3.3  BIOLOGICAL RESOURCES

The biological resources that may be affected directly or indirectly by the Spartina Control Program include the intertidal habitats (mudflats, tidal creeks, sloughs, tidal marshes) of the San Francisco Estuary, shallow subtidal habitats near them (sloughs and nearshore bay habitats), and habitats immediately adjacent to the Estuary, particularly diked baylands where access and staging areas for eradication activities may occur, and the plants and animals that inhabit these places. This section focuses on those aspects of the Estuary's biological resources that may be affected by the proposed project and alternatives.

3.3.1 Environmental Setting

A recent comprehensive overview of the biological communities and species of the San Francisco Estuary is provided in the Baylands Ecosystem Habitat Goals Project (Goals Project 1999, 2000). The ecological communities (populations of interacting species in different tidal habitats) of the San Francisco Estuary are influenced by position along numerous physical gradients of the Estuary, and the variation in distribution of the species that compose them. An overview of relevant ecological communities, and key species of concern, is presented below. Descriptions of these habitats and species emphasize aspects likely to be most sensitive to changes caused by eradication measures or cordgrass invasions themselves.

Biological Communities

Biological (ecological) communities are the interacting populations of the species associated in particular habitats defined by physical, chemical, geographic, and topographic gradient boundaries. To understand individual environmental impacts to species, it is necessary to recognize their relationships within biological communities in potentially affected areas of the San Francisco Estuary. Many of these biological communities and features that comprise them were shown previously in Figure 1-7.

Tidal Marsh Communities. Tidal marsh essentially consists of herbaceous (non-woody) vegetation that is periodically flooded by tidal waters with varying degrees of salinity. Tidal marshes include areas that are normally waterlogged as well as areas that are infrequently or intermittently flooded. Low marsh cordgrass species (e.g. Atlantic smooth cordgrass, Pacific cordgrass, English cordgrass) typically grow in tidal marsh zones flooded by daily tides. High marsh cordgrasses like Chilean cordgrass and salt-meadow cordgrass typically grow in higher marsh elevations, which are tidally flooded less frequently, often only a few days per month. Tidal marsh can establish on terrestrial substrates (tidally flooded soils which originated in non-tidal lands, especially in high marsh), but most of the tidal marsh in the San Francisco Estuary is established on estuarine sediment mixed with varying proportions of decomposed vegetation (peaty or muck-like organic matter). Most tidal marsh is typically described in terms of the dominant plant species, appearance of the vegetation, and the landforms on which they occur.

Tidal salt marsh vegetation. Tidal salt marshes are prevalent in San Francisco Bay, where the salinity of tidal waters in the summer growing season often approach or even exceed ocean seawater. Tidal salt marsh along channel banks and areas which are submerged twice daily by tides (low marsh zone, below mean higher high water) historically were dominated by a single species, Pacific cordgrass (Spartina foliosa), a colonial marsh grass usually less than one meter tall. Relatively uncommon native annual pickleweed (Salicornia europaea) establishes at the upper portion of this zone in sheltered sites, but low salt marsh was essentially a pure stand of Pacific cordgrass prior to the introduction of non-native cordgrasses.

The upper salt marsh plain, which is flooded only by the higher tides of the month, not daily tides (near the elevation of mean higher high water; the middle or high marsh zone, depending on classification) is dominated in San Francisco Bay by patchy mosaics of perennial pickleweed (Salicornia virginica), saltgrass (Distichlis spicata), jaumea (Jaumea carnosa), and numerous less frequent low-growing salt-tolerant herbs. In young salt marshes, the marsh plain vegetation is sometimes nearly pure stands of pickleweed. The salt marsh plain vegetation in the Estuary is usually less than 30 to 40 centimeters (12 to 16 inches) tall. Pacific cordgrass is sparse or absent on the marsh plain, usually confined to its lowest elevations. In historic salt marsh conditions, grasses such as saltgrass dominated the salt marsh only in local zones (Cooper 1926).

California salt marsh vegetation is relatively diverse and species-rich compared with Atlantic salt marshes, which are generally dominated by either grasses (often pure stands of Atlantic smooth cordgrass) or grass-like plants throughout the marsh. Even higher plant species diversity and vegetation structure occurred in high salt marsh zones of San Francisco Bay, flooded only by the highest tides of the year. These occurred along natural levees at tidal creek banks, bay edges of alluvial fans, and contacts and transitions to other environments such as grasslands, freshwater riparian scrub or woodland near streams or seeps, freshwater marshes, beaches, salt pans, and lagoons (Baye et al. 2000, Holstein 2000). Natural high salt marsh communities are rare today, displaced by weedy flood control levees and shoreline stabilization. Gumplant (Grindelia stricta var. angustifolia), a tall, evergreen subshrub, dominates the narrow high marsh zone along the banks of mature tidal creeks, where it provides critically important high tide cover for marsh wildlife. It also often occurs in high marsh zones along upland edges."

Tidal brackish marsh vegetation. Where the salinity of tidal water is significantly diluted by stream or urban wastewater discharges, the physiological harshness of saline water that restricts the growth of many plant species is eased, and marsh community diversity increases. Marshes that vary between nearly freshwater conditions and salinities about half as strong as undiluted seawater are broadly described as brackish marshes (though many salinity classifications of marshes exist). Brackish marshes in the San Francisco Estuary vary in vegetation composition a great deal, and the relative abundance of dominant brackish marsh plants is highly sensitive to short-term climate changes that influence salinity, flooding, and sediment deposition. Most of northern San Pablo Bay and all of the Suisun Bay region (Suisun Marsh and the Contra Costa marshes) tidal marshes are brackish. Brackish marshes were historically also locally common along the edges of many portions of San Francisco Bay (Cooper 1926, Baye et al. 2000).

Pacific cordgrass thrives in diluted salinity of brackish tidal marshes, growing more productively than in full-strength seawater. Other, larger plants tolerant of lower salinities and even greater immersion in water, also thrive in brackish marshes. Although cordgrasses often establish colonies in brackish intertidal muds, alkali bulrush (Scirpus maritimus and intergrades with S. robustus), tules (S. acutus, S. californica), and cattails (Typha spp.) can invade and overtop lower-growing Pacific cordgrass vegetation in brackish marshes. These taller emergent brackish marsh plants often establish as the dominant pioneers on channel banks and upper mudflats in brackish reaches of the Estuary. The marsh plain in brackish tidal marshes is much richer in plant species and more variable and diverse in structure compared with tidal salt marshes in San Francisco Bay. Many of the rarer plants in the Estuary occur in brackish marsh plains or high brackish marsh.

Tidal marsh animal communities. Animal communities of tidal marshes of the San Francisco Estuary are relatively mobile, and are less often narrowly restricted to a single fixed marsh vegetation zone or patch. They may move according to tides, storm surges, or seasons. Insect communities of the San Francisco Estuary marshes are not well studied, and even basic descriptive information about insect species composition and trophic relationships (food webs) are limited (Maffei 2000). The terrestrial arthropod fauna of tidal marshes in the Estuary are dominated by brine flies, leafhoppers, plant hoppers, mites, and spiders (Resh and Balling 1979). Insects and spiders are abundant in the middle and upper high marsh zones, and crustaceans (including amphipods) are abundant in moist organic tidal litter wracks, and in frequently flooded marsh. Many are important consumers of detritus from decomposing plant litter, a critical link in the tidal marsh food web.

Vertebrate wildlife of tidal marshes is better studied than insects, particularly waterbirds (shorebirds, waterfowl, wading birds, terns and gulls). Short-legged shorebirds seldom roost or feed in thick salt marsh vegetation, but occasionally roost at high tides on smooth wracks (tidal litter mats) in the high marsh. Short-legged shorebirds instead frequent shallow or emergent flats lacking vegetation. Wading birds (egrets, herons) and long-legged shorebirds (e.g. willets, marbled godwits, long-billed curlews, whimbrels) do roost or forage on the marsh plain, along low marsh banks of tidal channels, and in the many shallow ponds and natural salt pans enclosed within the marsh plain. Long-legged shorebirds, however, generally prefer open flats when they emerge from tidal flooding. Rails (clapper rails, black rails, Virginia rails, and sora), in contrast, spend nearly all their time within vegetated areas of tidal marsh and small channels, where they forage on benthic invertebrates in the muddy substrate. Northern harriers ("marsh hawks") are frequent and characteristic avian predators of San Francisco Estuary tidal marshes. Black-shouldered kites and red-tail hawks also hunt in tidal marshes, as well as osprey. Songbirds (perching birds or passerines) which spend much or most of their lives in San Francisco Estuary tidal marshes include several endemic subspecies of song sparrow (each geographically restricted to part of the Estuary), and the salt marsh common yellowthroat. Many other songbirds are occasional or incidental visitors to tidal marsh habitats.

Emergent tidal marsh plains are often rich in small mammal populations, particularly higher marsh plains. Both non-native rodents (Norway rat, roof rat, house mouse) and native rodents (California vole, western harvest mouse, salt marsh harvest mouse, salt marsh wandering shrew, Suisun shrew, and ornate shrew) inhabit salt marshes seasonally or year-round, depending on the species and ecological conditions in adjacent habitats. They tend to occur mostly in the sub-shrubby perennial vegetation of the marsh plain, not in low cordgrass marsh. Abundant small mammals, in turn, attract raptor foraging in tidal marshes. Small mammals are temporarily displaced from tidal marshes during extreme tidal flooding events, and seek refuge in sheltering debris, tall vegetation, and local high ground with cover to shield them from birds of prey (Johnston 1957).

Large mammals also inhabit tidal marshes in the San Francisco Estuary. Resident bay colonies of harbor seals use some specific tidal marsh localities as "haul-outs". These are areas above frequent high tides to rest and bask, usually near feeding areas. Haul-outs are also used for pupping. Traditional seal haul-out sites in tidal marshes of San Pablo Bay and San Francisco Bay often are high marsh plains with close access to deeper tidal channels, adjacent to gently sloping unvegetated banks (actually devegetated in places by seal activity). Seals do not move through wide cordgrass marshes on very gentle intertidal gradients (Lidicker and Ainley 2000). Coyotes hunt in North Bay tidal marshes and diked baylands (P. Baye, pers. observ. 2001), and the non-native red fox, a significant predator of California clapper rails, is now widely established in San Francisco Bay and San Pablo Bay, particularly where access to marsh feeding areas is facilitated by artificial levees or uplands where they travel or build dens (Harding 2000). Raccoons and skunks also are widespread in modern tidal marshes. Feral cats frequently inhabit marsh areas at the urban interface adjacent to landfills, urban development, and other areas where food and shelter are available.

