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1
Spartina Introductions and
Consequences in Salt Marshes
arrive, survive, thrive, and sometimes hybridize*
D. R. Strong and D. A. Ayres
Maritime Spartina species define and maintain the shoreline along broad expanses of
temperate coasts where they are native. The large Spartina species grow lower on the
tidal plane than other vascular plants; tall, stiff stems reduce waves and currents to
precipitate sediments from turbid estuarine waters. With the right conditions, roots grow
upward through harvested sediments to elevate the marsh. This engineering can alter
the physical, hydrological, and ecological environments of salt marshes and estuaries.
Where native, Spartinas are uniformly valued, mostly for defining and solidifying the
shore. The potential to terrestrialize the shore was the rationale of many of the scores of
Spartina introductions. In a time of rising sea levels, these plants are valued as a barrier
to the sea in native areas and in China and Europe where they have been cultivated.
In contrast, in North America, Australia, Tasmania, and New Zealand, nonnative
Spartinas are seen as a bane both to ecology and to human uses of salt marshes and
estuaries. Four of the seven large-scale invasions involved interspecific hybrids between
introduced and native Spartinas, or intraspecific hybridization between formerly
allopatric populations. Rapid evolution driven by selection of genotypes particularly
adapted for invasive behavior could be the cause of observed high spread rates of hybrid
cordgrass. The study of Spartina introductions is a rich mixture of social and basic
sciences, with interaction of human values, ecology, and evolution.
Spartina species, cordgrasses, are powerful
ecosystem engineers and grow over a great
range of elevations in the intertidal zone (see
chap. 16 in this volume). Their tall, stiff stems
*“Arrive, Survive, and Thrive” as a rubric for species introduction and invasion was coined by Kevin Rice, Richard
Mack, and Spencer Barrett.
reduce wave energy and cause sediments carried in estuarine waters to precipitate (see
chap. 2); the plants then grow into these sediments with the result of marsh elevation. The
motivation for many early Spartina introductions was to stabilize shorelines and terrestrialize intertidal lands. Storm and tidal defenses in
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a time of rising sea levels are more recent values
for these plants on the low coasts of Europe and
China, as well as where the maritime Spartina
species are native. In other places, such as
North America, Australia, Tasmania, and New
Zealand, the potent ecosystem engineering of
nonnative and hybrid Spartinas is seen as a
bane both to ecology and to human uses of salt
marshes and estuaries.
Many of the scores of Spartina introductions
for which we have records have been purposeful, and a few have come about as inadvertent
hitchhikers on other human activities. Most introductions failed, some spread little, and a few
have spread widely by dint of the ability of the
seed of these plants to float on the tide. Seedladen inflorescences can disperse great distances within rafts of wrack, which form in the
fall when the aboveground parts of the plant
senesce. The four most extensively introduced
species are the maritime species S alterniflora,
S. patens, S. densiflora, and the allopolyploid of
recent origin, S. anglica.
Growing near docks, cordgrasses were an
abundant and convenient source of cushioning
for ballast. The oldest known introduction, S.
densiflora, from South America to the Gulf of
Cadiz, Spain, in the sixteenth century (Castillo
et al. 2000), may well have been ballast packing.
The first records of this practice are from seventeenth-century England (Ranwell 1967). On the
East Coast of North America, bales of S. patens
and S. alterniflora were packed as cushions
among heavy items in the holds of ships (Civille
et al. 2005). However, the large numbers of
voyages from the Atlantic to the Pacific from the
sixteenth century onward resulted in no known
introductions of Spartina. All of the Pacific introductions came with the twentieth century, and
none are known to have resulted from ballast.
The first recorded introductions of S. alterniflora were to France (1803) and England
(1816) from North America. In both countries,
the invasions led to stands of the plant that
were used by people. For example, early in the
nineteenth century, residents used S. alterniflora
to thatch roofs on the Itchen River, England
4
(Marchant 1967). These invasions initially
thrived then receded. Patches of dieback are
not unusual for S. alterniflora (Mendelssohn
and McKee 1988) and S. anglica (Goodman,
Braybrooks, and Lambert 1959). S. alterniflora
apparently did not spread much beyond its introduction sites in Brittany and the southwest
of France (Baumel et al. 2003), and it is now
extremely rare in the United Kingdom (Gray,
Marshall, and Raybauld 1991). In both countries, early ranges of S. alterniflora overlapped
with S. maritima in multiple places, giving
great potential for hybridization. Marchant
(1967) speculates that these S. alterniflora
introductions were from ships’ ballast from
America. While it is possible that the European
introductions were inadvertent, it is also
reasonable that European visitors to North
America purposefully carried the plant home.
S. alterniflora is a much taller and more robust
plant than the European S. maritima, and the
American species had obviously greater potential to produce fodder and fiber. It is also reasonable to assume that people who used the
plant would encourage its growth and spread.
The contrast between salt marshes along the
Atlantic Coast of North America, the center of
diversity for Spartina, and those where cordgrasses have been introduced illustrates the influences of these plants. In Atlantic North
American estuaries, there are no invasive cordgrasses, and the natives are distinctly valuable
in maintaining the shoreline habitat (Warren
et al. 2002). Only at the fringes of the range of
the genus—in Europe, the South Atlantic, and
the Pacific—do native and invading Spartinas
coexist. In estuaries of the Pacific, Australia,
Europe, and China, nonnative Spartinas bring
large changes (see chap. 16 in this volume).
Human introductions of Spartinas have led to
hybrids, some of which spread rapidly and are
powerful ecological engineers. Four of the
seven largest invasions are by hybrids between
introduced and native Spartinas (S. anglica in
Europe, China, and Puget Sound, Washington;
and S. alterniflora ⫻ S. foliosa in San Francisco
Bay, California) and another (S. alterniflora to
invasions in north american salt marshes
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China) was by intraspecific hybrids selected for
vigor and fertility. The other two large-scale invasions are S. alterniflora in Willapa Bay,
Washington, which is not hybridized, and S.
densiflora in Humboldt Bay, California, which
could bear a remnant of hybridization with S.
alterniflora (Baumel et al. 2002).
Spartina is a small genus of halophytic
species in the Chloridoideae, a monophyletic
lineage of the Poaceae (Hsiao et al. 1999). Most
species are native to the maritime, north temperate Atlantic, New World (Mobberley 1956;
Baumel et al. 2002). S. alterniflora is native to
the Atlantic shore of South America, and S.
densiflora is native to both the Atlantic and
Pacific of South America. Before S. anglica,
only one species was native to Western Europe
(S. maritima); S. anglica is an allopolyploid hybrid species that arose in the nineteenth century, in Europe, shortly after one of its parents,
S. alterniflora, was introduced there from the
New World. S. maritima was the European,
male parental species (Ferris, King, and Gray
1997). North America is home to most species.
