desorption of physically adsorbed C2H6 are
approximately 7.7 kcallmol and 1013 s-i,
respectively (7), the activation energies, Ery
and preexponential factors, kr(0) for dissociative
chemisorption may be evaluated easily
(these values are also listed in Table 1).
From these results, the electronic and
geometric effects on C-H bond activation
of these four surfaces of Pt and Ir can be
discussed quantitatively. The E. values given
in Table 1 provide the magnitudes by
which the Ir surfaces of a given geometry
are more active than the corresponding Pt
surfaces and by which the corrugated (110)
surfaces of each metal are more reactive
than their atomically flat (111) counterparts.
By comparing samples of the same
crystallographic orientation, we find that
the Er value on Ir is 5.0 to 6.3 kcal/mol
lower than that on Pt. For each metal, the
corrugated (110)-(1x2) surfaces have Er
values that are 4.8 to 6.1 kcal/mol lower
than those of the close-packed (111) surfaces.
Consequently, the Pt(1 10)-(1 x 2)
and Ir(111) surfaces have approximately
equal activity toward C2H6 activation,
demonstrating that the difference in geometric
structure compensates for the intrinsic
electronic difference between the two
metals. It is known from photoemission and
x-ray absorption studies that changes in surface
structure induce subtle, and yet significant,
changes in the electronic structure of
the catalyst surface (20). Hence, at the core
of the structure sensitivity issue is the profound
influence microscopic surface geometry
has on surface electronic structure, and
the continued study of this important effect
is of great interest in the heterogeneous
activation of saturated hydrocarbons.
REFERENCES AND NOTES
1. J. H. Sinfelt, Bimetallic Catalysts: Discoveries,
Concepts, and Applications (Wiley, New York,
1983), pp. 130-157.
2. A. E. Shilov, Activation ofSaturated Hydrocarbons
by Transition Metal Complexes (Reidel, Dordrecht,
Netherlands, 1984); R. H. Crabtree,
Chem. Rev. 85, 245 (1985); B. Meunier and B.
Chaudret, Eds., Perspectives in the Selective Activation
of C-H and C-C Bonds in Saturated
Hydrocarbons, vol. CXXX of the NATO Advanced
Study Institutes Series (Reidel, Dordrecht, Netherlands,
1987).
3. D. F. McMillen and D. M. Golden, Annu. Rev.
Phys. Chem. 33, 493 (1982).
4. J. C. Rasser, Platinum-Iridium Reforming Catalysts
(Delft Univ. Press, Delft, Netherlands, 1977),
pp. 156-193.
5. M. A. Van Hove, W. H. Weinberg, C.-M. Chan,
Low-Energy Electron Diffraction: Exprirnent Theoiy,
and Surface Structure Determination (SpringerVerlag,
Heidelberg, Gernany, 1986), pp. 265-272.
6. T. S. Wittrig, P. D. Szuromi, W. H. Weinberg, J.
Chem. Phys. 76, 3305 (1982); P. D. Szuromi, J. R.
Engstrom, W. H. Weinberg, ibid. 80, 508 (1984).
7. P. D. Szuromi, J. R. Engstrom, W. H. Weinberg, J.
Phys. Chem. 89, 2497 (1985).
8. L. E. Firment and G. A. Somorjai, J. Chem. Phys.
66, 2901 (1977).
9. J. A. Rodriquez and D. W. Goodman, J. Phys.
Chem. 94, 5342 (1990).
78
10. Y.-K. Sun and W. H. Weinberg, J. Vac. Sci.
Technol. A 8, 2445 (1990).
11. C. B. Mullins and W. H. Weinberg, J. Chem. Phys.
92, 4508 (1990).
12. J. J. Vajo, W. Tsai, W. H. Weinberg, Rev. Sci.
Instrum. 56, 1439 (1985). The Ir(111) crystal was
cut, polished, and prepared with standard techniques.
The crystal surface was cleaned between
experiments by heating to 1000 K for 5 min at an
°2 pressure of 5 x 10-8 torr flowing through the
microreactor, followed by annealing to 1625 K for
1 min to desorb the surface oxygen. Thermal
desorption spectra of CO, which were in complete
agreement with previously published ones from
the clean lr(111) surface [C. M. Comrie and W. H.