Estuarine Beach Communities. Central San Francisco Bay historically supported extensive sand beaches, and beaches made of shell fragments (mostly fossil oysters) are still widespread along the shores of the South Bay. Sand spits, some approaching the size of marine beaches, prevailed along the bay/marsh interface from what is now Richmond to Alameda, and were also common along the northern San Francisco peninsula. These areas were also the main centers of urban waterfront development, and were destroyed so early after settlement that little is known directly about them. Historic beaches in San Francisco Bay were generally restricted to shorelines where bay waves directly attack and re-work exposed, submerged deposits of sand or shell, or sandy deltas of tributary streams (see Section 3.1, Geomorphology and Hydrology).

Physically dynamic estuarine beaches provide naturally open, sparsely vegetated roosting habitats for shorebirds flooded off of preferred feeding areas, such as tidal mudflats. Some shorebirds and terns typically nest on sand beaches, especially sand spits, but there are no records of nesting in the vestigial urban-edge beaches of San Francisco Bay. Instead, the western snowy plover and California least tern exploit today's extensive artificial playa-like (beach plain and salt flat) habitats, such as emergent artificial salt pan beds and even derelict runways (Page et al. 2000, Feeney 2000).

Modern beaches have regenerated at some shoreline positions near those of their historic predecessors, derived from the same sediment sources. Some of these support vestiges of estuarine beach and dune communities. Some modern sand beaches of the bay, such as Crown Beach (Alameda) and Roberts Landing sand spit (San Leandro) are being converted to low-energy tidal salt marsh in the shelter of Atlantic smooth cordgrass and its hybrids.

One endangered plant, California sea-blite (Suaeda californica) probably was restricted largely to salt marsh edges of sand and shell beaches of San Francisco Bay, rather than typical salt marshes. Other rare plants are associated with sandy high salt marsh environments (Baye et al. 2000). Several rare species of tiger beetles native to San Francisco Bay occur primarily in beach or dry pan habitats (Maffei 2000). Drift-lines and organic debris on beaches provide refuges of high moisture and organic matter, and can produce abundant insect and amphipod populations.

Communities of Lagoons, Ponds, and Pans. Within tidal marsh ecosystems, marshes establish in relatively waterlogged soils, but subsurface water movement and drainage to nearby tidal creeks moderates waterlogged soil conditions, providing some gas exchange. Where tidal waters become impounded in poorly drained depressions, wide flats, or behind barrier beaches that act as natural dams for streams, extreme waterlogging or salt accumulation can cause toxic soil conditions. Salt accumulation and sulfide accumulation (indicated by "rotten egg" scent) in very poorly drained areas cause dieback of emergent marsh vegetation, or severely inhibit its establishment. These areas lacking extensive cover by emergent vegetation form distinct and important habitat types in the Estuary. Some types of marsh pans are subject to invasion and modification by at least one non-native cordgrass that can tolerate greater waterlogged soil conditions than native species.

Most of the original tidal marshes in the San Francisco Estuary were rich in small to moderate-sized (fractions of an acre to several acres) pans -- shallow tidal pools embedded in the marsh plain. Tidal marsh pans in the marsh plain lack drainage outlets and are infrequently flooded by tides that overtop the marsh plain. They are often rounded in outline, and have steep banks less than a foot high, with soft muck beds. This type of salt marsh pan is often shallowly flooded for most of the winter and spring, and is intermittently flooded in summer. In its flooded phase, it often supports extensive colonies of submerged aquatic vegetation, equivalent to eelgrass and other seagrass meadows. Wigeon-grass (Ruppia maritima, not a true grass) is the prevalent submerged vegetation of natural salt pans in San Francisco and San Pablo Bays. It tends to become covered by filamentous algae when stagnant pans warm in summer, and is often mistaken for pure algal mats. Wigeon-grass canopies in pans support rich invertebrate communities, providing important habitats for dabbling ducks, diving ducks, and geese. They die back when the pan evaporates in summer between peak high tides, forming saline or hypersaline mats of dried algae and fabrics of dead wigeon-grass foliage.

Some salt pans may be entirely barren of any vegetation. Even these produce rich aquatic invertebrate communities that provide important habitat for some shorebirds (avocets, black-necked stilts, and yellowlegs) which otherwise would find little foraging habitat in vegetated tidal marsh plains. Salt pans are relatively abundant in natural tidal marshes that formed pre-historically, but are usually scarce in recently formed marsh plains that lack complex, irregular tidal creek patterns. In Suisun Marsh, tidal marsh pans are brackish, and these are even scarcer today than natural salt pans. Brackish pans support a greater diversity of submerged aquatic plant species.

The smallest tidal marsh pans (less than 0.25 acre), and marsh pans encroached by emergent vegetation, can produce abundant salt marsh mosquitoes. Larger pans have turbulent open water surfaces (internal wind-generated waves), which discourage survival of mosquito larvae. When tidal marsh pans become invaded by emergent vegetation, they produce very poorly drained marsh and still, sheltered water surfaces that encourage successful mosquito breeding (Balling and Resh 1983, J. Collins, pers. comm.).

Extensive natural salt ponds (evaporation basins producing beds of crystalline salt) no longer exist in San Francisco Bay, but were locally characteristic features of the Hayward shoreline. Similarly, natural lagoons (brackish to saline ponds, infrequently and intermittently tidal) no longer exist in the Estuary. Equivalent habitats are provided by "intake" solar salt evaporation ponds - permanently flooded, shallow saline waters that support soft-bottom benthos, entrapped estuarine fish population, wigeon-grass beds (submerged aquatic vegetation), and large algae. The management of salt ponds depends on tidegates used as water intakes. Sediment accretion and cordgrass growth can obstruct intakes.

Brackish lagoons are also represented by a few permanently flooded waterfowl-managed ponds in Suisun Marsh. Waterfowl-managed ponds depend on operation of water intakes (tidegates) to flood and drain tidal waters, either on artificial seasonal schedules, or partially choked daily tidal flows. The surrogate lagoon habitat represented by early-stage solar salt evaporators is significant in that it excludes the growth of all cordgrasses, even invasive non-native cordgrasses established in adjacent populations. No cordgrass species in San Francisco Bay can tolerate extreme hypersaline soils or prolonged, deep flooding.

Mudflat Communities. Intertidal flats in the San Francisco Estuary are mostly soft, unconsolidated sediment habitats made of physically unstable bay mud (fine silt and clay; mudflats) on very gentle gradients. By definition "tidal flats" do not include steeply sloping, consolidated mud banks of tidal channels. A minority of intertidal flats are made of sandy sediments (especially in the Central Bay), or fossil shell deposits and lag surfaces of shell over softer muds.

The permanent bottom-dwelling residents (benthic infauna) of mudflats are invertebrates, such as clams, worms, snails, and crustaceans. These permanent residents of the mudflat are highly dynamic, however, and adjust to the physically unstable surface of the mudflat. Turnover of populations and species is also high following sequences of major pulses of salinity changes. The vast majority of total living mass of benthic infauna in the San Francisco Estuary are non-native species introduced through international shipping in San Francisco Bay ports. The principal ecological values of mudflats are not for the resident native biological diversity, but for the estuarine production, trophic (food web) support to fish and wildlife, and biogeochemical "processing" (transformation) of sediment and water provided by mudflats (Goals Project 1999). In contrast with the intertidal fauna of rocky shores, which includes many sessile (physically attached, fixed) invertebrates, the mudflat infauna is composed of mobile invertebrates adapted to the unstable surface of the mudflat, which is subject to daily erosion and redeposition by bay waves and tidal currents. Disturbed intertidal mudflats are rapidly recolonized by the prevalent infauna.

Mudflats are submerged twice daily and periodically become habitat for a diverse, mobile estuarine fish community. Fish in submerged mudflats feed on benthic infauna (invertebrates living under the mud) epibenthos (invertebrates living on the submerged mud surface), other fish, and drifting detritus or plankton. No eelgrass beds occur in intertidal mudflats in San Francisco Bay; they are restricted to shallow subtidal habitats in areas of relatively less turbid bay tidewaters, where they provide important habitat for benthic invertebrates and fish. Fish assemblages vary with geographic position in the Estuary, often in relation to large-scale and local salinity gradients, abundance of plankton (the foundation of the food web), and habitat structure.

Anadromous fish (species migrating upstream to freshwater rivers to spawn), estuarine fish, and marine fish occur in the submerged intertidal mudflats and tidal marsh channels. Juveniles of anadromous fish (such as salmon and steelhead) use vegetated edges of mudflats and marsh tidal channels as nursery and feeding habitats, providing both food and shelter from predators. Pacific herring and anchovy feed on drifting plankton in shallow or deep open waters. They provide a prey base for many larger fish. Flatfish species (flounder, sole, halibut, turbot), sculpin, and goby species are common bottom fish in both shallow and deepwater habitats. Cartilaginous fish (rays and sharks) are commonly found in shallow submerged mudflats, including leopard sharks, brown smoothhound, and bat rays. Rays are bottom feeders, taking benthic invertebrates by disturbing bottom sediments. Many non-native fish have also permanently established in the San Francisco Estuary.

Most of the San Francisco Estuary's tidal flats occur today in the South and North Bays; less mudflat area naturally occurs in Suisun Bay. The unvegetated surface of mudflats, combined with their very high productivity (infauna rich in calories and protein), makes their production available to migratory shorebirds and waterfowl of the Pacific Flyway. These waterbirds cannot feed, or feed only marginally, in consolidated (root-bound) emergent tidal marsh substrate and its vegetation. The bare soft bottom of mudflats submerged at high tide also provides rich feeding for diverse native fish populations (Goals Project 1999) and terns, including the endangered California least tern.

The essential unvegetated character of tidal flats in the San Francisco Estuary is due to an interaction between wave energy (forces of erosion and deposition from waves generated by winds blowing across the bay), intertidal slopes, and vegetation. Wave erosion during storms trims back the leading edge of cordgrass clones. Wave erosion also is responsible for maintaining mudflat area as sea level rises (converting the lower intertidal zone to subtidal habitat). The physical limitation of native marsh plants to resist wave-driven substrate dynamics is key to the maintenance of mudflat habitat and its proportions in the Estuary.

Subtidal and Intertidal Channels. A characteristic feature of historic San Francisco Estuary tidal marshes is the very high density of irregular, sinuous, branched tidal channels that extensively penetrate the marsh plain. This structure is related to the properties of native marsh plants, especially, the tidal elevations to which they are limited, and the effect their below-ground parts have on the cohesiveness of marsh substrate. Native wildlife, such as California clapper rails, and many native estuarine fish exploit the extensive channel networks in San Francisco Estuary tidal marshes, which provide close proximity of vegetative cover (predator refuge) and productive feeding in narrow channel beds and banks. Diving ducks and bay ducks, in contrast, congregate in larger tidal sloughs to feed or rest. Fish communities in channel habitats are essentially similar to those of mudflats submerged at high tide (see Mudflat Communities, above).

Salt marshes on coasts dominated by larger, robust cordgrass species, such as the Atlantic coastal plain, lack these complex and high densities of tidal channels, and instead develop simpler drainage systems and vast cordgrass meadows.

