Episodic global dispersal in shallow water marine
organisms: the case history of the European
shore crabs

Carcinus maenas

and

C. aestuarii

James T. Carlton

and Andrew N. Cohen

2 1

Maritime Studies Program, Williams

College-Mystic Seaport, Mystic, CT, USA and

San Francisco Estuary Institute, Oakland,

CA, USA

Abstract

Aim

This paper evaluates global collection records, evidence of anthropogenic transport

methods, and experimental and distributional data relative to temperature requirements
to understand the historical and potential dispersal of a well-known genus of estuarine
crab.

Location

The records analysed are from temperate and tropical coastal ocean areas.

Methods

The study is based primarily on literature analysis and examination of

museum specimens.

Results

The human-mediated successful global dispersal of the European shore crabs

Carcinus maenas

(Linnaeus, 1758) and

C. aestuarii

(Nardo, 1847) occurred in three

major episodes: around 1800, in the 1850s–70s, and in the 1980s–90s. The nineteenth
century introductions occurred through transport by ships (probably in hull fouling or in
solid ballast), while the introductions in the 1980s could have occurred through a greater
variety of dispersal mechanisms (ships

hull fouling and seawater system fouling; fouling

on semisubmersible drilling platforms; ballast water; transport with fisheries products
intended for food or bait; scientific research; releases from aquaria maintained for
educational or scientific purposes; or intentional non-governmental releases for human
food production). These introductions have resulted in

Carcinus

establishment in five

temperate regions outside of its native Europe in Atlantic North America, Australia,
South Africa, Japan and Pacific North America, while releases into tropical regions have
not established populations.

C. maenas

range in both its native and introduced regions

appears to be regulated by similar temperature parameters, enabling an assessment of its
potential distribution.

Main conclusions

The second episode of

Carcinus

global dispersal, the period from the

1850s to 1870s, may be part of a broader surge of world-wide invasions caused by an
increase in shipping.

Keywords

Australia, ballast water, biological invasion, California,

Carcinus aestuarii

Carcinus

maenas

Carcinus mediterraneus

, dispersal, Europe, fouling, green crab, introduction,

invasion history, Japan, South Africa, United States.

*Correspondence: James T. Carlton, Maritime Studies Program, Williams College-Mystic Seaport, 75, Greenmanville Avenue, PO Box 6000, Mystic, CT 06355,
USA. E-mail: jcarlton@williams.edu

Journal of Biogeography,

, 1809–1820

2003 Blackwell Publishing Ltd

I N T R O D U C T I O N

Despite growing recognition of the extent of invasions in
coastal waters (Cohen & Carlton, 1998; Carlton, 1999a,
2001; Ruiz

et al.

, 2000; Grosholz, 2002), little is known of

the temporal patterns of these invasions. Detailed histories
of marine invasions and the timing of human-mediated
transport mechanisms have been developed for only a few
species. These include the Atlantic snail

Littorina littorea

Linnaeus, 1758 (Carlton

et al.

, 1982), the Asian seaweeds

Sargassum muticum

Yendo (Fensholt) (Critchley, 1983) and

Codium fragile tomentosoides

(van Goor) Silva (Carlton &

Scanlon, 1985), the Indian Ocean isopod

Sphaeroma walkeri

(Stebbing, 1905) (Carlton & Iverson, 1981) and the Asian
isopod

Synidotea laevidorsalis

Miers, 1881 (Chapman &

Carlton, 1991, 1994).

The recent establishment of the European shore (or

green) crab

Carcinus maenas

(Linnaeus, 1758) (Fig. 1) on

the Pacific coast of North America (Cohen

et al.

, 1995;

Grosholz & Ruiz, 1995) prompted us to review and cor-
rect the description of its global spread over the past two
centuries, both to clarify patterns in its dispersal and to
provide a basis for predicting its further range expansion.
We also review the distribution and spread of its congener

C. aestuarii

(Nardo, 1847) (

C. mediterraneus

Czer-

niavsky, 1884), briefly consider other invasion episodes
contemporaneous with one major period in

Carcinus

dis-

persal history, and suggest that further investigation may
reveal a period in the nineteenth century when new inva-
sions began to increase dramatically because of a surge in
global shipping.

M A T E R I A L S A N D M E T H O D S

We examined collections for older reported material of

Carcinus

at the Smithsonian Institution National Museum of

Natural History, Washington, DC (NMNH) and at the Yale
University Peabody Museum of Natural History, New
Haven, CT (PMNH). In addition, we assembled and rean-
alysed all previous (and some long overlooked) reports and
records of

Carcinus

from around the world.

The existence of two species,

C. maenas

and

C. aestuarii

has been argued on various morphological grounds. In

material that we examined we distinguished these species
using morphological characters as previously described
(Cohen

et al.

, 1995). Recently, molecular genetic techniques

have been utilized to distinguish these species (Geller

et al.

1997; Bagley & Geller, 2001).

R E S U L T S

Global pattern of episodic dispersal

Carcinus maenas

is native to Atlantic Europe and perhaps

northwest Africa (Appendix 1, Fig. 2) while

C. aestuarii

native to the Mediterranean Sea and perhaps the Canary
Islands (Appendix 1). In common with many coastal marine
invertebrates, the extreme high and low latitude range
records may represent occasional larval sets to the north or
south, or temporary range expansions related to favourable
but transient climatic and environmental conditions.

