· The San Francisco Estuary can now be recognized
as the most invaded aquatic ecosystem in North America. Now recognized
in the Estuary are 212 introduced species : 69 percent of these
are invertebrates, 15 percent are fish and other vertebrates,
12 percent are vascular plants and 4 percent are protists.
· In the period since 1850, the San Francisco
Bay and Delta region has been invaded by an average of one new
species every 36 weeks. Since 1970, the rate has been at least
one new species every 24 weeks: the first collection records of
over 50 non-native species in the Estuary since 1970 thus appear
to reflect a significant new pulse of invasions.
· In addition to the 212 recognized introductions,
123 species are considered as cryptogenic (not clearly native
or introduced), and the total number of cryptogenic taxa in the
Estuary might well be twice that. Thus simply reporting the documented
introductions and assuming that all other species in a region
are nativeóas virtually all previous studies have doneóseverely
underestimates the impact of marine and aquatic invasions on a
region's biota.
· Nonindigenous aquatic animals and plants
have had a profound impact on the ecology of this region. No shallow
water habitat now remains uninvaded by exotic species and, in
some regions, it is difficult to find any native species in abundance.
In some regions of the Bay, 100% of the common species are introduced,
creating "introduced communities." In locations ranging
from freshwater sites in the Delta, through Suisun and San Pablo
Bays and the shallower parts of the Central Bay to the South Bay,
introduced species account for the majority of the species diversity.
· The major bloom-creating, dominant phytoplankton
species are cryptogenic. Because of the poor state of taxonomic
and biogeographic knowledge, it remains possible that many of
the Estuary's major primary producers that provide the phytoplankton-derived
energy for zooplankton and filter feeders, are in fact introduced.
· Introduced species are abundant and dominant
throughout the benthic and fouling communities of San Francisco
Bay. These include 10 species of introduced bivalves, most of
which are abundant to extremely abundant. Introduced filter-feeding
polychaete worms and crustaceans may occur by the thousands per
square meter. On sublittoral hard substrates, the Mediterranean
mussel Mytilus galloprovincialis is abundant,
while float fouling communities support large populations of introduced
filter feeders, including bryozoans, sponges and seasquirts. The
holistic role of the entire nonindigenous filter-feeding guildóincluding
clams, mussels, bryozoans, barnacles, seasquirts, spionid worms,
serpulid worms, sponges, hydroids, and sea anemonesóin
altering and controlling the trophic dynamics of the Bay-Delta
system remains unknown. The potential role of just one species,
the Atlantic ribbed marsh mussel Arcuatula demissa, as
a biogeochemical agent in the economy of Bay salt marshes is striking.
· Introduced clams are capable of filtering
the entire volume of the South Bay and the northern estuarine
regions (Suisun Bay) once a day: indeed, it now appears that the
primary mechanism controlling phytoplankton biomass during summer
and fall in South San Francisco Bay is "grazing" (filter
feeding) by the introduced Japanese clams Venerupis
and Musculista and the Atlantic clam Gemma. This
remarkable process has a significant impact on the standing phytoplankton
stock in the South Bay, and since this plankton is now utilized
almost entirely by introduced filter feeders, passing the energy
through a non-native benthic fraction of the biota may have fundamentally
altered the energy available for native biota
· Drought year control of phytoplankton by
introduced clamsóresulting in the failure of the summer
diatom bloom to appear in the northern reach of the Estuaryóis
a remarkable phenomenon. The introduced Atlantic soft-shell clams
(Mya) alone were estimated to be capable at times
of filtering all of the phytoplankton from the water column on
the order of once per day. Phytoplankton blooms occurred only
during higher flow years, when the populations of Mya and
other introduced benthic filter feeders retreated downstream to
saltier parts of the Estuary.
· Phytoplankton populations in the northern reaches of the Estuary may now be continuously and permanently controlled by introduced clams. Arriving by ballast water and first collected in the Estuary in 1986, by 1988 the Asian clam Potamocorbula reached and has since sustained average densities exceeding 2,000/m2. Since the appearance of Potamocorbula, the summer diatom bloom has disappeared, presumably because of increased filter feeding by this new invasion. The Potamocorbula population in the northern reaches of the Estuary can filter the entire water column over the channels more than once per day and over the shallows almost 13 times per day, a rate of filtration which exceeds the phytoplankton's specific growth rate and approaches or exceeds the bacterioplankton's specific growth rate.
· Further, the Asian clam Potamocorbula
feeds at multiple levels in the food chain, consuming bacterioplankton,
phytoplankton, and zooplankton (copepods), and so may substantially
reduce copepod populations both by depletion of the copepods'
phytoplankton food source and by direct predation. In turn, under
such conditions, the copepod-eating native opossum shrimp Neomysis
may suffer a near-complete collapse in the northern reach.
It was during one such pattern that mysid-eating juvenile striped
bass suffered their lowest recorded abundance. This example and
the linkages between introduced and native species may provide
a direct and remarkable example of the potential impact of an
introduced species on the Estuary's food webs.
· As with the guild of filter feeders, the
overall picture of the impact of introduced surface-dwelling and
shallow-burrowing grazers and deposit feeders in the Estuary is
incompletely known. The Atlantic mudsnail Ilyanassa
is likely playing a significantóif not the most importantórole
in altering the diversity, abundance, size distribution, and recruitment
of many species on the intertidal mudflats of San Francisco Bay.
· The arrival and establishment in 1989-90
of the Atlantic green crab Carcinus maenas in
San Francisco Bay signals a new level of trophic change and alteration.
The green crab is a food and habitat generalist, capable of eating
an extraordinarily wide variety of animals and plants, and capable
of inhabiting marshes, rocky substrates, and fouling communities.
European, South African, and recent Californian studies indicate
a broad and striking potential for this crab to significantly
alter the distribution, density, and abundance of prey species,
and thus to profoundly alter community structure in the Bay.
· Nearly 30 species of introduced marine,
brackish and freshwater fish are now important carnivores throughout
the Bay and Delta. Eastern and central American fish -- carp,
mosquitofish, catfish, green sunfish, bluegills, inland silverside,
largemouth and smallmouth bass, and striped bass -- are among
the most significant predators, competitors, and habitat disturbers
throughout the brackish and freshwater reaches of the Delta, with
often concomitant impacts on native fish communities. The introduced
crayfish Procambarus and Pacifastacus
may play an important role, when dense, in regulating their prey
plant and animal populations.
· Native waterfowl in the Estuary consume
some introduced aquatic plants (such as brass buttons) and native
shorebirds feed extensively on introduced benthic invertebrates.
· The Atlantic salt-marsh cordgrass Spartina
alterniflora, which has converted 100s of acres of
mudflats in Willapa Bay, Washington, into grass islands, has become
locally abundant in San Francisco Bay, and is competing with the
native cordgrass. Spartina alterniflora has broad potential
for ecosystem alteration. Its larger and more rigid stems, greater
stem density, and higher root densities may decrease habitat for
native wetland animals and infauna. Dense stands of S. alterniflora
may cause changes in sediment dynamics, decreases in benthic algal
production because of lower light levels below the cordgrass canopy,
and loss of shorebird feeding habitat through colonization of
mudflats.
· The Australian-New Zealand boring isopod Sphaeroma quoyanum creates characteristic "Sphaeroma topography" on many Bay shores, with many linear meters of fringing mud banks riddled with its half-centimeter diameter holes. This isopod may arguably play a major, if not the chief, role in erosion of intertidal soft rock terraces along the shore of San Pablo Bay, due to their boring activity that weakens the rock and facilitates its removal by wave action. Sphaeroma has been burrowing into Bay shores for over a century, and it thus may be that in certain regions the land/water margin has retreated by a distance of at least several meters due to this isopod's boring activities.
· Introduced freshwater and anadromous fish
have been directly implicated in the regional reduction and extinction,
and the global extinction, of four native California fish. The
bluegill, green sunfish, largemouth bass, striped bass, and black
bass, through predation and through competition for food and breeding
sites, have all been associated with the regional elimination
of the native Sacramento perch from the Delta. The introduced
inland silversides may be a significant predator on the larvae
and eggs of the native Delta smelt. Expansion of the introduced
smallmouth bass has been associated with the decline in the native
hardhead. Predation by largemouth bass, smallmouth black bass
and striped bass may have been a major factor in the global extinction
of the thicktail chub in California.
· The situation of the California clapper
rail may serve as a model to assess how an endangered species
may be affected by biological invasions. The rail suffers predation
by introduced Norway rats and red fox; it may both feed on and
be killed by introduced mussels; and it may find refuge in introduced
cordgrass, although this same cordgrass may compete with native
cordgrass, perhaps preferred by the rail. Other potential model
study systems include introduced crayfish and their displacement
of native crayfish; introduced gobies and their relationship to
the tidewater goby; and the combined role that introduced green
sunfish, bluegill, largemouth bass, and American bullfrog may
have played in the dramatic decline of native red-legged and yellow-legged
frogs.
· Although some of the fish intentionally
introduced into the Estuary by government agencies supported substantial
commercial food fisheries, these fisheries all declined after
a time and are now closed. The signal crayfish, Pacifastacus,
from Oregon, whose exact means of introduction is unclear, supports
the Estuary's only remaining commercial food fishery based on
an introduced species.
· The striped bass sport fishery has resulted
in a substantial transfer of funds from anglers to those who supply
anglers' needs, variously estimated, between 1962 and 1992, between
$7 million and $45 million per year. However, striped bass populations
and the striped bass sport fishery have declined dramatically
in recent years.
· Government introductions of organisms for
sport fishing, as forage fish and for biocontrol have frequently
not produced the intended benefits, and have sometimes had harmful
"side effects," such as reducing the populations of
economically important species.
· Few nonindigenous organisms that were introduced
to the Estuary by other than government intent have produced economic
benefits. The clams Mya and Venerupis,
both accidentally introduced with oysters, have supported commercial
harvesting in the Bay or elsewhere on the Pacific coast, and a
small amount of recreational harvesting in the Bay (though these
clams may have, to some extent, replaced edible native clams);
the Asian clam Corbicula is commercially harvested for
food and bait in California on a small scale; the Asian yellowfin
goby is commercially harvested for bait; muskrat are trapped for
furs; and the South African marsh plant brass buttons provides
food for waterfowl. There do not appear to be any other significant
economic benefits that derive from nongovernmental or accidental
introductions to the Estuary.
· A single introduced organism, the shipworm
Teredo navalis, caused $615 million (in 1992
dollars) of structural damage to maritime facilities in 3 years
in the early part of the 20th century.
· The economic impacts of hull fouling and
other ship fouling are clearly very large, but are not documented
or quantified for the Estuary. Most of the fouling incurred in
the Estuary is due to nonindigenous species. Indirect impacts
due to the use of toxic anti-fouling coatings may also be substantial.
· Waterway fouling by introduced water hyacinth
has become a problem in the Delta over the last fifteen years,
with other introduced plants beginning to add to the problem in
recent years. Hyacinth fouling has had significant economic impacts,
including interference with navigation.
· Perhaps the greatest economic impacts may
derive from the destabilizing of the Estuary's biota due to the
introduction and establishment of an average of one new species
every 24 weeks. This phenomenal rate of species additions has
contributed to the failure of water users and regulatory agencies
to manage the Estuary so as to sustain healthy populations of
anadromous and native fish, resulting in increasing limitations
and threats of limitations on water diversions, wastewater discharges,
channel dredging, levee maintenance, construction and other economic
activities in and near the Estuary, with implications for the
whole of California's economy.
Much remains unknown in terms of the phenomena,
patterns, and processes of invasions in the Bay and Delta, and
thus large gaps remain in the knowledge needed to establish effective
management plans. The following are examples of important research
needs and directions:
Only a few of the hundreds of invaders in the
Estuary have been the subject of quantitative experimental studies
elucidating their roles in the Estuary's ecosystem and their impacts
on native biota. Such studies should receive the highest priority.