Many maritime salt marshes of the Atlantic
and Gulf coasts of North America are dominated by S. alterniflora, the smooth cordgrass,
which ranges from Canada through the Gulf of
Mexico and along the Atlantic coast of South
America. The second-most widespread and
abundant North American species is S. patens,
the salt hay grass, which ranges from Canada
through the Gulf and into Mexico and into the
Caribbean. Pacific maritime estuaries have
only two natives, S. foliosa in California from
San Francisco Bay south through Baja
California, and S. densiflora in the Pacific of
Chile and the Atlantic of South America. The
Argentine S. longispica is inferred to be a hybrid
of the native S. densiflora and S. alterniflora
there (Orensanz et al. 2002). While no evidence exists that such species as S. alterniflora
and S. densiflora are hybridized, they are hexaploids. Research will possibly reveal evidence
of hybridization in their history, such as that
hinted at in S. densiflora in Humboldt Bay,
California (Baumel et al. 2002). In this review,
we focus on Spartina species that have been
introduced beyond their native ranges.
SPARTINAS ARE ECOSYSTEM ENGINEERS
Spartinas can be particularly influential to other
species especially when they affect marsh elevation of the marsh. In one well-studied marsh in
New England, the accumulation and loss of
mineral sediment and organic matter have maintained equilibrium of the marsh surface with sea
level for four thousand years (Redfield 1972).
Modification and regulation of the environment
that is mediated biologically and large relative to
abiotic influences is termed ecological or ecosystem engineering (Jones, Lawton, and Shachak
1994, 1997). Although ecological engineering by
organisms is neither a simple nor a single phenomenon (Reichman and Seabloom 2002),
wide-ranging discussion over the past decade has
verified ecological engineering as widely important in nature; the concept comprises a multifaceted set of notions with evolutionary, ecosystem,
and community implications as well as shortertermed autecological ones (Bruno 2000).
Spartina plants are the head engineers in
temperate marshes where they occur, just as
are mangroves in the tropics. Spartinas epitomize organisms with powerful reciprocal
influences between biotic and physical environmental features and have been called
“foundation species” (Pennings and Bertness
2001). The ecosystem engineering prowess of
Spartinas comes from their erect, stiff stems,
which create drag, dissipate hydrodynamic
forces, and reduce wave height and current velocity (see fig. 1.1). Stiffer stems are more costly
metabolically than more flexible stems and can
be seen as an adaptation to harvest sediment,
which increases plant fitness (Bouma et al.
2005). Sediments that are delivered to marshes
by the tides, storms, rainfall, and riverine input
(Allen and Pye 1992; Neumeier and Ciavola
2004) are trapped within the Spartina canopy.
Roots grow up through the harvested sediment,
elevating the marsh. With these influences,
cordgrasses can affect the ecology of the marsh
spartina introductions and consequences
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Spartina
Zostera
Dissipated wave height, δh (mm/m)
Stiff strips
Flexible strips
SF
SG
10
SF
ZF
SG
1
100
1000
10,000
100,000
FIGURE 1.1 Drag as a function of wave energy for Spartina anglica and Zostera noltii. The stiff culms of S. anglica give a
higher slope of drag with increasing wave energy than the flexible stems of Z. noltii. The high drag lows water movement,
which results in sediment deposition. From Bouma et al. 2005, fig. 6.)
well above and below where they grow on the
tidal plane.
With the appropriate conditions, the sediment harvesting of S. alterniflora can maintain
broad, flat monospecific salt marsh platforms
close to the mean high tide. In a South Carolina
estuary, primary productivity of S. alterniflora
was greatest toward the lower tidal elevation tolerance of Spartina, at a depth between 40 and
60 centimeters below mean high tide (see
fig. 1.2). This was where most sediment was
trapped and salinity lowest. Hypoxia limited
productivity at depths below maximum productivity, while hypersaline pore water owing to
evaporation limited growth at higher elevations;
stunted, short-form S. alterniflora grew at these
higher elevations. This processes created a
potentially hump-shaped function of primary
productivity with position along the intertidal
gradient (Morris et al. 2002). It is these relationships that allow S. alterniflora marshes to maintain equilibrium with sea-level changes over
short and very long time scales.
6
The coast of the Mississippi Delta was built
on sediments deposited by the river and elevated in this manner by S. alterniflora as sea levels rose during the Holocene (Redfern 1983).
Decreasing sediment supply has led to loss of
coast areas in the delta (Stockstad 2005). In the
Netherlands, a declining sediment budget could
affect many aspects of salt marshes and S.
anglica dynamics in the future (Riese 2005). In
San Francisco Bay, a deficit of sediment will
hamper restoration of the massive South Bay
Salt Ponds. Sediment supply in the south arm
of the estuary is less than 1 million cubic yards
(MCY) per year, while the restoration project
will require well over 100 MCY (Siegel and
Bachland 2002). In New Zealand, both introduced S. alterniflora and S. anglica accreted so
much sediment as to negatively affect mangroves and salt marshes (Lee and Partridge
1983). In Ireland (Hammand and Cooper
2002), the United Kingdom (Goss-Custard and
Moser 1988), Tasmania (Kriwoken and Hedge
2000), and San Francisco Bay (Stralberg et al.
invasions in north american salt marshes
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Stable region
Unstable
2800
Aboveground production (g.m–2.yr–1)
2400
2000
1600
1200
800
400
0
0
10
20
30
40
50
Depth below MHT, D (cm)
60
70
80
FIGURE 1.2 The curved relationship between net productivity of Spartina alterniflora as a function of position on the
intertidal plane (depth below mean high tide [MHT]). Highest productivity occurs near the lowest elevations where salinities
are lowest; at slightly lower elevations, hypoxia reduces productivity so much that S. alterniflora is excluded. At elevations
above the peak productivity, evapotranspiration increases sediment salinity, which limits growth. Open circles are data from
low marsh; closed circles, from high marsh. From Morris et al. 2002, fig. 2.
2004), nonnative Spartinas and hybrids cover
the soft sediments and exclude the invertebrate
food of shorebirds.
RATIONALES, HISTORIES, AND EVOLVING
VALUES IN SPARTINA INTRODUCTIONS
And that old man asked me to think of
United States Marines in a Godforsaken
swamp. “Their trucks and tanks and howitzers are wallowing,” he complained, “sinking in stinking miasma and ooze.” He
raised a finger and winked at me. But suppose, young man, that one Marine had with
him a tiny capsule containing a seed of icenine, a new way for the atoms of water to
stack and lock, to freeze. If that Marine
threw that Seed into the nearest puddle.
