sand bar freshens the estuary and may cause upstream flooding until the bar is overtopped and washed out. These seasonal changes in hydrology also lead to variable inundation of bordering wetlands. Examples of this estuary type include Pes-

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cadero Creek, Pajaro River, Salinas River, Estero de San Antonio, and Estero Americano.

A

40

Complex Patterns of Ecosystem Variability

Salinity

Habitat Diversit y within E stuaries

Dry season

30 Wet season

20 10

Nitrate + nitrite (µ M)

Estuarine ecosystems include a mosaic of interconnected habitat types (Figure 19.4) commonly classified by their salinity and elevation. From river to the sea, tidal freshwater habitats are not salty, but their water levels rise and fall with the tides. Brackish habitats are also affected by tides but have a larger saltwater component and salinity ranging up to about 18 (i.e., approximately half seawater and half freshwater). Marine habitats have salinity above 18. Another categorization defines habitats by their position along the elevational gradient from the intertidal to subtidal zone. Vegetated marsh often occupies the upper intertidal zone from the highest reach of the tide down to mean tide level or, in freshwater systems, as low as mean lower low water (Atwater et al. 1979). Riparian trees and shrubs can occur within intertidal elevations, especially under fresher conditions. Tidal fresh, brackish, and salt marsh ecosystems include a mosaic of habitat types including tidal creeks and bare pannes as well as areas of dense marsh vegetation. Below marshes, the lower intertidal and subtidal zones can be further distinguished by pelagic (water column) and benthic (bottom) habitats. Mudflats and sandflats are the dominant habitat type in the intertidal zone, although there may also be rocky areas or oyster or seagrass beds. Soft bottom sediments dominate the benthos in the subtidal zone but again can be interrupted by patches of rocky areas, bivalve reefs, or seagrass.

River

Ocean

B

80 60

Wet season

40 20

Dry season

0 0

4

8 12 Distance (km)

16

Figure 19.5 Estuaries are characterized by large spatial gradients. Source: http://lmer.marsci.uga.edu/tomales/tb_diss_metadata.html, accessed June 10, 2015. A Distribution of surface salinity (practical salinity scale, unitless)

As transitional ecosystems between rivers and oceans, estuaries are characterized by sharp spatial gradients and large variability measured at times scales ranging from hours to decades. We illustrate examples of chemical and biological variability in the subtidal habitats of Tomales Bay and San Francisco Bay.

Spatial Patterns A prominent feature of spatial variability in estuaries is the longitudinal salinity gradient, a result of mixing between ocean water (salinity about 35) and riverine freshwater, seen in lagoonal estuaries such as Tomales Bay during the wet season (Figure 19.5a). In this state estuaries have a low-salinity or freshwater landward domain, a marine seaward domain, and transitional brackish habitats between the two. Each salinity domain has its own characteristic chemistry, biological communities, and biogeochemical and ecological processes (Smith and Hollibaugh 1997). California’s estuaries shift to a different state during the dry season, when freshwater inflow is reduced or absent, salinity increases, and the salinity gradient can reverse as a result of salt concentration by evaporation. In this state estuaries function as shallow marine ecosystems or evaporative salt flats depending on climate and closure patterns. Therefore the seasonal input of freshwater is an essential process of estuarine dynamics that alters the mixture of ocean and river water within estuaries and drives fast seaward flows that transform estuaries from long-retention systems to flowthrough systems with short residence times (days to weeks).

along the ocean-river continuum of Tomales Bay, from its mouth toward the head of the bay, during the dry season (September 5–7, 1991) and the wet season (March 5–7, 1991). B Distributions of nitrate + nitrite concentration along Tomales Bay

during the dry season and wet season.

Rivers and oceans have distinct chemical compositions, so estuarine chemistry also varies along the salinity gradient. Relative to ocean water, rivers generally have elevated concentrations of nutrients, organic carbon, trace elements, and toxic contaminants, so a common spatial pattern is progressive seaward dilution of river-derived constituents, illustrated by the gradient of nitrate+nitrite (key forms of nitrogen used by primary producers) along Tomales Bay during the wet season (see Figure 19.5b). However, we see that nitrate+nitrite concentrations fall in Tomales Bay during the dry season when the river supply is lost. Moreover, the spatial gradient reverses because residence time in the upper estuary is long enough for denitrification to remove nitrate faster than it is supplied by land runoff. Therefore complex patterns in estuaries are manifested as seasonally varying spatial gradients that result from fluctuating river flow, mixing of water sources having distinct compositions, and fast biogeochemical transformations.

Patterns of Variability over Time Biological variability in estuaries is driven by many processes including human disturbances, seasonal and interannual flow variability, and tidal oscillations. This variability Estuar ies 367


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A

40 Chl-a (µg L-1)

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Figure 19.6 Estuaries are characterized by variability over a spectrum of time scales. Data sources: (A, B) ; (C) . A Variability at time scales of years and decades (chlorophyll-a

in northern San Francisco Bay, Interagency Ecological Program Station D7). B Months and years (surface chlorophyll-a [solid line] and salinity

[dashed line] in South San Francisco Bay, USGS Station 27, timing of peak annual freshwater inflow indicated). C Hours (chlorophyll fluorescence at the Dumbarton Bridge, South

San Francisco Bay, January 25–27, 2003, cycle of tidal oscillation indicated).

includes ecological regime shifts, such as the abrupt decrease of phytoplankton biomass (measured as chlorophyll- a) in northern San Francisco Bay after introduction of the filterfeeding clam Corbula (Potamocorbula) amurensis in 1986 (Figure 19.6a). This fivefold reduction in the phytoplankton food supply was followed by population crashes of zooplankton species and native fishes that rely on these zooplankton as a food resource. Many estuaries have recurring seasonal patterns of biological variability, and a common pattern is peak chlorophyll-a during spring when the water column is stratified. Stratification develops when the input of buoyant freshwater overcomes the mixing power of tides and wind so the water column becomes partitioned into a low-salinity surface layer and a higher-salinity bottom layer.

This establishment of a shallow, sunlit surface layer promotes fast phytoplankton growth, so a prominent seasonal pattern in South San Francisco Bay is the spring bloom (high surface chlorophyll-a) when river inflow is high and salinity is low (Figure 19.6b). Years of low river flow, such as 1994, are years of weak salinity stratification and damped spring blooms; years of high river flow and strong salinity stratification, such as 1995, are years of large, prolonged spring blooms. Blooms have transformative effects on water chemistry caused by rapid phytoplankton uptake of nutrients, trace elements, and CO2 (causing pH shifts), and they are followed by bursts of population growth by bacteria, ciliates, copepods, amphipods, and bivalves as their phytoplankton food supply increases (Cloern 1996). Therefore, complex patterns are also manifested in estuaries as linked biogeochemical and biological variability tied to seasonal and interannual fluctuations of river flow and its influence on vertical mixing. Seasonal salinity variations are also pronounced in California salt marshes. Soil salinity in Spartina-dominated areas regularly inundated by tides fluctuates with salinity variability in adjacent estuarine waters, while seasonal salinity fluctuations in the upper, less frequently flooded marsh areas are more influenced by evapotranspiration and rainfall. These seasonal salinity shifts affect plant distributions because seed germination in tidal marshes is restricted to periods of low salinity (Noe and Zedler 2001). Estuaries also have pronounced variability at time scales of hours to days, and some of this variability reflects the strong oceanic influence on California’s estuaries. For example, episodic occurrences of low dissolved oxygen in bottom waters of San Francisco Bay are caused by intrusions of low-oxygen deep ocean water brought to the surface by wind-driven upwelling and then transported into the estuary. Tides generate hourly variability as horizontal gradients of constituents such as chlorophyll-a oscillate over a fixed location (Figure 19.6c). The amplitude of these oscillations is comparable to that of annual phytoplankton cycles in lakes and oceans, but these estuarine cycles repeat twice daily. This example illustrates the challenge of understanding estuarine plankton dynamics based on sampling from a fixed position where variability results from the combination of fast water motions (tidal oscillatory transport) and biological processes such as growth and grazing.

Biota and Their Roles in the Ecosystem The Biological Communities The spatial gradients and temporal variability of estuaries result in varied assemblages of plant and animal species that are key components of California’s rich biological diversity. Studies of biological communities reveal distinctive patterns of diversity and variability, and they illustrate eight principles (labeled in the text that follows) of how estuaries function as ecosystems (Box 19.1).

Primary Producers

Estuaries have five major primary producer groups—phytoplankton, benthic microalgae, macroalgae such as Ulva spp., seagrass such as Zostera marina, and tidal marsh vascular plants. Unlike terrestrial ecosystems where most primary pro-

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Box 19.1 Eight Principles of Estuarine Ecology Estuaries have properties distinct from other ecosystems because of their geographic setting at the landsea interface. We highlight eight principles of estuarine ecology: 1. Fate of primary production. Much of the primary production in estuaries is contributed by fast-growing algae; unlike vascular plants, most of that production is consumed rather than stored in structural biomass. 2. Plant distributions. Estuarine plant communities vary systematically along the gradients of habitat type between open water and marsh plains, and between saline and freshwater. 3. Seasonal patterns. California’s estuaries do not share one common community or seasonal pattern of primary producers because their habitat mosaics are spatially diverse and seasonally dynamic. 4. Roles of microbes. Estuaries receive external inputs of organic matter, are fast-running biogeochemical reactors, and prokaryotes are the key agents of biogeochemical transformations. 5. The salinity gradient. Biological communities vary along the estuarine salinity gradient, and pelagic biota (plankton, fish) are continually redistributed as the salinity gradient oscillates with seasonal fluctuations of freshwater inflow. 6. Habitat connectivity. Chemical and biological variability in estuaries are strongly influenced by vertical exchanges between water and bottom sediments and horizontal exchanges between subtidal and intertidal habitats. 7. Estuaries are open ecosystems. For example, fish communities are structured by immigrations of marine species whose population abundances track annual climate variability across ocean basins. 8. Biota as agents of element transport. Migratory fish and invertebrates transfer carbon and nutrients from tidal marshes and other shallow-water habitats to the open estuary and to the ocean, while salmon transfer carbon and nutrients from the ocean to rivers.