Urgently required is a San Francisco Bay Shipping
Study which both updates the 1991 data base available and expands
that data base to all Bay and Delta ports. A biological and ecological
study of the nature of ballast water biota arriving in the Bay/Delta
system is urgently required. Equally pressing is a study of the
fouling organisms entering the Estuary on ships' hulls and in
ships' seachests, in order to assess whether this mechanism is
now becoming of increasing importance and in order to more adequately
define the unique role of ballast water. A Regional Shipping Study
would provide critical data for management plans.
Studies are required on the mechanisms and the
temporal and spatial scales of the distribution of introduced
species by human vectors after they have become established. Such
studies will be of particular value in light of any future introductions
of nuisance aquatic pests.
This study has identified a major, unregulated
vector for exotic species invasions in the Bay: the constant release
of invertebrate-laden seaweeds from New England in association
with bait worm (and lobster) importation. In addition a new trade
in exotic bait has commenced, centered around the importation
of living Vietnamese nereid worms, and both the worms and their
substrate deserve detailed study. These studies are urgently needed
to address the attendant precautionary management issues at hand.
The application of modern molecular genetic techniques
has already revealed the cryptic presence of previously unrecognized
invaders in the Bay: the Atlantic clam Macoma petalum,
the Mediterranean mussel Mytilus galloprovincialis, and
the Japanese jellyfish Aurelia "aurita." Molecular
genetic studies of the Bay's new green crab (Carcinus)
population may be of critical value in resolving the crab's geographic
origins and thus the mechanism that brought it to California.
Molecular genetic studies of worms of the genus Glycera
and Nereis in the Bay may clarify if New England populations
have or are becoming established in the region as a result of
ongoing inoculations via the bait worm industry. Molecular analysis
of other invasions will doubtless reveal, as with Macoma
and Mytilus, a number of heretofore unrecognized species.
Fishery, bait, and other utilization studies should
be conducted on developing or enlarging the scope of fisheries
for introduced bivalves (such as Mya, Venerupis,
and Corbicula), edible aquatic plants, smaller edible fish
(such as Acanthogobius), and crabs (Carcinus and
Eriocheir).
Studies are needed on the potential distribution,
abundance and impacts of zebra mussels (Dreissena polymorpha
and/or D. bugensis) in California, to support efforts to
control their introduction and to design facilities (such as water
intakes and fish screens) that will continue to function adequately
should the mussels become established.
The economic impacts of wood-boring organisms
(shipworms and gribbles) and of fouling organisms (on commercial
vessels, on recreational craft, in ports and marinas, and in water
conduits) are clearly very large in the San Francisco Estuary,
but remain largely undocumented and entirely unquantified. A modern
economic study of this phenomenon, including the economic costs
and ecological impacts of control measures now in place or forecast,
is critically needed.
Largely qualitative data suggest that the economic,
ecological, and geological impacts of the guild of burrowing organisms
that have been historically and newly introduced have been or
are forecast to potentially be extensive in the Estuary. Experimental,
quantitative studies on the impacts of burrowing and bioeroding
crustaceans and muskrats in the Estuary are clearly now needed
to assess the extent of changes that have occurred or are now
occurring, and to form the basis for predicting future alterations
in the absence of control measures.
While primary attention must be paid to preventing
future invasions, studies should begin on examining the broad
suite of potential post-invasion control mechanisms, including
biocontrol, physical containment, eradication, and related strategies.
A Regional Control Mechanisms Workshop for past and anticipated
invasions could set the foundation for future research directions.
1. Introduction 1
2. Methods 4
3. Introduced Species in the Estuary 10
4. Cryptogenic Species in the Estuary 149
5. Results 154
By Taxonomic Group 154
By Native Region 155
By Time Period 157
By Transport Mechanism 160
6. Discussion 167
Ecological Impacts 167
Economic Impacts 190
Future Invasions 202
7. Conclusions 210
Major Findings 210
Research Needs 215
References 218
Appendix 1A. Introduced Terrestrial Plants, Birds and Mammals Reported from the San Francisco Estuary
Appendix 1B. Descriptions of Introduced Terrestrial Plants Reported from the San Francisco Estuary
Appendix 1C. Descriptions of Introduced Terrestrial Mammals Reported from the San Francisco Estuary
Appendix 2. Earlier Inoculations into the San Francisco Estuary and Nearby Waters
Appendix 3. Descriptions of Introduced Plants and Invertebrates in Areas Adjacent to the San Francisco Estuary
Appendix 4. Introduced Organisms in the Northeastern Pacific Known only from the San Francisco Estuary or its Watershed
Appendix 5. Introduced Marine, Estuarine and Aquatic Organisms in Four Regional Studies
Table 1. Introduced organisms in the San Francisco Estuary 141
Table 2. Cryptogenic species in the San Francisco Estuary 150
Table 3. Treatment of introduced species as marine or continental,
for analysis by native region 156
Table 4. Associations of introduced species in the San Francisco
Estuary 170
Table 5. Patterns of invasion along the salinity gradient in the
San Francisco Estuary and the adjoining coast 180
Table 6. Positive economic impacts of marine, estuarine and aquatic
organisms introduced into the San Francisco Estuary 191
Table 7. Negative economic impacts of introduced marine, estuarine
and aquatic organisms 196
Table 8. Recent records of nonindigenous species in the San Francisco
Estuary whose establishment is uncertain 203
Table 9. Introduced species in adjacent areas with the potential
to invade the San Francisco Estuary 205
Table 10. Examples of ongoing inoculations of nonindigenous species
into the San Francisco Estuary 207
Figure 1. The San Francisco Estuary 5
Figure 2. Invasions by taxonomic group: lower-level aggregation 154
Figure 3. Invasions by taxonomic group: higher-level aggregation 155
Figure 4. Invasions by native region 157
Figure 5. Invasions into the San Francisco Estuary by period 159
Figure 6. Invasions into the Northeastern Pacific by period 159
Figure 7. Invasions by type of transport mechanism 161
Figure 8. Some examples of damage caused by the wood-boring shipworm
Teredo navalis in the San Francisco Estuary 194
Scores of individuals, scientists, agency representatives and
members of the public assisted us with the compilation of the
species records in this report. We gratefully acknowledge these
workers for their contributions in the appropriate portion of
the text. Members of the First (October 1993) and Second (July
1994) San Francisco Bay Expeditions (John Chapman, Jean Chapman,
Sarah Cohen, Terry Gosliner, Claudia Mills, Luis Solarzano and
John Rees) were of inestimable help in our field and subsequent
systematic work. John Chapman spent many hours working over recent
collections of San Francisco Bay peracarid crustaceans to resolve
the status of numerous amphipods and isopods. Gretchen Lambert
identified several sets of ascidians from the Bay, and William
Banta and Marianne DiMarco-Temkin aided with the identification
of bryozoans. Gary Gillingham (Kinnetic Laboratories, Inc., Santa
Cruz), Mike Kellogg (City and County of San Francisco), Heather
Peterson (California Department of Water Resources) and Jan Thompson
(U. S. Geological Survey) provided extensive species list from
benthic surveys under their respective aegises. James Orsi (California
Department of Fish and Game) provided assistance in our research
on zooplankton and Doris Sloan (University of California) on foraminifera.
Over the past four centuries thousands of species of fresh water, brackish water and salt water animals and plants have been introduced to the United States (Elton, 1958; Carlton, 1979a, 1989, 1992b; Moyle, 1986; Hickman, 1993; Carlton & Geller, 1993). In some regions, such as the Hawaiian Islands, aboriginal introductions date back more than two millennia (Mooney & Drake, 1986). The taxonomic, habitat and trophic range of this vast nonindigenous biota is impressiveóranging from exotic flatworms (Rectocephala exotica) in the lily ponds of Washington, D. C., to Mexican crabs (Platychirograpsus spectabilis ) in Florida rivers, to aquatic rodents such as the South American nutria (Myocaster coypu) in the southern United States.
The human role in changing the face of North America, in terms of the abundance and diversity of the animals and plants of lakes, rivers, estuaries, marshes, and coastlines, has been demonstratively profound:
· Sea lampreys (Petromyzon marinus) invaded the Great Lakes, destroying extensive native fisheries; the Eurasian carp (Cyprinus carpio), released in New York in 1831, is now a national pest; Nevada's Ash Meadows killifish (Empetrichthys merriami) became extinct at the hands of introduced mosquitofish, mollies, crayfish, and bullfrogs; and scores of exotic fish species now dominate aquatic habitats from Florida to New York and from the Atlantic drainage to California.
· Asian clams (Corbicula fluminea) spread across all of North America in only 40 years, moving from west to eastófrom the Columbia River to California and then quickly across the southern United States to the Atlantic seaboard, a dramatic and startling invasion of this canal- and pipe-fouling clam (McMahon, 1982). Fifty years later, European zebra mussels (Dreissena polymorpha and Dreissena bugensis) are similarly spreading across North Americaóthis time from east to west, from the Great Lakes to the Mississippi and into Oklahoma.
· Alien plantsóincluding the spectacularly successful purple loosestrife (Lythrum salicaria), Eurasian watermilfoil (Myriophyllum spicatum) and water chestnut (Trapa natans)óare now the dominant, and at times the only, vegetation, for hundreds of square miles of aquatic and marsh habitats in North America.
Despite these many invasions, there are with rare exception no syntheses of the spatial and temporal patterns, mechanisms or impacts of these nonindigenous aquatic and estuarine organisms. For the great majority of invasions, records are scattered among thousands of scientific papers and buried in general monographs, student theses, government reports, consultant studies and anecdotal accounts. While a comprehensive review of freshwater and marine invasions would be extraordinarily useful, an initial approach to understanding the ecological and economic impacts of nonindigenous animals and plants in U. S. aquatic and marine environments may be attained through case studies: the assessment of the role of invasions in defined geographic regions, focusing on historical and modern-day dispersal pathways, on the biological, ecological and economic consequences of invasions, and on prospects for future invasions.
We present here such a regional study, focusing on one of the
largest freshwater and estuarine ecosystems of the United States:
the San Francisco Bay and Delta region, a region known to have
sustained numerous invasions for over a century.
At the time of our study there was no synthesis available of the diversity and impacts of the nonindigenous aquatic and estuarine species of the San Francisco Bay and Delta region, an area that extends from the inland port cities of the Central Valley to the coastal waters of the Pacific Ocean at the Golden Gate.
This region includes examples of most of the common aquatic habitats found throughout the warm and cool temperate climates of the United States and, as such, represents an ideal theater for assessing the diversity and range of effects of aquatic invasions. Within the Bay-Delta Region are fresh, brackish, and salt water marshes, sandflats and mudflats, rocky shores, benthic sublittoral habitats of a wide sediment range, eelgrass beds, emergent aquatic macrophyte communities, planktonic, nektonic, and neustonic communities, extensive fouling assemblages, and communities of burrowing and boring organisms in clays and wood. Also represented is a vast range of habitat disturbance regimes. Over a 140-year period of substantial human commercial and other activitiesósince about 1850óa minimum of more than 200 plants, protists and animals from the aquatic and coastal habitats of eastern North America, Europe, Asia, Australia, and South America have invaded these ecosystems.