Kurt Vonnegut, Cat’s Cradle
Many Spartina introductions were the product of high, if vague, hopes to solidify soft mud
and increase the economic value of salt
marshes. The “most obvious economic application of Spartina is to use it for the reclamation
and stabilization of muddy foreshores. There is
no plant in the world better fitted for this particular purpose” (Oliver 1925, 84). Though muted,
early concerns about Spartina introductions anticipated those of today: overly optimistic scenarios, adverse effects on other economic uses
of estuaries and salt marshes (e.g., oyster culture and navigation), limited agricultural value
of reclaimed salt marshes, decreased recreational and aesthetic value of beaches invaded
by the plant, and threats to the ecology and wild
life of salt marshes (Ranwell 1967). “Whether
the result will in the end be beneficial or to the
spartina introductions and consequences
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contrary will depend greatly on local conditions.
In any case it will be a change worth watching
and studying” (Stapf 1908, 34). Herbicide applications to introduced Spartina were under way
in the United Kingdom by the mid–twentieth
century (Ranwell and Downing 1960).
EUROPE
Today in Iberian and Mediterranean regions, S.
maritima gives desired protection against erosion during storms; unlike the more robust
species and hybrids forming the bulk of this
review, the small, diffusely growing S. maritima
does not accrete sediment during calm periods
(Neumeier and Ciavola 2004). The distribution
of S. maritima may have been influenced by
humans; it “has been known for a long time
(since 1629), and is beyond doubt truly indigenous to Europe” (Stapf 1908, 33). At the same
time, this species is found along the west coast
of Africa and in South Africa (Mobberley 1956).
It is possible that S. maritima is a Southern
Hemisphere (“tropical”) species long ago introduced to Europe by early shipping (Marchant
1967, fig. 3). A report of Spartina pollen in early
Holocene sediments of South Africa (Meadows
and Baxter 2001) raises the possibility of fragmented S. maritima populations strung along
the Atlantic coasts of southern Europe and
Africa. Such a distribution would mirror the
disjunctive populations of S. alterniflora that
range along the South American Atlantic coast.
S. patens, first detected in Europe in 1849, was
thought until recently to be native there
(Mobberley 1956). It has long been widespread
and harvested for hay and fodder on the Atlantic
and the Mediterranean coasts of Europe as well as
in its native range (Ainouche, Baumel, and
Salmon 2004). Reports of the invasive S. patens in
Spain (Javier et al. 2005) do not mention any desirable features of the species, such as protection
against erosion. Forming dense monocultures, it
is now seen as a threat to native high marsh vegetation in natural areas of the Mediterranean and
Iberian coasts (Castillo et al. 2005).
S. densiflora, a native of Chile and
Argentina, is believed to have been introduced,
8
either accidentally or purposefully, in the sixteenth century to the southwestern corner of
Spain on the Atlantic. In the Gulf of Cadiz, S.
densiflora has spread to eight estuaries and a
number of shoreline habitats including dunes,
high marsh, salt pans, and intertidal flats. A
North African invasive population is presumably derived from the Spanish introduction
(Castillo et al. 2005).
S. anglica is presumed to have invaded
France by floating without human aid across
the English Channel. It was first detected in
France in 1906, at Baie des Veys, Normandy
(Baumel, Ainouche, and Levasseur 2001). The
invasion proceeded during the remainder of the
twentieth century from Normandy southward
through Brittany mainly without human intervention. S. anglica now occupies nearly all suitable habitats along this shore of France. The
prodigious abilities to accrete sediment of S.
anglica can greatly change intertidal elevations
and ecology where it has invaded in France
(Guénégou et al. 1991).
The Netherlands and Germany were invaded by S. anglica during the 1920s (Gray et al.
1991). It grew lower than the native vegetation
and trapped volumes of sediment there. The
influence of S. anglica is now greatest in areas
with most available sediment, and its influence
decreases to the north where colder winters hinder the plant (Bakker et al. 2002). In the southern Netherlands, S. anglica was important for
holding sediments and building elevated land
that is now being restored with native vegetation (de Jonge and de Jong 2002). S. anglica
spread to Ireland in the 1930s and is now seen
as a bane to natural areas and conservation. The
intentions are to eradicate it from Ireland, and
only a shortage of funds has prevented attainment of this goal (Hammond and Cooper
2002). The twentieth century saw a shift from
agriculture to sea defenses as the major human
value of salt marshes in both the Netherlands
and the United Kingdom.
Rising sea levels and increasing storm
strength maintain the value of S. anglica in
parts of Europe as a protection from coastal
invasions in north american salt marshes
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flooding (Bouma et al. 2005). Productivity of
S. anglica in the United Kingdom could increase with rising temperatures and higher atmospheric CO2 concentrations, but other
factors, such as competition with other marsh
species, complicate this picture (Gray and Mogg
2001). In the Netherlands, human influences
on salt marshes have long rivaled, if not
exceeded, those of weather, geology, and hydrology. In the late twentieth century, terrestrialization of the shore has vied for limited fine
sediments with ecologically and economically
valuable intertidal mud flats—a phenomenon
called “the Wadden Sea squeeze” (Delafontaine,
Flemming, and Mai 2000). The sediments
from large rivers that would feed the marshes of
shallow coastal areas are now shunted offshore
down deep shipping channels into the North
Sea (Riese 2005).
Sediment loss via shipping channels is also a
threat to coastal marshes of Louisiana in North
America (Redfern 1983). The dredged, deepwater passage of the Mississippi River carries
sediments offshore into the Gulf of Mexico. Six
hundred square kilometers of coastal Louisiana
salt marsh have washed into the sea in the last
decade, and the loss is greater during hurricanes (Stockstad 2005). Were these sediments
to be delivered over the fresh- and saltwater
marshes of Louisiana, as before dredging of the
Mississippi channels, the rate of coastal loss
would be much less (Committee on the
Restoration and Protection of Coastal Louisiana
2006). Vast monospecific stands of S. alterniflora define this coast, and the prodigious
sediment-holding and -elevating capacities of
this plant would contribute substantially to the
maintenance of the land there.
Protection from the sea is the value of S.
anglica in the southeastern United Kingdom,
where the Earth’s crust is subsiding while sea
level rises. However, multiple values of restoration, conservation, mariculture, and sea defense
combine—and even come into conflict—in salt
marsh issues in the United Kingdom. For
example, the removal of S. anglica in marsh
restoration and conservation has led to lawsuits
based on allegations that liberated sediment
harmed nearby oyster culturing (Kirby 1994).