Eelgrass (Zostera marina) canopies provide important habitats for fish (foraging, shelter), and for geese where the vegetation grows intertidally or in very shallow subtidal zones. Establishment of eelgrass beds is also limited by current velocities: high tidal current energy can erode bottom sediments and uproot small colonies. Eelgrass is scarce in the turbid waters of San Francisco Bay and San Pablo Bay. In San Francisco Bay it is limited to subtidal areas, in contrast with low-turbidity, sandy marine estuaries, where it also grows intertidally (Phillips 1984). It is relatively more abundant in tidal channels and subtidal shallows in marine embayments with stabler sandy mud bottoms and clear water.

Special-Status Species

The San Francisco Estuary provides habitat for a large number of rare, threatened, and endangered species, and even more declining species of concern for conservation (Goals Project 1999, 2000). Those species that are subject to direct, indirect, or cumulative effects of cordgrass control are described in abbreviated, relevant detail here. Special-status species that occur in affected habitats are summarized in Appendix F, and species of particular relevance to this project are discussed in detail below.

California Clapper Rail (Rallus longirostris obsoletus). The endangered California clapper rail is one of the most important ecological issues related to invasive cordgrass eradication, because of complex and variable short-term and long-term impacts from the cordgrass invasion and the proposed eradication measures. The species, Rallus longirostris, is protected under the Migratory Bird Treaty Act, and this subspecies is Federally and State-listed as endangered.

The California clapper rail is one subspecies among many geographic "races" of the species in North America. Clapper rails resemble small chickens with long bills and legs, reflected in the common name, "marsh hen". California clapper rails specifically inhabit tidal salt and brackish marshes. Historically, California clapper rails ranged from Humboldt Bay to Morro Bay, with the core of the species' population in San Francisco Bay. Today, it is largely restricted to San Francisco Bay and San Pablo Bay, with occasional to regular vagrants reported from Tomales Bay (J. Evans, pers. comm.). Recent known clapper rail nesting locations are shown in Figure 3.3-1.

Clapper rails are opportunistic, omnivorous feeders. They feed mostly under or near stands of cordgrass, which shelter many of the food items clapper rails depend on, such as crustaceans, bivalves, insects, and even small mammals or birds. Within a tidal marsh, their "home ranges" and nest sites are usually keyed to small tidal creeks or channel edges. They generally avoid uniform marsh plains lacking tidal creeks, and seek channels or ditches with vegetation overhanging banks or covering the bank slopes.

View Figure 3.3-1

California clapper rails generally avoid exposure outside of dense vegetation cover, where they are vulnerable to predation by hawks (especially northern harriers) or terrestrial predators (especially non-native red fox). The spread of the red fox in the South Bay during the 1980s destroyed many rail populations, and nearly caused the extinction of the species there. California clapper rail populations rebounded following red fox population control efforts, but red fox have since spread to the North Bay as well. Successful clapper rail breeding populations in the South Bay often depend on adequate access for red fox control operations (Harding 2000, Evens and Albertson 2000). Clapper rails are most vulnerable to predation during extreme high tides, when almost all emergent vegetation cover is submerged, exposing rails visually to predators. During these periods, clapper rails seek cover in almost anything that stands above the flooded marsh vegetation, including debris, tall semi-evergreen native vegetation (particularly gumplant, Grindelia stricta var. angustifolia), and even invasive tall-form Atlantic smooth cordgrass and its hybrids.

In the San Francisco Estuary, California clapper rails do not construct "floating" nests within Pacific cordgrass stands, as their southern California counterparts do (light-footed clapper rail, R. longirostris levipes). They naturally nest in tall, dense pickleweed or gumplant vegetation near small tidal creek banks in San Francisco and San Pablo Bays. However, they have recently been reported to nest locally within tall-form Atlantic smooth cordgrass vegetation in San Francisco Bay (J. Evans, K. Zaremba, pers. comm.).

California Black Rail (Laterallus jamaicensis coturniculus). The California black rail also is a relatively secretive tidal marsh resident, more often detected by its calls than actual sightings. The San Francisco Estuary supports the largest coastal population, mostly in northern San Pablo Bay and around Suisun Bay. They have been rare to locally extinct in San Francisco Bay in recent decades. It is now presumed extirpated in San Francisco Bay, but vagrants or new founders may occur. California black rails spend most of its time in dense cover of brackish tidal marshes, and prefer mixed pickleweed vegetation. They sometimes appear in freshwater or salt marshes along the coast. California black rails nest in tall grasses and grass-like vegetation as well as mixed pickleweed vegetation well above ordinary high tides. Like clapper rails and other resident marsh birds, the abundance of black rails corresponds with tidal creeks that dissect the marsh plain, and the availability of adequate, well-distributed high tide escape cover. Its distribution within the San Francisco Estuary suggests affinity for brackish tidal marsh vegetation (pickleweed, bulrush and tule), but it does occur in moderate densities where typical salt marsh dominant vegetation (pickleweed/cordgrass) prevails. Breeding birds do not utilize young cordgrass marshes, but may feed in cordgrass areas outside the breeding season. Black rails are declining in abundance within the Estuary (Trulio and Evens 2000, Evens et al. 1991). The species, Laterallus jamaicensis, is protected under the Migratory Bird Treaty Act, and this subspecies is currently listed as endangered in California, but not under Federal law.

California Least Tern (Sterna antillarum browni). California least terns are migratory, seasonal inhabitants of the San Francisco Estuary, where they breed in colonies. They arrive at California in April, and establish nests in May and June. Their natural coastal breeding habitats are sand spits and flats with minimal, sparse vegetation. In San Francisco Bay, natural habitats (suitable isolated, large beaches and flats) are now nearly absent, and California least terns have adapted to colonize man-made habitats with similar key features, such as barren levee crests or dry beds of salt ponds, and paved or other isolated areas with extensive, barren, flat artificial surfaces and little human activity. Their principal breeding colony in the region is at the former Alameda Naval Air Station on an abandoned runway, now managed for tern breeding (Feeney 2000). California least terns are ecologically similar to other, larger native terns, some of which (Forster's tern, Caspian tern) also breed in the San Francisco Estuary, and are themselves species of concern. Their nests all are vulnerable to terrestrial predators (rats, fox, skunks, raccoons), and avian predators (hawks, gulls). The species, Sterna antillarum, is protected under the Migratory Bird Treaty Act, and this subspecies is Federally and State-listed as endangered.

Like other terns in the San Francisco Estuary, California least terns forage in shallow bay waters for small, slender fish, particularly schools of northern anchovy and silversides. They commonly forage over productive tidal flats when they are submerged at high tide. The E.B. Roemer Marsh, Alameda and Roberts Landing area in San Leandro are established feeding areas: both have extensive sand flats, and both are being invaded by Atlantic smooth cordgrass. California least terns also feed in tidally connected man-made lagoons with low turbidity and abundant populations of small fish (e.g. salt intake ponds). Least terns teach their fledged young how to fish, and some roosts and feeding areas in San Francisco Bay are particularly used as post-fledging feeding sites for juveniles acquire feeding skills. Rich feeding in San Francisco Bay is important in building energy reserves needed for migration (Feeney 2000).

Western Snowy Plover, Pacific Coast Population (Charadrius alexandrinus nivosus). There are many subspecies (geographic races) of the small, pale shorebird in the species Charadrius alexandrinus (Kentish plover) worldwide (Hayman et al. 1986). The western U.S. subspecies, known as the western snowy plover (C. alexandrinus nivosus), inhabits playas (salt flats, dry beds of seasonal saline lakes) of the interior states, and beaches on the Pacific Coast. The population of the Pacific Coast constitutes a relatively distinct breeding unit. San Francisco Bay is one of the most productive breeding sites along the central California coast, while breeding success has often declined at natural beach breeding sites (U.S. Fish and Wildlife Service 2001). Like the California least tern, the western snowy plover has adapted to exploit the artificial playa-like habitats provided by dry beds of solar salt evaporation ponds and bare, linear levees. The natural analogues of these habitats in San Francisco Bay were extensive sand and shell spits, and natural salt ponds, primarily in the Berkeley-Oakland-Alameda shoreline. These were largely destroyed by urban and port development early in the State's history, (1850s to 1870s) prior to local breeding records for the species. Almost all of the Estuary's breeding colonies are in the South Bay. The San Francisco Bay population typically ranges around 200 to 300 adult birds. The subspecies is protected under the Migratory Birds Treaty Act and is Federally listed as threatened, but is not currently State-listed.

Western snowy plovers feed on insects and other small invertebrates found in sand or firm mud, edges of saline waters, decomposing algal mats or around moist, rich organic debris. In San Francisco Bay, they feed in salt ponds, levees, and sand flats at low tide. Brine flies are an important component of their diets in salt pond beds and levees. Like California least terns, they nest in small scrapes on relatively barren or very sparsely covered (debris, low vegetation) surfaces, preferring light-colored surfaces which mask their pale tan-gray backs. They are vulnerable to nest predators, including mammals (Norway rat, red fox, skunk, raccoon) and birds (ravens, falcons, hawks, gulls).

Salt Marsh Common Yellowthroat (Geothlypis trichis sinuosa). The common yellowthroat (Geothlypis trichis) is a small warbler with a complex of subspecies. The salt marsh subspecies (G. t. sinuosa) is recognized as a distinct breeding population, with geographic distribution, habitats, and morphological traits that subtly grade into some other subspecies. It inhabits tidal salt and brackish marshes in winter, but breeds in freshwater to brackish marshes and riparian woodlands during spring to early summer. Common yellowthroats feed on insects gleaned from vegetation or the ground. Salt marsh common yellowthroats occur in estuarine marshes along the coast from Tomales Bay to Santa Cruz, but the San Francisco Estuary represents the largest area of suitable tidal marsh habitat (Terrill 2000). Recent re-estimates of population size in the Estuary's tidal marshes (Nur et al. 1997) have been higher than those of the 1970s (Terrill 2000). The subspecies is a Federal and State "species of concern" due to major decline of both habitat and populations in the past decade, but is not currently listed as endangered or threatened.  The common yellowthroat is protected under the Migratory Birds Treaty Act.