duction is from photosynthesis of vascular plants, algal photosynthesis is a large component of estuarine primary production (Jassby et al. 1993). This is important because algae grow rapidly, and most of their production goes into energyrich biochemicals that are a high-quality food resource consumed as fast as it is produced. The biomass of algal producers in estuaries turns over rapidly (up to one thousand times faster than vascular-plant producers) (Cebrian 1999), and most is consumed instead of stored in structural biomass (Principle 1). The relative importance of the five producer groups varies with habitat attributes such as water depth and light availability, substrate stability, and nutrient concentrations. Phytoplankton tend to be the dominant primary producers in deep water and codominant with benthic microalgae in shal-

low subtidal habitats. As depths decrease toward the shore, light reaches the bottom and subtidal habitats can then be colonized by attached forms—seagrasses, benthic microalgae, and macroalgae. Benthic microalgae and macroalgae are generally the dominant primary producers on mudflats and sandflats where seagrasses are limited by desiccation and temperature stress. Freshwater, brackish, and salt marsh dominates the higher intertidal zone, with flood-tolerant riparian shrubs and trees at the upper edge of the ecotone from the aquatic to terrestrial habitat. The composition of estuarine plant communities varies systematically along the gradients of habitat type, from open water to marsh plains and from saltwater to freshwater (Principle 2). This principle applies across California’s estuarine ecosystems. Primary production in muddy, turbid estuaries like San Francisco Bay is dominated by phytoplankton photosynthesis (Jassby et al. 1993), although the historical loss of tidal marsh habitat within San Francisco Bay and elsewhere has greatly reduced the contribution of vascular plants to overall estuarine productivity. Shallow lagoons with clearer water (such as Tomales, Humboldt, Morro, and San Diego Bays) provide ideal habitats for seagrasses and attached algal forms. River mouth estuaries (such as the Santa Clara River and Eel River) have limited seagrass extent due to instability of bottom sediments, variable salinity, and high turbidity. In these types of estuaries phytoplankton and benthic microalgae typically dominate the shallow, unvegetated subtidal habitat of the main channel, while macroalgae and marsh plants dominate in side channels and adjacent floodplains. Vascular plant productivity is also strongly affected by the estuarine salinity gradient, with productivity reduced at higher salinities (Callaway et al. 2012a). A synoptic study across twenty-three southern California lagoon and river mouth estuaries illustrates seasonal changes in the biomass of three components: phytoplankton, benthic algae, and submerged aquatic vegetation (Ruppia spp.; McLaughlin et al. 2013). Macroalgae are ubiquitous throughout the year, with peak biomass in the summer and fall (Figure 19.7). Benthic microalgae and phytoplankton biomass peak in spring, and Ruppia biomass is ephemeral. Summer biomass accumulates to high levels in estuaries where tidal inlets are restricted by a sand bar, illustrating how biological communities respond to physical processes that alter rates of estuary-ocean exchange. California’s estuaries do not share one common community or seasonal pattern of primary producers because their habitat mosaics are spatially diverse and seasonally dynamic (Principle 3).

Microbes

The most abundant organisms in estuaries are the Bacteria and Archaea—the microbial community of prokaryotes. A liter of estuarine water contains one billion to ten billion bacterioplankton; abundance is about a thousand times higher (per unit volume) in sediments. This biomass doubles every few days (Hollibaugh and Wong 1996), and it is consumed at a comparable rate by flagellates, ciliates, and filter-feeding invertebrates such as bivalve molluscs, so bacterial production is an important supply of energy, carbon, and nutrients to estuarine consumers. The microbial community is extremely rich, with estimates of thousands to tens of thousands of taxa per liter of water and even greater diversity in sediments. Estuar ies 369


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March 2009

SAV Macroalgae Phytoplankton Benthic Benthicmicroalgae microalgae Phytoplankton Macroalgae SAV

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Devereaux Lagoon (DL) UCSB Campus Lagoon (UCL) Goleta Slough (GS) Santa Clara River (SCR) Mugu Lagoon–Muted (MLM) Mugu Lagoon–Full (MLF) Zuma Canyon (ZC) Topanga Canyon Lagoon (TC) Ballona Lagoon (BL) Ballona Wetlands (BW) Anaheim Bay/Seal Beach–Muted (SBM) Anaheim Bay/Seal Beach–Full (SBF) Bolsa Chica–Muted (BCM) Bolsa Chica–Full (BCF) Santa Ana River Wetlands (SAR) San Juan Creek (SJC) San Mateo Lagoon (SMC) Santa Margarita Estuary (SME) Agua Hedionda Lagoon (AHL) Batiquitos Lagoon (BQL) San Elijo Lagoon (SEL) Los Penasquitos Lagoon (LPL) Mission Bay–Full (MB) San Diego River (SDR) San Diego Bay–Full (SDF) San Diego Bay–Muted (SDM) Tijuana River Estuary (TJE)

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From north to south:

Figure 19.7 No single community or seasonal pattern exists that governs all of California’s estuarine primary producers, because their habitat mosaics are spatially diverse and seasonally dynamic. This concept is illustrated in plots of biomass (g C m-2) of phytoplankton, macroalgae, benthic microalgae, and submerged aquatic vegetation (SAV) in twenty-three southern California estuaries during March 2009 (top panel) and September 2009 (bottom panel). Note log scale on y-axis. Source: McLaughlin et al. 2013.

Estuaries receive allocthonous inputs of organic matter as plant biomass and detritus from oceans and rivers and autochthonous inputs from primary production. The prokaryotes play essential roles in the metabolism of this organic matter and the cycling of reactive elements. Microbial activity helps break down toxic organic contaminants such as pesticides or spilled hydrocarbons, and it transforms detrital organic matter having low food value into nutritious prokaryote biomass that can reenter the food web. Microbial oxidation of organic matter releases carbon dioxide, typically at a rate faster than carbon fixation by photosynthesis, so many estuaries are heterotrophic ecosystems, reflecting the importance of external supplies of organic carbon. In aerobic waters the prokaryotes use oxygen for respiration as they metabolize organic compounds; this is a key process of oxygen consumption in estuaries. In the absence of oxygen, either in anoxic waters or in bottom sediments, specialized prokaryotes respire other compounds—sulfate, nitrate, and oxidized metals such as iron, selenium, and arsenic. The product of prokaryotic sulfate respiration is sulfide, which binds and precipitates many heavy metals but is also toxic to fish and invertebrates. Another is reduced iron, which is soluble and diffuses into the overlying oxygenated water where

it precipitates to scrub the water column of heavy metals and phosphorus. Other anaerobic processes include methylation of mercury that makes this toxic element more bioavailable and mobile, and reduction of selenate and selenite to elemental selenium that is precipitated in sediments. Microbial respiration of nitrate removes a large fraction of the nitrogen pollution delivered from land runoff or wastewater. Although prokaryotes are small in size, their biochemical reactions have large-scale significance to the water quality and life support functions of estuarine ecosystems. Estuaries are fast-running biogeochemical reactors, and prokaryotes are the key agents of these processes (Principle 4).

Invertebrates

Estuarine invertebrates are a taxonomically diverse group of (mostly small) animals that consume detritus, microbes, algae, or other invertebrates and are an essential food resource for many vertebrates. They comprise two distinct communities: benthic species that live on or in the bottom sediments, and pelagic species that are components of the plankton. The pelagic community is dominated by mesozooplankton including copepods. Low-salinity regions of San Francisco

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Bay include copepods, such as Eurytemora affinis, that have largely been replaced by non-native species, including Pseudodiaptomus forbesi, Limnoithona tetraspina, and Acartiella sinensis. Higher-salinity zones include native Acartia spp. as well as non-native Tortanus dextrilobatus, Pseudodiaptomus marinus, and Oithonia davisae (Kimmerer 2004). These spatial patterns illustrate Principle 5: biological communities vary along the salinity gradient; the pelagic forms (plankton, fish) are translocated along the estuary as the salinity gradient moves with changes in freshwater inflow (see Figure 19.5a). Larger zooplankton in upper San Francisco Bay include native (e.g., Neomysis mercedis) and introduced (Hyperacanthomysis longirostris, formerly Acanthomysis bowmanii) mysid shrimp as well as and native and introduced (e.g., Gammarus daiberi) amphipods. Abundances of gelatinous zooplankton such as jellyfish appear to be expanding, and population outbursts of Aurelia spp. are common in central and northern California estuaries (e.g., Tomales Bay, Bolinas Lagoon). Heavily invaded estuaries like San Francisco Bay now have annual blooms of several non-native species, including hydrozoans Maeotias marginata, Moerisia sp., and Blackfordia virginica. The benthic invertebrates are dominated by molluscs, crustaceans, and polychaetes, many of which are nonnative (Cohen and Carlton 1995). Common molluscs include gastropods such as the native mudsnail (Cerithidea californica), non-native mudsnails (Batillaria attramentaria and Ilyanassa obsoleta), and non-native oyster drills (Urosalpinx cinerea). Bivalve molluscs include several widely distributed invaders like the Manila clam (Venerupsis philippinarum), soft-shell clam (Mya arenaria), and two species—t he mussel (Geukensia demissa) and clam (Corbula [Potamocorbula] amurensis)—which have transformed their environments. Native clams include harvestable species such as the geoduck (Panopeus generosa), Washington clams (Saxidomus gigantea), and horse clams (Tresus spp.), which have declined substantially. Common estuarine crustaceans include Bay shrimp, especially of the genus Crangon, small shore crabs such as Hemigrapsus oregonensis in higher tidal elevations in northern and central California and fiddler crabs (Uca crenulata) common in southern California. Lower tidal elevations support native rock crabs (Cancer productus, C. antennarius), Dungeness crabs (Metacarcinus magister), and non-native green crabs (Carcinus maenas). Dozens of amphipod species include many introduced species such as the highly invasive Grandidierella japonica and Ampithoe valida. There are also burrowing shrimp (Neotrypaea californiensis and Upogebia pugettensis) and in southern California spiny lobsters (Panulirus interruptus). The few structured habitats in California estuaries include beds of the native oyster (Ostrea lurida) and bay mussels (Mytilus trossulus/galloprovincialis) as well as eelgrass (Zostera marina). These limited habitats support species such as hydroids, colonial botryllid tunicates, caprellid shrimp, isopods, and several shrimp species not found in the majority of estuarine habitats. The invertebrate communities illustrate Principle 6: estuaries have distinct vertical components, a water column overlaying bottom sediments, and lateral components organized along the transition from subtidal to intertidal habitats. These components are tightly coupled: for example, many benthic invertebrates have life stages that enter the plankton, microbial respiration in sediments removes oxygen, and filtration by benthic invertebrates removes phytoplankton from the overlying water.