Complications for managing S. anglica in
European Union countries arise from needs to
meld traditional with modern uses of the shoreline differently among regions (Pethick 2002).
Moreover, the human values of salt marshes are
evolving rapidly. “Until the last decade, salt
marsh has often been conceived as coastal
wasteland with minimal economic value, which
has led to considerable loss through land reclamation for use as agriculture, caravan sites, industrial developments and marinas.” (King and
Lester 1995, 181). In recent years, sea defenses
that include S. anglica have risen to the highest
levels among these multiple values of salt
marshes (King and Lester 1995), but this can
conflict with conservation. In parts of the United
Kingdom, dense monospecific swards of S.
anglica replaced mud flats and excluded native
invertebrates and the shorebirds that feed on
them (Goss-Custard and Moser 1988; Frid,
Chandrasekara, and Davey 1999). Subsidence of
the southeastern UK coast means a sediment
deficit in the long run, and even S. anglica can afford little protection to rising sea levels under
these conditions.
NEW ZEALAND
Early in the twentieth century, there was unabashed enthusiasm for the potential of nonnative Spartina in New Zealand. “For thousands of
years tidal salt mud flats the world over have
made entrances to harbours unsightly and
treacherous and have remained as vast areas of
waste flats. . . . In the past they have provided an
almost unconquerable challenge to man. . . .
Now such mud can be conquered, and . . . reclaimed to form useful and stable farmlands.
This plant which has such an important role
is . . . Spartina townsendii” (Harbord 1949, 507).
By 1950, the slow growth of introductions of
S. anglica and S. ⫻ townsendii on the North
Island of New Zealand shifted attention to S.
alterniflora, albeit with a soft counterpoint of
caution. “Extensive areas of tidal flats round
New Zealand’s coastline, usually difficult and
spartina introductions and consequences
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costly to develop, have become the subject of
renewed interest with the introduction of the
maritime grass Spartina alterniflora, which will
enable many farmers to capitalize on these
naturally fertile soils. . . . However, farmers are
warned that the adverse influences may not
always be readily apparent” (Blick 1965, 275). In
the subsequent decade or so, attitudes reversed
from conquering to preserving salt marshes. “In
some places the problems caused by its spread
are virtually insurmountable. With renewed appreciation of estuarine wetlands in their natural
states, planting of any species of Spartina
around the coast of New Zealand should not be
allowed to take place. Suitable control and eradication measures need to be developed where
Spartina is already present” (Partridge et al.
1987, 567). During the last sixteen years, new
herbicides and new methods of application have
eradicated all meadows and patches of S. anglica
on the South Island (Miller 2004).
AUSTRALIA AND TASMANIA
The motivations for introduction of S. anglica
into Australia were vague and mostly the product
of little more than curiosity among European
colonists about what might grow there. Unlike
the United Kingdom, the Netherlands, and New
Zealand, where farmland from marshland was a
focused objective, Australia had no general engineering or agricultural problems to be solved by
the plant (Boston 1981). The successful plantings
were clustered in southwestern Australia, where
the last recorded planting was made in 1962.
In Tasmania, the objective for S. anglica was
clear: “to stabilize the mudflats so that they
would eventually be above high water level and
become relatively useful land . . . [and] . . . force
stream flow into the central part of the river,
creating a scouring effect and keeping the
main channel free of mud” (Wells 1995, 12).
Plantings of S. anglica were done from 1930
until 1968. Values changed and the negative
results of the plant came into focus: reduction
of areas of soft sediments where shorebirds
forage, harm to native animal communities,
large unwanted changes to the appearance of
10
the shore and beaches, and lack of access to the
water across the S. anglica sward, which had
been an open shore (Hedge and Kriwoken
2000). S. anglica was also seen as a threat to the
Tasmanian oyster industry (Hedge and
Kriwoken 2000). During the early 1990s, S.
anglica was seen as undesirable and was removed with herbicides and other means in both
Australia and Tasmania (Wells 1995). In recent
years in Tasmania, opinion has shifted to retaining S. anglica as a habitat and food source for
native species that have lost habitat to land
clearing and industrial activity (M. Sheehan,
personal communication)
CHINA
Shorelines in China have been densely occupied for thousands of years, and shoreline dynamics have long been affected as much by
human activities as by geology, weather, and
hydrology (Li et al. 1991). In the last half of the
twentieth century, several species of Spartina
were introduced. While future coastal sediment
loads will decrease with new dams (Chen et al.
2005), recent decades have seen staggeringly
large volumes of sediment discharged from the
vast, densely populated watersheds of the
Yangtze, Yellow, and Pearl rivers. From two to
three square kilometers of new intertidal lands
appeared on these sediments annually (Han
et al. 2000). Some botanically inclined authors
have praised introduced Spartinas in China.
S. anglica, introduced in 1963, was planted in
about a hundred locations over 2,700 kilometers of coastline and spread to 33,000 hectares
by the 1980s. Accreting sediment at high intertidal levels, S. anglica was touted as protecting
dikes from erosion during typhoons and contributing to the creation of new pastureland (as
part and parcel of polderizing: diking, freshwater flooding, and drainage). Spartina was harvested for green manure, animal fodder, fish
food, and cellulose for paper and rope (Chung,
Zhuo, and Xu 1983, 1993). The taller S. alterniflora was planted widely in China in 1975 and
grew lower on the tidal gradient than S. anglica.
It accreted sediment at a prodigious rate in a
invasions in north american salt marshes
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band two hundred kilometers long and ninety
kilometers wide by 1997 (Chung et al. 2004;
Zhang et al. 2004). Brief accounts of concern
that S. alterniflora displaces native marsh species
have been published recently (Zhang et al.
2004; Xie et al. 2001; An et al. 2004). At least
some view nonnative Spartina to be distinctly
undesirable in China (Ding et al. 2008).
A different perspective comes from the literature of physical geography, where Spartina
comprises no more than the most minor of
footnotes. Coastal areas of China are extremely
vulnerable to sea level rise (Han et al. 2000).
Agriculture by diking has been practiced on the
shores of the Pearl River Delta since the Han
Dynasty, beginning around 200 BCE. Age-old
human effects on the shoreline accelerated with
industrial development when China opened to
the outside world. Dikes have always been the
main means of reclamation of intertidal lands,
and building of dikes does not need Spartina.
Dikes line almost the entire Pearl River Delta,
and any appearance of a tidal flat is immediately
diked, drained, and flushed of salts. Wetlands,
mangroves, and tidal flats have been completely
eliminated. The entire region is on very low,
muddy, subsiding ground that is vulnerable to
freshwater floods from inland and typhoon
flooding from the sea.