Prior lists or descriptions of the introduced freshwater, anadromous and estuarine fish fauna in the San Francisco Bay-Delta region were provided by Moyle (1976b) and McGinnis (1984); of freshwater mollusks by Hanna (1966) and Taylor (1981); of marine mollusks by Nichols et al. (1986); and of introduced marine and estuarine invertebrates by Carlton (1975, 1979a,b), supplemented by Carlton et al. (1990). Silva (1979) and Josselyn & West (1985) noted some introductions of marine and brackish seaweeds, but no comprehensive assessment of possibly introduced seaweeds had been made. Atwater et al. (1979) provided a list of introduced vascular plants in San Francisco Bay salt marshes, but appear not to have distinguished between aquatic plants that are characteristically found within marshes and essentially terrestrial plants that are occasionally found at the edges of or within marshes. During our study the Bay-Delta Oversight Committee of the California Department of Water Resources produced a briefing paper summarizing some of the previously published information on introduced fish, wildlife and plants of the Bay-Delta region (BDOC, 1994), and Orsi (1995) published a list of introduced estuarine copepods and mysids.
No information had been compiled on possible introductions among freshwater invertebrates (including species of freshwater sponges, jellyfish, flatworms, oligochaete and polychaete worms, snails, clams, crustaceans, insects and bryozoans), freshwater macroalgae, or fresh, brackish or salt water phytoplankton. Protozoan introductions had been similarly neglected.
Based on the information available prior to our study, and on
consideration of extant lists of aquatic or marine introductions
in other regions (Leppäkoski, 1984; den Hartog, 1987; Mills
et al., 1993, 1995; Jansson, 1994), we had estimated that the
number of aquatic and estuarine introductions in the Bay-Delta
system could exceed 150 invertebrate species, 20 fish species,
10 algal species, and 100 vascular plant species.
The present work is the first regional case study in the United States of the diversity and ecological and economic impacts of nonindigenous species in aquatic and estuarine habitats. Previous studies (Mills et al., 1993, for the Great Lakes; Mills et al., 1996, for the Hudson River) have largely concentrated on species check-lists with a minimal review of ecological or economic effects of the exotic biota. We intend the present study to be a comprehensive synthesis which may serve as a comparative model for other regional studies in U. S. waters.
The present study also sets forth detailed and clear criteria for determining which species are present and established within the study zone. Prior regional surveys of aquatic introductions have implied but rarely defined these criteria, a situation that impedes ready quantitative comparisons between regions. We include (Chapter 5) a supplemental list of vascular plant species based upon criteria which we judge to approximate the criteria in prior regional surveys of aquatic introductions in the USA, in order to facilitate such comparisons.
The present study is also the first regional survey of introductions to include a listing (although preliminary) of cryptogenic speciesóspecies which are neither demonstrably native or introduced (Chapter 4). As discussed by Carlton (1996a), the development of such lists is a necessary first step in correcting prior tendencies to profoundly underestimate the potential extent of biological invasions and in providing a more complete basis for understanding the sources, characteristics and frequency of success of biological invaders.
Both older (Elton, 1958) and newer (e. g. Mooney & Drake, 1986; Drake et al., 1989) reviews of biological invasions propose a number of theoretical models to explain the success of animal and plant invasions in regions where they did not evolve. However, for most such studies, comprehensive data sets on the diversity of invasions, temporal patterns of invasion, and ecological impacts have not been available by which to test the applicability or robustness of invasion theory. The present study provides an extensive review of an introduced biota exceeding 200 taxa in a defined geographic region, and thus provides a rare data set with which to test invasion models.
The study zone for this report is defined as the estuarine and
aquatic habitats that are within the normal range of tidal influence
in San Francisco Bay, the Sacramento-San Joaquin Delta and tributaries,
and referred to herein as the San Francisco Estuary or the Estuary
(Fig. 1). The primary data set (Chapter 3 and Table 1) contains
all demonstrably nonindigenous organisms that are characteristically
found in estuarine or aquatic habitats (including marshes, mudflats,
etc.), and for which there is significant evidence supporting
their establishment within the study zone.
Inclusion in the primary data set thus requires evidence demonstrating that the organism in question is (1) not native to the Estuary, and (2) currently established in the Estuary.
We define native organisms as those organisms present aboriginally, which for the Bay-Delta region means prior to 1769 when the first European explorers entered the area. The types of evidence that we utilized to determine the native versus introduced status of aquatic and estuarine organisms, as discussed by Carlton (1979a) and Chapman & Carlton (1991, 1994), include:
· global systematic evidence (involving taxonomic information from both morphology and molecular genetics) and biogeographic evidence, including the global distribution of closely related species;
· the existence of identifiable mechanisms of human-mediated transport;
· historical evidence of presence or absence;
· archaeological evidence of presence or absence;
· paleontological evidence of presence or absence;
· the extent to which distribution can be explained by natural dispersal mechanisms;
· rapid or sudden changes in abundance or distribution;
· highly restricted or anomalously disjunct distributions (in comparison to distributions of known native organisms);
· occurrence in assemblages with other known introduced species; and
· for parasites or commensals, occurrence on introduced organisms.
We define established organisms as those organisms present and
reproducing "in the wild" whose numbers, distribution
and persistence over time suggest that, barring unforeseen catastrophic
events or successful eradication efforts, they will continue to
be present in the future. "In the wild" implies reproduction
and persistence of the population without direct human intervention
or assistance (such
as reproductive assistance via hatcheries or periodic renewal of the population through the importation of spat), but may include dependence on human-altered or created habitats, such as water bodies warmed by the cooling-water effluent from power plants, pilings, floating docks, and salt ponds or other manipulated, semi-enclosed lagoons. The types of evidence that we used to assess establishment include:
· population size;
· persistence of the population over time;
· distribution (broad or restricted) of the population, and trends in distribution;
· for species dependent on sexual reproduction, the presence of both males and females, and the presence of ovigerous females; and
· the age structure of the population as an indicator of
successful reproduction.
Beyond the primary data set, we considered and compiled information on several additional categories of organisms, including:
· cryptogenic organisms, that is, organisms in the Estuary that are neither demonstrably native nor introduced (Table 2);
· nonindigenous organisms that have been reported from or were intentionally introduced to the Estuary, but which did not become established or for which there is inadequate evidence regarding their establishment (Table 8 and Appendix 2);
· nonindigenous organisms which are established in aquatic environments tributary to or adjacent to the Estuary, and which may in the future extend their range into the Estuary (Table 9);
· nonindigenous organisms which are not characteristically
found in estuarine or aquatic habitats but which have been occasionally
reported from or may make occasional use of the Estuary (Appendix
1).
Probably the largest and most difficult "gray zone" between the primary data set and organisms in these additional categories involves those nonindigenous plants reported from coastal or freshwater wetlands for which specific information on occurrence within the tidal boundaries of the Estuary is not available. Although previous regional studies of aquatic invasions (Mills et al., 1993, 1995) have included many such gray-zone plants, we limited inclusion in our primary data set to those that both: (a) have habitat descriptions indicating that they are primarily marsh plants, and not primarily terrestrial or moist ground plants occasionally found in or near marshes; and (b) have been reported specifically from the Delta, and not just from the Central Valley or the Bay Area generally. Similar questions arose, though less commonly, with other types of organisms, to which we applied similar logic.
Those candidate organisms which are not listed in Table 1 because
of criterion (a), are instead listed in Appendix 1. Adding the
plants in Appendix 1 to the organisms in Table 1 would produce
a list of nonindigenous organisms for the Estuary comparable those
produced for the Great Lakes (Mills et al., 1993) and the Hudson
River (Mills et al., 1995), as discussed further in Chapter 5.
Candidate organisms which failed to meet criterion (b) are listed
in Table 9. Even following these restrictive criteria, we may
have included in Table 1 some plants that are found in the Delta
region in marshes or diked ponds, but not in tidal waters.
Initial lists of taxa in the above-described categories were compiled from the prior studies discussed in the introduction and from a review of the regional biological and systematic literature including regional monographic studies, keys, field guides and checklists; from published (mainly in the gray literature) and unpublished species lists generated by public agencies and private consultants; and from discussions with taxonomists, field biologists, refuge managers and consultants familiar with the region.
Further information on the species thus identified was developed through a review of the pertinent current and historical biological literature, museum records and specimen collections, and interviews with biologists. We also undertook limited field work in order to check the presence or distribution of certain species, and to check for the presence of previously unreported species in some rarely sampled habitats. This information was used to develop the following species lists:
· Table 1, listing introduced species in the Estuary;
· Table 2, listing cryptogenic species in the Estuary;
· Table 8, listing species recently recorded from the Estuary but whose establishment is uncertain;
· Table 9 and Appendix 3, listing introduced species in adjacent aquatic habitats;
· Appendix 1, listing terrestrial species that may occasionally be found in the Estuary;
· Appendix 2, listing older inoculations of nonindigenous species that did not become established; and
· Appendix 4, listing introduced species in the northeastern
Pacific known only from the Estuary.
For each species listed in Table 1 we determined where possible:
· the date of first collection or observation or planting in the Estuary, in California and in northeastern Pacific waters or coastal states or provinces; and where this was unavailable, the date of the first written account of the organism in the area;
· the native range of the species;
· the immediate geographic source of the introduction;
· the transport mechanism;
· the organism's current taxonomic status, most frequently utilized synonyms, and common names; and
· its current spatial distribution and abundance in the Estuary.
We included common names from Turgeon et al. (1988) and Carlton (1992) for mollusks, Cairns et al. (1991) for coelenterates, Williams et al. (1989) for decapods, Gosner (1978) for other invertebrates, Robins et al. (1991) for fish and Hickman (1983) for higher plants.
The data are presented in the species descriptions in Chapter
3 and summarized (in large part) in Table 1. Some of these data
are also provided for the species listed in Tables 8 and 9 and
the appendices. We also reviewed the available information on
the ecological roles and economic impacts of individual introduced
species and of introduced species assemblages. This information
is summarized in the species descriptions in Chapter 3 and discussed
in Chapter 6.
The primary data set in Chapter 3 and Table 1 was quantitatively
analyzed with regard to taxonomic groups, native regions, timing
and transport mechanisms. The results are presented in Chapter
5.
The numbers of species per taxonomic group were tabulated at two
levels of aggregation. A first tabulation was done at the taxonomic
levels of order (for vertebrates), phylum (for invertebrates),
subkingdom (for plants) and kingdom (for protozoans). A second,
more highly-aggregated, tabulation was done at the levels of class
(vertebrates), a traditional, non-phyletic grouping (invertebrates),
and kingdom (plants and protozoans).
The numbers of species per native region were tabulated with regard to eleven marine regions and five continental regions. The marine regions consist of the eastern and western portions of the North and South Atlantic oceans and the North and South Pacific oceans, the Indian Ocean, the Mediterranean Sea, and the Black and Caspian Seas. The Western South Pacific region consists primarily of waters around Australia and New Zealand. The five continental regions consist of North America, South America, Eurasia, Africa, and Australia/New Zealand. Where an organism's native range included more than one region, that organism's count was split proportionally.
We analyzed the timing of introductions in terms of both the date of first record in the Estuary, and the date of first record in the northeastern Pacific. The numbers of species were tabulated in four 30-year periods with the first beginning in 1850 and the last ending in 1969, and one 26-year period (1970-1995). In the few cases where an organism's date of first record was a period that spanned parts of two tabulation periods, that organism's count was proportionally divided between the periods.
We distinguished two different types of dates of first record. The first and preferred type is the date of initial planting or first observation or collection of the species in the area. Where this was unavailable, we reported the earliest date available (date of writing, submission or publication) of the first written account of the species in the area. In Table 1, dates of first written account are preceded by the symbol '²', meaning that the date of first planting, observation or collection was on or before (in some cases, perhaps a considerable time before) the indicated date. Dates of first written account were excluded from the quantitative analysis.
We also excluded from the analysis those dates of first record that we judged to be a clear artifact of collecting bias, or a fortuitous discovery of a species in a restricted habitat or locality, and whose inclusion would have contributed to a misleading picture of the temporal pattern of invasions in the Estuary. This is discussed further in Chapter 5 under "Results." These dates are marked by asterisks (*) in Table 1.