Tidal Marsh Subspecies of Song Sparrows (Melospiza melodia)

                        San Pablo Bay song sparrow (M. m. samuelis)

                        Suisun song sparrow (M. m. maxillaris)

                        Alameda song sparrow (M. m. pusillula)

Song sparrows are wide-ranging North American perching birds that inhabit a wide range of habitats. Local populations with distinct geographic and ecological affinities have evolved in the San Francisco Estuary, and are treated as subspecies. Each has undergone major declines in tidal marsh habitats, and proportionate declines in populations. The distribution of the region's three tidal marsh subspecies roughly correspond to San Pablo Bay, Suisun Bay area marshes, and San Francisco Bay. The tidal marsh song sparrow subspecies hold territories in tidal marshes all year, and breed in tidal marshes. They nest in areas of tall, emergent marsh vegetation above ordinary high tides especially in high marsh above tidal creek banks. They feed widely in the tidal marsh, gleaning insects off of vegetation. Within tidal marshes, San Pablo Bay song sparrows favor complex tidal marsh topography formed by marsh plains with dense networks of irregular tidal channels; they avoid homogeneous cordgrass. This habitat preference also applies to San Francisco song sparrows. Their territories follow configurations of tidal channels rather closely (Cogswell 2000). Suisun song sparrows nest in tall tules with local pickleweed. They also frequent tall vegetation along the edges of tidal marshes. Song sparrows are protected under the Migratory Birds Treaty Act. The subspecies are Federal and State "species" of concern, but are not currently listed as endangered or threatened.

Salt Marsh Harvest Mouse (Reithrodontomys raviventris)

Southern subspecies (R. r. raviventris)

Northern subspecies (R. r. halicoetes)

The salt marsh harvest mouse is a small mammal that inhabits salt marshes and brackish marshes only in the San Francisco Estuary. Its ecological distribution is closely (but not always exclusively) associated with vegetation including pickleweed, and its abundance often corresponds with the thickness, height, and continuity of pickleweed cover. It has two ecologically similar but distinct subspecies, one in the South Bay (the most critically endangered populations) and a more widespread and frequent subspecies in the North Bay and Suisun Bay marshes. Both subspecies are Federally and State-listed as endangered.

Though the salt marsh harvest mouse is adapted to tidal salt marshes, the young, small, isolated remnant tidal marshes of the South Bay are often deficient or lacking in salt marsh harvest mouse populations. This may be due to immature marsh topography and elevation, especially lack of well-distributed high marsh topography and vegetation cover, making the populations vulnerable to catastrophic flooding (drowning and excessive exposure to birds of prey) during extreme high tides that submerge the tidal marsh. Many of the largest South Bay populations occur in diked nontidal salt marsh, or diked marshes with limited tidal flows choked by tidegates. Salt marsh harvest mice are seldom if ever found in cordgrass marsh. They chiefly depend on pickleweed, plants associated with pickleweed, and green terrestrial grasses adjacent to tidal marshes, to which they disperse in spring. Environmental factors which constrict the development of tall, thick growth of salt marsh or brackish marsh above the cordgrass vegetation zone, or limit the development of high tide escape cover, are detrimental to conservation of the species. Prolonged, deep submergence of marsh vegetation at any time of the year is detrimental to the stability of their populations, particularly in smaller salt marsh patches (Shellhammer 2000a, U.S. Fish and Wildlife Service 1984).

Tidal Marsh Shrews (Sorex species). The salt marsh wandering shrew (Sorex vagrans halicoetes) and Suisun shrew (Sorex ornatus sinuosis) are small carnivorous mammals with high demand for abundant prey with high nutritional and energy value, including insects, amphipods (beachhoppers), isopods, and other small invertebrates. Unlike the salt marsh harvest mouse, they do not adapt well to diked non-tidal salt marshes, which are seasonally dry, or to upland grasslands. They tend to occur mostly in low, dense vegetation and under mats of tidal debris in tidal marsh plains. Like the salt marsh harvest mouse and other small mammals, they also depend on the availability of adequate cover during extreme high tides, which submerge vegetation cover and expose them to predators. Wandering shrews and ornate shrews are taxonomically difficult, and local distinct marsh populations or subspecies may intergrade with more widespread types within their species. Currently, the salt marsh wandering shrew is geographically limited to the South Bay. The Suisun ornate shrew occurs in the North Bay and Suisun Marsh (Shellhammer 2000b, MacKay 2000). Though rare and dependent on highly reduced habitat, they do not currently have protected status under State or Federal endangered species laws. The subspecies are Federal and State "species of concern."

California Red-Legged Frog (Rana aurora draytonii). California red-legged frogs are formerly widespread amphibians native to freshwater marsh habitats, subsaline coastal lagoons (stream-mouth estuaries periodically impounded by beach ridges), creeks and riparian habitats, and seasonal ponds. In modern landscapes, their habitats include man-made seasonal wetlands such as stock ponds and ditches. Their limited salt tolerance (around 4 parts per thousand salinity, lower than most of Suisun Marsh in summer) restricts them to wetlands landward and peripheral to tidal marshes in modern San Francisco Bay. They require standing water for breeding, but disperse widely in uplands during summer, remaining inactive in small mammal burrows. They periodically return to freshwater refuges to rehydrate, but they can remain inactive in upland burrows for many weeks. The subspecies is Federally listed as threatened, but is currently not State-listed.

San Francisco Garter Snake (Thanophilis sirtalis tetrataenia). Like the California red-legged frog, the San Francisco garter snake inhabits freshwater marshes, riparian habitats, and seasonally disperses to burrows in uplands. One of the largest remaining populations occurs in a freshwater to subsaline non-tidal marsh west of Highway 101, across from the San Francisco International Airport. It is not reported from tidal marsh habitats, but channelized freshwater drainages (flood control channels) along the northern San Francisco Peninsula could provide potential linkages between suitable habitat and tidal marshes, but it has not been detected in creeks discharging to the Bay (Jennings 2000). The subspecies is Federally and State-listed as endangered.

Harbor Seal (Phoca vitulina richardi), San Francisco Estuary Resident Populations. Harbor seals are permanent residents of San Francisco Bay and San Pablo Bay. Harbor seals, like all mammals, are protected by the Federal Marine Mammal Protection Act, but they are not listed as endangered or threatened under the Endangered Species Act. They feed on fish in deepwater habitats (channels, open bay), but use emergent shores as "haul-outs," where they come ashore to rest, and also to pup (give birth to offspring). Several haul-out sites in the Estuary occur on high tidal marshes, such as Tubbs Island/Midshipman's Point, and Dumbarton Point, and other areas of Newark Slough, Mowry Slough, and Calaveras Point. Haul-outs are necessarily directly connected to deepwater habitats, have gently sloping terrain, and must be free from human disturbances from boats or land (Lidicker and Ainley 2000, Allen et al. 1984). Seals trample and wallow vegetation to sparse, low mats. They do not access haul-outs through wide, dense, tall cordgrass marshes.

Southern Sea Otter (Enhydra lutris nereis). The historic range of the sea otter extended from Baja California to the Aleutian islands. The species has been fragmented to two isolated population segments by historic hunting, which nearly drove the species to extinction. Sea otters were formerly abundant in San Francisco Bay, which presumably provided rich feeding areas. They feed on bivalves, abalone, urchins, crustaceans, cephalapods (squid relatives) and fish. Along the central California coast, sea otters are established from Point Sur to Pacifica, San Mateo County. Vagrant sea otters are periodically reported in San Francisco Bay (Ainley and Jones 2000). The nearest estuary that supports sea otters is Elkhorn Slough, a historically brackish semi-tidal lagoon and marsh forced to full marine tidal influence by jetties at Moss Landing. Shallow intertidal habitats in San Francisco Bay, which could potentially support recovery and re-establishment of sea otters in San Francisco Bay are subject to invasion by Atlantic smooth cordgrass. Estuarine habitat of sea otters in Elkhorn Slough is also potentially vulnerable to spread of Atlantic smooth cordgrass from San Francisco Bay. The southern sea otter is Federally and State-listed as endangered.

Tiger beetles (Cicindela senilis senilis, C. oregona, C. haemorrhagica). Insects of San Francisco Estuary tidal habitats are very poorly understood in terms of both taxonomy (biological diversity of species) and their ecological interactions within estuarine communities. They also are sensitive to changes in tidal marsh habitats. Several species of tiger beetle (Cicindela spp.), large insects with large eyes and toothed, conspicuous mandibles, have become rare (or sub-regionally extinct) in the San Francisco Estuary. C. haemorrhagica and C. oregona are associated with maritime and estuarine beaches. C. senilis senilis is found on high channel banks, levees, and salt pond margins today, and were probably historically dependent on natural habitats between the edges of tidal marsh and large pans (Maffei 2000). Alluvial fans and sandy deltas, now largely eliminated from the urbanized edges of the Estuary, may have been potential habitat as well.

Winter- and Spring-Run Chinook Salmon (Onchorhyncus tschawytscha). Chinook salmon populations native to the Sacramento-San Joaquin river systems are segregated into distinct populations, reproductively isolated by different migration times. The winter-run and spring-run Chinook salmon migrate upstream from the sea to spawn in gravel beds of freshwater streams in winter and spring. The winter-run and spring-run populations have been Federally listed as endangered. Loss and degradation of spawning habitat, mass entrainment of young in water diversions, and reduced delta outflows (also due to water diversions) are among the leading threats to the survival and recovery of the species. Smolts (juvenile salmon spawned upstream) move through the Estuary to feed in shallow water habitats, including salt marsh channels and submerged tidal mudflats. Adults also pass through the Estuary during seasonal migrations upstream, and forage in both intertidal and subtidal habitats. They feed primarily on invertebrates and small fish. National Marine Fisheries Service has designated all tidal waters of the San Francisco Estuary as critical habitat for winter-run Chinook salmon. Tidal marsh and other estuarine habitats are reported to have an important role in Chinook salmon life-history. Tidal marshes are important habitats for small juveniles (fry), while older smolts tend to use deeper waters. Fry tend to occur near the shelter of submerged channel bank or marsh edge vegetation at high tide, and retreat with submerged habitat as the tide falls (Maragni 2000, U.S. Fish and Wildlife Service 1996)

Steelhead (Onchorhyncus mykiss irideus). Steelhead are trout species in the same genus as salmon, and they have life-histories essentially like those of Chinook salmon. Steelhead in the San Francisco Estuary are among the populations Federally listed as threatened. Adults and juveniles pass through the Estuary and feed in subtidal and intertidal habitats, including tidal marsh channels and submerged mudflats, as they migrate upstream to freshwater streams or downstream to marine habitats. Steelhead are drift-feeders, consuming a wide range of aquatic invertebrates and small fish. Adult steelhead migrating upstream seldom feed. Small steelhead runs occur in South Bay tributaries (e.g. San Francisquito Creek, Guadalupe River, Alameda Creek), and in many creeks and rivers of the North Bay and Suisun Bay areas. The importance of tidal creeks and other transient estuarine habitats for steelhead is not well understood (Maragni 2000).

Delta Smelt (Hypomesus transpacificus). Delta smelt are small, short-lived estuarine fish that migrate between shallow freshwater stream habitats in which they spawn, and brackish reaches of the San Francisco Estuary. Delta smelt also spawn at the terminal ends of tidal creeks in fresh-brackish tidal marshes. Downstream habitat is primarily limited to intertidal and subtidal habitats of Suisun Bay and its tidal marshes, but they occur also in San Pablo Bay, particularly during and after heavy freshwater flows. They may persist in tributaries of San Pablo Bay during periods of reduced salinity. They generally are limited to estuarine salinity below 10 to 14 parts per thousand, and are usually found in tidewater salinity 2 parts per thousand or less. Their abundance in the Estuary is variable, and appears to be related to both Delta outflows and food supplied by plankton production. The species is Federally and State-listed as threatened.