Weinberg, J. Chem. Phys. 64, 250 (1976)], were
measured frequently to verify the cleanliness of
the surface. Furthermore, because kinetic data
are known to be extremely sensitive to surface
conditions, the high degree of reproducibility of
the data presented here indicates the absence of
surface contamination. The 13C-labeled ethane
[1,2-di-13C]C2H,, 99 atom % 13C) was obtained
from Icon Services and was introduced into the
microreactor from a gas-handling manifold that
was pumped by a diffusion pump to a base
pressure below 10-7 torr.
13. Under these experimental conditions the dissociative
chemisorption of C2H6 is irreversible, and
no gas-phase carbon-containing products of a
surface self-hydrogenolysis reaction are formed.
The titration conditions and procedure were selected
to ensure the complete oxidation of the
surface carbon to 13CO2.
14. The measurements of C2H- activation at defect
sites on our Ir(1 11) sample have been done
separately and will be reported elsewhere (D. F.
Johnson and W. H. Weinberg, in preparation).
15. C. T. Rettner, H. E. Pfnur, D. J. Auerbach, Phys.
Rev. Left. 54, 2716 (1985); A. C. Luntz and D. S.
Bethune, J. Chem. Phys. 90, 1274 (1989); M. B.
Lee, 0. Y. Yang, S. T. Ceyer, ibid. 87, 2724
(1987).
16. W. H. Weinberg, in Dynamics of Gas-Surface
Collisions, C. T. Rettner and M. N. R. Ashfold, Eds.
(Royal Society of Chemistry, Cambridge, 1991),
pp. 171-220; G. Ehrlich, in ChemistryandPhysics
ofSolidSurfaces VII, R. Vanselow and R. F. Howe,
Eds. (Springer-Verlag, Heidelberg, Germany,
1989), pp. 1-64.
17. W. H. Weinberg, in Kinetics of Interface Reactions,
H. J. Kreuzer and M. Grunze, Eds. (Springer-Verlag,
Heidelberg, Germany, 1987), pp. 94-
121; W. H. Weinberg, Langmuir9, 655 (1993).
18. C. T. Campbell, Y.-K. Sun, W. H. Weinberg,
Chem. Phys. Lett. 179, 53 (1991).
19. C. T. Rettner, E. K. Schweizer, H. Stein, D. J.
Auerbach, Phys. Rev. Lett. 61, 986 (1988).
20. M. Cardona and L. Ley, Eds., Photoemission in
Solids I and 11, vols. XXVI and XXVII of Topics in
Applied Physics (Springer-Verlag, Heidelberg,
Germany, 1978); J. W. Gadzuk, in Electronic
Structure and Reactivity of Metal Surfaces, vol.
XVI of the NATO Advanced Study Institutes, Series
B, E. G. Derouane and A. A. Lucas, Eds.
(Plenum, New York, 1976),pp. 341-387; J. C.
Fuggle and J. E. Inglesfield, Eds., Unoccupied
Electronic States: Fundamentals for XANES,
EELS, IPS, and BIS, vol. LXIX of Topics inApplied
Physics (Springer-Verlag, Heidelberg, Germany,
1992); J. H. Sinfelt and G. D. Meitzner, Acc.
Chem. Res. 26, 1 (1993).
21. This work was supported by the Department of
Energy (grant DE-FG03-89ER14048), the Donors
of the Petroleum Research Fund administered by
the American Chemical Society (grant ACS-PRF-
23801-AC5-C), and the Universitywide Energy
Research Group of the University of Califomia.
1 March 1993; accepted 27 April 1993
Ecological Roulette: The Global Transport of
Nonindigenous Marine Organisms
James T. Cariton and Jonathan B. Geller
Ocean-going ships carry, as ballast, seawater that is taken on in port and released at
subsequent ports of call. Plankton samples from Japanese ballast water released in
Oregon contained 367taxa. Mosttaxawith a planktonic phase in their life cycle were found
in ballast water, as were all major marine habitat and trophic groups. Transport of entire
coastal planktonic assemblages across oceanic barriers to similar habitats renders bays,
estuaries, and inland waters among the most threatened ecosystems in the world. Presence
oftaxonomically difficult or inconspicuous taxa in these samples suggests that ballast
water invasions are already pervasive.