Fish

The fish communities of California’s estuaries range from resident species dominating small lagoons in southern California to anadromous species dominating river-mouth estuaries in northern California (Allen et al. 2006). Some species are permanent estuarine residents, including delta smelt (Hypomesus transpacificus), splittail (Pogonichthys macrolepidotus), topsmelt (Atherinop affinis), California killifish (Fundulus parvipinnis), several species of gobies, and spotted sand bass (Paralabrax maculatofasciatus). Marine migrants reproduce or rear in estuaries, anadromous species migrate from the ocean to spawn in freshwater, catadromous species migrate from freshwater to spawn in the ocean, and some freshwater and marine species move into estuarine habitats seasonally. Some species use estuaries in the north and south differently because of California’s latitudinal gradients of freshwater inflow and temperature. For example, Pacific staghorn sculpin (Leptocottus armatus) is a resident species in southern California lagoons but a marine migrant in northern California estuaries that receive high winter-spring freshwater inflow. Like the invertebrates, fish communities include two groups: demersal (bottom-living) species such as flatfish, sturgeon and rays, and pelagic species such as anchovies, herring, and smelt. Estuarine fish populations often have large annual fluctuations. Three different patterns are illustrated from longterm studies of San Francisco Bay (Figure 19.8): (1) an abrupt increase of English sole (Parophrys vetulus) abundance after 1999; (2) episodic appearances of California halibut (Paralichthys californicus); and (3) long-term decline of delta smelt (Hypomesus transpacificus). These patterns reflect different life histories and susceptibilities to human disturbance. English sole is a demersal marine fish that migrates into estuaries as juveniles to rear. It is a cold-temperate species affiliated with the northern biogeographic Oregon Province (Briggs and Bowen 2012). Its abrupt population increase followed a 1999 transition of the northeast Pacific Ocean from its warm to its cool phase (see below). California halibut is a warmtemperate demersal marine fish that rears in estuaries and is affiliated with the southern California Province. Its episodic appearances in San Francisco Bay occurred during or immediately after El Niño events. Estuaries are open ecosystems, and their fish communities are structured by the immigration of marine species whose population abundances track largescale climate patterns (Principle 7).

Birds

A great diversity of bird taxa exploit the wide range of habitat types available in estuarine ecosystems (Takekawa et al. 2011). Dabbling ducks feed in shallow subtidal habitats, but individual species exploit different food resources: northern pintails (Anas acuta) feed primarily on small seeds filtered from bottom sediments, while northern shovelers (Anas clypeata) primarily feed on invertebrates and seeds suspended in water. Diving ducks and piscivorous birds use a greater diversity of subtidal habitats. Ruddy duck (Oxyura jamaicensis) dive to feed on benthic organisms in shellfish beds, plant beds and in the water, and species such as the great egret (Ardea alba) feed primarily on fish. Piscivorous birds forage in most subtidal habitat types. For example, Brandt’s cormorant (Phalacrocorax penicillatus) in San Francisco Bay forages in the benthos,

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160000

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invertebrates. Many marsh species are gleaners, foraging on the marsh surface for invertebrates and seeds. Many species of shorebirds, waterfowl, and seabirds migrate between wintering and breeding habitat along the Pacific coast from Alaska and eastern Siberia to South America following the Pacific Flyway. Along the way these birds require wetland habitats to rest and forage to build energy to complete their journey. Estuaries along the Pacific Flyway provide some of the most important stopover locations because of the abundance and diversity of food resources available. Four California estuaries are listed as sites of importance by the Western Hemisphere Shorebird Reserve Network (Table 19.2). At least forty-three species of shorebirds are found in wetlands along the Pacific coast, with the largest numbers found in San Francisco Bay. An average 66.7% of the total numbers of thirteen focal shorebird species surveyed in fifty-six wetlands along the Pacific coast between 1988 and 1995 were found in San Francisco Bay during the fall (Page et al. 1999). Thus California’s estuaries have global significance for sustaining populations and biodiversity of migratory birds.

0 1980

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Year Figure 19.8 Three patterns of annual fish abundance in the San Francisco Bay–Delta: (A) decadal-scale shift from low to high abundance, in juvenile English sole (Parophrys vetulus); (B) episodic year classes, in juvenile California halibut (Paralichthys californicus); and (C) a long-term decline, in delta smelt (Hypomesus transpacificus). Sources: English sole and California halibut data from the San Francisco Bay Study of the California Department of Fish and Wildlife (CDFW) (1980–2 012); delta smelt data from CDFW Fall Midwater Trawl Survey (1967–2 012). Panels A and C are centered around long-term mean abundances.

over hard bottom substrate and in the water column while the brown pelican (Pelecanus occidentalis) and Clark’s grebe (Aechmorphous clarkia) only forage within the water column. Intertidal mudflats support large numbers of shorebirds that feed primarily on invertebrates. At least forty-three species of shorebirds coexist within California estuaries because of evolutionary adaptations of bill shapes and body sizes allowing species to exploit food resources at different water and mud depths (Page et al. 1999). For example, the short bill of the least sandpiper (Calidris minutilla) restricts its foraging to shallow depths on the upper edge of mudflats while long-billed curlew (Numenius americanus) can probe deeper into mudflats for food (Figure 19.9). Tidal marsh habitat is important for songbirds, shorebirds, rails, herons, egrets, and ducks. Some species are tidal marsh obligates such as the Ridgeway's Rail (Rallus longirostris obsoletus), which uses cordgrass for cover as it moves along tidal channels to forage on

Interactions between Communities

The primary producers, decomposers, grazers, and predators of estuaries are tightly connected through trophic (feeding) linkages. These linkages are revealed when abundances of predators increase or decrease abruptly, with effects that cascade to change abundances of their prey and organisms at lower trophic levels. Such a trophic cascade occurred in San Francisco Bay after 1999 when large numbers of marine predators—bottom-feeding fish (e.g., English sole, see Figure 19.8a), crabs (e.g., Dungeness crab), and shrimp—m igrated from the coastal Pacific into the bay. Heavy predation by these marine immigrants reduced the abundance of clams in the estuary, releasing grazing pressure on phytoplankton and allowing its biomass to grow (Cloern et al. 2010). This restructuring of biological communities followed a shift in the climate system across the North Pacific as the NPGO became positive and coastal upwelling intensified (Figure 19.10), signaling an increase in coastal productivity and strong recruitment of marine predators that migrate into estuaries to feed. A four-level trophic cascade was triggered in Elkhorn Slough by population recovery of an apex predator (sea otter [Enhydra lutris]) leading to declines of its prey (Cancer crabs), increases of grazers preyed upon by crabs (the isopod Idotea resecata and sea slug [Phyllaplysia taylori]), and biomass decrease of microalgae scraped off surfaces by the grazers (Hughes et al. 2013). Microalgae grow on leaves of vascular plants and inhibit their growth, so an unanticipated outcome of the otter recovery in Elkhorn Slough was synchronous recovery of seagrass (Zostera marina) as microalgal growth was removed from its leaves by the abundant grazers. In both estuaries changing abundance of crabs that prey upon grazers led to changing biomass of microalgae, either phytoplankton or attached forms.

Services Provided by Estuarine Biota and Their Habitats Coasts attract human settlement, and many of the world’s great cities such as London, Rio de Janeiro, Tokyo, New York, and San Francisco were built on estuaries because of the resources and services they provide. Although estuaries

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B

E

A

C

D

Figure 19.9 Shorebirds illustrate dramatic morphological adaptations allowing many species to coexist within the same locations. Long-billed curlew (A) have a long bill that allows them to probe deep into mudflats for food. The black-necked stilt (B) uses its delicate, slightly recurved bill to capture prey by pecking or sweeping its bill at or near the water surface. The long-billed curlew and black-neck stilt are tall, allowing them to forage in deeper waters, while dowitcher (C) and willet (D) are medium-sized shorebirds, which forage in shallower depths. In contrast, least sandpiper (E) are one of the smallest shorebirds, and their foraging is restricted to shallow water on the upper edges of mudflats. Photos: Tom Grey.

Table 19. 2 California estuaries recognized as important for shorebird conservation by the Western Hemisphere Shorebird Reserve Network (WHSRN)

Estuary

WHSRN Class

Description

Elkhorn Slough

Site of Regional Importance

At least 20,000 birds annually

South San Diego Bay

Site of Regional Importance


Humboldt Bay Complex

Site of International Importance


San Francisco Bay

Site of Hemispheric Importance


Note: Classes of importance are based on the observed number of birds at each site within a year.

occupy only 0.3% of Earth’s surface, they provide goods and services valued highest per unit area ($22,832 ha-1 yr-1) among all the world’s biomes (Costanza et al. 1997). Beyond the dollar value, estuaries are beautiful and fascinating places where people boat, swim, bird, hunt, walk, take photographs, view wildlife, and conduct research.

Salmon and steelhead transfer carbon and nitrogen from the coastal ocean to rivers and adjacent terrestrial systems when consumed by predators and scavengers and their carcasses decay (Gende et al. 2002, Merz and Moyle 2006). Fish and invertebrates that rear in estuaries transfer carbon and nutrients from tidal marshes and other shallow-water habitats to the open estuary and to the ocean, while salmon transfer carbon and nutrients from the ocean to the rivers (Principle 8).