Sacramento Splittail (Pogonichthys macrolepidotus). Sacramento splittail is the only species in a unique genus of large, native minnows. It inhabits the Sacramento-San Joaquin river system and the Delta, including the brackish northern reaches of the San Francisco Estuary. The species has been collected in tidal waters as salty as 18 parts per thousand salinity, but splittail abundance is greatest in salinity lower than 10 parts per thousand. Within the Estuary, it occurs primarily in the Suisun Bay area, but reaches northern San Pablo Bay regularly in years of high river discharge. Sacramento splittail have been very rarely collected in San Francisco Bay. They spawn in fresh or nearly fresh, nonsaline shallow waters with submerged vegetation. Within the Estuary, they are reported to be most abundant in small tidal creeks, particularly those with freshwater discharges or partially submerged marsh vegetation (Sommer 2000). The species is Federally and State-listed as threatened.

Tidewater Goby (Eucyclogobius newberryi). Tidewater gobies are rare, small estuarine fish related to sculpin. The species is Federally listed as endangered. Tidewater gobies primarily inhabit coastal stream mouths, which become intermittent lagoons dammed by beach ridges, impounding brackish waters. The tidewater goby's historic geographic range is from Humboldt County to southern California, including San Francisco Bay. They also occur in subtidal brackish estuarine habitats, but little survey information is available from San Francisco Bay. The few historic records from San Francisco Bay are old; no populations have recently been confirmed. Former collection sites include Berkeley Aquatic Park (1950). Greater predation in large estuaries, compared with intermittent habitat of coastal lagoons, may limit them in San Francisco Bay (Swift et al. 1989, U.S. Fish and Wildlife Service 1994). The species is Federally listed as endangered, but northern and central coast populations have been proposed for delisting (U.S. Fish and Wildlife Service 1999).

California Sea-Blite (Suaeda californica). California sea-blite is a low, sprawling, fleshy gray-green shrub related to pickleweed. This Federally endangered plant was historically native only to San Francisco Bay and Morro Bay (San Luis Obispo Co.). Habitat of California sea-blite is restricted to the upper edges of tidal marshes or bay shorelines, generally in coarse, well-drained substrate such as sand, sandstone, or shell fragments. Historic records of California sea-blite in San Francisco Bay are known from Richmond, Berkeley, Oakland, Alameda, San Francisco, South San Francisco, and Palo Alto, all locations of historic sand or shell beaches with adjacent salt marsh. The original native San Francisco Bay population of California sea-blite became completely extinct some time around or after 1960. A pilot project to re-establish a colony propagated from Morro Bay stock was initiated at a constructed tidal marsh in the Presidio of San Francisco in 1999. The recovery of this species in San Francisco Bay would depend on maintenance and restoration of estuarine sand beaches with salt marsh transition zones, a habitat threatened by Atlantic smooth cordgrass invasion. Beach-salt marsh transition zones are also a prime habitat for Spartina patens in its native range. The species is Federally listed as endangered, but is not State-listed.

Suisun Thistle (Cirsium hydrophilum var. hydrophilum). Suisun thistle is among the rarest and most endangered plants in the San Francisco Estuary. Suisun thistle is a stout, tall short-lived perennial thistle, superficially resembling the weedy European bull thistle. It grows along tidal creek banks and high brackish marsh plains at very few locations in very old tidal marshes around upper Suisun Slough, near Rush Ranch and Peytonia Slough. It was historically reported only from Suisun Marsh, where it was formerly associated with Bolander's water-hemlock, once a common and conspicuous plant there. In addition to loss of nearly its entire original tidal marsh habitat, its survival is threatened by many biological and physical changes in Suisun Marsh, including an introduced weevil that feeds on its seedheads, an aggressive brackish marsh weed (Lepidium latifolium), and large-scale hydrologic manipulations aimed at salinity control for non-tidal waterfowl pond management (SEW 1998, Baye et al. 2000). The last remaining habitat for this species is within the potential invasion range of Spartina patens (well-established at Southhampton Marsh, the western extreme of Suisun Marsh), Chilean cordgrass and Atlantic smooth cordgrass. This variety is Federally and State-listed as endangered.

Soft Bird's-Beak (Cordylanthus mollis ssp. mollis). Soft bird's-beak is an annual herb with creamy-yellow flowers and glistening glandular hairs on its foliage that exude salt. It is native only to the tidal marshes around Suisun Bay and northern San Pablo Bay. Its historic range was very similar to its modern range, but its abundance has declined severely with the loss of its essential tidal marsh habitat. It occurs in both salt marsh and brackish marsh, but the vast majority of populations recorded are in brackish high marsh habitats, where it typically occurs in mixtures of pickleweed and other associated salt marsh herbs, including edges of pans, terrestrial ecotones, and tidal creek bank edges (Rugyt 1994). At Southhampton Marsh, Benicia, one colony is being encroached by Spartina patens and the highly invasive perennial pepperweed (Lepidium latifolium). At Point Pinole, the locations of former colonies have been colonized by Spartina densiflora. Most of the species' ecological and geographic range is within the potential range of the aggressive Atlantic smooth cordgrass hybrid swarm. The subspecies is both Federally and State-listed as endangered.

Northern Salt Marsh Bird's-Beak (Cordylanthus maritimus ssp. palustris). Northern (or Point Reyes) salt marsh bird's-beak is a low annual herb of the high salt marsh, typically in low or sparse vegetation or the edges of pans. In the San Francisco Estuary, it has showy rosy-pink flowers and purplish gray-green foliage bearing salt crystals, exuded from specialized glands. It occurs in tidal salt marshes from southern Oregon to San Francisco Bay. It has been locally extinct south of the Golden Gate in San Francisco Bay for many decades, where it was formerly widespread and abundant as far south as Alviso. A few populations remain only in salt marshes of the Estuary's Marin shores (northern Sausalito, Mill Valley, Greenbrae, Bucks Landing [Gallinas Creek], and the Petaluma Marsh). Marin County (Creekside Park, Corte Madera) is the center of spread of Spartina densiflora, and the point of introduction of English cordgrass. Large populations of northern salt marsh bird's-beak occur in west Marin's maritime salt marshes (Bolinas Lagoon, Point Reyes, and Tomales Bay), many appearing distinct from San Francisco Bay types. Most of the subspecies' ecological and geographic range is within the potential invasion range of all non-native cordgrasses of the San Francisco Estuary. It is closely related and difficult to distinguish in most respects from the Federally listed southern salt marsh bird's-beak (C. maritimus ssp. maritimus), which ranges from Morro Bay to Baja California. The northern subspecies is treated as a species of concern, but has no special legal status.

Pacific or California Cordgrass (Spartina foliosa). Pacific cordgrass is the Pacific Coast's ecological equivalent of Atlantic smooth cordgrass, and its close relative. It is the sole historic dominant low salt marsh species from Bodega Bay to Baja California. Though common, the recent discovery of strong and rapid genetic assimilation by Atlantic smooth cordgrass indicates a high risk that this species may become extinct in San Francisco Bay, and eventually throughout its range as the Atlantic smooth cordgrass hybrid swarm disperses and fills out its potential niche in the California coast. It was recently discovered that the overwhelming fertility and abundance of Atlantic smooth cordgrass pollen was causing Pacific cordgrass to reproduce only hybrids, rather than its own species, in the presence of Atlantic smooth cordgrass. Prior to this discovery, Pacific cordgrass was not considered a species of concern (Antilla et al. 1999, Ayres et al. 2001); now it is believed that the species is in danger of extinction. Previously, competition alone was the main threat to this species, which allowed for the possibility of persistent co-existence with Atlantic smooth cordgrass rather than a genetic "winner-take-all" outcome of hybridization between species (Strong and Daehler 1994). The species is not currently Federally or State-listed as endangered or threatened, but is under evaluation because of the rapidly changing genetic threat to the species.

Bolander's Spotted Water-Hemlock (Cicuta maculata var. bolanderi). Bolander's spotted water-hemlock is a very rare perennial herb resembling parsnips, closely related to the wider-ranging spotted water-hemlock (C. maculata var. maculata). Historically "conspicuous and abundant" in Suisun Marsh (Greene 1894), it occurs in small, rare populations there today, mostly along banks of tidal creeks (B. Grewell, unpubl. data). It was associated with the Suisun thistle (Greene 1894). Its extreme decline was only recently recognized. Most of the threats that affect Suisun thistle also affect this plant. The variety is not currently Federally or State-listed, but is under evaluation because of its apparent extreme rarity and habitat decline.

Mason's Lilaeopsis (Lilaeopsis masonii). Mason's lilaeopsis is a creeping, mat-forming perennial herb with a grass-like appearance. It grows among low, turfy vegetation along eroding marsh banks at the edges of tidal channels or bay-edge marshes, often in peaty marsh soil, or thin sediment deposits. It occurs in scattered populations in the San Francisco Estuary from lower Tubbs Island (Sonoma County) through Suisun Bay and the Delta. Wave-trimming and channel bank erosion are important factors that maintain its dynamic, unstable habitat in some locations. Chilean cordgrass aggressively colonized analogous habitat at Point Pinole, San Pablo Bay, and Atlantic smooth cordgrass has established below wave-cut marsh scarps and eroding channel banks, promoting stabilization and dense cover of vegetation. The species is classified as rare by the State, but is not Federally or State-listed as endangered or threatened.

Salt Marsh Owl's-Clover (Castilleja ambigua, affinity with ssp. ambigua). Salt marsh owl's-clover is an annual herb with showy tubular, pouched flowers, related to bird's-beak. Historically widespread in tidal marshes of the San Francisco Estuary, it is now restricted to salt marsh edges of Point Pinole, near an arrested invasion of Spartina densiflora. Typical C. ambigua ssp. ambigua, or johnny-nip, is widespread in coastal grasslands of California and Oregon. The distinctive San Francisco Bay population contains mostly purple-tinged plants and flowers which do not match the diagnostic description for the subspecies C. ambigua ssp. ambigua, and appear distinct from typical yellow-white flowered upland grassland forms of that subspecies in the region. The San Francisco Bay population has no protective legal status.