Biological invasions are a great threat to
the integrity of natural communities of
plants and animals and to the preservation
of endangered species (1). Most invasion
studies have focused on terrestrial and
freshwater systems in which one or a few
successful invaders have had a catastrophic
impact on native species (2). Island ecosystems,
such as New Zealand and the HawaiJ.
T. Carlton, Maritime Studies Program, Williams
College, Mystic Seaport, Mystic, CT 06355, and Department
of Biology, Williams College, Williamstown,
MA 01267.
J. B. Geller, Department of Biological Sciences, University
of North Carolina at Wilmington, Wilmington,
NC 28403.
ian Islands, have in particular been devastated
by the invasion of nonindigenous
species (1-3). Invasions in marine systems
have been less studied (4), but are of such
magnitude that marine invasions may be
leading to profound ecological changes in
the ocean.
Any mechanism for rapidly transporting
large volumes of water containing
plankton from shallow, coastal waters
across natural oceanic barriers has the
potential to facilitate massive invasions of
entire assemblages of neritic marine organisms.
Such a mechanism exists in the
transport of ballast water and plankton by
ocean-going ships (5), a dispersal mechaSCIENCE
* VOL 261 * 2 JULY 1993
mnugnmgnnnunngon;9nnu2ROM9
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nism that has no analog in terrestrial
ecosystems. We report here a survey of
plankton in ballast water.
Ships have used water as ballast regularly
since the 1880s, drawing ambient water into
ballast tanks and floodable holds for balance
and stability (6). This water is discharged
while under way and at subsequent ports-ofcall
as cargo is loaded (7). Water taken
aboard may contain any planktonic organisms
in the water column (8). Thus, rich
plankton assemblages may be entrained by
vessels and then released within days or
weeks on a continent or island thousands of
kilometers away.
Table 1. Frequency of occurrence and abundance of organisms in ballast
water from ships arriving from Japan to the Port of Coos Bay, Oregon, after
a transoceanic trip of 11 to 21 days [average 15.1 (SD 1.9) days].
Specificity of identification depended on the phylum or division considered.
Ships (%) in which taxon was Adult
Taxon Species Abundant Common Rare(n) (>100/ (10 to 100/ (<10/ Present Habitat* Trophic groupt
replicate) replicate) replicate)
Crustacea
Cirripedia
Harpacticoida
Calanoida and Cyclopoida
Decapoda
Euphausiacea
Stomatopoda
Cumacea
Mysidacea
Isopoda
Caprellidea
Gammaridea
Hyperiidea
Ostracoda
Cladocera
Chelicerata
Acarina
Echinodermata
Asteroidea
Echinoidea
Ophiuroidea
Holothuroidea
Chordata
Urochordata
Pisces
Hemichordata