We analyzed the stocks of organisms that have been introduced to the Estuary in terms of the transport mechanisms (also called "transport vectors," "means of introduction" and "dispersal mechanisms") that brought them to the northeastern Pacific. We utilized thirteen categories of mechanisms, as defined in Table 1 and discussed in Chapter 5 under "Results." Where multiple possible transport mechanisms were determined for an organism, that organism's count was divided proportionally among the possible mechanisms.
Bryopsis sp. [CODIALES]
Silva (1979) reported an unidentified species of Bryopsis
which only reproduces asexually in the Bay and which he described
as exhibiting weedy behavior: developing explosively and frequently
being cast ashore in large quantities, creating a nuisance as
it decomposes. It has been observed in the Bay since at least
1951, from Alameda to Richmond on the East Bay shore and at Coyote
Point. Bryopsis occurs in ship fouling (pers. obs.) and, in concert
with the other introduced seaweeds, we tentatively suggest ship
fouling as the mechanism of introduction.
Codium fragile tomentosoides (Suringar, 1867) Hariot, 1889
[CODIALES]
DEAD MAN'S FINGERS, SPUTNIK WEED, OYSTER THIEF
Codium fragile is native to the northern Pacific, and is found in North America on exposed coasts from Alaska to Baja California (Abbot & Hollenberg, 1976). The weedy subspecies C. f. tomentosoides is native to Japan (where it is eaten) and was introduced to Europe in the nineteenth century and to New York, probably as ship fouling, around 1956, subsequently spreading north to Maine and south to North Carolina (Carlton & Scanlon, 1985; includes discussion of coastal transport mechanisms). It was first collected in San Francisco Bay in 1977, probably introduced as ship fouling (Carlton et al., 1990), and as of 1985 not reported from any other site in the northeastern Pacific (Carlton & Scanlon, 1985).
In San Francisco Bay C. f. tomentosoides is common intertidally
and subtidally attached to rocks, seawalls, piers and floating
docks. Josselyn & West (1985) report it as common (found 60-100%
of the time) at Coyote Point, and frequent (30-60%) at Redwood
City, Palo Alto. In 1993-94 we found it on floating docks in the
East Bay from Richmond to San Leandro and at Pier 39 in San Francisco.
Sargassum muticum (Yendo, 1907) Fensholt, 1955 [FUCALES]
Sargassum muticum is a Japanese species which was first collected in North
America in 1944 in British Columbia, apparently introduced in shipments of Japanese oyster spat (Crassostrea gigas), and subsequently spread both north and south into protected waters. It was reported from Coos Bay in 1947, Crescent City in 1963 and Santa Catalina Island in 1970, and is now found at scattered sites from Alaska to Baja California (Abbott & Hollenberg, 1976; Silva, 1979). It was introduced to Europe in the early 1970s, apparently also in shipments of Japanese oyster spat (Druehl, 1973; Critchley, 1983; Danek, 1984).
S. muticum was first observed in San Francisco Bay by Silva on the riprap at the entrance to the Berkeley Marina in 1973. It has been reported on the pilings of the Golden Gate Bridge, in the San Francisco Yacht Harbor, on the inside breakwater at Fort Baker, at Angel Island, Sausalito and the Tiburon Peninsula, on the east side of Yerba Buena Island, at Crown Beach in Alameda, and from Albany and Richmond (Silva, 1979; Danek, 1984). Josselyn & West (1985) found it commonly (60-100% of the time) at Tiburon Peninsula and infrequently (5-30%) at Twin Sisters.
In San Francisco Bay S. muticum appears to be restricted to low intertidal areas with hard substrate and moderate to high salinity. Germlings grow at salinities down to 10 ppt (to 20 ppt according to Norton (1977)), but maximum survival is at 25-30 ppt salinity. Low salinities and storms eliminated the Tiburon population in the winter and spring of 1983 (Danek, 1984). S. muticum was more abundant at Crown Beach, Alameda during the drought years of 1990-91 than it is at present (pers. obs.).
Both lateral branches and fertile fronds of S. muticum break
off regularly and float and disperse by currents and wind drift,
surviving afloat for up to 3 months, and can initiate new populations
(Danek, 1984). Danek (1984) reports that "in Britain S.
muticum has become the dominant species at low tide levels,
and is a successful competitor against indigenous species such
as Cystoseira and Laminaria...it forms large floating
mats (Fletcher & Fletcher, 1975) causing problems for fishermen
and small boat navigation." An eradication program in England
was "largely unsuccessful" (Silva, 1979). In Canada,
Druehl (1973) considers it to be replacing populations of Zostera
in some places, and Dudley & Collins (1995) report that it
has become a dominant intertidal species in the Channel Islands
and Santa Barbara area. However, Silva (1979) states that "there
is no evidence that S. muticum is displacing the native
biota of San Francisco Bay."
Callithamnion byssoides Arnott [CERAMIALES]
Callithamnion byssoides is native to the northwestern Atlantic
from Nova Scotia to Florida (Taylor, 1957). It was not listed
in Silva's (1979) review of Central Bay benthic algae, but Josselyn
& West (1985) found it attached to rocks "near MLLW throughout
the northern and southern reaches of the bay" in collections
between 1978 and 1983. They report it as frequent (found 30-60%
of the time) at Redwood City, Palo Alto and China Camp, and infrequent
(5-30%) at Tiburon Peninsula, Point
Pinole and Crockett. Callithamnion species are common fouling
species (WHOI, 1952). C. byssoides may have been transported
to San Francisco Bay as ship fouling, or possibly with the algae
used to pack New England bait worms or lobster.
Polysiphonia denudata (Dillwyn) Kützing [CERAMIALES]
Polysiphonia denudata is native to the Atlantic coast from Prince Edward Island to Florida and the tropics, commonly occurring in tide pools and in shallow bays attached to rocks, shells and wharves (Taylor, 1957). It was not listed by Silva (1979) in his review of Central Bay benthic algae, but Josselyn & West (1985) reported it as a "common drift algae during summer months, especially in South San Francisco Bay" (citing Cloern, pers. comm.), and as drift or epiphytic in both San Pablo Bay and South Bay in collections between 1978 and 1983. They further suggest that "the extensive decaying mats observed by Nichols (1979) in Palo Alto during the summer of 1975" may have been P. denudata. We (JTC) observed a sometimes abundant Polysiphonia, which we presume to have been P. denudata, in Lake Merritt, Oakland in 1963-64.
Polysiphonia species are common fouling species or artificial
structures, including ships (WHOI, 1952; Fletcher et al., 1984),
and a species of Polysiphonia was the organism most tolerant
of copper- and mercury-based anti-fouling compounds in tests in
Florida (Weiss, 1947), suggesting that P. denudata probably
arrived in San Francisco Bay as hull fouling, although introduction
by ballast water is possible. Josselyn & West (1985) reported
P. denudata as frequent (30-60% of the time) at Point Pinole,
and infrequent (5-30%) at stations on the western shore of the
South Bay, on the Marin shore, and at Crockett. It apparently
reproduces asexually in San Francisco Bay, and is not reported
from other Pacific coast estuaries (M. Josselyn, pers. comm.,
1985).
Chenopodium macrospermum J. D. Hooker var. halophilum
(Philippi) Standley [CHENOPODIACEAE]
SYNONYMS: Chenopodium macrospermum J. D. Hooker var. farinosum
(Watson) Howell
Probably native to South America, this plant is found in wet places
and marshes at low elevations between Orange County and Washington
state, including the coastal California (Munz, 1959) the San Francisco
Bay Area and the Delta (Hickman, 1993).
Cotula coronopifolia Linnaeus, 1753 [ASTERACEAE]
BRASS BUTTONS
Brass buttons is a native of South Africa that has become established along the Pacific coast from California to British Columbia, and is reported as adventive in New England (Peck, 1941; Muenscher, 1944; Steward et al., 1963). In 1878, Lockington (1878) reported it as an introduced plant common in wet places on the San Francisco peninsula. As it was likely to have spread to the Bay's littoral zone by around that time, we have taken 1878 as the date of first observation in the Estuary. It was probably introduced in ships' ballast (as suggested by Spicher & Josselyn, 1985).
In California brass buttons has variously been reported as common
in salt and freshwater marshes along the coast (Robbins et al.,
1941; Mason, 1957; Munz 1959; Hickman, 1993), as present in San
Francisco Bay saltmarshes (Jepson, 1951), as common in wet places
near high-tide levels in the tidal marshes around Suisun Bay (Atwater
et al., 1979), and as uncommon in the Delta (Madrone Assoc., 1980;
Herbold & Moyle, 1989). A 1981 aerial survey of Suisun Marsh
classified 3,800 acres, or 5% of the area surveyed, as Cotula
habitat (Wernette, 1986), and in 1989 it was found at 18 of 48
sites. Along with alkali bulrush, saltgrass or fat hen, brass
buttons comprised the principal vegetation at two sites in each
of 1987, 1988 and 1989 (Herrgesell, 1990). Waterfowl frequently
graze on brass button seeds, and the diked, brackish marshes around
Suisun Bay are managed in part to promote its growth (Josselyn,
1983).
Lepidium latifolium Linnaeus [BRASSICACEAE]
BROADLEAF PEPPERGRASS, PERENNIAL PEPPERWEED, TALL WHITETOP
Broadleaf peppergrass is a native of Eurasia, where it is reported from Norway to North Africa and east to the Himalayan region. It has been introduced to many parts of the United States, Mexico and Australia, and is found on beaches, tidal shores, saline soils and roadsides throughout most of California (Hickman, 1993; Young & Turner, 1995; May, 1995). Suggested mechanisms of transport to North America along the New England coast prior to 1924 include transport in gluestock (animal bones) shipped from Europe, the seeds adhering to scraps of tissue or burlap sacking (Morse, 1924, cited in May, 1995); with material shipped to a dye and licorice works (Eames, 1935, cited in May, 1995); and clinging to the wool of sheep (Rollins, 1993, cited in May, 1995).
Broadleaf peppergrass was discovered in Montana in 1935, and in California near Oakdale, Stanislaus County in 1936, possibly having been transported with beet seed (May, 1995). By 1941 it was reported from San Joaquin and Yolo counties on the edge of the Delta (Robbins et al., 1941). Herbarium specimens exist from Grizzly Island (collected in 1960), Antioch Dunes (1977) and the Bay shoreline at Martinez and Point Pinole (1978). It was reported as common in the tidal marshes of the San Francisco Estuary (Atwater et al., 1979), and uncommon in the Delta (Madrone Assoc., 1980; Herbold & Moyle, 1989). Recently it has been reported as invasive and spreading in shallow ponds and adjacent moist uplands in the Central Valley wildlife refuges, and in high tidal marsh areas and diked seasonal wetlands in Suisun Marsh (where hundreds of acres on Grizzly Island are affected) and throughout the Bay (Trumbo, 1994; Dudley & Collins, 1995; Malamud-Roam, pers. comm., 1994; May, 1995).
Broadleaf peppergrass produces large amounts of seed, can reproduce asexually by spread of rhizome sections, and is tolerant of a broad range of environmental conditions (Trumbo, 1994; May, 1995). It often becomes established on disturbed, bare soils, and was also observed in pickleweed (Salicornia) plains and among Scirpus spp. (May, 1995). May (1995) reports that it may be intolerant of frequent or prolonged flooding, and our observations suggest that it is limited to the upper edge, or often above the upper edge, of tidal inundation.
Trumbo (1994) suggests that at Suisun Marsh peppergrass first
got established in agricultural areas, then as farms closed during
the 1950s expanded rapidly "unchecked by frequent cultivations
and crop competition" and invaded wildlife areas of the marsh.