Outside of Europe,

C. maenas

-hybrids have

become established in five major regions of the globe (the
northwest and southeast Atlantic Ocean, and the northwest,
northeast and southwest Pacific Ocean) and

C. aestuarii

-hybrids in two of these (the southeast Atlantic

Ocean and the northwest Pacific Ocean). We suggest that

Carcinus

has successfully spread around the world in three

major episodes: (1) in a period around 1800, (2) in the
1850s–70s, and (3) in the 1980s–90s.

Carcinus maenas

was first reported in two regions outside

of Europe in 1817. Material recently relocated in the

His-

torical Collections

of the Muse´um Nationale d’histoire

Naturelle (MNHN) and labeled

Red Sea

was collected by

Savigny either during the expedition to Egypt in 1799–1801
or a little later, and illustrated and identified as

C. maenas

(Savigny, 1817; Audouin, 1826; D. Guinot, pers. comm.,
1999). Based upon pleopod morphology, the specimens are

C. maenas

(D. Guinot, pers. comm., 1999). The collection of

C. maenas

in the Red Sea prior to the 1869 opening of the

Suez Canal suggests transport on a ship travelling around
Africa.

The only other early nineteenth-century record of

Carci-

nus

outside of Europe was in North America, where it

became established. Major transatlantic trade routes were in
place by this time, with ships carrying manufactured goods
from Europe to North America in trade for tobacco, furs,
indigo, naval stores, and other products (Natkiel & Preston,
1986). Say (1817) reported

C. maenas

[mistakenly describ-

ing it as a new species (Appendix 1)] from the east coast of
the USA without providing a specific locality. Rathbun
(1930) believed that Rafinesque’s (1817) report of

Portunus

menoides

from New York and New Jersey referred to

C. maenas,

but since Rafinesque noted two wrist spines as

opposed to the single spine of

Carcinus,

his material may

have been

Ovalipes ocellatus

(Herbst, 1799). De Kay (1844)

reported

C. maenas

abundant in Long Island Sound and at

Newport, Rhode Island.

Writing in 1871, Verrill

et al.

(1873) reported

C. maenas

distribution to be from New Jersey to Cape Cod and sug-
gested that the crab’s failure to range as far north as it did in

Figure 1

Carcinus maenas

(Linnaeus, 1758) from Rathbun (1930).

2003 Blackwell Publishing Ltd,

Journal of Biogeography

, 1809–1820

1810 J. T. Carlton and A. N. Cohen

Europe indicated that it was a distinct species. However,

C. maenas

continued to move north. It was collected at

Provincetown on the northeast tip of Cape Cod in 1872, at
Boston and in southern Maine in the 1890s, and at the
Canadian border in 1951. By 1964, it had spread around the
Bay of Fundy and south-eastern Nova Scotia as far as
Halifax, by 1982 had advanced another 130 km to Mar-
ie-Joseph, and in the late 1990s reached Cape Breton Island,
passed through Canso Strait and arrived on the eastern shore
of Prince Edward Island (Smith, 1879; Glude, 1955; Welch,
1968; Nova Scotia Museum collections; Gillis

et al.

, 2000).

Several workers, including Rachel Carson in

The Edge of the

Sea

(Carson, 1955), have suggested that

C. maenas

north-

ward expansion along the Gulf of Maine and into Canada
was related to warming trends (Glude, 1955; Taylor

et al.

1957; Welch, 1968; Vermeij, 1978), but it is possible that
these movements were a gradual post-introduction filling of

C. maenas

potential range.

Carcinus

resumed its transoceanic voyages in the late

1850s. Crabs reported as

C. maenas

were collected in 1857

at Rio de Janeiro, Brazil (Heller, 1865), in 1866 in the Bay of
Panama (Smith, 1879), in 1866 or 1867 in Sri Lanka (Wood-
Mason, 1873), and in 1873 in the Hawaiian Islands (Streets,
1877). Alcock (1899), followed by later workers, reported

C. maenas

off the coast of Pernambuco, Brazil

, but provi-

ded neither a reference nor a collection date. Records from

India

cited by various authors also originate with Alcock

(1899) who, however, was apparently referring to the Sri
Lanka record (Chopra & Das, 1937). Later workers (Ed-
mondson, 1954; Almac¸a, 1962, 1963) questioned Streets

report of

Carcinus

from Hawaii. For all these records the last

reported examination of any specimens occurred prior to

aestuarii

s being recognized as a separate species in the 1950s

(Forest, 1957; Holthuis & Gottlieb, 1958). However, we
examined Streets

Hawaiian specimen (NMNH 2299) and

the 1866 specimen from the Bay of Panama (PMNH 9535),
and confirm that both are

C. maenas

. Although some mod-

ern workers continued to include these many locations
within the distribution of

C. maenas

, there have been no

additional records reported from these sites and we conclude
that

Carcinus

is established only at the locations described in

Appendix 1A.

Of all the

C. maenas

transported to the corners of the

world from Europe or North America in the latter half of
the nineteenth century, one distant population survived. In
the spring of 1900, Fulton & Grant (1900) reported

C. maenas

plentifully distributed

in the region of Port

Phillip, Victoria, Australia, where local anglers frequently
caught it in their nets. While Fulton & Grant (1900) noted
that

C. maenas

was neither found in a careful search of Port

Phillip in 1855 nor mentioned in Haswell’s (1882) mono-
graph on Australian decapods, they later (1902) suggested
that

C. maenas

may have been transported to Australia as

early as the 1850s on lumber ships from Europe. In concert
with the pattern noted above, we suggest that

C. maenas

may have arrived in Port Phillip by the 1870s or 1880s, and
was well established by 1900. At the least, the date of
establishment of

C. maenas

in Australia can be assumed to

be no later than the mid 1890s, given its abundance in the
spring of 1900. Indeed, in 1877, Streets had already noted
the existence of a specimen of

C. maenas

(which we have

been unable to locate) questionably labelled from Australia.