Enteropneusta
Chaetognatha
Phoronida
Bryozoa
Annelida
Spionidae
Polynoidae
Other Polychaeta
Hirudinea
Platyhelminthes
Nemertea
Mollusca
Bivalvia
Gastropoda
Sipuncula
Nematoda
Rotifera
Cnidaria
Anthozoa
Scyphozoa
Hydrozoa: Obelia
Other Hydrozoa
Radiolaria
Foraminifera
Tintinnida
Other ciliata
Dinoflagellata
Diatomacea
Chlorophyta
Rhodophyta
Zosteraceae
5
5
25
14
1
1
3
2
4
1
8
1
1
1
1
1
2
1
2
10
2
1
3
1
3
11
3
28
1
33
1
9
10
1
1
1
2
1
1
21
2
3
2
4
4
128
2
2
1
11.0
17.0
61.6
3.1
0
0
0.6
0.6
0
0
0
0
0
0
0
1.2
0.6
0
0
0.6
0
0
3.1
0.6
3.1
23.9
1.2
5.0
0
0.6
6.3
22.0
2.5
0
0
0
0
0
0
0
0
0.6
15.7
6.7
54.7
0
0
0
31.0
29.0
25.7
4.4
0
0
1.3
5.0
1.3
0
1.4
0
0
0
0
1.9
1.9
0
0
0
0
0
14.5
3.8
5.7
40.3
3.1
18.8
0
8.8
0
23.9
16.4
0
0
0
0
0
1.4
0.6
0
2.5
11.3
11.4
20.7
0
0
0
41.0
28.0
11.3
40.8
1.3
2.5
11.3
28.0
32.1
2.5
22.0
10.7
2.5
0.6
83.0
74.0
98.6
48.3
1.3
2.5
13.2
33.6
33.4
2.5
23.4
-10.7
2.5
0.6
HE
HE, SE, PL, EB
PL, SE
SE, HE, EB
PL
HE, SE
SE, I, PL
SE, PL
HE, EB
EB
SE, HE
PL
HE, SE, PL
PL
5.0 5.0 HE
11.3
15.0
3.1
5.7
14.4
17.5
3.1
5.7
S
SC, H
C, H, SC
0, H, C, D, SC, S
0
C
D
H, D
SC, 0, D, H, P
C, 0
H, D, S
C
H
H
D, SC
HE, SE
HE, SE
HE, SE
I, HE, SE
5.7 6.3 HE, EB
3.2 3.2 PL
0.7
29.5
24.5
20.8
20.7
38.0
45.3
0.7
55.3
5.7
25.2
42.8
2.5
9.4
8.2
1.3
1.9
21.4
19.5
18.9
6.3
16.3
9.5
17.6
3.8
1.2
0.7
0.7
47.1
28.9
29.6
84.9
42.3
69.1
0.7
64.7
12.0
71.1
61.7
2.5
9.4
8.2
1.3
1.9
22.8
20.1
18.9
9.4
43.3
27.6
92.4
3.8
1.2
0.7
PL
HE, SE
HE, EB
SE, HE
SE, HE
l, EB, SE, HE
PL
SE, HE
SE, HE, I
HE, SE, I
SE, HE
SE, HE
SE, HE, EB
PL
HE
PL
HE, EB, PL
HE, EB, PL
PL
EB, HE, SE, PL
PL
PL
SE, HE, PL
SE, HE
SE, HE
SE
C, SC
H, SC
D, SC
D, S
S
C
D
C
S
S
D, H, C, S
D
SC, C, S
p
C, SC, P
C
D, S
D, SC, H, C
D
D, SC
0, H
S, C
S, C
S,C
S. C
C, 0
C, D, SC
C, SC
PP
PP
PP
PP
PP
SCIENCE * VOL. 261 * 2 JULY 1993
*EB, epibiotic (living on other organisms); HE, hard bottom epifaunal; 1, infaunal; PL, planktonic; SE, soft bottom epifaunal. tC, carnivore; D, deposit feeder; H, herbivore;
0, omnivore; P, parasite; PP, primary producer, S, suspension feeder; SC, scavenger. *Ciliate abundance not estimated.
---------- - Iiiiiiiiiiiiinu
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We sampled ballast water from 159
cargo ships in Coos Bay, Oregon. The
ships and their ballast water originated
from 25 Japanese ports (9). Plankton from
these vessels included 16 animal and 3
protist phyla, and 3 plant divisions (Table
1). All major and most minor phyla were
represented (10), including 47 ordinal or
higher taxa and a minimum of 367 distinctly
identifiable taxa (11). The supraspecific
diversity demonstrates the wide
taxonomic spectrum represented and emphasizes
the broad implications of this
phenomenon (12).