Fish Nursery and Migration Corridors

Ecologically and commercially important fish and invertebrates rear in warm estuarine waters over soft bottoms rich with small invertebrates. Many of these species reproduce in the ocean, the small juveniles migrate into estuaries to rear, and the larger juveniles migrate back to the ocean. This group includes Dungeness crab, Bay shrimp (Crangon spp.), brown rockfish, English sole, speckled sanddab, and starry flounder in northern California. Other species—such as leopard shark, Pacific herring, and the surfperches in northern California and yellowfin croaker, California halibut, and diamond turbot in southern California (Allen et al. 2006)—migrate from the ocean to estuaries to reproduce, where the young rear. California estuaries also serve as migration corridors for anadromous salmon, steelhead, sturgeon, striped bass, and American shad.

Organic Carbon Production, E xport, and Storage

The vascular plants of estuarine marshes have very high rates of primary production. For example, annual production of pickleweed (Sarcocornia pacifica, formerly Salicornia virginica) ranges up to 690 g C m-2 in San Francisco Bay, 2,860 g C m-2 in Los Peñasquitos Lagoon, and 1,050 g C m-2 in Tijuana Estuary (Grewell et al. 2007). This carbon supply becomes part of a detrital pool that fuels benthic food webs in estuaries and is exported to oceanic deep water as a food and energy source. The rate of organic carbon production in tidal marshes exceeds the rate of anaerobic decomposition, so these habitats are efficient at storing carbon belowground. Annual rates Estuar ies 373


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1999-2010 1999-2010

Figure 19.10 Biological communities in San Francisco Bay were restructured after a 1999 climate shift when the North Pacific Gyre Oscillation (NPGO) shifted from negative to positive; coastal upwelling (and biological productivity) intensified; and predator (ten species of bottom-feeding fish, crabs, and shrimp) abundances increased, leading to decreased abundance of grazers (clams) and then to increased phytoplankton biomass. Dark circles show medians (climatic indices, abundances [CPUE, catch per unit effort] or biomass) for the periods 1980–1998 and 1999–2 010. Source: Redrawn from Figure 17 in Cloern and Jassby 2012.

of soil carbon sequestration in salt and brackish marshes of San Francisco Bay average about 80 g C m-2 (Callaway et al. 2012b). Managed freshwater marshes in the Sacramento–San Joaquin Delta are very productive (1,300 to 3,200 g C m-2 yr-1) and can accrete approximately 4 cm yr-1 of organic-rich sediment (Miller and Fuji 2010). As a result, creation of “farmed” wetlands is now being considered to sequester carbon to mitigate atmospheric CO2 emissions.

energy that fuels production of organisms we harvest. Phytoplankton primary production ranges from 70 to 810 g C m-2 yr-1 in Tomales Bay (Cole 1989) and from 30 to >400 g C m-2 yr-1 in San Francisco Bay (Alpine and Cloern 1992, Cloern and Jassby 2012). These measures imply a thirtyfold range of potential fish production, and this large variability implies comparable variability of consumer production in California’s estuaries. We harvest some of this production in the form of cultured oysters, a practice that began in San Francisco Bay during the nineteenth century and was colorfully chronicled in Jack London’s Tales of the Fish Patrol (Asprey 2010). Oyster culture in San Francisco Bay was doomed by declining water quality, but introduced Pacific oysters (Crassostrea gigas), mussels, clams, scallops, abalone, and brine shrimp are cultured in Humboldt Bay, Tomales Bay, Drakes Estero, Morro Bay, and Agua Hedionda. We once harvested another component of estuarine production through commercial fishing, an important source of food that has disappeared from California estuaries (see below).

Flood Buffering

Aquatic plants dampen currents and waves to protect shorelines, and marsh vegetation attenuates storm and flood impacts. While hurricane-force storms are unlikely in California, erosion and flooding are still major coastal concerns (Hanak and Moreno 2011). As sea level continues to rise, tidal marshes will play an increasingly valuable role in buffering adjacent terrestrial systems from flooding and storm impact, although their sustainability is uncertain in the face of rapidly accelerating sea level rise (Stralberg et al. 2011).

Waste Assimilation

Microbes provide a suite of ecosystem services such as nitrification-denitrification, which converts organic nitrogen into nitrogen gas (Figure 19.11) and regulates accumulation of nitrogen delivered to estuaries from agricultural runoff and sewage. Without this service nitrogen pollution would accumulate unchecked in estuaries to levels that degrade water quality, and costly actions would be required to reduce human inputs of nitrogen. These kinds of biological processes are unseen and their values are not recognized, but we can estimate the monetary value of processes such as microbial removal of nitrogen pollution. The mean denitrification rate in estuaries is 5,600 kg N km-2 yr-1 (Seitzinger et al. 2006). The area of California’s estuaries and coastal wetlands is approximately 3,300 km2 (Larson 2001, Gleason et al. 2011), so these habitats potentially remove about 2 x 107 kg N annually. The average cost of nitrogen removal in sewage treatment plants is $275 kg-1 N (CBP 2002), so the nitrogen-removal service provided by California’s estuaries has an annual value exceeding $5 billion in 2002 dollars. Tidal marshes and their microbial communities also trap and sequester nutrients and contaminants, thereby improving water quality and buffering coastal waters from contaminants carried by urban runoff.

Food Production

Half of U.S. commercial fish harvest is of estuarine-dependent species. Fish production is strongly correlated with phytoplankton primary production (Houde and Rutherford 1993) because phytoplankton photosynthesis provides much of the

Opportunities to Understand Processes of Evolution

Tidal marshes in California are hot spots of bird and mammal biodiversity and habitat for nineteen endemic subspe-

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N2, N2O

N fixation

Gas evasion

DIN, PON Atmos dep’n

N2

Oxygenated

FW, POTW

DON PON Organic N

N2O OCEAN

DIN, D/PON

N2O

on

2

NO

fic itri

-

ati

n

De

N2

DN

RA

Anoxic

BURIAL

NH4+

DIN, D/PON

NO2-

mmox Ana

PON burial

Nitrification NO3NO2-

Nitrification

NH4+

Figure 19.11 Diagram of nitrogen (N) cycling in estuaries. N sources and sinks are shown in block arrows around a box that encloses withinestuary transformations. The box is divided into water column (light blue, generally oxygenated) and sediment (light brown, typically anoxic below a depth of a few millimeters). On left, N enters the estuary as dissolved inorganic nitrogen (DIN) and either dissolved or particulate organic nitrogen (DON and PON, or “D/PON”). DIN is assimilated by biota in the estuary to cycle between organic and inorganic forms (such as ammonium, NH4+). FW: freshwater (riverine inflow and groundwater); POTW: publicly owned treatment works (discharges from municipal and industrial treatment works). N fixation and atmospheric N deposition, indicating nitrogen deposited in the estuary as dust or in precipitation, are two additional input sources. OCEAN indicates two-way tidal exchange of N with the coastal ocean. Gas evasion is the loss of fixed nitrogen that has been converted to gaseous forms (N2, nitrogen gas; and N2O, nitrous oxide) by microbial processes (ammonia oxidation, denitrification [blue] and the microbial process of anammox [anaerobic ammonium oxidation, green]). BURIAL indicates permanent burial in sediments. Fixed N cycles between NH4+ regenerated by microbial degradation or excretion by animals and D/PON in biomass and detritus. PON can be buried temporarily in surface sediments, where it can undergo degradation or be buried permanently. Aerobic microbes oxidize NH4+ to nitrite (NO2-) and then to nitrate (NO3-), with some production of N2O as a by-product (nitrification, red), while NO2- and NH4+can be combined in anammox to yield N2. NO3- can be taken up by phytoplankton to reenter the internal cycle of assimilation and regeneration shown on the left. Nitrate is converted to N2 by denitrification (blue), which also yields some N2O, or is converted to NH4+ by another microbial respiratory process called dissimilatory reduction of nitrate to ammonia or DNRA (orange). Illustration by James T. Hollibaugh.

cies (Table 19.3). Tidal marsh populations tend to be grayer or darker than their more terrestrial analogs (Greenberg and Maldonado 2006), and tidal marsh bird races often have longer, thinner bills (Grenier and Greenberg 2005). The benefits of these differences and the mechanisms that maintain them are not known, but two interesting possibilities for advancing evolutionary biology are evident. First, new information about bird bill size diversity is opening the door to reconsidering seminal work in evolutionary biology. Greenberg et al. (2012) showed that sparrow bill size varies with maximum summer temperature in tidal marshes, and they hypothesize that bills diffuse heat and thus help conserve water—key adaptations in saline habitats with little shade. Therefore, heat regulation as well as feeding ecology must be considered when studying adaptations in bill morphology—a fundamental system from which Darwin developed the theory of evolution via

natural selection (Darwin 1845). Second, tidal marshes may be sites of incipient ecological speciation, which has been identified rarely in terrestrial vertebrates and almost never in birds. Most examples of speciation are thought to occur when populations become geographically isolated. Ecological speciation, on the other hand, arises from divergent selection across ecological gradients within connected populations. Three California tidal marsh song sparrow subspecies are morphologically distinct despite geographic contact with subspecies occupying terrestrial habitats (Chan and Arcese 2003). Ecological gradients between terrestrial habitats and tidal marsh are steep (including large changes in hydrology, salinity, and vegetative structure) and likely require concomitant adaptation to successfully exploit tidal marsh resources. These gradients provide opportunities to learn whether and how such adaptations lead to reproductive isolation. Estuar ies 375


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Table 19. 3 Mammals and birds endemic to California tidal marshes

Common name

Scientific name (with subspecies)

Distribution

Ridgeway's Rail

Rallus longirostris obsoletus

San Francisco Bay

R. l. levipes

Southern California

Common yellowthroat

Geothlypis trichas sinuosa

San Francisco Bay

Song sparrow

Melospiza melodia samuelis

San Pablo Bay

M. m. pusillula

San Francisco Bay

M. m. maxillaris

Suisun Bay

Savanna sparrow

Passerculus sandwichensis beldingi

Southern California

Ornate shrew

Sorex ornatus sinuosus

San Pablo Bay

S. o. salaries

Monterey Bay

S. o. salicornicus

Los Angeles Bay

Wandering shrew

Sorex vagrans halicoetes

South San Francisco Bay

Salt marsh harvest mouse

Reithrodontomys raviventris raviventris

San Francisco Bay

R. r. halicoetes

San Pablo and Suisun Bays

Western harvest mouse

Reithrodontomys megalotis distichlis

Monterey Bay

R. m. limicola

Los Angeles Bay

California vole

Microtus californicus paludicola

San Francisco Bay

M. c. sanpabloensis

San Pablo Bay

M. c. halophilus

Monterey Bay

M. c. stephensi

Los Angeles coast

Source: Greenberg and Maldonado 2006.