Other Declining High Marsh Plant Species of Concern. A large number of tidal marsh plants which were historically widespread or at least locally abundant have become either regionally uncommon, rare or locally extinct. Most occur in the high marsh zone, which has been compressed by steep levee slopes in most of the San Francisco Estuary. Some are perennial species that may be mistaken for more widespread species with similar appearance, and others are ephemeral spring annuals that are readily identified during brief flowering periods. Examples include Suisun aster (Aster lentus), California saltbush (Atriplex californica), centaury (Centaurium trichanthum), downingia (Downingia pulchella), smooth goldfields (Lasthenia glabrata ssp. glabrata), maritime spikeweed (Hemizonia pungens ssp. maritima) and numerous others (Baye et al. 2000). The high marsh zone is subject to periodic storm deposition of tidal litter, which smothers vegetation and creates openings favorable to establishment of some species. Extreme drift-line deposits, however, can accumulate as persistent wracks along steep levees and destroy most high marsh vegetation. This occurs along segments of southern Hayward shoreline where Atlantic smooth cordgrass litter is produced in abundance.

3.3.2 Analysis of Potential Effects on Biological Resources

The impacts evaluation is divided into three parts: First, the criteria used to determine the significance of the project effects on biological resources are described. Then a general discussion of the impacts of the various treatment methods is presented; this discussion is followed by specific enumerated project impacts and mitigation measures. Potential effects and mitigation measures are summarized in Table 3.3-1 and Table 3.3-2, respectively.

Significance Criteria

The thresholds for "significance" of impacts to biological resources are based in part on specific regulatory standards from relevant environmental laws or regional plans, and on interpretation of the general biological context and intensity of effects within the ecosystem.

The principal environmental laws pertinent to evaluation of the level of significance to environmental impacts in the San Francisco Estuary include the California Environmental Quality Act (CEQA), the Clean Water Act (CWA, including specific guidance on evaluation of impacts to wetlands and other special aquatic habitats), the California and Federal Endangered Species Acts (CESA, ESA), and Migratory Bird Treaty Act. Other State government agency plans and laws which apply to the quality of habitats in the San Francisco Estuary include the California Fish and Game Code, the McAteer-Petris Act and San Francisco Bay Conservation and Development Commission's Bay Plan (BCDC Bay Plan), the Suisun Marsh Preservation Act, the Porter-Cologne Act and the San Francisco Regional Water Quality Control Board's Basin Plan for San Francisco Bay. The endangered species recovery plans for the California clapper rail and salt marsh harvest mouse, and native fish of the Sacramento-San Joaquin Delta (U.S. Fish and Wildlife Service 1984, 1996) and the multi-agency Baylands Ecosystem Regional Habitat Goals Project (Goals Project 1999) are also important plans specific to habitats and species of the San Francisco Estuary. All of these laws, regulations, and plans recognize the ecological importance of intertidal mudflats, and estuarine salt and brackish marshes, and estuarine fish habitats.

CEQA includes the following mandatory findings of "significance" for biological resources if the project would:

•       Substantially reduce the habitat of a fish or wildlife species;

•       Cause a fish or wildlife species to drop below self-sustaining levels;

•       Threaten to eliminate a plant or animal community; or

•       Reduce the number or restrict the range of an endangered or threatened species.

CEQA also requires consideration of the project's compliance with local, State, or Federal policies or plans for the protection of sensitive species or habitats. These include Habitat Conservation Plans, Natural Community Conservation Plans, Section 404 of the Federal Clean Water Act, the Migratory Bird Treaty Act, the Bald Eagle Protection Act, and local regulations such as Creek Protection Ordinances.

The Clean Water Act's section 404(b)(1) guidelines for evaluation of discharges of dredged or fill materials (one incidental aspect of numerous proposed activities considered in this EIS/R) provide specific guidance for evaluating significant impacts to special aquatic sites, including wetlands in Subpart H. These include factors that cause or contribute to "significant degradation of the Waters of the United States," with emphasis on the persistence and permanence of effects. Determinations essential to determination of "significant degradation" must include:

•       Recolonization of indigenous organisms;

•       Wildlife and wildlife habitat (reproduction, food supply, cover, resting areas, nurseries, etc.)

•       Threatened and endangered species, and their habitats (reproduction, food supply, cover, resting areas, nurseries, etc.)

•       Proliferation of undesirable competitive species

•       Wetlands and mudflats, and vegetated shallows

The baseline, for determination of a significant impact is the existing San Francisco Estuary ecosystem. The "existing conditions" of an ecosystem are not static, but involve dynamic changes in the status and trends that are reasonably foreseeable over an ecologically meaningful timeframe. As described earlier in this section, a 1-2 year period is the short-term timeframe, a 5-10 year period is the intermediate time frame, and a 50-year period is used as the long-term timeframe for ecological evaluations.

Therefore, for the purposes of the following evaluation, biological effects are considered "significant" within an appropriate time-frame and ecological context if they cause relatively high magnitude, persistent, or permanent changes in the following factors, compared with a dynamic environmental baseline rooted in existing conditions:

•       Substantially reduce the population size, distribution, viability, or recovery potential of a rare, threatened, or endangered species, or species of concern;

•       Changes in the population size, distribution, viability, or resilience of a native fish, wildlife, or plant species;

•       Changes in the range, patterns, or fluctuation (dynamics) of physical or chemical attributes of physical estuarine habitats (tidal waters or substrates).

•       Changes in stability or structure of estuarine habitats.

•       Conflicts with local, State, or Federal biological resource protection plans, policies, and regulations.

Variables Affecting Biological Predictions and Analyses

Major variables affecting the long-term maturation of tidal marshes cannot be determined with high confidence. Future rates of sea-level rise, future sediment budgets, and complex interactions between new dominant invader plant species in new physical estuarine conditions are examples of such variables. The closest comparable cordgrass invasion, the more advanced spread of Atlantic smooth cordgrass in Willapa Bay, Washington, occurs in a different tidal marsh plant community and estuarine setting, one without any native cordgrass species or currently listed endangered resident marsh plants, fish, and wildlife. The future consequences of continued spread or eradication of invasive cordgrass in San Francisco Bay can be inferred by comparing San Francisco Estuary marshes with native marshes of the four introduced cordgrass species and with other estuaries that have already been colonized by these cordgrasses. Biological impacts of non-native cordgrass eradication efforts have been assessed in many other estuaries, and provide a range of analogous environments to help evaluate conditions in the San Francisco Estuary.

Another indeterminate aspect of predicting ecological outcomes of the Invasive Spartina Project is its nature as a regional coordination program, rather than a single site-specific project with specifically defined project logistics (time, methods, location, etc.). The following evaluation of biological impacts addresses the broader regional scope of potential effects and mitigation for adverse impacts to biological resources. Ecological evaluations consider various contingencies to cover the range of eradication methods that would be most applicable to a given type of impact. These address different types of local environments (mudflats, mature marshes with creek systems, simple young marsh strips, beaches, etc.) and different methods of removal (mechanical excavation or dredging; cropping methods such as repeated mowing or disking; methods which leave a matrix of killed roots and rhizomes physically in place, such as herbicides, drowning, or smothering; etc.). Evaluations emphasize biological resource issues that are likely to apply generally to many or most potential projects, as well as issues that can be addressed only at larger regional scales, beyond individual projects.

General Impacts of Proposed Treatment Methods

The following overview of cordgrass control methods and materials (the Spartina control "toolbox") emphasizes some of the operational, physical, and physiological aspects of eradication work that is particularly relevant to interpretation of biological impacts to species and communities affected.

Amphibious Vehicles and Equipment. Various eradication methods depend on use of vehicles designed to operate in semi-aquatic environments. Some support equipment or attachments for mowing vegetation, ripping and shredding vegetation and substrate, or excavation of marsh substrate. Amphibious vehicles are usually designed to operate with low ground pressure, distributing weight on specialized tracks or tires. All amphibious vehicles, however, crush and cause dieback of marsh vegetation, particularly sub-shrubby vegetation with brittle stems. The amount of vegetation dieback often depends on the number of vehicle passes, the shear strength of the substrate, and the season. Vehicles passing over brittle vegetation in summer tend to cause the most dieback. Soft sediment, which causes ruts or depressions, or shearing of sediment below tires or tracks, often magnifies the impact of vehicle passes on marsh vegetation. Insects, benthic invertebrates, and small mammals have a definite but unquantified risk of being crushed by vehicles. Marsh-nesting birds may be disturbed by vehicles, and abandon territories or home ranges to less suitable (and competitive) locations. Nests may be destroyed inadvertently by marsh vehicles. The insufficiently surveyed populations of rare plants, including dormant seed banks or bud banks, are also subject to destruction by mobilization of marsh vehicles.

The pattern of invasive vegetation colonies in the marsh or mudflat determines the potential for unavoidable track disturbance if vehicles are used. Also important is the location of potential entry points to the marsh. Marsh entry points that are close to both target colonies and to maintenance or access roads on the land or levee side help to avoid excess vehicle track formation. This is not always the case for larger marshes far from roads or levees.

Vehicles working in unpredictable patterns of soft marsh substrates with many small tidal creeks run the risk of becoming stuck or mired. This would necessitate the entry of additional equipment to remove stuck vehicles. Such operations cause substantial local marsh disturbance, and may require additional rehabilitation or marsh restoration.

Vehicles working in marshes are seldom if ever refueled in the marsh itself. Such refueling would result in risks of fuel spills. Floating barge-mounted equipment, in contrast, is more likely to require refueling while working in sloughs.

"Mats," large wooden blocks placed over tough geotextile fabric to distribute the weight of equipment and protect underlying marsh vegetation, are sometimes used in conjunction with heavy equipment in tidal marshes. Mats limit the mobility of equipment to work in a few areas. They reduce, but do not eliminate, damage to marsh vegetation.

Small vehicles are routinely used in tidal marshes of the San Francisco Estuary for monitoring and treating production of mosquitoes. They leave both temporary and persistent tracks, depending on frequency of use. Most vehicle access to tidal marshes in the region is limited to restoration or enhancement of tidal creeks or ditches (improvement of tidal circulation), debris removal, and eradication.

Mechanical Disturbance of Substrates. Some eradication methods involve destabilizing the surface substrates of tidal marshes and mudflats in the course of removing or damaging both above-ground and below-ground parts of invasive cordgrasses. In mudflats, removal of stabilizing root and rhizome systems re-exposes the mudflats to normal patterns of erosion and redeposition by waves and tidal currents. Exposure of deeper, coal-black anoxic (oxygen-starved) muds causes rapid oxidation of chemically reduced substances such as iron sulfide and hydrogen sulfide. In contrast with dredging that occurs in subtidal, deepwater environments, excavation, dredging or similar actions applied to cordgrass necessarily occur in intertidal environments, and generally while exposed to air. Plumes of turbid water or blackened, anoxic suspended sediments in the water column, associated with excavation disturbances under water, are not aspects of upper and middle intertidal disturbances during low tide. If dredging of cordgrass were conducted at high tide when the bottom is shallowly submerged, general immediate impacts would be intermediate between those typical of navigational dredging and intertidal excavation.