SAN FRANCISCO BAY, CALIFORNIA
The salt marshes of San Francisco Bay are a casualty of 150 years of “reclamation,” in which the
vast majority of intertidal and supertidal habitat,
both brackish and salty, were diked and drained
for agriculture, urban development, and industry (Williams and Faber 2001). The remaining
125 square kilometers, 5 percent of those found
by Euro-Americans in this huge Pacific Coast estuary, are the foundation of conservation efforts
with shorebirds of the Pacific flyway and of three
federally endangered species (a mammal, a bird,
and a plant). These tenuous salt marshes, and
brackish and freshwater wetlands upstream,
form a narrow buffer for wildlife and ecosystem
services between San Francisco Bay and surrounding human population and agriculture.
Introduced Spartina played virtually no role
until 1975, when the U.S. Army Corps of
Engineers planted S. alterniflora, which hybridized with the native S. foliosa soon afterward
(Faber 2000).
Ironically, native S. foliosa was a poster child
for the destruction of salt marshes. “This species
is useful in reclaiming salt marshes, and in several places about San Francisco Bay it has modified the coast line and increased the acreage of
many farms. The town of Reclamation received
its name from the fact that in that vicinity many
acres of land have been reclaimed chiefly by the
use of this grass” (Merrill 1902, 6). Actually,
Reclamation was not a town but rather a “locality” with few inhabitants on San Pablo Bay,
upstream on the Sacramento River from San
Francisco Bay (Durham 1998). A post office was
established at Reclamation in 1891 and discontinued in 1903 (Salley 1977). S. foliosa is a
modest ecosystem engineer, small, diffusely
growing, and shallow rooted. It is but a minor
league sediment trapper compared to S. anglica,
S. alterniflora, and the massive S. alterniflora ⫻
S. foliosa hybrids now spreading through San
Francisco Bay. Reclamation, California, originally salt- and freshwater marshes and now extensive hay and oat fields, was formed by diking,
dredging, and draining the wetlands. While
S. foliosa probably made little contribution to the
reclamation, it is playing a role in restoration of
a small fraction of the shore. Conservation interests opened 340 hectares to the sea during the
1990s, and S. foliosa will grow to form a band at
the lowest tidal elevation on at least part of erstwhile Reclamation, California (Marcus 2000).
INVASIVE SPARTINAS ON THE PACIFIC
COAST OF NORTH AMERICA
Perhaps the first Pacific introduction was S.
densiflora to Humboldt Bay, California, speculated to have been introduced there as early as
the 1850s from Chile (Spicher and Josselyn
1985; Kittleson and Boyd 1997) and identified
in 1984 (Faber 2000). In 1999, it was found in
329 hectares and 94 percent of the salt marshes
spartina introductions and consequences
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of Humboldt Bay (Pickart 2001). S. densiflora
was dominant over a wide tidal range, from low
Salicornia virginica marsh to the species-rich
high marsh (Eicher 1987). It is the object of control by herbicides and cutting, as it threatens
two rare plant species classified as endangered
under State of California and federal regulations, Menzies’ wallflower, Erysimum menziesii,
and the beach Layia, Layia carnosa (Pickart
2005). S. densiflora from Humboldt Bay was
planted at least twice in San Francisco Bay in
the 1970s and 1980s (Faber 2000) and had
spread from Marin County to about five
hectares at three sites by 1999 (Ayres et al.
2004). In 2002, a few plants of unknown origin
were found in Gray’s Harbor, Washington
(Murphy 2004); and in 2005, it was discovered
in Vancouver, Canada (G. Williams, personal
communication).
The first known Pacific introduction of S.
alterniflora is to Willapa Bay, Washington, an
estuary forty-four kilometers long and twenty
kilometers wide just north of the Columbia
River. The plant probably arrived as a hitchhiker
in live oyster shipments rather than from
shipping ballast (Civille et al. 2005). The first
Euro-American settlements on Willapa Bay exploited native oysters and began export to San
Francisco in the 1850s. The oyster industry grew
rapidly, but by the 1880s, native oysters were in
decline owing to overexploitation in Willapa Bay.
For a few years, Atlantic oysters, Crassostrea virginica, were imported from populations cultivated in San Francisco Bay. If California
cordgrass, S. foliosa, was introduced in these
shipments, it was never detected and has become extinct in Willapa Bay. In 1893, eighty barrels of Atlantic oysters were imported to Willapa
Bay directly from Atlantic marshes on the new
transcontinental railroad. The origins of the oysters were from areas in New York Harbor and
Long Island, where native S. alterniflora flourished. Upon arrival at Willapa Bay, after the
nine- to thirteen-day rail journey, the contents of
the barrels were spread widely in the intertidal.
More than three hundred railcars of eighty to
one hundred barrels each of oysters were
12
imported to Willapa Bay from New York between 1893 and 1919. Cordgrass seed and plants
could easily have been placed into the barrels
with the oysters. Most likely, the introduction
was inadvertent. We know of no economic value
for cordgrasses at that time and place, and the
abundant discussion in the press during the
early twentieth century about introductions
from the Atlantic to the Pacific Coast of oysters
and other species with commercial potential
lacks any mention of Spartina. Whether the
large colonies of smooth cordgrass that appeared in several places in Willapa Bay a few
decades later were introduced and spread inadvertently or had some intentional component is
not known. Oystermen, who were the biggest
users of the bay in the early twentieth century,
viewed the plant as undesirable (Sayce 1988).
The earliest written record is an anecdotal
account that implies but does not say that S. alterniflora was in the bay in 1911 (Sheffer 1945).
The earliest photographs of it show large plants
in several widely spaced areas in Willapa Bay
(Civille et al. 2005). A Sheffer photograph of
1940 (Civille et al. 2005), the earliest known of
smooth cordgrass in Willapa Bay, shows a plant
or group of plants about 42 meters in diameter,
covering nearly 1,385 square meters. Aerial photographs from 1945 show similarly large plants
at seven widely separated sites on the bay, some
twenty kilometers apart from one another.
Present-day growth rates of S. alterniflora in
Willapa Bay suggest that the plants in the photos were about fifty years old. This implies that
S. alterniflora had dispersed, or was spread by
humans, widely in Willapa Bay and thrived very
soon after the earliest oyster trains dumped oysters there from the Atlantic, in 1893 (see fig. 1.3).