The Human Dimension In their undisturbed state, estuaries have the capacity to support animal abundances and diversity that are difficult for us to imagine today, but the living resources of California’s estuaries have been greatly altered as the human population has grown (see Chapter 8, “Ecosystems Past: Vegetation Prehistory”). Reports from San Francisco Bay by eighteenth-century explorers described: “countless fowl, ducks, geese, cranes, and other kinds” (Crespí and Brown 2001), “the spouting of whales, a shoal of dolphins or tunny fish, sea otter, and sea lions” near the Golden Gate, and “great piles of fresh-water mussels” and “very fine salmon in abundance” being fished by native residents (Bolton 1933). John E. Skinner’s (1962) remarkable history of fish and wildlife resources tells that this biological richness persisted into the late nineteenth century: “No other area in California can match the rich fisheries potential of this region. This potential lies in the wealth of marine life found within its bays and adjacent coastal waters”; “sardines are reported so abundant in San Francisco Bay that they literally obstruct the passage of boats”; and Dungeness crabs “are taken in immense numbers in seines, together with many shoal water species of fish, yet the supply seems to be undiminished” (Skinner 1962). It turns out that these supplies did have bounds because an era of rapid declines of waterfowl, fish, and shellfish populations began in the early twentieth

century. These losses reflect a deep and broad human footprint on California’s estuaries.

The Many Forms of Human Disturbance L andscape Transformation

In the 250 years since Crespí’s journey, California’s estuaries have been dredged to create ports or harbors, or leveed, filled, or drained (see Figure 19.1), contributing to a loss of over 91% of the state’s wetlands (Dahl 1990, Goodwin et al. 2001). Through filling and excavation we have disproportionately eliminated tidal flats, tidal marshes, and salt flats, and many estuaries now have a much higher proportion of open-water habitat than they did historically. For example, nearly half of San Francisco Bay was exposed at low tide in the 1850s compared to less than a quarter today (Goals Project 1999). In the Sacramento–San Joaquin Delta, wetland area was historically fourteen times greater than open-water area; today open- water area is five times greater than wetland area (Whipple et al. 2012). These kinds of changes have resulted in an overall homogenization of California’s estuarine landscapes—in other words, a loss of habitat diversity. In particular, freshwater and hypersaline estuarine habitat mosaics are rare or even unrecognized today. Though extensive salt flats

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were once dominant features of many northern San Diego County estuaries, almost none remain today (Beller et al. 2014). Most traces of the Santa Clara River’s dune-dammed lagoon complexes have been completely erased (Beller et al. 2011). The early and nearly complete loss of freshwater tidal marshes in the Bay-Delta estuary has dramatically changed the landscape and reduced the estuary’s habitat and biological diversity (Vasey et al. 2012, Whipple et al. 2012). A related landscape transformation is the alteration of tidal circulation within estuaries, in particular the restriction of tidal exchange by dikes, berms, and operations of water-control structures that reduce tidal range. The stagnant conditions in areas of tidal restriction can amplify the effects of nutrient enrichment, leading to accumulation of high algal biomass (Hughes et al. 2011); and they lead to reduced diversity of estuarine communities (Ritter et al. 2008). Conversely, some historically intermittently closing systems have experienced enhancement of tidal circulation— for example, through the construction of jetties. Another ubiquitous landscape transformation is river damming that facilitates water storage, consumption, and interbasin transfers that have greatly altered the timing and magnitude of freshwater inflow to many California estuaries. The median inflow to San Francisco Bay is only 60% of the inflow that would occur from an unimpaired watershed. Inflow reductions result from water storage during the wet season and exports during the dry season (Cloern and Jassby 2012). Conversely, importation of water from the Bay-Delta watershed has increased summer river discharge in urban watersheds of southern California by 250% or more (TownsendSmall et al. 2013). Human modification of freshwater inflow has wide-reaching effects on estuaries through changes in transport processes, sediment input, water quality, and salinity—c hanges that have degraded habitat quality for some native fishes (Feyrer et al. 2011), facilitated invasions by nonnative species (Winder et al. 2011), and altered plant distributions in salt marshes (Watson and Byrne 2009).

Species Introductions

Human introductions of non-native plants and animals are also major disturbances to natural communities and their habitats (see Chapter 13, “Biological Invasions”). California estuaries are some of the most highly invaded coastal systems on the planet (Ruiz et al. 2000), with upwards of 235 introduced species of invertebrates and algae and 20 species of marine/estuarine fishes (Schroeter and Moyle 2005). San Francisco Bay is the most invaded (217 non-native species), followed by Los Angeles/Long Beach (95), Elkhorn Slough (80), San Diego (78), and Humboldt Bay (77) (Figure 19.12a). Vectors for invasive species include discharge of ship ballast water, hull fouling, sales of live bait and seafood, aquarium/ ornamental species trade, and transport via aquaculture (Figure 19.12b). Many of these vectors are poorly understood and largely unregulated. For instance, thousands of nonnative plants and animals are imported into the U.S. annually through the aquarium/ornamental trade (Williams et al. 2013), but the likelihood of release and probability of their survival in California estuaries is often not known (Chang et al. 2009). Introductions of plant species have also profoundly changed California’s marsh communities, particularly in the high marsh and ecotone between marsh and uplands where plant diversity peaks (Traut 2005, Wasson and Woolfolk 2011).

Two case studies from San Francisco Bay illustrate the power of disturbance from species introductions. Following intentional introduction of the non-native marsh plant Spartina alterniflora from the U.S. Atlantic coast in 1974, this species hybridized with the native Spartina foliosa, creating a hybrid that spread throughout most of central and south San Francisco Bay (Hogle, 2010). Hybrid Spartina dramatically altered ecosystem function by colonizing previously unvegetated mudflats and reducing water flow, significantly increasing deposition of fine sediments and reducing biomass of benthic invertebrates by 90% (Neira et al. 2006). This invasion eliminated mudflat habitats that previously supported shorebirds, fishes, and crabs, and it was followed by local extirpation of the native Spartina. Another invasion with ecosystem-wide impacts was introduction of the clam Corbula (Potamocorbula) amurensis from the west Pacific, likely from ballast water. Within a year of its 1986 introduction, this clam carpeted the bottom sediments of the upper estuary. Water filtration by the clam population led to a fivefold drop of phytoplankton biomass and primary production and elimination of the summer phytoplankton bloom (Figure 19.12c). This transformed the estuary to a state of chronic food limitation of zooplankton, and populations of native copepods, mysid shrimp, and rotifers fell abruptly. These zooplankton taxa are key food resources for some indigenous fish, such as delta smelt, and they were replaced by smaller copepods having lower food value (Winder and Jassby 2011). This loss of pelagic production is a contributing factor to population declines of planktivorous fish now designated as threatened or endangered species. The Corbula introduction is an iconic example of how non-native species can reorganize biological communities and significantly alter ecosystem processes such as primary production.

Pollution

Some California estuaries are contaminated by pollutants at levels that threaten ecosystem or human health. Sediments in half of southern California estuaries have high concentrations of toxic metals such as zinc and organic pollutants such as polynuclear aromatic hydrocarbons, pesticides, and polybrominated diphenyl ethers (PBDEs) (SCB [Southern California Bight 2008 Regional Monitoring Program Coastal Ecology Committee] 2012). The California mussel and the California sea lion have PBDE concentrations among the highest measured in the U.S., a concern because these contaminants disrupt nervous system development and hormone regulation (Kimbrough et al. 2009, Meng et al. 2009). Many California estuaries also receive high nitrogen loadings from wastewater treatment plants and urban and agricultural runoff, leading to poor water and habitat quality from excess production of phytoplankton biomass in Elkhorn Slough and Santa Clara River Estuary, macroalgae in Newport Bay and Morro Bay, and hypoxia (low dissolved oxygen levels) in Elkhorn Slough, Newport Bay, and Tijuana Estuary (Bricker et al. 1999, Hughes et al. 2011, McLaughlin et al. 2013). Hypoxia in intermittently tidal estuaries such as San Elijo and Los Penasquitos Lagoon has forced actions to maintain a permanently open inlet to increase tidal flushing, causing the extirpation of brackish water species such as the endangered tidewater goby. In response to these water quality issues, the U.S. Environmental Protection Agency and the state of California have developed sediment quality objectives and are developing nutrient Estuar ies 377


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Approximate area affected (ha) Figure 19.12 Hundreds of non-native species have been introduced into California waters via ship-based vectors including ballast water and hull fouling as well as via aquaculture, live bait, and ornamental trades. These introductions have had numerous negative consequences for ecosystem function and human economies. A Numbers of established non-native species of invertebrates and algae in major California embayments ordered from north to south

showing total number for each bay. Source: Fofonoff et al. 2011. B Contributions of vectors to introductions of 145 non-native marine species that have each been brought into California via multiple

vectors (N=389 vector × species combinations). Source: Williams et al. 2013. C Box plot of monthly mean chlorophyll-a values in Suisun Bay before and after the introduction of Corbula (Potamocorbula) amurensis in

1986. The dashed line represents phytoplankton concentrations below which zooplankton populations may be food limited. Source: Cloern and Jassby 2012. D Plot of approximate eradication costs as a function of the area invaded for recent successful eradication programs for estuarine invasions,

including Caulerpa taxifolia (uppermost point). Note the log scale for both invaded area and eradication costs. Source: Edwin D. Grosholz, unpublished data.

criteria to ensure that beneficial uses provided by California estuaries (e.g., fish spawning, shellfish harvest, and water contact) are not impaired by contaminants (Sutula et al. 2007).

What Has Been Lost? What Is at Risk? Human Health Advisories

Inputs of toxic metals have been reduced dramatically in some estuaries, such as San Francisco Bay, through source controls and advanced wastewater treatment. But nonpoint sources (urban runoff, atmospheric deposition) and legacy pollutants that persist in sediments remain challenging problems. As a result, state advisories limit human consumption of some fish and shellfish because of high levels of mercury, PCBs, or pathogens.