All major marine trophic groups were
represented (Table 1) including carnivores,
herbivores, omnivores, deposit feeders,
scavengers, suspension feeders, primary
producers, and parasites, although the last
were rare. Taxa characteristic of most temperate
shallow-water marine communities
were represented, including those from infaunal,
soft and hard bottom epifaunal,
epibiotic, and planktonic habitats. The balTable
2. Examples of recent invasions probably mediated by ballast water.
Native Year introduction
Higher taxon Taxon Species distribution Introduced to first recognized
(reference)
Alexandrium catenella
Alexandrium minutum
Gymnodinium catenatum
Phyllorhiza punctata (*,t)
Cladonema uchidai (t)
Mnemiopsis leidyl
Teneridrilus mastix (*)
Desdemona omata (*)
Marenzelleria viridis
Bythotrephes cederstroemi
Rhopalophthalmus
tattersallae (*)
Neomysis japonica
Neomysis americana (*)
Nippoleucon hinumensis
Pseudodiaptomus inopinus
Pseudodiaptomus marinus
Pseudodiaptomus forbesi
Sinocalanus doerrii
Oithona davisae
Limnoithona sinensis
Centropages abdominalis
Centropages typicus
Acartia omoril
Hemigrapsus sanguineus
Charybdis helleri
Salmoneus gracilipes (*)
Hippolyte zostericola (*)
Exopalaemon sty/iferus (*)
Tritonia plebeia
Potanocorbula amurensis
Dreissena polymorpha
Dreissena sp.
Rangia cuneata (*)
Theora fragilis
Musculista senhousia (t)
Ensis americanus
Membranipora
membranacea (*)
Gymnocephalus cemuus
Proterorhinus marmoratus
Neogobious melanostomus
Butis koilomatodon
Rhinogobius brunneus
Mugiligobius sp.
Sparidentex hasta
Parablennius thysanius
Japan
Europe?
Japan
Indo-Pacific
Japan, China
Western Atlantic
China
South Africa,
Australia
U.S. Atlantic
Europe
Indian Ocean
Japan
U.S. Atlantic
Japan
Asia
Japan
China
China
Asia
China
Japan
U.S. Atlantic
Japan
Asia
Indo-Pacific, Israel
Japan, Micronesia
Western Atlantic
Indonesia, India
Europe
Asia
Eurasia
Eurasia
Southern U.S.
Asia
Japan
U.S. Atlantic
Europe
Europe
Black Sea
Mediterranean
Indo-west Pacific
Japan
Taiwan,
Philippines
Arabian Sea
Philippines,
Indian Ocean
Australia
Australia
Australia
California
California
Black Sea
California
Italy
Germany
Great Lakes
Kuwait
Australia
Argentina, Uruguay
California
Oregon
Columbia River
California
California
California
California
Chile
California
Chile
Texas
Chile
New Jersey
Colombia
(Caribbean)
California
Colombia (Atlantic)
Iraq, Kuwait
Massachusetts
California
Great Lakes
Great Lakes
New York
California
New Zealand
Australia
Germany
New Hampshire,
Maine
Great Lakes
Great Lakes
Great Lakes
Nigeria, Cameroon
Panama Canal
Arabian Gulf
Hawaii
Australia
Hawaii
SCIENCE * VOL. 261 * 2 JULY 1993
Dinoflagellata
Scyphozoa
Hydrozoa
Oligochaeta
Polychaeta
Cladocera
Mysidacea
Cumacea
Copepoda
Decapoda:
Brachyura
Decapoda:
Caridea
Gastropoda
Bivalvia
Cnidaria
Ctenophora
Annelida
Crustacea
Mollusca
Ectoprocta
Pisces
1986 (6)
1986 (6)
1986 (6)
1981 (28)
1979 (23)
1987 (26)
1984 (29)
1986 (30)
1983 (31)
1984 (32)
1981 (33)
1977 (34)
1979 (35)
1980? (23)
1979 (23)
1990 (36)
1986 (37)
1987 (37)
1978 (38)
1979 (39)
1983 (40)
1979 (39)
1983 (41)
1985 (42)
1983 (40)
1988 (43)
1987 (44)
1986 (45)
1984 (46)
1983 (47)
1983 (4)
1986 (23)
1988 (24)
1990 (25)
1991 (48)
1982 (23)
1980 (49)
1982 (49)
1979 (50)
1987 (51)
1987 (52)
1990 (53)
1990 (53)
1983 (54)
1972 (54)
1987 (55)
1987 (56)
1985 (57)
1971 (58)
*Suggested herein as a ballast-mediated invasion. tAn altemative means of dispersal includes transport as external fouling on ships' hulls. Here we suggest that transport
as ephyrae (for Scyphozoa) and hydromedusae (for Hydrozoa) are as probable as transport as fouling polyps.