Maritime Spartina seed disperses long distances quickly without human help by floating
on tides and currents. There is no evidence that
maritime Spartina has a seed bank, and all recruitment comes from seeds less than a year
old. Floating seed was responsible for virtually
the entire invasion of Willapa Bay, and rhizome
fragments have made virtually no contribution
to the spread of S. alterniflora there (Civille et al.
invasions in north american salt marshes
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M
B
C
B
C
H
D
D
K
E
E
G
G
F
A
F
2000
1945
L
FIGURE 1.3 The relative abundance of the earliest known colonies of Spartina alterniflora in
Willapa Bay, Washington, in 1945 (left) and the growth of this plant by 2000 (right). Note the
proximity of the earliest known colonies of S. alterniflora to the approximate locations of oyster
beds at the beginning of the twentieth century (Jensen Spit, North Cove, Kindred Slough, Palix
River, Nemah River, and Seal Slough).
2005). New areas have consistently been invaded at densities so low that young individual
plants grew separated by meters of open intertidal mud. These isolated recruits grew rhizomatously into isolated circular plants, each
composed of a single genet. The lack of other
emergent plants on the open mud makes new
colonies of cordgrass obvious on aerial photographs, reminiscent of bacterial colonies
growing on agar. Over several decades, isolated
plants grew rhizomatously into continuous
meadows of S. alterniflora. These meadows
completely cover the intertidal mud (Davis,
Taylor, Civille, et al. 2004).
Isolated plants comprised a very large fraction of S. alterniflora in Willapa Bay through the
twentieth century and contributed little to the
spread of the invasion because they set very
little seed (Davis, Taylor, Civille, et al. 2004).
The meadows produced most of the seed and
were responsible for driving the invasion. The
seed set of meadow plants was nearly tenfold
that of isolated plants, 20 percent compared to
2 percent of florets set seed, respectively. While
92 percent of meadow plants produced at least
some seed, only 37 percent of isolated plants
produced any seed at all. The lower reproductive rate of isolated plants than of those in
meadows was an Allee effect. Because the lowest densities of isolated recruits had high survival, grew rhizomatously, and did set some
seed, the Allee effect was weak (Taylor et al.
2004). S. alterniflora is self-incompatible, outbreeding, and therefore requires pollen from
another plant in order to set seed (Daehler
1998). The cause of the Allee effect was sparse
pollen among the isolated plants. Only in the
much older meadows was the density of the
spartina introductions and consequences
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wind-borne pollen sufficient for substantial
seed set in Willapa Bay (Davis, Taylor,
Lambrinos, et al. 2004).
The coverage of S. alterniflora in Willapa Bay
grew at a remarkably constant 12 percent or so
annually over the fifty-five-year history of aerial
photographs. In 2000, nearly a hundred years
after the invasion began, the invader covered
about 1,670 hectares, or 27 percent of the 6,000
hectares of the intertidal habitat of Willapa Bay.
Without the Allee effect, the invasion would
have covered virtually the entire bay long ago
(Taylor et al. 2004).
Other small infestations of S. alterniflora
appeared in Washington, Oregon, and northern
California during the twentieth century. Duck
hunters introduced S. alterniflora to Dike Island
in Padilla Bay, Puget Sound, Washington, between 1940 and 1946 (Riggs and Bulthuis
1994). The seed was provided by a nursery in
Wisconsin, but there is no record of the maritime area from which the nursery obtained the
seed. The Padilla Bay introduction had spread
to cover about 1.4 hectares by 1979 and about
4.9 hectares by 1991. Flowering stems were
first seen in October 1992. Some of this seed
was viable, and seedlings had appeared around
Dike Island by the late 1990s. Control efforts
are greatly reducing S. alterniflora and S. anglica
in Padilla Bay (Riggs 2005). In the 1990s,
several small infestations were discovered: in
Grays Harbor, Washington, twenty-five kilometers to the north of Willapa Bay; in Conner
Creek farther north; and in the Copalis River yet
farther to the north (Murphy 2004). These presumably arose from seed that floated northward
in S. alterniflora wrack on currents from Willapa
Bay, without human help. The environmental
community in Washington is aware of several
other small infestations of S. alterniflora in
Puget Sound (Riggs 2005; Murphy 2004), and
we infer that the lack of reporting indicates that
these either have been eradicated or are not
spreading.
In Oregon, S. alterniflora from Georgia on
the Atlantic Coast of North America was
purposefully planted in the 1970s, in the
14
Siuslaw River at the entry to Coos Bay, Oregon
(Frenkel and Boss 1988). The patch had grown
to cover about two hectares by 1994, when it
was sprayed with herbicides and dug up. With
no visible growth, it was declared to be eradicated in 1997. In 2005, five culms of S. alterniflora were found on the same site, and another
patch of this species was discovered downstream in Coos Bay, presumably brought there
as rhizome material in dredge spoils from the
first site (Howard et al. 2007). This indicates
potential for local dispersal by rhizomes. In
Humboldt Bay of northern California, a single
large patch of S. alterniflora was presumably
eradicated by the efforts of the California
Department of Fish and Game during the
1980s or early 1990s (Cohen and Carlton 1995).
The Pacific Coast of North America had two
known introductions of S. anglica, both recent.
That in Puget Sound was planted in 1961, perhaps with seed from England (Hacker et al.
2001). During the intervening forty years or so,
the infestation spread to more than seventy
sites over a roughly linear course of about 160
kilometers to affect 3,300 hectares and to cover
solidly nearly 400 hectares. The San Francisco
population of S. anglica was detected in the
1980s and by 2004 had grown to only twentyfour individuals covering 360 square meters.
The largest plant was eight meters in diameter,
and what was inferred to be the oldest plant was
six meters in diameter (Ayres et al. 2004).
In August 2003, S. anglica was discovered
in southwest British Columbia, Canada, in the
Fraser River estuary, the largest estuary on the
Pacific Coast of Canada (Williams et al. 2004).
Seeds presumably originated from the S. anglica populations in Puget Sound, which extend as far north as Orcas Island, about twelve
miles south of the Fraser River mouth. By
October, mapping had been completed, and
manual removal began. Surveys in November
discovered another invaded site in Boundary
Bay. In 2004, a multiagency committee was
established to conduct removal, begin outreach and education of naturalists, and enlist
volunteer support.
invasions in north american salt marshes
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S. patens, salt marsh hay, has been introduced to the Pacific Coast of North America, as
well as to Europe and China (described earlier).
It was first known in Oregon as three small
patches in a 1939 aerial photograph of Cox
Island in the Siuslaw River. Fifty years later, it
had grown to ninety large monospecific patches
(Frenkel and Boss 1988). In San Francisco Bay,
two plants of S. patens were found in 1970 at the
mouth of Suisun Bay near the town of Benicia,
in the Southampton marsh (Ayres et al. 2004).