Habitat Losses

California estuaries have lost vast areas of their historic marshes, including salt marshes, brackish marshes, and tidal freshwater marshes (Goals Project 1999, Van Dyke and Wasson 2005). Eelgrass and oyster beds, which provide important structured habitat, have also been negatively impacted by anthropogenic activities such as introduction of nonnative species (Wasson 2010) and eutrophication (Hughes et al. 2013).

Species Losses

The cumulative effects of habitat loss, pollution, introduced species, and other disturbances such as dredging, water diversions, and river damming have taken a large toll on Califor-

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Table 19.4 California’s threatened or endangered species that require or use estuarine and tidal marsh habitats

Class

Common name

Scientific name

Status

Mammal

Southern sea otter

Enhydra lutris nereis

FT

Salt-marsh harvest mouse

Reithrodontomys raviventris

SE FE

California least tern

Sterna antillarum browni

SE FE

Western snowy plover

Charadrius alexandrinus nivosus

FT

Ridgeway's Rail

Rallus longirostris obsoletus

SE FE

California black rail

Laterallus jamaicensis coturniculus

ST

Light-footed clapper rail

Rallus longirostris levipes

SE FE

Belding’s savannah sparrow

Passerculus sandwichensis beldingi

SE

Tidewater goby

Eucyclogobius newberryi

FE

Chinook salmon spring run

Oncorhynchus tshawytscha

ST FT

Chinook salmon winter run

Oncorhynchus tshawytscha

SE FE

Steelhead

Oncorhynchus mykiss

FE or FT by region

Coho salmon

Oncorhynchus kisutch

SE FE

Longfin smelt

Spirinchus thaleichthys

ST

Delta smelt

Hypomesus transpacificus

SE FT

Green sturgeon

Acipenser medirostris

FT

Pacific eulachon, southern DPS

Thaleichthys pacificus

FT

Bird

Fish

spell out?

Source: California Department of Fish and Wildlife 2013. Note: Populations of these species are listed as either threatened (T) or endangered (E) under criteria of the California state (S) or U.S. federal (F) Endangered Species Acts.

nia’s estuarine biota. Population declines of seventeen species of birds, fish, and mammals have reached levels so low that these are now designated as threatened or endangered species (Table 19.4). Many other animals and plants are species of concern because their populations have fallen to levels that might not be sustainable. Others have been locally extirpated, such as the tidewater goby from San Francisco Bay.

Loss of E stuarine Fisheries

Perhaps the most compelling indicator of the power of human disturbance is the loss of commercial fishing from California’s largest estuary. San Francisco was once a leading fishing center of the U.S. Today, other than a small herring fishery and several bait fisheries, not a single remaining commercial fishery for shellfish or finfish remains in this great estuary. At its peak, commercial fishing on San Francisco Bay employed forty-four hundred fishermen who sailed a thousand vessels and annually caught over a thousand tons each of oysters (once the most valuable fishery on the U.S. Pacific coast), clams, shrimp, salmon, shad, striped bass, and flatfish (Skinner 1962). Commercial hunting provided 250,000 ducks yearly to San Francisco markets, and more were taken for the table. But within decades stocks of all harvested species plummeted, and one by one commercial fisheries for these estuarine species were closed, permanently. These indicators of human disturbance now motivate policies to protect, restore, and sustain California’s estuaries and the species they support.

Plans for Recovery and Protection Public Policies

Tidal marshes and other estuarine habitats have received significant conservation and restoration attention because of their regulatory protection under the federal Clean Water Act (CWA) and Endangered Species Act (ESA). Listing of endemic fishes as threatened or endangered (see Table 19.4) has been the major impetus for the Bay Delta Conservation Plan (BDCP), and intermittently tidal estuaries are now managed to protect the endangered tidewater goby (Lafferty et al. 1999). California’s 1965 McAtter-Petris Act was a landmark step in protection of estuarine and coastal habitats, creating the San Francisco Bay Conservation and Development Commission for the protection of the bay. State and federal laws require mitigation of human impacts, including habitat restoration to offset unavoidable wetland impacts, and these laws have led to substantial restoration of estuarine wetlands (Environmental Law Institute 2007).

Habitat Restoration

Projects are under way in many California estuaries to restore lost or degraded habitats. Dikes and water control structures are being removed to restore more natural tidal exchange. Sediment addition projects are increasing elevation in estuarine habitats that subsided due to diking, thus enabling resEstuar ies 379


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toration of salt marsh. Native oyster and eelgrass restoration projects are enhancing populations of these estuarine endemics and the structured habitat they create. Debate exists about the effectiveness of mitigation-based restoration, and movement has begun toward more pro-active, large-scale planning to protect ecosystems rather than the project-by-project, mitigation-based approach typical under CWA and ESA. For example, the Southern California Wetlands Recovery Project established regional goals for coastal and estuarine restoration in southern California. Similarly the Habitat Goals Project (Goals Project 1999) integrated large-scale habitat management within San Francisco Bay. The scope of many projects is now so large that they have regional effects. For example, the South Bay Salt Pond Restoration Project is the largest program of tidal marsh restoration in the western U.S., restoring 6,100 hectares of former salt ponds to promote recovery of special-status species that depend on estuarine-marsh habitats (SBSPRP 2012). In addition, the state of California has put substantial effort into planning through marine protected areas that include about 12% of available estuarine habitat (Gleason et al. 2012). Goals of the BDCP include restoration of at least 26,000 hectares of tidal habitat in the Sacramento–San Joaquin Delta (BDCP 2013). The plan also addresses water management as a stressor on estuarine biota—a critical issue for California estuaries that is likely to become more challenging as the climate system and freshwater demand continue to change.

Controlling Species Introductions

Managing vectors for invasive species includes the regulation of ship ballast water under the 2003 California Marine Invasive Species Act. Large ships are now required to manage ballast through—for example, midocean ballast exchange to minimize likelihood of ship-based introductions to estuaries. Invasive species management also includes large-scale eradication programs (Figure 19.12d). The most successful has been eradication of the Mediterranean alga Caulerpa taxifolia from Aqua Hedionda Lagoon and Huntington Harbor. This effort cost more than $6 million over several years and involved intensive treatment methods. An equally large program to eradicate hybrid Spartina from San Francisco Bay has cost several million dollars over a six-year period and, to date, has removed 90% of the Spartina hybrid. There have also been many small-scale programs to remove recently introduced species having limited distribution, such as the Japanese kelp Undaria pinnatifida that was first found in southern California in 2000 and arrived in Monterey Bay shortly thereafter. This rapidly growing species can profoundly change estuaries because of its large size (>2 meters). It also fouls docks, ship hulls, and moorings. Since 2010, small populations have been found in San Francisco Bay and Half Moon Bay. Other small-scale efforts have been successful at manually removing the snail Littorina littorea in Orange County and the alga Ascophyllum nodosum in San Francisco Bay. Other efforts remain unsuccessful or incomplete at control of snails (Batillaria attramentaria and Undaria pinnatifida) in Monterey Bay and San Francisco Bay and Japanese eelgrass (Zostera japonica) in Humboldt Bay (Williams and Grosholz 2008).

A Long View of California’s Estuaries The landscapes and biological communities of California estuaries have been transformed, some beyond recognition, from those viewed by Spanish explorers in the eighteenth century. These ecosystems will continue to evolve, but the pace and trajectories of future changes are uncertain. Three central questions emerge as we develop long views to anticipate future pressures that will further change California’s ecosystems and plan strategies for adapting to them.

What Will Drive Future Changes? Continued growth of California’s population, projected to exceed fifty million by 2050 (CDF 2012), implies intensification of commerce, agriculture, urbanization, waste production, energy and water consumption, land development, and continued translocations of plants and animals—the human pressures that transformed coastal landscapes during the past century. Estuarine ecosystems will also continue to respond to multidecadal climate oscillations that restructure biological communities. We can anticipate intense disruption of coastal ecosystems by the next megaflood, the last of which filled San Francisco Bay with freshwater in 1862 (Dettinger and Ingram 2013). These drivers of change will interact with regional manifestations of global climate change—accelerating sea level rise, altered timing and magnitude of runoff, acidification of seawater, warming of air and water, and growing frequency of extreme events such as storms, heat waves, and extended droughts (Cloern et al. 2011).

What Is at Risk? If unchecked, these growing pressures will drive further changes in the freshwater inflow, sediment supply, geomorphology, habitat composition and connectivity, water quality, productivity, and biological communities of California’s estuaries. Tidal marshes and mudflat habitats are not sustainable if sea level rises faster than sediment accretion (Stralberg et al. 2011), a likely scenario in estuaries such as San Francisco Bay where sediment input has been reduced by river damming and channelization (Schoellhamer 2011). Populations of dozens of plant and animal species native to California estuaries have fallen to levels so low they might not be sustainable as human pressures intensify. Extinctions of native species will likely occur in synchrony with continued population expansions of non-native species, particularly those adapted to warming waters, salinity regimes created by highly managed freshwater inflows, and further homogenization and fragmentation of coastal habitats. Extirpation of rare species can be triggered by extreme events (Zedler 2010), so sustainability of California’s at-risk estuarine species will become increasingly challenged if projections of more frequent and intense heat waves, droughts, and storms are realized. The uncertain future of estuarine habitats and biological communities also implies uncertain provision of the myriad benefits we derive from them. Susceptibility of human populations and infrastructure to inundation by storm surges grows as tidal marshes are lost, and so does the capacity of estuarine systems to sequester carbon (Canuel et al. 2012) and

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of tidal marshes to filter contaminants from urban runoff. Warming will promote faster growth of algae, so habitat quality will potentially degrade as macroalgae proliferate further in nutrient-rich estuaries (Lotze and Worm 2002). Warming will accelerate ecosystem respiration and decrease oxygen solubility, leading to growing potential for hypoxia of estuarine waters. We can anticipate significant cumulative effects of these kinds of changes on populations of migratory birds that rely on California’s estuaries; on marine fish and invertebrates that use estuaries as nursery or migratory habitat; on our culture and harvest of food from coastal waters including the potential to restore commercial fishing in estuaries; and on opportunities for future generations to glimpse the natural beauty, diversity, and living resources of California’s estuaries that awed early Spanish explorers.