Dredging or excavation of anaerobic bay mud may expose buried sediments with higher levels of mercury, or more biologically available forms of it. Mercury is a heavy metal present in bay muds from natural and artificial sources, and background levels in San Francisco Bay are very high compared with most estuaries nationally. Biological activity of mercury is dependent in part on microbial transformation of mineral forms of mercury to organic forms, principally methylmercury. Mercury in organic materials can be ingested by benthic organisms, which in turn, may be consumed by fish, birds, and mammals, and can thereby bioaccumulate in higher organisms in the food chain.

The irregular, rough topography left by mechanical disturbances to soft sediments is subject to brief increases in erosion until it is planed off by wave action. Both mudflats and prevailing benthic infauna are adapted to mobility of the upper few centimeters of the mudflat surface, and regularly move and resettle as sediment is lifted by wave erosion and redeposited. Depressions in exposed mudflats caused by natural bioturbation, such as foraging by bat rays, tend to be ephemeral. Any shallowly buried substances, whether natural biogeochemical products (like toxic sulfides) or artificial contaminants, would be remobilized and dispersed following excavation, digging, or other mechanical disturbance of the substrate.

Dislodged or cut plant material (stems, rhizomes, roots, live or dead foliage) from mechanically disturbed sites is likely to redeposit at more stable positions in the Estuary than open marsh or mudflats. They typically accumulate as drift-lines or debris patches near where the contemporary high tide level is intercepted by emergent vegetation downwind. Debris also collects where coves or angles occur in the shoreline. Much above-ground biomass of cordgrass is shed in winter rather than late summer or fall. Fragments of rhizomes may remain viable in cold Bay water and cold air temperatures, but quickly lose viability if exposed to air at mild or warm temperatures, or exposed to sun. Stem fragments with viable buds may regenerate clones if they are rapidly deposited in shallow mud.

Disturbed mudflat substrates are not more likely to be recolonized by marsh vegetation or non-native invaders after disturbance. Disturbed tidal marsh vegetation and substrate, in contrast, is highly vulnerable to invasion by numerous non-native plants, which take advantage of openings in the vegetation canopy and temporary freedom from interference from established vegetation. Disturbed substrates, such as ditch spoils or recently capped levees, often become nuclei for additional invasions by multiple salt marsh weeds.

Flooding and Draining. Impounding standing water in marshes can cause significant, but reversible, changes in marsh soils. The degree to which conditions are reversible depends on the duration of the impoundment. The extensive segments of the large "strip marsh" of pickleweed along the northern edge of San Pablo Bay impounds shallow water (up to 18" deep) for months in winters of high rainfall and high tides, killing hundreds of acres of pickleweed. The marsh vegetation regenerates in years of reduced marsh flooding. Long-term, persistent impoundment, however, allows marsh organic matter to slowly decompose under extreme oxygen-deficient conditions, causing depression of the marsh surface and accumulation of toxic sulfides, which acidify the soil after marsh drainage is restored (Portnoy 1997). If cordgrass stems are mowed in winter to prevent gas transport from live or dead stems to roots and rhizomes below ground, high mortality is likely to occur by the end of the growing season following flooding treatment. Therefore, marsh impoundments used for cordgrass eradication are likely to be in place for less than one year.

When tidal marshes are diked and drained, rather than flooded, they undergo rapid physical and chemical changes. Organic matter decomposes when microbes are exposed to air; clays shrink when dewatered; and sulfides formed in oxygen-free mud transform to sulfates forming strong acids (Portnoy, 1999). Therefore, diking and draining, although conceivably effective for killing cordgrass, would adversely impact marsh soils and restoration, and the longer salt marsh soils are diked and drained the more difficult these adverse soil changes are to reverse. For these reasons, diking and draining will only be used in critical situations where no other method is feasible, and only after careful evaluation and planned mitigation. Diked salt marsh soils that remain permanently flooded undergo relatively slower and less significant changes. Diked flooded salt marshes would eliminate existing standing vegetation, but are readily re-colonized by youthful salt marsh vegetation if the diking is brief.

Low berms can be constructed by excavation equipment or "inflatable dams" used for dewatering construction sites - tubes of geotextile fabric inflated by pumping water in them. Both methods involve mobilization of equipment in the tidal marsh, which is inherently disturbing to vegetation and wildlife. Earthen berm construction requires excavation of a borrow ditch, and multiple "lifts" (layers of piled mud) to raise elevations as drained mud shrinks. Destruction of berms by backfilling the borrow ditch leaves a depression because of the shrinkage in sediment volume in drained conditions. The drained and rewetted mud also tends to become somewhat to very acidic. Inflatable dams leave less persistent impacts to marsh vegetation and topography.

Burning. Burning tidal salt marsh vegetation is difficult. Most vegetation has high water content, salt that absorbs moisture, and some have succulent stems and leaves. Fuel generally has to be added to salt marsh vegetation to ignite it. Brackish marsh vegetation, which has a higher proportion of tall, grass-like plants, is easier to burn. Burning vegetation in the Bay Area can be difficult because of air quality controls. Dikes, salt ponds, and tidal channels typical of the south San Francisco Bay provide natural firebreaks.

Glyphosate Herbicide Application. The potential biological and ecological impacts of glyphosate (the active ingredient in the two proposed herbicides, Rodeo and Aquamaster), associated surfactants (detergent-like additives that allow herbicides to penetrate plant tissues to be effective) and inert ingredients resulting from the use of herbicides are addressed below.

Literature Review. Much of the general information about physiological effects of glyphosate mixtures on animals has been assembled and reviewed by EXTOXNET (Extension Toxicology Network). EXTOXNET is an independent collaborative information project about pesticides, established by the Cooperative Extension Offices of Cornell University, Oregon State University, the University of Idaho, the University of California at Davis, and the institute for Environmental Toxicology, Michigan State University. EXTOXNET literature review and synthesis regarding biological effects of glyphosate usage is presented in Appendix E-3. EXTOXNET does not produce original research, recommendations, or conclusions about pesticides.

Disagreements occur over interpretation of scientifically peer-reviewed experimental results and field studies dealing with glyphosate and surfactants. Different results from different experimental methods and circumstances, a normal aspect of repeated scientific experimental work, also have occurred over several decades of research on glyphosate. It is possible that future research may further change prevailing scientific opinion about the toxicology and environmental fate of glyphosate mixes. To provide context for interpretation of prevailing scientific views, this EIS/R includes a critical review of the scientific literature by a pesticide reform advocacy group, NCAP (Northwest Coalition for Alternatives to Pesticides), a response to the review by the pesticide manufacturer, and a related article by a toxicologist (Appendix E-1). Like EXTOXNET, NCAP synthesizes literature rather than produce original research, but in contrast to EXTOXNET, NCAP asserts opinions about published scientifically peer-reviewed research. Neither EXTOXNET nor NCAP information and views are specifically endorsed or followed in this EIS/R. This EIS/R summarizes contemporary and comprehensive peer-reviewed scientific literature about the biological toxicity of glyphosate and surfactants approved for aquatic application.

Terminology. Direct toxicity refers to both acute and chronic toxicity that occur as a result of direct contact, or dermal exposure, with contaminated media such as water or sediment (as opposed to indirect contact, which occurs through ingestion of contaminated prey or other media). Acute toxicity refers to death of the subject organism (lethality) during short-term exposure (generally up to 96 hours). Chronic toxicity refers to sublethal adverse effects (such as disease, reduced growth, or reproduction) during long-term exposure.

Acute toxicity data are often presented in terms of an LC50, which represents the concentration of the toxin that has been found to result in lethal effects to 50% of the test organisms, or EC50, which represents the concentration that has been found to result in sub-lethal effects to 50% of the test organisms. Data can also be presented in terms of a no-observable-effect concentration (NOEC), the concentration for which no effects were observed, or lowest observable effect concentration (LOEC), the lowest concentration for which effects were observed.

Bioaccumulation is the process by which living organisms can retain and concentrate chemicals directly from their surrounding aquatic environment (i.e., from water, bioconcentration) and indirectly from sediments, soil, and food. Biomagnification is a form of bioaccumulation in which the concentration of a chemical in a higher-trophic-level organism is higher than that in the food that the organism consumes.

Conceptual Exposure Model. The known properties of the herbicides, potential methods of application, and the ecological characteristics of the Estuary were evaluated to develop a conceptual model (Figure 3.3-2) and identify likely receptors and exposure pathways. This model includes identification of primary and secondary herbicide sources, release mechanisms, exposure media, exposure routes, and potential ecological receptors.

For effects to occur, a receptor and a complete exposure pathway must be present. An exposure pathway is only considered complete when all four of the following elements are present: project- related source of a chemical, a mechanism of release of the chemical from the source to the environment, a mechanism of transport of the chemical to the ecological receptor, and a route by which the receptor is exposed to the chemical.

The exposure routes associated with the complete pathways include direct contact with the herbicide mixture during and immediately after application, ingestion of contaminated surface water and sediments, direct contact with contaminated surface water and sediments, and food-web exposure. The conceptual model (Figure 3.3-2) illustrates the links between sources, release and transport mechanisms, affected media, exposure routes, and potentially exposed ecological receptors. Although several complete exposure pathways may exist, not all pathways are comparable in magnitude or significance. The significance of a pathway as a mode of exposure depends on the identity and nature of the chemicals involved and the magnitude of the likely exposure dose. For birds and mammals, ingestion, is generally the most significant exposure pathway.

Dermal contact is expected to be insignificant and unquantifiable due to the nature of the site and frequent movement, ranging habits, and furry or feathery outer skin of most wildlife species. Inhalation may be significant during herbicide application, but is difficult to quantify for ecological receptors, and little toxicity data exists for organisms other than mammals.

Because Project applications of herbicides would occur only once or twice a year and compounds in the herbicide mixture are not expected to persist in significant concentrations for more than several hours, chronic exposure is not likely. Therefore, this evaluation focuses on acute toxicity, which would occur when the compounds are present at relatively high concentrations during and immediately following application.

Food-web exposures become significant only if chemicals with a tendency to bioaccumulate or biomagnify are present. The adverse effects associated with bioaccumulative chemicals relate to their propensity to transfer through the food web and accumulate preferentially in adipose or organ tissue. Basic routes for exposure to bioaccumulative compounds by organisms are the trans port of dissolved contaminants in water across biological membranes, and ingestion of contaminated food or sediment particles with subsequent transport across the gut. For upper-trophic-level species, ingestion of contaminated prey is the predominant route of exposure, especially for hydrophobic chemicals.