He claims that it competes with pickleweed, thereby reducing habitat
for the endangered saltmarsh harvest mouse, and that its dense
growth is unsuitable for use as nesting cover by waterfowl, although
May (1995) reports that waterfowl nests have been observed in
monotypic stands of peppergrass. BDOC (1994) states that it may
outcompete and displace certain rare native marsh plants, such
as Lilaeopsis masoni and Cordylanthus mollis mollis.
CDFG has tested burning, discing and herbicide treatments as control
measures for pepper grass, which is ranked as a "B"-level
plant pest by the California Department of Food and Agriculture
(BDOC, 1994).
Limosella subulata Ives, 1817 [SCROPHULARIACEAE]
AWL-LEAVED MUDWORT
Limosella subulata is native to Europe or the east coast
of North America, and found in southern British Columbia and in
fifteen western states. It is reported from muddy and sandy intertidal
flats in the Delta (Muenscher, 1944; Munz, 1959; Atwater et al.,
1979; Herbold & Moyle, 1989; Hickman, 1993).
Lythrum salicaria Linnaeus [LYTHRACEAE]
PURPLE LOOSESTRIFE
Native to Europe, purple loosestrife is invasive worldwide. It was introduced to North America by the early 1880s, either as seeds in solid ballast or in the wool of sheep, or as a cultivated plant. It can grow in monospecific stands, competes with cattails and other marsh plants (Mills et al., 1993), and is listed as a noxious weed in California (Hickman, 1993).
Purple loosestrife was reported by Munz (1968) in Nevada and Butte
counties, but not mentioned by Munz (1959) or Mason (1957). It
is now found in low elevation marshes, ponds, streambanks and
ditches throughout much of California, including the Sacramento
Valley and the Bay Area (Hickman, 1993).
Myriophyllum aquaticum (Velloso) [HALORAGACEAE]
PARROT'S FEATHER
SYNONYMS: Myriophyllum brasiliense Cambess.
A South American native, parrot's feather is found in ponds, ditches,
streams and lakes in warm temperate and tropical regions throughout
the world. Escaped from cultivation in California and reported
from six counties from Humboldt to San Diego ("set out in
these areas by dealers in aquatics for the purpose of market propagation;"
Mason, 1957), from the Coast and Cascade ranges and from central
western California (Hickman, 1993), and from tidal marshes and
sloughs in the Delta (Atwater et al., 1979; Madrone Assoc., 1980).
BDOC (1994) reports that parrot's feather "provides excellent
mosquito habitat," and that the USDA has investigated the
use of herbicidal and biological controls.
Myriophyllum spicatum Linnaeus [HALORAGACEAE]
EURASIAN MILFOIL
SYNONYMS: Myriophyllum exalbescens in part
Eurasian milfoil is a native of Eurasia and North Africa that has invaded lakes in the eastern United States and Canada. Its first documented occurrence in North America was in the Potomac River, Virginia in 1881, though it is thought to have arrived much earlier (Reed, 1977, cited in Mills et al., 1993). In the early 1970s it reportedly made up over 90 percent of the plant biomass in Lake Cayuga, New York, where it may have been eventually controlled by an exotic moth, Acentria niveus (Anon., 1994). Control efforts have also included cutting, water drawdown and herbicide applications (Mills et al., 1993). Eurasian milfoil reportedly can outcompete native plants through shading, clog pipes and entangle boat propellers, and foul beaches with decaying mats of dead plants. It spreads as discarded material from aquaria and entangled on boats and trailers moved between watersheds (Mills et al., 1995).
Hickman (1993) reports this plant as uncommon in ditches and lake
margins in the Bay Area and the San Joaquin Valley, and BDOC (1994)
reports it from the Delta. Munz (1959) reported Myriophyllum
spicatum ssp. exalbescens common throughout cismontane
California in quiet water below 8,000 feet, Atwater et al. (1979)
reported M. s. ssp. exalbescens in Snodgrass Slough
on the Sacramento River in the Delta in 1976, and Madrone Assoc.
(1980) reported water milfoil (as M. s. var. exalbescens
and M. exalbescens) common in the Delta. Hickman (1993)
states that M. s. ssp. exalbescens was misapplied
to M. sibiricum, which he treats as a native (but which
we consider cryptogenic (Table 2) based on its reported range
which includes Pacific coastal and eastern Northern America and
Eurasia). Based on reported distribution and abundance, we consider
Munz's (1959) exalbescens to be M. sibiricum and
the Delta reports of exalbescens since 1976 to refer, at
least in part, to M. spicatum.
Polygonum patulum Bieberstein [POLYGONACEAE]
SMARTWEED
Native to eastern Europe, Polygonum patulum is reported
as uncommon in and around salt marshes in the Bay and Delta area
(Munz 1959; Hickman, 1993). It belongs to a closely related (and
possibly hybridizing) group of introduced or cryptogenic species,
often found in or adjacent to fresh or saline wetlands, including
Polygonum aviculare (cryptogenic), argyrocoleon
(Asian), prolificum (eastern North America) and punctatum
(cryptogenic).
Rorippa nasturtium-aquaticum (Linnaeus) Hayek [BRASSICACEAE]
WATERCRESS
SYNONYMS: Nasturtium officinale R. Br.
Radicula nasturtium-aquaticum (Linnaeus) Britt. & Rendle
Rorippa nasturtium Rusby
Sisymbrium nasturtium-aquaticum
Watercress is a perennial aquatic plant native to Europe which has been widely cultivated for its edible greens, and which has escaped and become common throughout North America in marshes, in slowly flowing creeks, around seeps, on wet banks, etc. Though probably present earlier, established populations were first reported from North America near Niagara Falls in 1847 and at Ann Arbor, Michigan in 1857 (Gray, 1848; Green, 1962; Mills et al., 1993). Peck (1941) reported it widely distributed in Oregon and Muenscher (1944) reported it from 41 states including California, Oregon and Washington.
Watercress is found in the Delta (Munz, 1959; Herbold & Moyle,
1989). Most authors (e. g. Jepson, 1951; Munz, 1959; Mills et
al., 1993, 1995; BDOC, 1994) consider this plant to be an introduction
from Europe, although Hickman (1993) treats it as a native plant
of temperate world-wide distribution.
Salsola soda Linnaeus [CHENOPODIACEAE]
Native to southern Europe, Salsola soda is found on mudflats, in open areas and among pickleweed in salt marshes, and on berms, among riprap and in open areas at and above the high tide mark at scattered sites in San Francisco Bay (Hickman, 1993; pers. obs.). It was first collected in July 1968 at the west end of the Dumbarton Bridge in the South Bay (Thomas, 1975). It has since been found at several sites in the South Bay from Candlestick Park to the San Francisco Bay National Wildlife Refuge, and on the Alameda shore; from Emeryville Marina to Hoffman Marsh, Richmond and at Richardson Bay in the Central Bay; and at Chevron Marsh, Richmond, at Pinole and at Tubbs Island in San Pablo Bay (Thomas, 1975; Tamasi, 1995; pers. obs.). At the Pinole shore it appears to be successfully competing with pickleweed Salicornia virginica in the high marsh, and like pickleweed is attacked by the parasitic plant Cuscuta salina (pers. obs.). A few plants were observed on a mudflat in Bodega Harbor in the summer of 1994 but not in 1995 (Connors, 1995; C. Daehler, pers. comm., 1995).
Its mechanism of introduction is something of a mystery, as no
known modern transport vectoróexcepting the unlikely possibility
of its use (and escape) as an ornamental plantóappears
to apply.
Spergularia media (Linnaeus) Grisebach [CARYOPHYLLACEAE]
SAND SPURREY
SYNONYMS: Arenaria media
Hickman (1993) noted that "Spergularia maritima (All.)
Chiov. may prove to be the correct name" for this species.
Sand spurrey is native to coastal Europe and has been introduced
to South America, eastern North America and Oregon. It is found
on salt flats, in and bordering salt marshes, and on sandy beaches
in Marin and Contra Costa counties (Munz, 1959; Hickman, 1993).
Atwater et al. (1979) listed it as common in tidal marshes of
the San Francisco Estuary.
Egeria densa Planchon [HYDROCHARITACEAE]
ELODEA, EGERIA, BRAZILIAN WATERWEED
SYNONYMS: Elodea densa (Planchon) Caspary
Anacharis densa (Planchon) Marie-Victorin
Elodea is a highly invasive aquatic plant from South America that clogs waterways and interferes with navigation. In 1944 Muenscher reported it as a recently established introduction in six eastern states from Massachusetts to Florida and in California, Steward et al. (1963) reported it from Oregon, and it has also become established in Europe (Hickman, 1993). It is widely used in aquaria and ornamental pools, and was probably introduced as discarded material or as an escape (Muencher, 1944; Munz, 1959). In California it was reported as infrequent at scattered locations by Mason (1957), and is now found on both sides of the Sierra Nevada, in the San Joaquin Valley, and in the San Francisco Bay area (Hickman, 1993).
Elodea is reported as common in waterways throughout the Delta
and in the Contra Costa Canal (Atwater et al., 1979; Herbold &
Moyle, 1989; Holt, 1992). It was found at 8 of 10 sites in the
Delta surveyed for littoral zone vegetation in 1988-90 (IESP,
1991). In the 1990s it has spread to new areas and deeper water
in the Delta and become more abundant, perhaps due to lower summer
water levels and warmer water temperatures (Holt, 1992; Thomas,
pers. comm.). Although elodea provides shelter for newly hatched
fish, it also clogs channels and berths, gets caught in water
intake of engines, and fouls propellers. Management of this species
included the use of an aquatic weed killer on about 35 acres of
Delta waterways in 1991 (Holt, 1992). Field tests are being conducted
on the use of Komeen, a copper-based herbicide, and biocontrol
agents are being investigated (Rubissow, 1994; BDOC, 1994).
Eichhornia crassipes (Martius) Solms-Laubach, 1883 [PONTEDERIACEAE]
WATER HYACINTH
Water hyacinth, "perhaps the world's most troublesome aquatic weed" (Hickman, 1993) is a native of tropical South America that has spread to more than 50 countries on five continents, and has become a massive problem in waterways in both Africa and Southeast Asia (Barrett, 1989). Its air-filled tissue (aerenchyma) enables it to float and spread rapidly within and between connected water bodies. It reproduces asexually by breaking apart into pieces each of which develops into a separate plant. This results in a rapid increase in biomass, and continuous mats of living and decaying water hyacinth up to two meters thick covering the water surface have been reported (Barrett, 1991).
Water hyacinth was introduced to North America in 1884 via the Cotton States Exposition in New Orleans. The plant was displayed in ornamental ponds and distributed as souvenirs to visitors, with the excess dumped into nearby creeks and lakes (Barrett, 1989; Joyce, 1992). It spread across the southeastern U. S. to Florida, where a 1895 invasion of the St. Johns River produced floating mats of water hyacinth up to 40 kilometers long (Barrett, 1989), and in several southeastern sites blocked the passage of steamboats and other vessels by 1898 (Joyce, 1992). According to Joyce, these problems led to the passage of the River and Harbor Act in 1899, authorizing the U. S. Army Corps of Engineers to maintain navigation channels in these areas. Control efforts included the spraying of sodium arsenite, which poisoned applicators and livestock (Joyce, 1992).