What Steps Can We Take? The future of California’s estuaries will be determined by the choices we make as a society and the way those choices are manifested through policies, such as those described in the previous section to restore, rehabilitate, and sustain estuarine ecosystems. We suggest seven general actions, grounded in contemporary scientific understanding of how estuaries function as ecosystems, to anticipate and lessen the threats to these vital California ecosystems:

. Use modeling tools to develop future scenarios (e.g.,

. . . . .

.

Cloern et al. 2011, Stralberg et al. 2011, Veloz et al. 2013) so that flexible plans of conservation and restoration anticipate environmental changes and have contingencies to accommodate them. Consider the habitat requirements of estuarine species when developing new strategies of freshwater management such as adaptations to changing climate and water demand. Take steps to conserve resources, such as water recycling and recovery of sewage nutrients, to dampen the pressures from a growing human population. Evaluate the overall costs and benefits of different policies by taking into account the economic and social value of goods and services provided by estuaries. Monitor and analyze environmental changes as they unfold so that adaptive policies can be implemented efficiently and their outcomes can be measured. Take bold steps, such as creating new kinds of partnerships between scientists and policy makers to identify those actions most likely to increase resilience and sustain biodiversity of California’s estuaries (Cloern and Hanak 2013). Teach Californians and visitors about the unique habitats, plant and animal communities of California’s estuaries, how they have changed in the past, and implications of the choices Californians and visitors make to shape the future evolution of these ecosystems in a fast-changing world.

Summary California’s 1,766-kilometer coast has more than four hundred lagoons, inlets, stream valleys, and bays—t ransitional

ecosystems at the land’s edge that we collectively refer to as “estuaries.” California’s estuaries have a diversity of sizes, forms, and habitat mosaics shaped by climate, coastal topography, and oceanography. Estuaries are strongly influenced by their connectivity to the Pacific Ocean through landward propagation of tides and waves and immigration of marine organisms, and by their connectivity to watersheds that deliver freshwater, sediments, nutrients, and contaminants from runoff. Estuaries are dynamic ecosystems with significant physical, chemical, and biological variability at time scales ranging from hours (tidal oscillations) to months (wet and dry seasons) to decades (shifts in the climate system) to centuries (changes in sea level, river flow, water quality, habitats, and biological communities). Organisms occupying the unique habitats of estuaries are important components of California’s rich biological diversity. They include a distinctive mix of algal and plant species and hundreds of species of invertebrates, fish, birds, and marine mammals. Some are “estuarine endemics,” limited in their distribution mostly or entirely to estuaries; others are coastal generalists that rely on estuaries for critical foraging, resting, or breeding habitat. For instance, some marine fish, crab, and shrimp use estuaries as nursery habitat, while other fishes including salmon, sturgeon, and shad migrate from ocean to rivers to spawn and return as juveniles, and many shorebirds, waterfowl, and seabirds rest and forage in California estuaries as residents or during annual migrations along the Pacific Flyway. Estuaries and their biota provide invaluable services to people. Commercial ocean fisheries include estuarine-dependent species such as Dungeness crab, English sole, and California halibut. Tidal marshes sequester substantial carbon, protect shorelines from storm surges and floods, and filter urban contaminants. We use estuaries to culture shellfish. Estuarine microbes assimilate human wastes and degrade many organic pollutants. The natural harbors of California provide ports for commercial transport. We are strongly attracted to coastal settings because of their breathtaking beauty and the many opportunities they provide for recreation. However, the landscapes and biological communities of California estuaries (and services they provide) have been transformed, some beyond recognition, from those viewed by Spanish explorers in the eighteenth century. Degradation has occurred through overfishing, dredging new channels, filling mudflats and tidal marshes for urban and agricultural uses, sewage disposal, introductions of hundreds of non-native plant and animal species, damming and diverting rivers, and contaminant inputs. As a consequence over 90% of California’s tidal marshes have been lost and fifteen species of mammals, birds, and fish are at risk of extinction, while non-native species dominate many estuarine communities. San Francisco Bay was once a major U.S. fishing center, but commercial fishing for most species was closed decades ago. An active sports fishery persists, but some fish remain contaminated with unsafe levels of mercury and PCBs. Concern over these changes motivates policies to reverse the effects of human disturbance, and large-scale programs are ongoing to restore estuarine ecosystems, curtail the introduction of non-native species, and improve water quality. Sustainability of California’s estuaries, their native species, and the services they provide is uncertain in the face of a growing human population and accelerating global change. Success will be determined largely by actions we take today.

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Acknowledgments Thanks to Ruth Askevold for production of Figure 19.1.

Recommended Reading Barnhart, R. A., M. J. Boyd, and J. E. Pequegnat. 1992. The ecology of Humboldt Bay, California: An estuarine profile. U.S. Fish and Wildlife Service. Biological Report 1. Accessed June 10, 2015. Caffrey, J. M., M. Brown, and B. Tyler, editors. 2002. Changes in a California estuary: An ecosystem profile of Elkhorn Slough. Elkhorn Slough Foundation, Moss Landing, California. Hollibaugh, J. T., editor. 1996. San Francisco Bay; the ecosystem. Pacific Division, American Association for the Advancement of Science, San Francisco, California. Morro Bay National Estuary Program. 2010. Estuary tidings. A Report on the Health of Morro Bay Estuary. Morro Bay, California. Accessed June 10, 2015. Rubissow Okamoto, A., and K. M. Wong. 2011. Natural history of San Francisco Bay. University of California Press, Berkeley, California. Zedler, J. B., C. S. Nordby, and B. E. Kus. 1992. The ecology of Tijuana Estuary, California: A national estuarine research reserve. NOAA Office of Coastal Resource Management, Sanctuaries and Reserves Division, Washington, D.C.

Glossary Acidification A downward shift in the pH of water making it more acidic. For example, carbon dioxide dissolved in water produces an acidic solution and ocean waters are becoming more acidic as atmospheric CO2 concentrations increase. This is a threat to calcified marine organisms such as corals, clams, mussels, and oysters. Allochthonous Material (organic carbon, nutrients, etc.) that originates outside of the system of interest, in contrast to autochthonous, which indicates material that is generated within the system. Allochthonous material thus represents a subsidy to the system, whereas autochthonous material is generated in the system at a direct cost to the system in terms of material and energy. Amphipods Members of the diverse crustacean order Amphipoda and are generally small consumers that are a large portion of organismal abundance and diversity in benthic habitats. Anadromous Fish that migrate from saltwater to freshwater to reproduce and the juveniles migrate back to saltwater to rear, sometimes over very long distances. For example, adult Chinook salmon migrate from the ocean to the rivers where they were born; the juvenile salmon migrate from the rivers to the ocean, where they rear for several years. Anaerobic decomposition Decomposition (or respiration) that takes place in anoxic environments. Since oxygen is not available to support respiration and the oxidation of organic matter, alternative respiration pathways are used. These may involve using oxidized compounds such as nitrate, iron oxyhydroxide (rust), arsenate, or sulfate as the terminal electron acceptor in place of oxygen. Anoxic Indicates environments devoid of oxygen, such as the deeper layers of water-saturated sediments. Bay Delta Conservation Plan (BDCP) A conservation strategy aiming to improve ecological function of the delta and protect water supplies provided by the State Water Project and Central Valley Project. The BDCP was initiated in 2006 and incorporates input from a wide range of state and federal

agencies, public water agencies, environmental groups, and other interested parties. The BDCP is intended to serve as a joint Habitat Conservation Plan (HCP) and Natural Community Conservation Plan (NCCP), providing protection for listed species, including a number of fish species within the delta, while also regulating permitted incidental take of these species. With the passage of the Delta Reform Act in 2009, the BDCP has been incorporated into a broader package of state and federal programs with similar goals of protecting delta ecosystems while managing water use and withdrawals from the delta. Benthic microalgae Microscopic single-celled algae (diatoms and dinoflagellates) and cyanobacteria that inhabit the surface layers (0–4 centimeters) of aquatic sediments. Benthic microalgae are ecologically significant in many freshwater and marine environments, including estuaries. They are a major food source for benthic feeders such as crustaceans, bivalves, and polychaete worms. Benthic microalgal communities also modify exchange of nitrogen and phosphorus between the water column and sediments and therefore play an important role in regulating water quality. Bivalves Members of the molluscan class Bivalvia and include what are commonly referred to as clams. California Marine Invasive Species Act A California law that was passed in 2003 and aims to reduce the import and impact of nonindigenous species within the state’s estuaries and coasts. The act regulates the discharge and treatment of ballast water in California ports and the removal of fouling organisms from hulls for large ships (over 300 tons) in order to reduce the importation and establishment of invasive marine species. Carbon sequestration The uptake of atmospheric carbon by plants or other photosynthetic organisms and the storage of this carbon in biomass or soil organic matter. Net carbon sequestration includes the consideration of counteracting emissions of greenhouse gases, converted into CO2 equivalents, primarily methane (CH4) and nitrous oxide (N2O). While methane is not commonly produced at salinities close to seawater, it can be produced in anaerobic, lowsalinity environments, such as tidal freshwater or low-salinity brackish wetlands. Catadromous Fish that migrate from freshwater to saltwater to reproduce; the juveniles migrate back to freshwater to rear. Chlorophyll-a The primary light-harvesting pigment of plants; used as a measure of phytoplankton biomass in lakes, rivers, estuaries, and oceans. Ciliates Members of the protozoan phylum Ciliophora and are typically characterized by the presence of slender hairlike organelles called cilia. Copepods Members of the crustacean subclass Copepoda, which includes small, generally planktonic species that are among the most abundant grazers of phytoplankton. Crustaceans Members of the well-known class Crustacea within the larger phylum Arthropoda, which also includes insects. Crustaceans include many common groups including shrimps, crabs, and lobsters as well as many planktonic species including copepods. Divergent selection A process that results in the increased survival and reproductive success within a population of two groups of individuals that have different characteristics from one another. Darwin’s finches are an example of divergent selection, where birds with deep bills typical of seed eaters and birds with narrow bills typical of insectivores evolved from a common ancestor. Ecological speciation The evolution of reproductive isolation between populations as a result of ecologically based divergent natural selection.