In a pattern reminiscent of its invasion of the north-

western Atlantic,

C. maenas

dispersed along the Australian

coast after a long quiescent period. In 1971, it was first
found to the north of Victoria, in 1976 to the west, and
in 1993 on the northeast coast of Tasmania. These move-
ments may represent a combination of natural spread and
introductions by shipping (Zeidler, 1978; Rosenzweig, 1984;
Gardner

et al.

, 1994). Genetic analyses indicate that the

Hawaiian Islands

(1873)

Western North

America

(1989-90)

Bay of

Panama

(1866)

Eastern

North America

(1817)

Europe &

North Africa

(native)

Pernambuco

(<1899)

Rio de

Janeiro

(1857)

South
Africa
(1983)

Red Sea

(<1817)

Madagascar

(1922)

Pakistan

(1971)

Sri Lanka

(1866-67)

Myanmar

(1933)

Perth

(1965)

Australia

(1900)

Tasmania

(1993)

Japan
(1984)

Figure 2

Occupied and Potential Range of

Carcinus maenas

(Linnaeus, 1758).

Black bands

: occupied range of

C. maenas

or populations

with

C. maenas

genes.

Gray bands

: potential range of

C. maenas

Black circles

: one-time collections of

Carcinus

species in regions without

established populations. First or one-time collection dates are given. See text and appendix for details of records, ranges, genetic information and
species identification.

2003 Blackwell Publishing Ltd,

Journal of Biogeography

, 1809–1820

Episodic global invasion patterns in shore crabs

1811

southern Australia population was founded from Europe,
and the Tasmania population was founded from southern
Australia (Bagley & Geller, 2001).

There were surprisingly few reports of

Carcinus

in new

locations from 1900 to 1970s and, curiously, all verified
records are from the greater Indian Ocean.

Carcinus

spe-

cimens collected in the Suez Canal in 1924 at 5 km from
the northern end (Calman, 1927) and in 1934 (Monod,
1938) were apparently

C. aestuarii

(Holthuis & Gottlieb,

1958). Three specimens of

C. maenas

were collected in

Nossi (Nosy) Be, Madagascar in 1922 (Guinot, 1967;
D. Guinot, pers. comm., 1995, 1997). Four large, parasi-
tized (castrated) male

C. maenas

were collected from

Maungmagan, Myanmar (Burma) in 1933 (Chopra & Das,
1937; Boschma, 1972). A single male

C. maenas

was col-

lected at Perth, Australia in 1965 (Zeidler, 1978), and a
single ovigerous female was collected at Karachi, Pakistan,
in the Arabian Sea in 1971 (Tirmizi & Ghani, 1983;
Tirmizi & Kazmi, 1996). There are no additional records
of

Carcinus

from any of these sites, and thus no indication

of the establishment of reproducing populations. The per-
iodic appearance of

Carcinus

in the greater Indian Ocean

during the twentieth century could be related to the
opening of the Suez Canal in 1869, or to the establishment
of a substantial population in southern Australia by the
1920s, or to both. If genetic material can be recovered from
these museum specimens (as has been carried out with
dried mollusc specimens from the nineteenth century;
Geller, 1999), then it may be possible to determine the
source population (Bagley & Geller, 2001) and thus the
likely transport route of these crabs.

Carcinus

third episode of successful dispersal began in

the 1980s. In 1983, crabs identified as

C. maenas

were

collected at Table Bay Docks in Cape Town, South Africa.
By 1988 these crabs had spread 20 km to the north to
Melkboostrand and 15 km south to Camps Bay (Le Roux

et al.

, 1990; Griffiths

et al.

, 1992).

Carcinus

remains

established only in the greater Cape Town region; a mating
pair found 117 km to the north on a bed of cultured
mussels in Saldanha Bay in 1990 remains the only record
outside of the Cape Town area, and none have been found at
Saldanha since (C. Griffiths, pers. comm., February 2000).
Genetic analyses revealed genotypes of both

C. maenas

and

C. aestuarii

at Table Bay Docks, with genetic variability

indicative of multiple invasions from the Atlantic and Medi-
terranean region of Europe (Geller

et al.

, 1997; Bagley &

Geller, 2001).

Crabs identified as

C. aestuarii

were collected in Japan in

Tokyo Bay in 1984, and in Sagami, Osaka and Dokai bays in
the 1990s (Sakai, 1986; Takeda & Horikoshi, 1993;
Watanabe, 1997; Furota

et al.

, 1999). The 1959 date given

by Sakai for the initial collection of these crabs is incorrect
(S. Watanabe, pers. comm., 1997). Genetic analyses revealed
genotypes of both

C. maenas

and

C. aestuarii

in Tokyo Bay

(Geller

et al.

, 1997). Microsatellite DNA indicates a single

invasion by a hybrid population from Europe (Bagley &
Geller, 2001), possibly from the transition zone in the wes-
tern Iberian Peninsula where crabs resembling both

C. maenas

and

C. aestuarii

are found (Almac¸a, 1961; Geller

et al.

, 1997), or from bays or harbours where the two species

have been mixed through human transport.