SPARTINA HYBRIDIZATION
In 1974, the U.S. Army Corps of Engineers conducted test plantings of S. foliosa and Salicornia
virginica on unconfined dredge spoils deposited
along Coyote Hills Slough (also known as
New Alameda Creek) near Fremont, California
(37⬚33⬘58.62⬙ N by 122⬚07⬘44.52⬙ W) as part of
a larger study to quantify and ameliorate the
impact of dredging and dredged material disposal in San Francisco Bay (U.S. Army Corps of
Engineers 1976). The immediate goal of these
plantings was to determine the feasibility of
using native marsh species to create a salt marsh
on dredge spoils confined in a former salt pond
(pond 3) adjacent to New Coyote Hills Slough,
while the eventual goal was to evaluate whether
this approach had potential utility as a means to
both dispose of dredge spoil and create new salt
marsh. After determining that native species
were able to establish from sown and tidally
borne seed, the Corps of Engineers inexplicably
planted S. alterniflora in pond 3 from seed it had
obtained from an environmental consulting
firm in Maryland (Faber 2000). According to
personal communication in 2005 between Jun
Bando of the University of California, Davis, and
L. Hunter-Cario, the firm’s nursery manager, the
S. alterniflora seed came from marshes in Maine
and Virginia in the 1970s. A genetic survey of
plants growing along Coyote Hills Slough in
1994 found equal numbers of S. alterniflora and
hybrids between S. alterniflora and S. foliosa, and
a single S. foliosa (out of forty-five specimens)
(Ayres et al. 1999).
In 1978, the Corps of Engineers planned to
use both native and exotic smooth Spartina to
control shoreline erosion at Alameda Island,
fifteen miles to the north of pond 3 (U.S. Army
Corps of Engineers 1978). When this population was genetically surveyed in 1998, only hybrid and smooth cordgrass was found; the
native species was absent (Ayres et al. 1999).
Similarly, the native species was absent from an
introduced population at San Bruno marsh that
contained equal numbers of hybrid and S.
alterniflora plants in 1994.
In recent surveys, hybrid cordgrass is spreading rapidly in the San Francisco estuary, while
the native and nonnative parents are now becoming rarer (Ayres, Baye, and Strong 2003;
Sloop 2005). The hybrid swarm hinders access
to shorelines, blocks flood control channels,
overgrows intertidal foraging areas of shorebirds, and without control could lead to the extinction of the native S. foliosa in San Francisco
Bay by means of competition and pollen swamping (Ayres et al. 2003). The potential spread of
these hybrids southward through the range of
S. foliosa, in southern California and Baja
California, carries the risk of global extinction of
S. foliosa (Ayres et al. 2003). A large control program is trying to eradicate hybrid cordgrass
from San Francisco Bay (www.spartina.org).
Hybridizations resulting from human introductions loom large in Spartina biogeography
and in the huge influence that nonnative cordgrasses have had in salt marshes around the
world. The history and incidence of Spartina hybridizations are incompletely known. For example, the S. densiflora in Humboldt Bay, California,
has genetic features that suggest introgression
from S. alterniflora (Baumel et al. 2002). S. ⫻
townsendii is a sterile F1 homoploid hybrid
species that formed in Southampton Water in
southeastern England in the nineteenth century
(Gray et al. 1991). The parental species were
S. alterniflora, introduced from America, and
S. maritima, presumably native to Europe. The
first notice of these homoploid hybrids noted was
in Southampton Water, England, in 1870. It was
given the name S. ⫻ townsendii (Marchant 1967),
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while other hybridizations of these parental
species occurred in France and are named S.
neyrautii (Ainouche et al. 2003). Only in
Southampton Water did subsequent chromosomal doubling occur. It gave rise to the fertile,
dodecaploid, allotetraploid species, S. anglica,
around 1890 (Gray et al. 1991).
S. anglica was spread and dispersed on its
own to salt marshes throughout Britain
(Raybould et al. 1991), France (Gray et al. 1991),
and beyond. The introduced S. alterniflora is
now extremely narrowly restricted in Britain, at
Southampton Water at the hybridization site
(Gray et al. 2001). S. alterniflora maintains
small, vigorous populations at the three sites in
France to which it was introduced in the early
twentieth century (Baumel et al. 2002). The
lack of spread could be due to pollen scarcity as
S. alterniflora is largely self-incompatible (Davis,
Taylor, Civille, et al. 2004; Davis, Taylor,
Lambrinos, et al. 2004).
S. ⫻ townsendii is rare today. It was not fully
discriminated from S. anglica until the 1960s,
after many years of exportation from Poole
Harbor. The Spartina nursery at Arne had both
forms in the sward in the 1950s. S. ⫻ townsendii
grew together with S. anglica in the south and
southeast of England and on the Isle of Wight
(Goodman et al. 1969, fig. 3). While little information exists on export to most places except
New Zealand, sterile S. ⫻ townsendii would have
been outcompeted by fertile S. anglica in mixed
swards. East Anglia marshes had both forms
through the 1930s and 1940s (Gray et al. 1991).
In a world survey, Ranwell (1967) grouped
S. ⫻ townsendii with S. anglica under the rubric
S. townsendii sensu lato (s.l.) and noted that by
1870, one or both of these hybrids had been
spread about the United Kingdom. While seed
of the allotetraploid S. anglica disperses on the
tide, the sterile diploid sets no seed and could be
spread only by humans or, rarely, by means of
floating vegetative fragments that might break
loose from an eroding bank. Globally, both were
spread widely and covered more than twentyeight thousand hectares around the world when
Ranwell (1967) recorded twenty-two successful
16
introductions and twenty-two failures. Specifically, for 1967, Europe saw thirteen success and
no failures; Australia and New Zealand, eight
successes and three failures; and Puget Sound,
one success, no failures. The rest were apparent
failures: India and Asia, seven; South Africa,
two; the Red Sea, one; the Mediterranean, one;
the western Atlantic, five; Greenland, one;
British Columbia, one; and Hawaii, one
(Ranwell 1967, fig. 1). The higher success rate
in Europe was matched by wider spread there
(in maximum estimated hectares in 1967): the
United Kingdom, 12,000; France, 8,000;
Netherlands, 5,800; Germany, 800; Denmark,
500; Ireland, 400; Tasmania and New Zealand,
each 40; Australia, 20; and Puget Sound, less
than 1.