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Ecotone A transition zone between two ecological habitats or community types (e.g., aquatic to terrestrial habitat; intertidal to subtidal habitat). It may be narrow or wide, appearing as a gradual blending of the two communities across a broad area, or it may manifest itself as a sharp boundary line. Endemic Found only in a defined geographic location, such as an island, continent, or other defined range. Organisms that are native to a place are not endemic to it if they are also found elsewhere. Evapotranspiration The transfer of water from land to atmosphere through the combined effects of direct evaporation from water and soil surfaces and of transpiration (the loss of water through leaf pores) in plants. Extirpation Local extinction. Ceasing to exist in a given area, though still present elsewhere. Local extinctions are contrasted with global extinctions. Local extinctions may be followed by a replacement of the species taken from other locations; wolf reintroduction is an example of this. Floodplain A floodplain is a relatively level area adjacent to a stream channel that is formed and maintained by the stream and periodically overflowed during flood events. Gastropods A class within the Molluscs, which typically (but not exclusively) have a calcified shell and include grazing herbivores, scavengers, and predators. Gastropods include common groups such as snails, chitons, and abalone. Geomorphology The study of landforms. The discipline is concerned with understanding not only the physical form of landscapes but also their origin, evolution, and the physical processes and dynamics that shape them. In estuaries, geomorphology can be used to both classify different types of systems (such as lagoons, bays, or river-mouth estuaries) and to characterize the distinct physical settings (e.g., bathymetry, topography) and processes (e.g., tidal currents and range, wave dynamics, sediment delivery, and transport through fluvial and tidal inputs) experienced by each system, as well as how these vary with time and space. Heterotrophic ecosystems Ecosystems, such as many estuaries, where total system respiration exceeds total system photosynthesis; this implies external inputs of organic carbon. These ecosystems are net consumers of organic carbon and net producers of carbon dioxide. Hydrodynamics The study of the dynamics of fluids in motion. In an estuary, this applies to the response of water levels and currents to multiple forcings, including tides, storm surges, barometric pressure changes, and freshwater inflows. Also, the hydrodynamical processes and patterns characteristic of a particular area—for example, “the hydrodynamics of Tomales Bay.” Hydroids A common name referring to species in the class Hydrozoa but typically referring to the polyp stage (attached, with arborescent feeding tentacles) of the life cycle. Hydrology The study of processes affecting the movement of water, usually in relation to land. These processes can include precipitation, snowpack accumulation and melt, surface flows, soil water movement, and percolation to aquifers. Also, the hydrological processes and patterns characteristic of a particular area—for example, “the hydrology of the Klamath basin.” Hydrozoans Members of the class Hydrozoa in the phylum Cnidaria. These sessile animals are generally attached to hard substrate and feed with tentacles and defend themselves with specialized stinging structures. Hypersaline Conditions where salinity regularly exceeds that of seawater (about 35 parts per thousand). Hypersalinity is common in Mediterranean-climate estuaries with relatively small watersheds and limited tidal exchange due to seasonal inlet closure, where evaporation can greatly exceed freshwater

inflow during the dry season. Extreme hypersalinity can exclude the growth of marsh vegetation; as a result, a salt flat or salt panne is an extreme expression of hypersaline conditions. The salinity of these estuaries can often fluctuate widely by season, with hypersaline summer conditions replaced by saline or even fresh-brackish conditions during the winter. Intertidal habitat Areas between high and low tides. During high tides these areas are submerged; during low tides these areas are exposed. Macroalgae A group of single to multicellular primary producers found in all aquatic ecosystems. Members of this functional group (including red, green, and brown algae and cyanobacteria) include such diverse forms as simple chains of prokaryotic cells, multinucleate single cells over 1 meter in length, and giant kelps over 45 meters in length with complex internal structures analogous to vascular plants. They provide the same ecological functions as vascular plants in terrestrial ecosystems but lack the structural tissues characteristic of plants. They are important primary producers in intertidal and shallow subtidal estuaries, providing food and refuge for invertebrates, juvenile fish, crabs, and other species. Some species of macroalgae thrive in nutrient-enriched waters to create extensive blooms, outcompeting other primary producers. Marine protected areas (MPAs) Areas along the California coast and estuaries that receive special protection under the Marine Life Protection Act, passed in 1999; MPAs were initiated to improve protection of marine ecosystems within the state. Four MPA regions have been established along the California coast as well as one within San Francisco Bay. MPAs include reserves (all harvesting excluded, including commercial, recreational, and geologic), parks (recreational harvesting allowed), conservation areas (select commercial and recreational harvest can be allowed), and recreational management areas (subtidal protection but waterfowl hunting allowed). Molluscs Members of the very common phylum Mollusca. Members typically have a hard calcified shell and include many familiar groups including snails, clams, mussels, squids, and octopods. Nitrification-denitrification The stepwise process whereby reduced nitrogen, present in water as an equilibrium mixture of ammonia (NH3) and ammonium (NH4+), is converted to dinitrogen gas. Ammonia is first oxidized to nitrite (NO2-) by one functional guild of prokaryotes. Some of this nitrite may be oxidized further by another functional guild of prokaryotes to yield nitrate (NO3-). These steps require oxygen and this two-step process constitutes nitrification. Some of the nitrite produced as an intermediate of nitrification may be used by another group of prokaryotes to oxidize ammonia via the anaerobic ammonia oxidation, or “anammox,” reaction, resulting in the production of dinitrogen (N2) gas. The organisms that mediate these steps are autotrophs, using the energy obtained from oxidizing ammonia to reduce carbon dioxide to organic carbon. Both nitrite and nitrate can be used by some heterotrophic prokaryotes to oxidize organic matter anaerobically, producing dinitrogen gas and carbon dioxide. The reactions that yield dinitrogen gas are referred to as autotrophic and heterotrophic denitrification, respectively. North Pacific Gyre Oscillation (NPGO) A climate pattern that is the secondary mode of sea surface height variability in the northeast Pacific (the primary mode is the Pacific Decadal Oscillation). The NPGO is significantly correlated with fluctuations of salinity, nutrients, and chlorophyll-a measured in long-term observations in the California Current and Gulf of Alaska (modified from http://www.o3d.org/npgo/). Panne Also known as salt panne, pan, marsh pond, or salina, panne is a type of shallow, natural depression that forms Estuar ies 383


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on poorly drained areas of tidal marsh plains, such as areas between drainage networks or along the upland-tidal marsh boundary. Pannes receive water during very high tides and lose water through evaporation and are usually unvegetated or sparsely vegetated. Some pannes can become encrusted with sea salt that precipitate as the tidal water evaporates. In some marshlands salts were historically harvested from pannes by native Californians and early settlers. Phytoplankton Microscopic algae suspended in water; an important component of the primary-producer community of lakes, rivers, and estuaries. Piscivorous Any animal that primarily consumes fish as part of its diet. Polychaetes Members of the most species rich class (Polychaeta) of worms in the phylum Annelida; these include species with a broad range of feeding modes and life histories and are among the most abundant and diverse benthic invertebrates in most estuaries. Primary producers Organisms in an ecosystem that produce biomass from inorganic compounds (autotrophs). In most cases these are photosynthetically active organisms (plants, cyanobacteria, and a number of other unicellular organisms). However, some unicellular organisms exist that that produce biomass from the oxidation of inorganic chemical compounds (chemoautotrophs). Because primary producers produce carbon from energy, they form the foundation for the food chain. In terrestrial ecoregions these are mainly vascular plants, while in aquatic ecosystems algae are the dominant primary producers (see “macroalgae,” “benthic microalgae,” “phytoplankton”). Prokaryotes The group of organisms that do not have membrane-bound nuclei. Nearly all are microscopic, though they may form colonies, mats, or other structures that are visible to the naked eye. They include members of the kingdoms Archaea and Bacteria but are distinct from microscopic members of the kingdom Eukarya, such as yeasts or unicellular plants. Familiar examples include Lactobacillus and Escherichia coli (E. coli). Reproductive isolation The inability of two different species to produce fertile offspring due to behavioral or physiological mechanisms. These barriers maintain the differences between species over time by preventing genetic mixing of the species. Stratification Vertical layering of water in a lake or estuary as low-density (warmer, fresher) surface water overlays higher-density (cooler, saltier) bottom water. Stratification impedes vertical mixing and allows for the establishment of vertical gradients of biota (e.g., phytoplankton) and chemical constituents (e.g., dissolved oxygen). Subspecies A category in biological classification that ranks immediately below a species. Subspecies are morphologically or genetically distinguishable from one another. Organisms that belong to different subspecies of the same species are capable of interbreeding and producing fertile offspring, but they often do not interbreed in nature due to geographic isolation or other factor. Subtidal habitat Any habitat adjacent to the coast that is submerged below sea level except during extremely low tides. These areas include mud, sand, rocks, artificial structures, submerged aquatic vegetation, and macroalgal beds. Tule A commonly used term for bulrush species native to California, including but not limited to hardstem bulrush (Schoenoplectus acutus), California bulrush (S. californicus), and Olney’s bulrush (S. americanus). Tule is dominant in freshwater and brackish marshes across the state. Tunicates Members of the chordate subphylum Tunicata, which include both planktonic and sessile species known

as sea squirts that can be important filter feeders in both planktonic and benthic habitats. Turbid Adjective describing rivers, lakes, or estuaries having large concentrations of suspended particles (e.g., sediments or phytoplankton) or dissolved constituents that cloud water and restrict light penetration to a shallow depth. Photosynthesis is confined to a thin surface layer in turbid waters. Watershed An area of land, usually defined by topography, from which all surface-water flows exit the at the same outflow point. Zooplankton Small animals suspended in water; most feed on phytoplankton, detritus, or single-celled organisms (ciliates, flagellates) and are a key food resource for early life stages of fish and adult plankton-feeding fish such as smelt, anchovies, and herring.

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