In 1989–90 crabs identified as

C. maenas

were collected in

San Francisco Bay, CA, along with a single large male from
the Estero Americano, a small estuary 45 km to the north.
By 1993–94

Carcinus

had spread to five small, nearby

estuaries from Elkhorn Slough (Monterey Bay) in the south
to Bodega Harbor, CA, in the north, a total distance along
the coast of 230 km.

Carcinus

was found in Morro Bay,

200 km south of Elkhorn Slough, in 1998 (E. Grosholz, pers.
comm., 1998). From central California

Carcinus

spread

rapidly northward (Appendix 1A). Specimens were found in
Humboldt Bay, CA, 320 km north of Bodega Bay, in 1995;
in Coos Bay, OR, 300 km further, in 1997; in several
additional bays in Oregon and in Willapa Bay, WA, and
Grays Harbor, WA, reaching 400 km further north, in 1998.
Specimens were then found in British Columbia in 1999 and
2000 (Appendix 1A). Multiple generations and considerable
numbers of crabs, including some ovigerous females, have
been found in some of these embayments. Some of these
populations may result from local reproduction, or from
recruitment of larvae from central California populations in
years with strong northward currents (El Nin˜o events). As of
June 2003 it is unclear which locations north of California
support established populations.

Genetic analysis of Bodega Harbor crabs indicate that the

population was founded from Atlantic North America
(Bagley & Geller, 2001).

D I S C U S S I O N

Dispersal mechanisms

Carcinus

has been transported around the world by a variety

of dispersal mechanisms associated with human activity,
with new mechanisms added over time. Natural transport
does not appear to have been responsible for founding any of
the transoceanic populations. Timing and genetics indicate
that the populations in Atlantic North America, Australia,
South Africa and Japan were founded from Europe, and the
Pacific North American population from Atlantic North
America (Bagley & Geller, 2001).

Carcinus

has not been

reported from floating algae or wood in the open ocean
(Cohen

et al.

, 1995), and in several laboratory studies its

planktonic larval period has been found to range from
17–27 days at 25

C to 44–80 days at 12

C (Williams,

1968; Dawirs, 1982; Dawirs and Dietrich, 1986; Harms and
Seeger, 1989; Mohamedeen and Hartnoll, 1989), with its
planktonic period potentially extended a few weeks more by
drift of postlarval crabs. Drifting from Europe or North
Africa via the Canary Current, North Atlantic Equatorial
Current, Antilles Current and Gulf Stream to reach near-
shore waters in the vicinity of New York would entail a
much longer voyage, including a passage through warm
equatorial waters estimated at 120–150 days (Scheltema,
1971) to 200–280 days (Thorson, 1961). The route from
Europe to South Africa runs counter to the prevailing current

2003 Blackwell Publishing Ltd,

Journal of Biogeography

, 1809–1820

1812 J. T. Carlton and A. N. Cohen

systems (Sverdrup

et al.

, 1942). The other passages are even

less likely. As with most other neritic, and particularly inner
shelf, invertebrates, transoceanic and interoceanic dispersal
in historical time is largely linked to human transport
mechanisms.

Carcinus

may have been moved about the world by at

least eight different transport mechanisms. These are:

(1)

Ship boring and fouling assemblages

. A number of

workers have linked

Carcinus

dispersal in the nineteenth

century to the movement of wooden-hulled vessels
which often were extensively bored by shipworms and
coated with dense fouling communities (Carlton, 1992;
Cohen

et al.

, 1995; Carlton, 1999a). Fulton & Grant

(1902) noted that many older vessels

had been patched

up with false bottoms which had become riddled with
[the shipworm]

Teredo navalis

and were fouled with

marine growths, affording ample shelter for the fry and
young crabs on their long voyage

. The change from

wooden to iron and steel ships that commenced in the
1880s, effectively began to eliminate these

internal

boring habitats in the hull. External ship fouling, while
vastly reduced in the twentieth century because of the
use of effective antifouling paints, faster vessel speeds,
and shorter time spent in ports, remains a potential
dispersal mechanism.

(2)

Solid Ballast

Carcinus

could have been transported

among rocks and stones used as solid ballast (Carlton,
1985, 1992) as suggested by G.M. Thomson (in Fulton
& Grant, 1900). The damp ballast holds of sailing
ships are known to have transported a diverse array of
maritime and terrestrial plants and animals (Lindroth,
1957).

Carcinus maenas

can live for at least 94 days

without food and resume normal feeding (Perkins

et al.

1965, cited in Clay, 1965), can live out of water at least
60 days when sheltered under seaweed, and more than
100 days when kept in bottles with gravel whose inter-
stices are filled with seawater (Perkins, 1967). Thus
nineteenth century transport with solid ballast would
appear possible. This transport mechanism has become
virtually extinct, replaced by the use of water ballast.

(3)

Fouled seawater pipes and sea chests

. In addition to

transport on fouled ship hulls,

Carcinus

could be trans-

ported among the organisms attached to the interior
surfaces of the seawater pipes or sea chests of ocean-
going vessels (Carlton, 1985, 1999b).

(4)

Semisubmersible exploratory drilling platforms

. A mod-

ern analogue of fouled hulls are the fouled frames of
exploratory drilling platforms, which are known to have
transported crabs across oceans (Carlton, 1987; Bercaw,
1993). These structures may be deployed at shallow
coastal sites for a long period of time, allowing the
development of an extensive fouling community, then
towed at relatively slow speeds to a new site in a distant
part of the world (where, in turn, there is ample time
for species to leave the platform). Le Roux

et al.