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last biota included meroplankton (organisms
spending part oftheir life cycle in the
water column), holoplankton (spending all
of their lives in the water column), demersal
plankton (benthic species that vertically
migrate into the water), and tychoplankton
(suspended benthic organisms). Ballast water
therefore acts as a phyletically and
ecologically nonselective transport vector.
Certain taxa occurred in high densities: we
estimated copepod densities were greater
than 1.5 x 103 per cubic meter and spionid
polychaete larvae, barnacle nauplii, and
bivalve veligers greater than 2 x 102 per
cubic meter (13).
Despite the lack of selectivity, certain
taxa predominate. Five phyla accounted for
more than 80% of taxa recorded: crustaceans
(31% ofall taxa present), polychaete
annelids (18%), turbellarian flatworms
(14%), cnidarians (11%), and mollusks
(8%). Taxa found in many or most vessels
included copepods (present in 99% of
ships), polychaetes (89%), barnacles
(83%), bivalve mollusks (71%), flatworms
(65%), diatoms (93%), gastropod mollusks
(62%), decapod crustaceans (48%), and
chaetognaths (47%).
For some taxa the number of released
individuals may vary greatly among ships,
whereas the frequency of release may be
high (Table 1). Gastropods were abundant
in only 2.5% of ships but present in 62% of
ships sampled, decapods were abundant in
only 3.1% and present in 48% of ships,
spionids were abundant in 24% ofships and
present in 85% of ships, and nonharpacticoid
copepods were abundant in 61% of
ships and present in 98% of ships.
Behavioral and life history traits make
some taxa less prone to being transported
by ballast water. Taxa with both a strictly
benthic life-style and with brooded or
crawl-away young [for example, brooding
gastropods, bivalves, and anthozoans (14)]
would rarely be in the water column when
ballast is pumped on board. Similarly,
organisms with an extremely short planktonic
life (sponges, direct-developing bryozoans,
and ascidians) would rarely be
caught. Nektonic organisms (such as fish)
may be able to resist either the water
intake pressures ofthe ballast pump or may
be able to avoid the plankton net. However,
any taxa likely to attach to algae
(15) could be takenup along with the drift
algae (16, 17).
In the past 20 years, numerous aquatic
invasions have occurred (Table 2). Many of
these now appear to be related to ballast
water transport (18). The taxa of these
documented invasions (Table 2) are all
represented (except comb jellies) in our
samples of ballast water (Table 1). However,
some higher taxa frequently found in
ballast water have not been often reported
as invasive species. Conversely, some higher
taxa that are reported relatively frequently
as invaders were not found frequently in
our samples. Although we recognize that
high frequency ofrelease does not necessarily
lead to successful invasions, we suggest
that there have been far more introductions
of polychaetes, flatworms, and diatoms
than have been reported. Invasions of intensely
studied larger-size animals (such as
fish, mollusks, and decapods) are more apparent
and thus more noticeable. We predict
that more invasions of both large and
small organisms will be recognized as susceptible
regions are investigated and that
new invasions will be discovered in wellstudied
regions (19).
Knowledge of species' natural geographic
distributions is of paramount importance
for interpreting patterns in ecology, evolution,
and biogeography. Unfortunately, the
systematics ofmost marine taxa are far from
complete, and the discovery of previously
unrecognized species in regions impacted by
ballast water release (almost all coastal
zones of the world) must now be viewed
critically as potential invasions (20). Conversely,
for easily identified species, unrecognized
historical transport may have led to
false conclusions of natural cosmopolitanism.
Thus, many introduced species may be
cryptic, having invaded and gone unrecognized
or been mistaken as native species.
Both these situations confound our understanding
of historical patterns of dispersal,
gene flow, and speciation: geographic barriers
to dispersal and gene flow are readily
breached by ballast water transport. Similarly,
we must now recognize that the composition
of aquatic communities may be
influenced by both recognized and cryptic
invasions.