The 1884 Cotton States Exposition was probably also the initial source of the water hyacinth that was reported from the Sacramento River near Clarksburg, California, in 1904 (Thomas & Anderson, 1983; Thomas, pers. comm., 1994). In California, water hyacinth spread gradually for many decades. Robbins et al. (1941) reported it from the Kings River in Fresno County and Warner Creek in San Bernardino County. It reached the Delta by the late 1940s or early 1950s, where the federal Bureau of Reclamation tried controlling it with herbicides around 1957 (Thomas & Anderson, 1983; L. Thomas, pers. comm., 1994). In 1959 Munz reported it as occasionally established in sloughs and sluggish water in the Sacramento and San Joaquin valleys and the Santa Ana River system. In 1972 the U. S. Army Corps of Engineers investigated water hyacinth on the Merced River and determined that it was not a flood hazard (Thomas & Anderson, 1983; L. Thomas, pers. comm., 1994). Atwater et al. (1979) listed it as common in tidal marshes, presumably in the Delta. Madrone Assoc. (1980) reported it as seasonally common in the southern and central Delta and clearing in the winter, when coot and other waterfowl fed on the dead plants.
Starting in the 1980s water hyacinth became a serious problem in the Delta watershed, blocking canals and waterways, fouling irrigation pumps, shutting down marinas, blocking salmon migration and, by 1982-83, blocking ferry boats at Bacon Island and preventing the island's produce from being shipped to market (CDBW, 1994; L. Thomas, pers. comm., 1994). The plant's abundance may have been drought-related, with plant densities building up when low river flows were unable to flush the year's growth out of the Delta. On the other hand, when a wet year arrived in 1993 the higher rainfall "washed surplus plants from the upstream channels into the Delta where it created a major problem by early summer, and it also appeared to trigger unprecedented seed growth." High flows also lowered chloride levels enabling plants to grow in parts of the western Delta that had previously been clear (CDBW, 1994).
On June 14, 1982 California Senate Bill 1344 became law, directing the California Department of Boating and Waterways (CDBW) to control water hyacinth in the Delta. CDBW set up barriers to keep large masses of floating plants out of navigation channels and sprayed the herbicides Weedar (2,4-D), Diquat and Rodeo (glyphosphate), at a cost that rose to about $400,000 annually. Program Supervisor Larry Thomas claims that if herbicides had not been used in 1986-1991, "water hyacinth would have shut the Delta down" (L. Thomas, pers. comm., 1994)
In some areas mechanical harvesting has been used to control hyacinth, but this is expensive (typically around $1,500 to $3,000 per acre) and disposal of the hyacinth can be a problem. Because of the cost, CDBW does not use mechanical harvesting (L. Thomas, pers. comm., 1994).
In 1982 and 1983 CDBW, working with the U. S. Department of Agriculture, imported and released three insects from South America as biological controls, the moth Sameodes albiguttalis (which did not survive) and the weevils Neochetina bruchi and N. eichhorniae. Although the two weevils became established in the Delta, there is no evidence that they control water hyacinth (Thomas & Anderson, 1983; L. Thomas, pers. comm., 1994).
Of the three flowering forms of water hyacinth, only medium-style plants have been found in California even though these plants are heterozygous for style length. This suggests that water hyacinth does not reproduce sexually in California. Conditions preventing sexual reproduction may include a lack of effective insect pollinators foraging in hyacinth (although honeybees Apis mellifera may be effective where they visit hyacinth), and a lack of open shallow water or saturated soil sites which are needed for germination and seedling establishment (Barrett, 1980, 1989).
Today water hyacinth is locally abundant in ponds, sloughs and waterways in the Central Valley, the Bay Area, and the southern Coast and Peninsular ranges (Hickman, 1993), and very dense in many waterways in the Delta. In 1988-1990 it was found in 4 of 10 sites in the Delta surveyed for littoral zone vegetation (IESP, 1991). In 1993 hyacinth again became very dense in parts of the Delta and the San Joaquin Valley drainage, despite herbicide treatment of around 1,500 acres (CDBW, 1994).
In the Philippines, the leaves of this troublesome weed are sold
as a market vegetable under the name of "waterlilly"
or "dahon" (Ladines & Lontoc, 1983).
Iris pseudacorus Linnaeus [IRIDACEAE]
YELLOW FLAG, YELLOW IRIS
A native of Europe, Iris pseudacorus was a popular garden flower that escaped from cultivation. The first populations reported in North America were from near Poughkeepsie, New York in 1868, from a swamp near Ithaca, New York in 1886 and from Massachusetts in 1889, and it was first reported from Canada at Ontario in 1940 (Mills et al., 1993, 1995). It is now widespread east of the Rocky Mountains (Hickman, 1993).
Jepson (1951) did not mention Iris pseudacorus, but Mason
(1957) reported that it "has escaped in Merced County and
is apparently moving down the watercourses." It has since
been found in irrigation ditches and pond margins in the San Francisco
Bay area, in the southern San Joaquin Valley, and in Sonoma County
(Munz, 1968; Hickman, 1993). Atwater (1980) found it was the only
common introduced plant on Delta islets, reporting it from the
banks of 4 out of 6 islets surveyed in 1978-79.
Polypogon elongatus Kunth, 1815 [POACEAE]
Native to South America, this plant is found in salt marshes and
on sand dunes in the Bay Area, including Contra Costa County,
and in the southern Coast Range (Munz, 1959, Hickman, 1993).
Potamogeton crispus Linnaeus, 1753 [POTAMOGETONACEAE]
CURLY-LEAF PONDWEED, CURLY PONDWEED
This pondweed is native to Europe and now found more-or-less worldwide, including Atlantic North America, California and Oregon (Steward et al., 1963). The earliest verified records in North America are from Delaware and Pennsylvania in the 1860s, although reports of it date back to 1807. It was deliberately introduced into parts of the Great Lakes basin to provide food for waterfowl, and is associated with fish hatcheries having perhaps been accidentally transported between watersheds in conjunction with fish stocking activities (Mills et al., 1993 citing Stuckey, 1979). It reportedly can grow in fresh, brackish or salt water (Mills et al., 1995).
It is uncommon in shallow water, ponds, reservoirs and streams
across most of cismontane California including the Bay Area and
the Central Valley (Munz, 1959; Hickman, 1993). In 1988-90 it
was found in 2 of 10 sites surveyed for littoral zone vegetation
in the Delta (IESP, 1991).
Spartina alterniflora Loiseleur-Deslongchamps [POACEAE]
SMOOTH CORDGRASS, SALT-WATER CORDGRASS
Spartina alterniflora is native to the coast of eastern North America from Maine to Texas (Muenscher, 1944) and has been introduced to Padilla Bay (1910), Thorndyke Bay (1930), Camano Island and Whidbey Island in Washington; the Siuslaw Estuary in Oregon; and New Zealand, England (1922) and China (1977) (Chung, 1990; Callaway, 1990; Callaway & Josselyn, 1992; Ratchford, 1995). Most literature states that S. alterniflora was first introduced to the northeastern Pacific in Willapa Bay, Washington, but both the date and mechanism of introduction to this site are unclear. In a brief note Scheffer (1945) reported first becoming aware of a cordgrass in Willapa Bay "about seven years ago"óthus about 1938óthat was identified as S. alterniflora in 1941. An oysterman reported first seeing the plants "about 1911," and Scheffer, believing that the first Atlantic oysters (shipped from Rhode Island) had been planted in Willapa Bay about 1907, concluded (apparently based on the coincidence in dates) that the cordgrass had been introduced with the oysters.
Sayce (1988) pointed out that Scheffer was mistaken about the initial date and origin of Atlantic oyster shipments to Willapa Bay, reporting that in fact the first shipment, of 80 barrels of oysters from estuaries near New York City and Chesapeake Bay, occurred in 1894, and that there were no subsequent introductions of Atlantic oysters for the next 50 years (although Carlton (1979a, p. 72) reports introductions of Atlantic oysters to Willapa Bay occurring in 1874 and 1894-1920s). Sayce did, however, continue to associate Spartina alterniflora with oyster shipments, stating that the Atlantic cordgrass was introduced with the 1894 shipment. She explained, "When the oysters were packed in barrels, in all likelihood the packing material was "salt grass" of one of two species, Spartina alterniflora or S. patens. S. patens has not been found in Willapa Bay. Either viable seeds or rhizomes of Spartina alterniflora were in the packing material." Nearly all subsequent authors have followed Sayce in reporting that S. alterniflora arrived in Willapa bay in 1894 as packing material for oysters. However, we have found no record of cordgrass ever having been used as packing material for any oyster shipments, nor is there any reason to think that hard-shelled oysters packed in barrels would need or benefit from additional packing. Thus, there is no basis for concluding that S. alterniflora was introduced to Willapa Bay in 1894.
Accordingly, we consider the first record of S. alterniflora in Willapa Bay to be "about 1911," and suggest solid ballast as the likeliest transport mechanism. Molecular genetic comparisons with east coast populations may clarify the source of the S. alterniflora stock in Willapa Bay (as has been done for San Francisco Bay S. alterniflora; C Daehler, pers. comm., 1995), providing additional information to resolve the probable means of transport.
Spartina alterniflora was separately introduced to San Francisco Bay in the early 1970s by the U. S. Army Corps of Engineers as mitigation for wetlands destroyed in the construction of the New Alameda Creek Flood Control Channel or as an experimental planting (anecdotal accounts and genetic analysis both indicating that the stock originated from Maryland; C. Daehler, pers. comm., 1995). It was planted at Pond 3 at the Coyote Hills Regional Shoreline. One source reported that after plantings of the native cordgrass S. foliosa did poorly, the area was replanted with the more robust S. alterniflora to produce a "successful" restoration.
S. alterniflora from Coyote Hills was later transplanted to San Bruno Slough near the San Francisco Airport by the Caltrans agency, either as mitigation for the Samtrans Bus Terminal or for erosion control. It may also have been planted in the Elsie Roemer Wildlife Refuge on the southwest shore of Alameda Island as part of yet another "restoration" project in 1983 or 1984, or for erosion control by the City of Alameda. It was found in Hayward Marsh in 1989 (Spicher & Josselyn, 1985; Calloway, 1990; Kelly, pers. comm., 1992; Faber, pers. comm., 1993; Taylor, pers. comm., 1993; Cohen, 1993).
In San Francisco Bay S. alterniflora is found both within existing salt marshes and extending into lower elevation mudflats. Comparing aerial photographs of the mouth of Coyote Hills Slough, Callaway (1990) saw no S. alterniflora in 1981 but counted 31 round patches in 1988 and 146 patches in 1990. Daehler & Strong (1994) found that "although some dense monocultures have formed," most S. alterniflora was growing in discrete circular patches separated by open mud, determined by isozyme analysis to consist of individual genetic clones. There are now a total of about 1,000 round or donut-shaped patches at southwestern Alameda Island and northeastern Bay Farm Island, San Leandro Bay, Hayward Marsh, Alameda Creek and Coyote Hills Slough (New Alameda Creek), and San Bruno Slough (near the San Francisco Airport). Smaller amounts are reported from the Estudillo Flood Control Channel south of the San Leandro Marina, the San Francisco Bay National Wildlife Refuge and the Cargill salt ponds near Newark, and the National Wildlife Refuge near Alviso (M. Taylor, pers. comm., 1993; J. Takekawa, pers. comm., 1994; C. Daehler, pers. comm., 1995).
New patches of S. alterniflora are established both from seed and vegetative fragments (Daehler & Strong, 1994). The cordgrass apparently arrived in Hayward as floating rhizomes (M. Taylor, pers. comm., 1993) and may be spread by dredges within the Cargill salt ponds (D. Strong, pers. comm., 1993). Daehler & Strong (1994) observed about 75 percent of patches setting very little seed in 1991-1992, and germination rates ranging from zero to 59 percent, and suggested that a few clones may be producing most of the seeds. On the other hand, Callaway (1990) found higher seed production (2,475 vs. 371 seeds/m2), higher seed viability (97% vs. 67%) and higher germination rates (average germination percentages of 77% vs. 49% in freshwater, and 37% vs. 14% in 25 ppt salinity) for S. alterniflora than for the native cordgrass Spartina foliosa in San Francisco Bay.