(1990)

suggested that

Carcinus

may have been transported to

South Africa by this means.

(5)

Ballast water

. As Cohen

et al.

(1995) noted,

Carcinus

larvae and juveniles are both transportable by ballast
water. As noted above, the duration of

C. maenas

planktonic larval stage is temperature-dependent, ran-
ging from 17 to 80 days. Ship voyages between relevant
regions of the globe could range from several weeks to
less than 2 weeks, depending upon the route, the type of
vessel and the number of port stops (Carlton

et al.

1995).

(6)

Seaweed transported with commercial fisheries products

Baitworms (glycerid and nereid polychaetes) and
American

lobsters

(

Homarus

americanus

Milne-

Edwards, 1837) are packed in the seaweed

Ascophyllum

nodosum

Linnaeus (Le Jolis) and air-shipped to markets

in North America, Europe, and elsewhere (Creaser

et al.

1983; Carlton, 1992; Lau, 1995; S. Fairservice, pers.
comm., 1996). These seaweeds, which harbour an
extensive living invertebrate fauna including

C. maenas

are routinely discarded into coastal and estuarine waters
by anglers, lobster importers and possibly restaurateurs
(Miller, 1969; Lau, 1995). Cohen

et al.

(1995) described

one

C. maenas

shipped with American Atlantic lobsters

to the north-eastern Pacific, and we have observed

C. maenas

in baitworm/algae shipments arriving in

California from Maine.

(7)

Education/research

Carcinus maenas

can be purchased

from biological supply houses, which will ship living
crabs to many destinations by overnight air express. The
popularity of

C. maenas

for experimental biology means

that at any given time it is probably present in many
college and university aquaria, poised for the escape or
release of adults or the discharge of small crabs or larvae in
flowing seawater systems, as has been documented for
other decapods in academic settings (Cohen

et al.

, 1995).

(8)

Private releases for fisheries purposes

. Finally, members

of the public could intentionally transport and release

Carcinus

in order to create new crab fisheries, as has

occurred with other crabs (Cohen

et al.

, 1995).

Predictions of future spread and range limits

Given the multitude of potential dispersal mechanisms now
operating to transport larval, juvenile, and adult

Carcinus

around the world, and given the potential for shorter-dis-
tance dispersal by natural or human-assisted mechanisms
once

Carcinus

has become established in a new region, it is

likely that these crabs will continue to both spread within the
regions they now inhabit outside of Europe and invade new
regions.

Cohen

et al.

(1995) reviewed the observational and

experimental evidence showing that

C. maenas

has an

upper temperature limit in the range of 18

–26

C based

on temperatures needed for successful reproduction and a
lower limit of around 0

C based on mortality of adult

crabs. Gillis

et al.

(2000) also report the death of crabs held

in ambient water after an extended exposure to water
temperatures of 0–1

C. Although other physical factors, or

2003 Blackwell Publishing Ltd,

Journal of Biogeography

, 1809–1820

Episodic global invasion patterns in shore crabs

1813

biological factors such as the presence of competitors,
predators or disease, can also influence distribution, Cohen

et al.

(1995) concluded that temperature explained the

general latitude limits of

C. maenas

in the Atlantic, with

equatorial limits characterized by average summer surface
temperatures of

C, and polar limits by average

winter ocean surface temperatures of

)

to 0

C (Sverd-

rup

et al.

, 1942).

C. maenas

potential range limits are in fact set by

factors correlated with average summer and winter surface
temperatures, then expansions of its populations within the
five regions outside of Europe where it now exists will be
limited as follows:

(1) In the northwest Atlantic,

C. maenas

will not extend

north of the lower Gulf of Saint Lawrence in Canada or
south of Chesapeake Bay.

(2) In Australia,

C. maenas

will reach a northern limit in

Western Australia around Jurien Bay, and in eastern
Australia south of Queensland. All of Tasmania lies
within its potential range.

(3) In southern Africa,

C. maenas

could spread north along

the west coast to the northern border of Namibia. It will
not become established in the Indian Ocean, where
summer water temperatures are too high.

(4) In the northwest Pacific, the waters along the north-

eastern shore of Honshu, the western shore of Hokkai-
do, and a part of the North Korean shore in the Sea of
Japan, fall within its temperature range. The distribution
of the two

Carcinus

species in Japan may ultimately

mimic their distribution in the north-eastern Atlantic:

maenas

to the north,

aestuarii

to the south (including the

Seto-naikai or Inland Sea, the

Japanese Mediterranean

)

with a transitional zone in which crabs of either geno-
type or hybrids may be found (around Tokyo, corres-
ponding to northern Morocco and the western part of
the Iberian Peninsula; Almac¸a, 1961).

(5) In the northeast Pacific, the potential range limits for

C. maenas

are, to the south, around Magdalena Island,

Baja California, Mexico, and to the north, north of the
Aleutian Peninsula around 60

N latitude.

These limits correspond generally with the borders of the

temperate shelf fauna as described by Ekman (1953). It
follows from this analysis that the many sites where one-time
collections of

C. maenas

have been reported – the Hawaiian

Islands, the Bay of Panama, Rio de Janeiro and Pernambuco
in Brazil, the Red Sea, Sri Lanka, Madagascar, Myanmar,
Pakistan and possibly Perth in Western Australia – are in
retrospect all too warm to support reproducing populations.
However,

C. maenas

remains absent from climatically suit-

able regions including New Zealand and the Pacific and
Atlantic coasts of South America from Tierra del Fuego,
Chile, to the northern border of Peru and the southern
border of Brazil. In all areas,

C. maenas

potential range may

be modified locally by bodies of water with naturally or
artificially warmer winter or cooler summer temperatures, or
altered on a larger scale by global climate change.