U.S. EPA's Hazardous Waste Identification Rule (USEPA 1999) identifies compounds that are recognized as having a low, medium or high potential for bioaccumulation. For bioaccumulation in aquatic systems, rankings were determined using bioaccumulation factors in fish, which are indicated in laboratory tests as having low octanol-water partitioning coefficient (or log K_ow)) values for organic compounds. Bioaccumulation potential is defined as follows:

Bioaccumulation potential	Bioaccumulation Factor (BAF)	log Kow
High	BAF >= 10,000	log Kow >= 4.0
Medium	10,000 > BAF >= 100	4.0 > log Kow >= 2.0
Low	BAF < 100	log Kow < 2.0

All reported bioaccumulation factor values for glyphosate in aquatic organisms are well below 100 (Ebasco 1993; Heyden 1991; Wang et al. 1994). The highest bioaccumulation factor of 65.5 was reported for tilapia (a species of fish) in fresh water (Wang et al. 1994). Other studies report much lower bioaccumulation factors in the range of 0.03 to 1.6 for fish (Ebasco 1993). Most studies report rapid elimination and depuration from aquatic organisms after exposure stops (Ebasco 1993). Therefore, bioaccumulation of glyphosate is considered to be low and food-web transfer is not considered to be a significant exposure route.

Chemicals of Concern. Chemicals of potential ecological concern that may be used in the herbicide mixture include glyphosate and its breakdown products; the surfactants R-11, Agri-dex, and LI 700; and the colorant Blazon. The effects of these chemicals on the biota of tidal wetlands depend on the composition of the solution and the physical, chemical, and biological fate in the environment. The chemical properties of glyphosate, surfactants, and colorants are described in Section 3.2, Water Quality. The ecotoxicological aspects are discussed in this section.

Glyphosate. Glyphosate is a non-selective herbicide (it kills all vascular plants regardless of species). Plants vary in their sensitivity to glyphosate exposure mostly by how readily it is absorbed and internally transported by plant tissues. Its action is systemic, meaning that it is transported within plant tissues from surfaces it contacts to affect remote parts of the plant, such as roots and rhizomes. Despite its high toxicity to plants, it is relatively low in toxicity to animals. This is due to its chemical nature and the physiological basis for its activity. Glyphosate is chemically similar to certain types of amino acids (components of proteins) found in plants, but not in animals. When glyphosate interacts with the physiological processes of manufacturing proteins in plants, it disrupts protein synthesis. Proteins are essential to all physiological processes in plants, and thus glyphosate exposure is generally highly lethal to plants. Glyphosate does not poison protein synthesis in animals, because it does not act as an analogue of amino acids metabolized in animals. Glyphosate has other effects on animals, however, as do many of its spray mix additives.

One ecologically significant feature of glyphosate is that it is strongly adsorbed by organic matter and fine sediment, such as clay or silt. Sediment films on plant surfaces strongly interfere with uptake and activity of glyphosate. In its chemically bound, adsorbed state, glyphosate is chemically intact, but physiologically inactive. Actual decomposition of glyphosate in the soil or sediment is distinct from its inactivation by adsorption. Glyphosate also desorbs (releases) from soil particles, but its strong affinity for fine mineral and organic particles maintains the predominantly bound, inactivated form (EXTOXNET, Ebasco 1993, Giesy 2000).

The primary breakdown product of glyphosate is aminophosphoric acid (AMPA), which is generally reported to be nontoxic to animals (EXTOXNET, Ebasco 1993). Glyphosate is decomposed by microbial activity in the soil. The reported rates of glyphosate decomposition and persistence in soil vary a great deal: most studies suggest rapid decomposition, while others detect persistence in the soil for more than a year (Ebasco 1993). Rates of decomposition by soil microbes vary with factors such as temperature, oxygen, and pH. Glyphosate may be used as a food substrate by bacteria, and can stimulate bacterial activity. It has been found to kill or inhibit the growth of some soil fungi in pure cultures, however. Little is known about how glyphosate affects the microflora in realistic soil environments, where important interactions such as soil adsorption can occur (Ebasco 1993).

Laboratory tests of glyphosate generally indicate it to be nontoxic or low in toxicity to mammals and birds, particularly at the concentrations or doses that occur in field conditions (EXTOXNET). Most information about glyphosate toxicity to mammals comes from experiments on rats, mice and rabbits, and some on dogs. Little information is available on toxicity of glyphosate or its breakdown products on most wildlife species. Toxic effects of glyphosate are usually achieved in laboratory animals at very high doses (hundreds or many thousands of times the exposure expected from concentrations and doses applied in field conditions) comparable to portions of animal diets, are often required to generate acute effects (EXTOXNET, Ebasco 1993, Giesy 2000).

Surfactants and Colorants. Three surfactants are approved for use with glyphosate in aquatic environments, and have been used to treat invasive cordgrass. They are known by trade names LI-700, Agri-dex, and R-11. Toxic effects of spray mixes of glyphosate are due primarily to surfactants rather than the active herbicide. These surfactants are non-ionic, meaning they do not dissociate into electrically charged particles in water, as salts do. They contain nonylphenol polyethoxylate (NPE) ingredients.

As described in Section 3.2, Water Quality, the Material Safety Data Sheet indicates that Blazon is non-toxic. Some additional information on surfactants and colorants is included in Section 3.2, Water Quality, and Appendix E-1 and E-2.

Toxicological Effects on Ecological Receptors. Herbicide solutions have the potential to affect organisms that live in the water column, including algae, non-target plants, fish and aquatic invertebrates. While some other receptors such as mammals and birds may spend a considerable portion of their time in the water, they are generally more likely to be affected by other exposure routes, primarily dermal contact during application and incidental ingestion of contaminated sediment during foraging.

Non-Target Aquatic Plants and Algae. Glyphosate is ineffective for treating submerged aquatic vegetation. It is likely that factors in the aquatic environment, such as suspended organic matter or sediment, interfere with glyphosate uptake by submerged plant tissues. Glyphosate also is slightly toxic or practically nontoxic to freshwater and marine algae and phytoplankton tested in both laboratory and field studies. Species of algae vary in their sensitivity to glyphosate in terms of population growth (EXTOXNET, Giesy 2000). Field studies indicate the least toxicity to phytoplankton (microscopic floating algae), possibly because of dilution and adsorption in open water and flooded marshes.

Few data are available on effects to marine algae, as most toxicity tests have been performed on freshwater species. Giesy et al. (2000) reviewed the data available on glyphosate toxicity to microorganisms, and found that acute toxicity EC50 values ranged from 2.1 to 189 mg/L. NOECs ranged from 0.73 to 33.6 mg/L. Giesy et al. (2000) also reviewed the data available on glyphosate toxicity to aquatic macrophytes, and found that acute toxicity EC₅₀ values ranged from 3.9 to 15.1 mg/L. It should be noted that these studies included tests on the (non-aquatic) Roundup formulation as well as other forms of glyphosate. The formulated product known as Roundup (glyphosate plus specific surfactants) is known to be more toxic than the (aquatic) Rodeo formulation (now called Aquamaster). For studies conducted on microorganisms using glyphosate tested as isopropylamine salt, EC₅₀ values ranged from 72.9 to 412 mg/L, and NOEC values ranged from 7.9 to 26.5 mg/L (Giesy et al. 2000). The lowest of these NOEC values (0.73 mg/L) is well above the maximum concentration of 0.026 mg/L reported by Paveglio et al. (1996) (see Section 3.2) and the immediate maximum geometric mean glyphosate concentration of 0.174 mg/L reported by Patten (2002). Therefore, these data indicate that impacts to non-target submerged aquatic plants or algae are not likely. Impacts in estuarine conditions with high concentrations of suspended sediment, which interfere with glyphosate activity, would be even less likely.

The NEPA Environmental Assessment conducted for Willapa Bay (Washington State 1997) included a review of field toxicity studies for non-target marine plants, which indicated that Rodeo tank mixes have had variable effects on non-target plants. Japanese eelgrass was adversely affected in one of two plots aerially treated with Rodeo and X-77 Spreader in Willapa Bay. Rodeo and X-77 Spreader applied by hand-held sprayer to eelgrass did not affect biomass in an eight-week study conducted in Padilla Bay.

Some adverse effects to non-target plants that are not completely submerged are likely to occur. However, these effects can be mitigated using the methods described in this section.

Aquatic and Benthic Invertebrates. Giesy et al. (2000) reviewed the data available on glyphosate toxicity to aquatic invertebrates. Few data were available for marine species, and those studies that did use marine species were conducted with glyphosate acid, not salt. Acute toxicity EC50 values for five marine species ranged from 281 mg/L to greater than 1000 mg/L, and NOEC values ranged from 10 to 1000 mg/L. Data compiled by Ebasco (1993) include mortality tests on two marine species, for which EC₅₀ values were found to be 281 mg/L and greater than 1,000 mg/L.

Grue et al. (2002) conducted laboratory studies to evaluate reproductive effects of exposure to Rodeo mixed with four different surfactants, including R-11, LI 700, and Agri-dex, on Pacific oysters. The EC50 for glyphosate alone was 68.1 mg/L, the EC₅₀ for the tank mix including Rodeo and R-11 surfactant was 29.9 mg/L, and the EC₅₀ for the R-11 surfactant alone was 1.0 mg/L.

The lowest of these NOEC and LC₅₀ values (10 mg/L) for glyphosate or glyphosate/surfactant mixtures is well above the maximum glyphosate concentration of 0.026 mg/L reported by Paveglio et al. (1996) and the immediate maximum geometric mean glyphosate concentration of 0.174 mg/L reported by Patten (2002) (see Section 3.2). Therefore, these data indicate that impacts to aquatic invertebrates due to post-application water concentrations of glyphosate are unlikely in experimental conditions. Impacts in estuarine conditions with high concentrations of suspended sediment, which interfere with glyphosate activity, would be even less likely.

Kubena et al. (1997) conducted sediment and water toxicity studies on marine invertebrates (oysters and amphipods). The LC₅₀ values for Rodeo and surfactant in water ranged from 200 to 400 mg/L, and the LC₅₀ values in sediment ranged from 1000 to 6000 mg/kg. These LC₅₀ values are well above the highest measured geometric mean sediment concentrations of 2.3 mg/L reported by Kilbride et al. (2001) and Patten (2002), as described in Section 3.2.

Field studies of glyphosate/surfactant applications to tidal mudflat invertebrate communities in Willapa Bay, Washington, agree with laboratory tests, which indicate low potential for adverse impacts to benthic invertebrates. Sampling of benthic invertebrates in mudflats up to 199 days after glyphosate/surfactant (X-77) applications revealed no short-term or long-term effects. Short-term laboratory tests of amphipods exposed to glyphosate and surfactants did not affect survival even at high concentrations relative to post-spray field conditions (Kubena 1996).

Fish. Giesy et al. (2000) reviewed the data available on glyphosate toxicity to fish. Although some data were available for anadromous species, it appears that all tests were conducted using freshwater test methods. Acute toxicity LC₅₀ values for glyphosate tested as isopropylamine salt ranged from 97 to greater than 1,000 mg/L and NOEC values ranged from <97 to 1,000 mg/L. Data compiled by Ebasco (1993) on one-day acute toxicity tests indicate EC₅₀ values ranging from 12.8 mg/L to 240 mg/L.

The lowest of these NOEC and LC₅₀ values (12.8 mg/L) for glyphosate or glyphosate/surfactant mixtures is well above the maximu