The second known hybridization of S.
alterniflora with a native species occurred in San
Francisco Bay after introduction of this Atlantic
native in 1976 by the U.S. Army Corps of
Engineers (Faber 2000). Most introductions of
S. alterniflora to the Pacific were beyond the
ranges of native Spartina species and posed no
possibility of hybridization. The northern limit
of the only native north temperate species in the
Pacific, S. foliosa, California cordgrass, is
Drake’s Estero, forty kilometers north of San
Francisco Bay. Introductions north of San
Francisco Bay, to Washington, Oregon, and
northern California, were into regions with no
native Spartina. California cordgrass, S. foliosa,
was the native parent species of these hybrids.
Although not known at the time, many of the
hybrids were purposefully spread during the
1980s from the earliest site of hybridization,
which was in pond 3, adjacent to Coyote Hills
Slough (New Alameda Creek) at the southeastern end of San Francisco Bay. Seed floating on
the tide spread the hybrids to many other
marshes over eastern and western shores of the
sixty kilometers of shoreline in the southern
arm of the bay. A few hybrid colonies established in salt marshes of Marin County, on the
north side of the Golden Gate. In the earliest
published record of this invasion (Callaway and
Josselyn 1992), cordgrasses assumed to be
invasions in north american salt marshes
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S. alterniflora, but probably hybrids, were found
to be competitively superior to, and to have a
wider tidal range than, the native S. foliosa.
Hybrids were detected in the mid-1990s
when plants were found that contained genetic
material unique to each parent (Daehler and
Strong 1997). The highly diverse nuclear and
cytoplasmic composition together with chromosome numbers equal to or close to the parents’
suggested that these plants comprised a swarm
of backcrossing hybrids rather than an allopolyploidization, as per S. anglica (Ayres et al. 1999;
Anttila et al. 2000). Much of the shoreline and
most creeks flowing into the southern arm of
San Francisco Bay were invaded by hybrid cordgrass by 2004 (see fig. 1.4).
Native California cordgrass, S. foliosa, is
shorter, with shallower roots, and grows less
densely than vigorous hybrid genotypes (Daehler
and Strong 1997). The vigorous subset of hybrid
genotypes is transgressive; it grew larger and
produced more inflorescences, pollen, and seed
than either parent species (Ayres et al. 1999,
2003). Transgressively vigorous hybrids are now
found at the two leading edges of the hybrid invasion. One leading edge is in the native marshes
Spartina patens
Spartina anglica
Spartina alterniflora/hybrid
Spartina densiflora
Coast line
N
0
12
km
FIGURE 1.4 Distribution of exotic cordgrasses in San Francisco Bay, 2001. From Ayres et al. 2004.
spartina introductions and consequences
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of dense S. foliosa growing above mean sea level.
In native marshes, hybrids spread by vegetative
competitive displacement of the native species
and by swamping native stigmas with pollen,
which leads to hybrid seed. Where large hybrids
are growing, most S. foliosa flowers set hybrid
seed. The other leading edge of the invasion is
below mean sea level on the vast, open, intertidal
mud flats of the bay. While very few recruits of
native California cordgrass appeared in open
areas in the San Francisco estuary in recent years
(Sloop 2005), the hybrid swarm increased
tremendously in numbers and coverage in both
native marshes and previously open mudflats.
Both vegetative expansion and multiple episodes
of seedling recruitment contribute to the invasion by hybrids.
The area of San Francisco Bay covered by hybrids in 1975 was about two hectares. By 1990,
about 650 circular plants expanding vegetatively were noted on aerial photos, and we estimated this to amount to five hectares. In 1993,
the number of such hybrids had increased to
one thousand, many had coalesced to form
meadows, and we estimated the cover to be
nearly ten hectares. In 2001, cover of hybrids
was 190 hectares. While exponential growth in
cover gives a semilog straight line, the semilog
plot of the data for hybrid cover from these
years gives a convex line. This indicates that the
rate of spread of hybrid cordgrass has increased.
The transgressive traits caused by hybridization
undoubtedly contributed greatly to the very
high rate of spread in San Francisco Bay.
In China, intraspecific hybridization of multiple S. alterniflora populations may have created genotypes with a propensity to spread
rapidly. Seeds and cutting of Spartina alterniflora from Morehead City, North Carolina,
Altamaha Estuary, Georgia, and Tampa Bay,
Florida, were sent to C. H. Chung at Nanjing
University in China in 1979 (Chung et al.
2004). They were grown in the Botanical
Garden their first year, and their growth was
carefully monitored. There were striking differences among the populations in phenotypic
characters; for example, the maximum height
18
of Georgia plants was almost three meters,
while the largest Florida plants were half that
height (An et al. 2004). Differences were also
found in isozyme banding patterns, indicating
genetic as well as phenotypic variation among
the populations. In 1981, rooted cuttings from
the nursery population were planted into a
1,300-square-meter field site at Luouyuan Bay.
Ecotypic differences persisted in the field plantation. In 1985, a nursery was established in a
village paddy near Chengmengkou using mixed
seed collected from the Luouyuan Bay field site.
Plants and/or seeds (references don’t say
which) from the nursery were outplanted into
three field sites for experimental monitoring.
The allopatric S. alterniflora provenances
cultured together in China could have readily hybridized. They were mixed within a small 1,300square-meter plot. The potentially hybrid seed
was sown into a common paddy, and then a mixture of genotypes was selected, with preference
for Georgia provenances, in the first large field trials. Adding to this genetic farrago, at some point
0.5 kilogram of seeds from North Carolina was
introduced, and one source claims that it was this
source that led to most of the salt marshes in
coastal China (An et al. 2004). It is not unlikely
that hybrids and the most vigorous progeny were
spread widely. Intraspecific hybridization could
well have played a role in the rapid spread of S. alterniflora thorough Chinese marshes.
The high planting densities in the Chinese
planting could have overcome Allee effects
(Davis, Taylor, Civille, et al. 2004; Davis, Taylor,
Lambrinos, et al. 2004). It is also possible that
the rapid spread is a product of evolution of selfcompatibility, which occurred in the hybrids of
S. foliosa ⫻ S. alterniflora in San Francisco Bay
(Sloop 2005). No interspecific hybridization is
known for Chinese S. alterniflora, but it is possible that the intraspecific hybridization of the
three North American provenances produced
self-compatible genotypes.
Acknowledgments. We thank Daniel Goldstein of
the University of California, Davis, library for help
with the history of Reclamation, California; Tjeerd
invasions in north american salt marshes
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Bouma and Alan Gray for advice about S. anglica
on the coast of the Netherlands and the United
Kingdom, respectively; Kevin Rice, Richard Mack,
and Spencer Barrett for coining “Arrive, Survive,
and Thrive”; and three anonymous reviewers for
helpful suggestions on the manuscript. T. B. C.
Shaw provided inspiration.
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