With

C. aestuarii

s native range bounded within the extent

of a largely enclosed sea (the Mediterranean) rather than by
latitude along ocean coasts, with a less extensive history of
invasion than

C. maenas

, and with considerably less pub-

lished work on its ecological and physiological tolerances,
there is less basis for estimating its potential range. However,

C. aestuarii

could likely become established in regions

equatorward of

C. maenas

potential range, with a trans-

itional zone of overlap.

Episodic dispersal of introduced marine organisms

One hypothesis among several regarding an apparent post-
1970s surge in global marine invertebrate, fish, and algal
invasions is that the increased invasion rate results from new
or intensified transport vectors (Carlton, 1996; Cohen &
Carlton, 1998). However, there is little information on
earlier periods marked by new or altered patterns of ship-
ping when there may have been similar episodes of global
invasions.

Patterns of episodic dispersal have been noted for a few

species. Carlton & Scanlon (1985) noted that the Asian
green alga

Codium fragile tomentosoides

spread to Europe

1900, to Atlantic North America in the 1950s, and then

to Pacific rim ports in the 1970s. Carlton & Iverson
(1981) similarly described episodic synanthropic dispersal
for the ship-fouling isopod

S. walkeri

, comprising a pre-

1870 period of spread around the Indian Ocean, southern
Africa and Australia, a post-1870 period related to the
opening of the Suez Canal in 1869, and a post-1940
period coincident with increased ship traffic during and
after World War II.

In the present paper, we suggest that

Carcinus

travelled

out from Europe in four episodes, first appearing in the Red
Sea and North America after 1800, then at several distant
global sites in the 1850s–70s, then a period of regional dis-
persal in the greater Indian Ocean after 1920 (which did not
lead to any established populations because the receiving
environment was inappropriate), and finally a series of suc-
cessful leaps to Japan, South Africa and the Pacific Coast of
North America (along with a shorter jump from southern
Australia to Tasmania) in the 1980s–90s.

The discovery of specimens or populations of

C. maenas

at several widespread locations (Brazil, Panama, Sri Lanka,
Hawaii and possibly Australia) around the world between
1857 and 1877 may be related to a post-1850 expansion of
world shipping. Global shipping patterns, in terms of
increased traffic, increased speed and new and expanded
routes, changed rapidly during this period (Natkiel &
Preston, 1986). With the advent of the clipper ships as a
mainstay, the California and Australian Gold Rushes altered
global shipping patterns for over a decade (1849–61, Natkiel
& Preston, 1986). The opening of the Suez Canal in 1869
changed shipping patterns again, forcing the Atlantic clipper
ships out of the China tea trade (the Red Sea being more
suited to steam than sail) and into the Australian wool trade
(outward via Cape of Good Hope, homeward via Cape

2003 Blackwell Publishing Ltd,

Journal of Biogeography

, 1809–1820

1814 J. T. Carlton and A. N. Cohen

Horn). During this period many long-distance sailing records
were set. For example, in 1853 the

Sovereign of the Seas

sailed from New York to Liverpool in 13 days, and in the
1866

Great Tea Race

between China and London, three

ships sailed 25,000 km in 99 days.

It was during this period that the Atlantic barnacle

Bal-

anus improvisus

Darwin, 1854, was first collected in the

northeast Pacific Ocean (in 1853 in San Francisco Bay;
Carlton & Zullo, 1969); the Eurasian hydroid

Cordylophora

caspia

(Pallas, 1771) was first collected in the northwest

Atlantic (in 1860 in Massachusetts; Verrill

et al.

, 1873); the

Indian Ocean isopod

S. terebrans

Bates, 1866 and the

Eastern Atlantic barnacle

Balanus trigonus

Darwin, 1854

were first collected in the southwest Atlantic (in Brazil in
1866 and 1867, respectively; Zullo, 1992; Carlton &
Ruckelshaus, 1997); and the Western Atlantic crab

Rhi-

thropanopeus harrisii

(Gould, 1841) was first collected in

Europe (in 1874 in the Netherlands; Buitendijk & Holthuis,
1949).

For many of these species these dates mark the beginning

of the next century of their global voyages. Whether pro-
portionally more taxa commenced global spread in the period
of the 1850s–70s, as opposed to the first half of the nineteenth
century, remains to be investigated. Still to be sorted out are
additional factors in the discoveries noted, including the effect
of an increasing number of exploratory naturalists deployed
in the latter half of the nineteenth century across the rapidly
opening – and rapidly changing – seas.

A C K N O W L E D G M E N T S

We thank the late Austin Williams (NMNH), Eric Lazo-
Wasem (PMNH), David Robinson (Academy of Natural
Sciences of Philadelphia), Danielle Guinot (MNHN), and
Derek S. Davis (Nova Scotia Museum), who helped with
museum records and specimens; Monique Fountain, Greg
Ruiz, Megumi Strathmann, Jan Thompson and anonymous
reviewers who provided helpful comments on earlier drafts;
Winnie Lau and Stanley Fairservice for information on the
baitworm industry; Roger Buttermore and Colm Gardner
for assistance with Tasmanian records, and Charles Griffiths
for assistance with South African records. Danielle Guinot,
Lucius Eldredge, Armand Kuris, and William Walton kindly
provided key references and translations for the Japanese
records of

Carcinus

, and Dr Guinot guided us to the Pakistan

literature.