Spartina alterniflora grows both higher and lower in the intertidal zone than S. foliosa (Calloway, 1990; D. Strong, pers. comm., 1993; in Willapa Bay its total vertical range is at least 66 percent of the tidal range, Sayce, 1988), and can accrete sediment at a rapid rate (Sayce, 1988; Josselyn et al., 1993). By growing at a lower elevation it may reduce the area of mudflats in San Francisco Bay as it has in Willapa Bay, Washington, where it has turned an estimated 1,800-2,400 acres (5-6 percent) of Willapa Bay's mudflats into cordgrass islands (Ratchford, 1995). Callaway & Josselyn (1992) listed potential adverse impacts as: competitive replacement of native cordgrass; altered habitat for native wetland animals because of larger and more rigid stems and greater stem densities; altered habitat for infauna because of higher root densities; changed sediment dynamics; decreased benthic algal production because of lower light levels below cordgrass canopy; and loss of shorebird foraging habitat through colonization of mudflats. In British estuaries, the invasion of mudflats by Spartina anglica has produced adverse effects on shorebirds (Goss-Custard & Moser, 1990; Callaway, 1990).
The potential loss of native cordgrass is of particular concern, because it provides habitat for the severely endangered California clapper rail, Rallus longirostris obsoletus. On the other hand, S. alterniflora could possibly provide more and better cover and therefore better protection for the rail, which is threatened by predation by the introduced red fox, Vulpes vulpes (P. Kelly, pers. comm., 1992; Cohen, 1992, 1993).
In San Francisco Bay, S. alterniflora is attacked by the sap-feeding planthopper Prokelisia marginata at densities (ranging from 116 to 332 insects per inflorescence) much higher than typically observed on the Atlantic coast, and by the sap-feeding mirid bug Trigonotylus uhleri. However, this does not appear to affect growth rates, seed production or germination rates (Daehler & Strong, 1994, 1995).
The California Department of Fish and Game eliminated S. alterniflora from Humboldt Bayin about 5 years by constructing
a dike around a clump "the size of a house" and covering
it with black plastic, at a cost of $30,000 to $40,000 (M. Taylor,
pers. comm., 1993; D. Strong, pers. comm., 1993). Burning and
herbicides have been tried in Great Britain (P. Kelly, pers. comm.,
1992). After trying weed eaters and burning, the East Bay Regional
Park District's current control strategy at Hayward Marsh is to
cover with black plastic. The herbicide Rodeo (glyphosphate) has
been used at San Bruno Slough. Smooth cordgrass has now so thoroughly
clogged the New Alameda Creek Flood Control Channel (the project
for which the plant was originally introduced as mitigation) that
the Army Corps has proposed 5 years of helicopter-spraying Rodeo
in the channel (P. Baye, pers. comm., 1994).
Spartina anglica C. E. Hubbard, 1968 [POACEAE]
ENGLISH CORDGRASS
The western Atlantic cordgrass Spartina alterniflora (2n=62)was introduced in ship ballast to Southampton Water on the south coast of England, where it was collected in 1829. S. alterniflora there hybridized with the British cordgrass S. maritima (2n=60), producing a sterile F1 hybrid known as S. townsendii or S. x townsendii (2n=62) which was first collected in 1870 near Southampton, though not recognized as a hybrid until 1956. Chromosome doubling in this hybrid produced a fertile form (2n=120-124), probably present by the late 1880s as evidenced by a marked expansion of range, and collected in 1892. S. maritima disappeared from Southampton and nearby areas as the new form multiplied (Marchant, 1967). In 1968 Hubbard recognized this form as a separate species and named it S. anglica. This new species has proved to be an effective invader of both formerly unvegetated mudflats and of salt marsh, and, through a combination of transplantings for marsh reclamation purposes, vigorous clonal growth and natural dispersal, it now occupies 10,000 hectares (25,000 acres) of the British coast (Spicher & Josselyn, 1985; Thompson, 1991).
Another dimension to this story is provided by Chevalier's suggestion (1923; reported by Marchant, 1967) that S. maritima is itself not native to Great Britain, but was introduced there with shipping (possibly in solid ballast) from Africa.
S. anglica was reported from France by 1894, where it spread rapidly (Marchant, 1967). To control shoreline erosion and create salt marshes, S. anglica has been exported from England to many parts of the world, including Germany, Denmark, the Netherlands, China (where it now occupies over 36,000 hectares, almost entirely derived from 21 plants introduced in 1963), Australia and New Zealand (in 1930, where it was later declared a "noxious weed") (Hedgpeth, 1980; Spicher & Josselyn, 1985; Chung, 1990; Callaway, 1990; Callaway & Josselyn, 1992). Chung (1990) listed as additional reasons for planting S. anglica in China the accretion of land for reclamation; the amelioration of saline soils; the production of green manure; the provision of pasture and fodder for sheep, goats, mules, donkeys, horses, pigs, cattle, dairy cows, buffalo, rabbits and geese; the production of feed for tilapia, grass carp and other farmed fish; the increased production of nereid worms for export sale and of other invertebrates; the creation of biomass for fuel production; and the production of raw material for paper-making.
In 1961 or 1962 the U. S. Department of Agriculture and Washington State University introduced what was then known as S. townsendii into Puget Sound, Washington. Ramets of these plants were introduced into San Francisco Bay at Creekside Park Marsh, Marin County, as part of a marsh restoration project in 1977. Botanists realized these plants were in fact S. anglica when they flowered in 1983 (Spicher & Josselyn, 1985; Callaway, 1990).
In England S. anglica has hampered shorebird movement and feeding and correlates with a decline in dunlin (Calidris alpina) numbers (Goss-Custard & Moser, 1990), and has reduced macroinvertebrate densities (Callaway, 1990).
S. anglica has proved to be highly invasive in many parts
of the world (e. g. southern Great Britain, new Zealand and China),
and Thompson (1991) argued that S. anglica was a more successful
invader in Europe than the similar S. alterniflora because
of greater vigor and selective advantages conferred by allopolyploidy.
However, in San Francisco Bay S. alterniflora is the aggressive
invader while S. anglica has not spread from the marsh
where it was originally planted (Spicher & Josselyn, 1985).
Daehler (pers. comm., 1994) suggests that the Bay is near the
equatorial limit of S. anglica's potential range, a supposition
supported by S. anglica's production of only 20% viable
seeds in 1983 and failure to flower in 1984 (Spicher & Josselyn,
1985).
Spartina densiflora Brongniart [POACEAE]
DENSE-FLOWERED CORDGRASS
Spartina densiflora is native to Chile and was introduced
to Humboldt Bay in the mid-nineteenth century, probably in the
shingle ballast of lumber ships returning from Chile (a mechanism
also thought to be involved in the transport of the shorehopper
Transorchestia enigmatica to San Francisco Bay). S.
densiflora was transplanted from Humboldt Bay to Corte Madera
Marsh in 1976 as part of a restoration project at a time when
it was thought to be an ecotype of the native S. foliosa.
(Spicher & Josselyn, 1985; Callaway, 1990; Faber, pers. comm.,
1993). It is currently found in salt marshes at Creekside Park,
Corte Madera Creek, Muzzi Marsh and Greenwood Cove, all in southeastern
Marin County (Spicher & Josselyn, 1985).
Spartina patens (Aiton) Muhlenberg [POACEAE]
SALTMEADOW CORDGRASS, SALT HAY
Saltmeadow cordgrass is native to the eastern United States from Maine to Texas and reported rarely from inland marshes in New York and Michigan. Meadows of this cordgrass were sometimes harvested for hay used in packing and bedding material (Muencher, 1944).
Munz (1968) listed Spartina patens as "reported from Southampton Bay in a marsh, northwest of Benicia, Solano County, Mall." Atwater et al. (1979) referred to "R. E. Mall's report of salt hay at Southampton Bay" but could not find it there or elsewhere in the estuary. In 1985 Spicher & Josselyn again found "an existing patch" of the plant in Southampton Marsh which "does not appear to have spread from its original location," and in 1993 Josselyn et al. listed it from San Bruno Slough in the South Bay. Spartina patens was also introduced to Cox Island, Siuslaw River, Oregon in 1930 (Callaway, 1990), and to China in 1977 (Chung, 1990).
Given that various Spartina species have been extensively
transplanted around the globe, and that S. patens was intentionally
planted in Oregon, it seems probable that S. patens arrived
in San Francisco Bay as a component of some marsh restoration
or erosion control project (transplanted either from Oregon or
the east coast).
Typha angustifolia Linnaeus, 1753 [TYPHACEAE]
NARROW-LEAF CATTAIL, NAIL ROD
Narrow-leaf cattail is native to Eurasia and was reported as a rare member of the coastal flora of the eastern United States in the 1820s (Mills et al., 1993). It is now common in the northeastern states and Canada, and found inland to the Great Plains, in California and in South America.
Jepson (1951) reported it from Inyo County south to cismontane southern California, and by 1959 Munz reported it from marshes in central California. Hickman (1993), who describes it as "possibly naturalized in California," reports it from the central and southern coastal region of California, including the San Francisco Bay Area, and inland to the Central Valley and Lake Tahoe. Josselyn (1983) described it as one of the dominant species in the middle elevation zone of tidal brackish marshes in San Francisco Bay.
Hybrids with the native Typha latifolia are common in central
California including San Francisco Bay tidal marshes, and are
known as Typha x glauca (Munz, 1968; Josselyn, 1983;
Hickman, 1993).
Several workers have investigated the ciliate protozoans that live with or in the introduced mollusks and boring/burrowing isopods of San Francisco Bay. We regard those species originally described from Atlantic waters as being introduced with their hosts into the Bay. Ancistrumina kofoidi, treated here as a cryptogenic species (Table 2), is an additional probable introduction.
Mechanisms of introduction of commensal and symbiotic protozoans
are the same as their hosts, and are discussed with the latter.
Mechanisms of introduction of free-living attached or errant protozoans
include ship-fouling, ship-ballast (rock, sand, and water), and
the planting of commercial oysters.
Trochammina hadai Uchio
This brackish water, benthic foraminifer is native to Japan. It has been found in sediment cores collected in 1990-93 from six stations in the South Bay and from three stations in the Central Bay near the Marin County shore. It has not been found in over 140 sediment samples collected in 1964-70 and 1980-81 from throughout the Bay (D. Sloan, pers. comm., 1995; McGann, 1995; McGann & Sloan, 1995), suggesting that the introduction occurred in the 1980s.
Furthermore, where it is present T. hadai appears to be abundant in the upper sections of cores, less abundant in lower sections, and absent at depth. For example, in a core from the South Bay, T. hadai accounts for 52.2% of the benthic foraminifera in the top 2.5 cm, 8.8% at 8-10 cm depth, 0.7% at 18-20 cm depth, and is absent from the next 33 sections examined down to 352 cm depth (McGann, 1995). In a core taken from Richardson Bay in the Central Bay, T. hadai accounts for 16% of the foraminifera at 0-2 cm from the surface, 38% at 20-22 cm, 26% at 40-42 cm, 23% at 60-62 cm, 18% at 80-82 cm, 2% at 100-102 cm and less than 1% at 120-122 cm (D. Sloan, pers. comm., 1995). This pattern of depth distribution is likely due to bioturbation or other types of sediment disturbance mixing foraminifer tests from recently-deposited, near-surface sediments downward into deeper and earlier-deposited sediments. T. hadai's depth distribution may thus provide a means of measuring the physical and biological processes that mix sediments in different parts of the Bay, which, aside from telling us something about those processes, will be critical to efforts to use sediment cores to decipher the Bay's environmental history.
