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Cohen, A.N., and J.T. Carlton, 1995. Nonindigenous Aquatic Species in a United States Estuary: A Case Study of the Biological Invasions of the San Francisco Bay and Delta, University of California at Berkeley, Williams College-Mystic Seaport Reprinted from a report of the United States Fish and Wildlife Service, Washington D.C., and the National Sea Grant College Program Connecticut Sea Grant Nonindigenous Aquatic Species in a United States Estuary: A Case Study of the Biological Invasions of the San Francisco Bay and Delta
Biological Study 1. The San Francisco Bay and Delta region is a highly invaded ecosystem. · 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. 2. A vast amount of energy now passes through and is utilized by the nonindigenous biota of the Estuary. In the 1990s, introduced species dominate many of the Estuary's food webs. · 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.
3. Introduced species may be causing profound structural changes to some of the Estuary's habitats. · 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. 4. While no introduction in the Estuary has unambiguously caused the extinction of a native species, introductions have led to the complete habitat or regional extirpation of species, have contributed to the global extinction of a California freshwater fish, and are now strongly contributing to the further demise of endangered marsh birds and mammals. · 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. 5. Though the economic impacts of introduced organisms in the San Francisco Estuary are substantial, they are poorly quantified. · 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. RESEARCH NEEDS 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: 1. Experimental Ecology of Invasions 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. 2. Regional Shipping Study 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. 3. Intraregional Human-Mediated Dispersal Vectors 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. 4. Study of the Baitworm and Lobster Shipping Industries 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. 5. Molecular Genetic Studies of Invaders 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. 6. Increased Utilization of Exotic 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). 7. Potential Zebra Mussel Invasion 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. 8. Economic Impacts of Wood Borers and Fouling Organisms 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. 9. Economic, Ecological and Geological Impacts of Bioeroding Nonindigenous Species 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. 10. Post-Invasion Control Mechanisms 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. Contact: Andrew N. Cohen, Energy and Resources Group, University of
California at Berkeley, Berkeley, California 94720 |