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Carcinus

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B I O S K E T C H E S

James T. Carlton

is Professor of Marine Sciences at Williams College, Williamstown, MA, USA, and Director, Williams-Mystic,

the Maritime Studies Program of Williams College and Mystic Seaport. Prof. Carlton was Founding Editor of the journal

Biological Invasions

. He is a 1996 Pew Fellow in Marine Conservation.

Andrew N. Cohen

directs the Biological Invasions Program at the San Francisco Estuary Institute in Oakland, CA, USA, which

conducts science and policy research on the extent and impacts of invasions, on species characteristics and environmental
factors that affect the success of invasions, and on understanding and managing the vectors that transport and release exotic
species. He is a 1998 Pew Fellow in Marine Conservation.

2003 Blackwell Publishing Ltd,

Journal of Biogeography

, 1809–1820

1818 J. T. Carlton and A. N. Cohen

A P P E N D I X 1 . G L O B A L D I S P E R S A L A N D
D I S T R I B U T I O N O F

C A R C I N U S M A E N A S

A N D

C . A E S T U A R I I

(A) Regions with established populations

Europe and North Africa
Carcinus maenas.

Native to the Atlantic coast of Europe

and Great Britain north to Iceland, the North Sea and
Norway to just north of 70

N latitude (Christiansen, 1969);

south to Portugal and Spain, and thence to Morocco and the
northern border of Mauritania (Monod, 1956, 1967; Forest
& Gantes, 1960). Almac¸a (1961) also identified material
from Ceuta, Morocco, just inside the Strait of Gibraltar, as

C. maenas

Carcinus aestuarii.

Native to the Mediterranean, Marmara

and Black seas (Alcock, 1899; Holthuis & Gottlieb, 1958).
Holthuis & Gottlieb (1958) also assign Suez Canal records
to

C. aestuarii

. Almac¸a (1961) identified material from the

Canary Islands (Heller, 1863) as

forma

mediterranica

(

aestuarii

), where it remains

rare to occasional

in abun-

dance (Perez, 1995).

Atlantic North America
Carcinus maenas.

Introduced by 1817 and reported as a

new species,

Cancer granulatus

(Say, 1817). Ranges from

New Jersey to Prince Edward Island. Prior to the 1870s
ranged north only to Cape Cod; starting in the late nine-
teenth century moved east and north along the Atlantic
coast: Provincetown, Massachusetts (MA) by 1872 (Smith,
1879), Boston, MA region and Kittery, Maine (ME) by 1893
(Bryant, 1906), Casco Bay, ME by 1904 (Rathbun, 1905),
south of Rockland, ME by 1907 (Glude, 1955), Winter
Harbor, ME by 1939 (Scattergood, 1952), Passamaquoddy
Bay, New Brunswick by 1951 (Scattergood, 1952), Minas
Basin to Wedgeport, Nova Scotia (NS) by 1953–54 (Glude,
1955) and Lockeport, NS by 1961 (Welch, 1968). By the
1960s it was well established in central western Nova Scotia
in the Halifax region (Peggy’s Cove, 1964, and other loca-
tions) (Nova Scotia Museum collections), and

Carcinus

carapaces and claws were found 130 km to the northeast at
Marie-Joseph, Guysborough County, in 1982 (D. Davis,
pers. comm., 1982, and Nova Scotia Museum collections).

After 16 years with no further reports along the western or

north-western Nova Scotia shore,

Carcinus

was detected in

1998 on Cape Breton Island in the Bras d’Or Lakes and along
the Gulf of St Lawrence coast. In August 1998, it was reported
on the eastern end of Prince Edward Island in St Mary’s Bay,
and by 1999 was collected at sites from North Lake in the
northeast to Gascoigne Cove in the southeast (M. Campbell,
pers. comm., 1999; Gillis

et al.

, 2000).

Several workers had earlier reported

C. maenas

from Cape

Breton Island and Northumberland Strait, NS (Vermeij,
1982; Williams, 1984, repeated by Squires, 1990; Gillis

et al.

, 2000) and from eastern Nova Scotia (Vermeij, 1982),

all based on Bousfield & Laubitz (1972). However, the
stations reported by Bousfield and Laubitz are actually from

south-western Nova Scotia, within the previously known
range.

Records south of New Jersey that may represent transient

larval sets derived from northern populations include Dela-
ware Bay (Deevey, 1960: larvae; Leathem & Maurer, 1980;
not observed every year), Lewes, Delaware (A. Hines, pers.
comm., 1993), and the Atlantic shore of Northampton
County, Virginia (Kingsley, 1879).

Carcinus

is not known

from Chesapeake Bay.

Genetic analysis of specimens collected at Mystic, CT

detected only

C. maenas

haplotypes (Geller

et al.

, 1997).

Australia
Carcinus maenas.

Introduced possibly prior to 1877 (Streets,

1877), and abundant in Port Phillip Bay near Melbourne,
Victoria by 1900 (Fulton & Grant, 1900, 1902). First found
northeast of Victoria in New South Wales in 1971, and west of
Victoria near Adelaide, South Australia in 1976. Ranges from
near Adelaide to Narooma in southern New South Wales
(Fulton & Grant, 1900; Zeidler, 1978, 1988; Rosenzweig,
1984). One specimen collected at Perth in 1965 (Zeidler,
1978), with no further records from Western Australia.
Introduced to northeast Tasmania by 1993; ranges from Little
Musselroe Bay to Georges Bay (Gardner

et al.