Although foraminifera have sometimes been observed in some types
of fouling (WHOI, 1952; ANC, pers. obs.), transpacific transport
in ship fouling seems unlikely for this benthic organism. Bottom
sediments and presumably benthic foraminifera as well are sometimes
churned up by wind turbulence or ship activity and taken in along
with water into ballast tanks; and foraminifera have been reported
from ballast water, though rarely (Carlton & Geller, 1993).
A benthic foraminifer could readily be transported with commercial
shipments of oysters, but there have been no significant plantings
of Japanese oysters in San Francisco Bay since the 1930s (Carlton,
1979a). A possible mechanism is transport in mud on anchors or
on anchor chains in chain lockers, as discussed by Schormann et
al. (1990).
Ancistrocoma pelseneeri Chatton & Lwoff, 1926
SYNONYMS: Parachaenia myae
This ciliate was described as Parachaenia myae by Kofoid
and Bush (1936) from the pericardial region and excurrent siphons
of the introduced clam Mya arenaria in San Francisco and
Tomales bays. Kozloff (1946) subsequently reported it from another
introduced clam, Macoma balthica, and from several native
clams in San Francisco and Tomales bays, and synonymized it with
the Atlantic ciliate Ancistrocoma pelseneeri, described
from Macoma balthica in Europe.
Ancistrum cyclidioides (Issel)
Kozloff (1946) recorded this European ciliate from the introduced
clam Mya arenaria in San Francisco Bay.
Boveria teredinidi Nelson, 1923
Pickard (1927) recorded this Atlantic protozoan from the gills
(ctenidia) of the introduced Atlantic shipworm Teredo navalis
in San Francisco Bay.
Sphenophyra dosiniae Chatton & Lwoff, 1926
This European ciliate was reported by Kozloff (1946) from the
introduced clam Mya arenaria and the native clam Cryptomya
californica in San Francisco Bay.
Cothurnia limnoriae Dons, 1927
This peritrich protozoan is found on the joints of the legs of
the introduced wood-boring isopod Limnoria (Mohr, 1959)
(in San Francisco Bay, as discussed elsewhere, only non-native
species of this gribble occur). It was reported from San Francisco
Bay by Kofoid & Miller (1927, p. 330, as Cothurnia
sp.), although it may have been present since Limnoria's
introduction about 1870. Although first described from Europe,
and later reported from southern California (Mohr, 1951), its
origins, like those of its host, are not known.
Lobochona prorates Mohr, LeVeque & Matsudo, 1963
This chonotrich protozoan occurs on the bristles (setae) of the
gills (pleopods) of the introduced wood-boring gribble Limnoria;
as with other gribble associates and the host species discussed
here, the origin is not known. Lobochona prorates was reported
by Kofoid & Miller (1927, p. 330, as Spirochona sp.;
see Mohr, 1966, p. 539) from San Francisco Bay, but may have been
introduced about 1870 with the isopod itself. It is widely reported
from southern California harbors (Carlton, 1979a).
Mirofolliculina limnoriae (Girard, 1883) Dons, 1927
SYNONYMS: Folliculina sp.
This heterotrich protozoan lives on the back of the pleotelson
of the introduced gribble Limnoria. As with the other Limnoria
associated ciliates, it is undoubtedly introduced, but its origins
remain unknown. It was reported from San Francisco Bay by Kofoid
& Miller (1927, p. 330, as Folliculina sp.).
Cliona sp.
BORING SPONGE
While the species level taxonomy of this yellow, shell-boring
sponge remains unresolved, Cliona is almost certainly represented
by one or more introduced species in San Francisco Bay. Bay populations
are likely to be referable to one or more of the common Cliona
found on oysters in Atlantic estuaries; these include Cliona
celata Grant, 1826 and Cliona lobata Hancock, 1849
(Carlton, 1979a, p. 218). Japanese species (or genomes) may also
be present. Atlantic Cliona were introduced with Atlantic
oysters. The first record is that of Townsend (1893), who observed
that in 1891 large numbers of oyster shells in the Bay "were
found honeycombed by the boring sponge."
Halichondria bowerbanki Burton, 1930
BOWERBANK'S HALICHONDRIA
SYNONYMS: Halichondria coalita
This Atlantic sponge, known from both Europe and Atlantic America,
was reported from the Pacific in San Francisco Bay in the early
1950s (Carlton, 1979a), and later from other sites including Humboldt
Bay (S. Larned, pers. comm., 1989) and Coos Bay (Hewitt, 1993).
It was either introduced with Atlantic oysters, with which it
occurs (pers. obs.) or as a fouling organism. In 1993-94 we found
Halichondria on most floating docks and with other fouling
in the South, Central and San Pablo bays, though not on docks
near the Golden Gate.
Haliclona loosanoffi Hartman, 1958
LOOSANOFF'S HALICLONA
SYNONYMS: Haliclona sp. B of Hartman, 1975
Haliclona ecbasis de Laubenfels, 1930
We newly follow and extend Van Soest (1976) in designating San Francisco Bay Haliclona as the Atlantic native Haliclona loosanoffi (although the recognition of this species in the Bay does not preclude more than one species being present). This is a common tan, yellow, and orange sponge of Bay fouling communities. This is the same species referred to as Haliclona sp. B by Hartman (1975), and is also the same species reported by Fell (1970) as Haliclona ecbasis from Berkeley Yacht Harbor, St. Francis Yacht Harbor, Redwood City and Carmel. Van Soest (1976) noted that Fell's (1970) description of H. ecbasis was very close to H. loosanoffi in all characters, including details of the life cycle, but came short of designating the Bay population as the Atlantic species solely because it was in the Pacific Ocean (Van Soest not considering the possibility that it was introduced). Haliclona, possibly including this species, have been reported from Puget Sound, Coos Bay, Bodega Harbor, and several bays in southern California (Carlton, 1979a, p. 216).
Haliclona loosanoffi is a common species of oyster communities on the New England coast (pers. obs.), and may have been introduced to the Bay with Atlantic oysters, although the earliest records are only from 1950 (Hartman, pers. comm., 1977). Its presence in fouling communities, however, means that it may have been introduced by ships as well.
In 1993 we found Haliclona on most floating docks in the
Central Bay and the seaward parts of South and San Pablo bays.
We did not find it in 1994 and 1995.
Microciona prolifera (Ellis and Solander, 1786)
RED BEARD SPONGE
This large, common Atlantic sponge is known from Canada to South Carolina. It was first found in San Francisco Bay in the mid- to late-1940s by Woody Williams (it was not noted by Light, 1941), who showed photographs to M. W. de Laubenfels (who initially identified it as the native Microciona microjoanna; Hartman, pers. comm., 1977). W. Hartman (pers. comm., 1977) found large colonies at Redwood City in 1950, and transplanted some of these for experimental purposes to Berkeley Yacht Harbor where it subsequently became established. Its bright orange-red finger-like colonies are unmistakable in the fouling communities around much of the Bay. In 1993-95 we observed it on several floating docks in the South Bay, the eastern shore of the Central Bay, and the southern part of San Pablo Bay.
Only two other populations are known on the Pacific coast, from Willapa Bay (Carlton, 1979a, p. 215) and Humboldt Bay (S. Larned, pers. comm., 1989).
Microciona could have been a late introduction with Atlantic
oystersóalong with the crab Rhithropanopeus harrisii
and the whelk Busycotypus canaliculatus which were first
found in San Francisco Bay at about this time, Microciona has
been collected from Atlantic oyster beds (Wells, 1961; Maurer
& Watling, 1973). Since it is a common fouling organism (ANC
& JTC, pers. obs.), it could also have been introduced in
ship fouling.
Prosuberites sp.
This undescribed American Atlantic sponge (Hartman, pers. comm.,
1977) was first collected in the Bay in 1953 on Angel Island (Carlton,
1979a, p. 217). It may have been introduced to San Francisco Bay
with Atlantic oysters or in ship fouling.
Numerous species of hydroids have been introduced to the Bay since
the Gold Rush. We treat 13 species here. Campanularia gelatinosa
and Halocordyle disticha (=Pennaria tiarella) may
still be present in the Bay, but there are no recent records,
and we thus list them in Appendix 2.
Blackfordia virginica Mayer, 1910
This Sarmatic hydroid, native to the Black and Caspian Seas, was first collected in 1970 in the Napa River and again in 1974 in the Petaluma River. It remained misidentified (as a species of Phialidium) until 1993 (Mills & Sommer, 1995), when we collected medusae in both rivers. In San Francisco Bay Blackfordia jellyfish eat copepods, copepod nauplii, and barnacle nauplii (Mills & Sommer, 1995).
Blackfordia may have been introduced in ships' fouling
or in ships' ballast water. The presence of widely scattered populations
in the Atlantic Ocean (Chesapeake Bay, Brazil, France, and Portugal)
and in India and China means that the source of the Bay's population
is unknown, although it is possible that if other populations
have diverged genetically, candidate source regions could be identified.
The introduction into the Bay in the 1980s-1990s of the clams
Potamocorbula and Theora, the mitten crab Eriocheir,
seven species of copepods, and other crustaceans, all from Asia,
might suggest a Chinese origin. Indeed, it is possible that the
recent populations of Blackfordia in the Bay represent
a reintroduction of the species.
Cladonema uchidai Hirai, 1958
This Japanese hydroid was first collected in San Francisco Bay in 1979 (Rees, 1982), although the polyps and medusae that have been studied to date have originated from laboratory or home aquaria containing fouling organisms from San Francisco Bay. The polyps in the laboratory were small (0.5 mm height) as were the medusae (3.5 mm height), and little remains known of this hydrozoan in the Bay.
Introduction with ship fouling or ballast water is possible, although
earlier introduction with Japanese oysters may have occurred if
Cladonema's habitat in Honshu includes oyster communities.
Clava multicornis (Forskaal, 1775)
CLUB HYDROID
SYNONYMS: Clava leptostyla Agassiz, 1862 of northeastern
Pacific authors; see Austin, 1984
Rees and Hand (1975) noted that this northwestern Atlantic hydroid
forms "large pink patches on pilings in estuaries."
It was first collected in the Bay in 1895 (Carlton, 1979b, p.
229), no doubt originating from ship introductions from the New
England coast, where it is common. Fraser (1937) described its
widespread distribution throughout the Bay as documented by Albatross
collections in 1912-13.
Cordylophora caspia (Pallas, 1771)
FRESHWATER HYDROID
SYNONYMS: Cordylophora lacustris Allman, 1844
This brackish and freshwater Sarmatic hydroid, native to the Caspian
and Black Sea regions, was first found in the Bay in the San Joaquin
River at Antioch. Specimens discovered in 1950 were considered
to have been collected "20 to 40 years" previously (Hand
& Gwilliam, 1951); we choose a date of 1930 as a first record.
It was also collected at a similarly early but uncertain date
from Lake Union in Seattle, and has now been reported from several
sites between San Francisco Bay and Vancouver Island, British
Columbia (Carlton, 1979a, p. 230). It is sufficiently widespread
around the world (Hand & Gwilliam, 1951), a distribution perhaps
achieved centuries ago, as to make the origin of the Bay's populations
unknown. It was likely introduced in ship fouling (WHOI, 1952)
or ballast water. Cordylophora is common in the Delta (Hazel
& Kelly, 1966) and on the concrete sides of the Delta-Mendota
water delivery canal (Eng, 1979), and has also been collected
in San Francisco's Lake Merced (Miller, 1958).
Corymorpha sp.
This tiny estuarine, orange-tinted hydroid was collected from soft mud bottoms on the eastern shore of the Bay at Point Richmond (1955-56) and in Oakland's Lake Merritt (1967) (Carlton, 1979a). It appears similar to the European Corymorpha nut