, 1994). Genetic

analysis of specimens collected at Falmouth, Tasmania
detected only

C. maenas

haplotypes (Geller

et al.

, 1997).

South Africa
Carcinus maenas and C. aestuarii.

One or both species, or

hybrids, were introduced by 1983 when crabs identified as

C. maenas

were collected at Table Bay Docks, Cape Town.

They remain established in the greater Cape Town area. One
pair found north in Saldanha Bay in 1990, and none since
(Le Roux

et al.

, 1990; C. Griffiths, pers. comm., February

2000). Barnard (1950) had noted that

C. maenas

may

eventually find its way to South Africa

. Genetic analysis of

Cape Town specimens detected haplotypes of both species
(Geller

et al.

, 1997).

Japan
Carcinus maenas and C. aestuarii.

Hybrids introduced by

1984 when crabs identified as

C. aestuarii

were collected in

Tokyo Bay. Spread to Sagami, Osaka and Dokai bays by
1990s [Sakai, 1986 (date of collection incorrectly given as
1959); Takeda & Horikoshi, 1993; Watanabe, 1997; Furota

et al.

, 1999; W. Walton, pers. comm., 1996). Genetic ana-

lysis of specimens collected in Tokyo Bay in 1995 detected
haplotypes of both species (Geller

et al.

, 1997), with

microsatellite DNA indicating a single invasion by hybrids
(Bagley & Geller, 2001).

Pacific North America
Carcinus maenas.

A 1961 report of

C. maenas

in Willapa

Bay, Washington (Ricketts

et al.

, 1968) cannot be confirmed

(J. Hedgpeth, pers. comm., 1991) and may represent either a
reporting error or an introduction that failed to establish
(Cohen

et al.

, 1995), as there were no further records from

2003 Blackwell Publishing Ltd,

Journal of Biogeography

, 1809–1820

Episodic global invasion patterns in shore crabs

1819

the region for 36 years. Similarly, a report of

C. maenas

Willapa Bay in the 1930s (Niesen, 1997) appears to be in
error (T. Niesen, pers. comm., 2001).

The first clear Pacific Coast records are from 1989-90

when

C. maenas

was collected in San Francisco Bay,

California (CA), where it is well established (Cohen

et al.

1995) and a single 85 mm-wide crab was collected in
Estero Americano, CA, 45 km north of San Francisco Bay,
in 1989 (J. Roth, pers. comm., 1989; Commins

et al.

1990). The latter specimen may not have been part of an
established population, as no other

Carcinus

were collected

north of San Francisco Bay until 1993, despite collecting
and other field activities in the area by students and staff of
the Bodega Marine Laboratory, and one trapping effort in
Estero Americano in 1992 (Cohen

et al.

, 1995). To the

south,

C. maenas

was collected in Elkhorn Slough in

Monterey Bay, CA in 1994, where it is established; and a
single crab was collected in Morro Bay, CA in 1998
(Grosholz & Ruiz, 1995; E. Grosholz, pers. comm., 1998).
To the north of San Francisco Bay, crabs, claws or exuvia
were collected in Bolinas Lagoon, Drakes Estero, Tomales
Bay, and Bodega Harbor, CA in 1993; Humboldt Bay, CA
in 1995; Coquille Bay and Coos Bay, Oregon in 1997;
Alsea Bay, Yaquina Bay, Siletz Bay, Salmon River estuary,
Netarts Bay and Tillamook Bay in Oregon, and Willapa
Bay and Gray’s Harbor in Washington, in 1998; Esquimalt
Harbor and Barkley Sound on Vancouver Island, British
Columbia (BC) in 1999; and Clayoquot Sound, BC in 2000
(Miller,

1996;

Richmond,

pers.

comm.,

1997;

B. Dumbauld, pers. comm., 1998; J. Morrison, pers.
comm., 1999 and 2000; Jamieson

et al.

, 1998; Yamada

et al.

, 2001). The crab appears established in Elkhorn

Slough, San Francisco Bay, Tomales Bay and Bodega
Harbor. Records at some of the other sites may indicate
self-sustaining populations, or may result from transient
larval sets from populations established elsewhere. Genetic
analysis of Bodega Harbor specimens detected only

C. maenas

haplotypes (Geller

et al.

, 1997).

(B) Records in regions without established
populations

Indian Ocean
Carcinus maenas

collected in the Red Sea by 1817 (Sav-

igny, 1817); one specimen of

Carcinus

sp. in Sri Lanka in

1866 or 1867 (Wood-Mason, 1873); three specimens of

maenas

in Madagascar in 1922 (Guinot, 1967, and pers.

comm., 1995, 1997); four specimens of

C. maenas

Myanmar in 1933 (Chopra & Das, 1937; Boschma, 1972);
and one specimen of

C. maenas

in the Arabian Sea in

Pakistan in 1971 (Tirmizi & Ghani, 1983; Tirmizi &
Kazmi, 1996).

Atlantic South America
Carcinus

sp. collected at Rio de Janeiro, Brazil in 1857

(Heller, 1865), and off Pernambuco, Brazil before 1899
(Alcock, 1899).

Tropical Pacific

Single specimens of

C. maenas

collected in the Bay of

Panama in 1866 (Smith, 1879), and in Hawaii in 1873
(Streets, 1877).

2003 Blackwell Publishing Ltd,

Journal of Biogeography

, 1809–1820

1820 J. T. Carlton and A. N. Cohen