Ships take up and release ballast water in
bays, estuaries, and inland waters and then
release this water into similar environments
around the world. Many of these bodies of
water are disturbed by the effects of extensive
urbanization (21), rendering them especially
susceptible to invasions (22) that
further alter community structure and function.
The invasion of the Asian clam Potanwcorbula
amurensis in San Francisco Bay
(23), the zebra mussels Dreissena polymrrpha
and Dreissena sp. in the Laurentian Great
Lakes (24, 25), and the comb jelly Mneniopsis
leidyi in the Black Sea (26) are dramatic
examples of the catastrophic impact of
ballast water introductions. The ecological
roles and impacts of invading species can
only be partially predicted from knowledge
of their biology and ecology in donor regions
(2). For these reasons, bays, estuaries,
and inland waters with deep water portsmarine
analogs ofdespoiled, highly invaded
oceanic islands-may be among the most
threatened ecosystems on the planet (27).
SCIENCE * VOL. 261 * 2 JULY 1993
REFERENCES AND NOTES
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6. Ballast water may be fresh, brackish, or marine,
depending upon the ballasting site. Sediments
may also be entrained; the release of such sediments
has been linked to the introduction of toxic
dinoflagellates (in their benthic cyst stage) in
Australia [G. M. Hallegraeff and C. J. Bolch, Mar.
Pollut. Bull. 22, 27 (1991); G. M. Hallegraeff,
Phycologia 32, 79 (1993)1, (57).
7. Ballast water may also be taken aboard and
discharged in many other pattems. For example,
offshore water may be ballasted in one ocean and
deballasted in another ocean, which would result
in the movement of oceanic taxa in addition to
neritic taxa.
8. Larger (>2 cm) organisms (such as fish) may fail
to pass through the intake grates or may be
destroyed by the impeller pump blades.
9. Shipswere sampled from 1986 to 1991. Five to six
vertical quantitative hauls were made in each
vessel using an 80-slm mesh, 0.5-im-diameter
plankton net towed at 0.5 m s-1 in 10 to 20 meters
of ballast water of floodable cargo holds. Samples
were examined alive under a stereomicroscope to
ensure the inclusion of fragile specimens. All
samples were preserved and retained. Specimens
of many taxa were cultured until they grew
to a size that permitted identification. Information
on the volume, source, and age of ballast water
was obtained. Cargo holds sampled contained an
average of 1.09 x 104 (SD = 2.7 x 103) metric
tons (=1.09 x 107 liters, SD = 2.7 x 106) ofwater;
total ballast water on board averaged 2.01 x 1 04
(SD = 6.4 x 103) metric tons (=2.01 x 107 liters,
SD =6.4 x 106) of water.
10. Two relatively common marine phyla not found in
our samples are the Porifera (sponges) and
Ctenophora (comb jellies). The absence of ctenophores
may reflect a bias against extremely fragile
taxa. Alternatively, ctenophore distribution is
often temporally and spatially uneven [K. Mountford,
Estuarine Coastal Mar. Sci. 10, 393 (1980);
E. Deason, Estuarine Coastal Shelf Sci. 15, 121
81
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(1982)] and their absence may reflect chance.
The planktonic larvae of sponges are short-lived
and may survive only short voyages.
11. True species diversity in these samples is underestimated
because larval and postlarval forms of
many species are morphologically indistinguishable.
Also, animal, plant, and protist taxa smaller
than 80 A.m (the size of the plankton net mesh)
were not efficiently retained.
12. We estimate (assuming 20 to 30 taxa per vessel,
and several thousand ships out of a world fleet of
35,000 with ballast water at sea at any given time)
that, on any one day, several thousand species
may be in motion in ballast water "conveyor belts"
around the world. Therefore, comparing known
invasions (Table 2) with any particular ballast
sample may rarely reveal the same taxa, underscoring
the importance of recognizing this phenomenon
at a supraspecific level.
13. Densities of plankton were estimated by mixing
and splitting each replicate, counting the organisms,
and multiplying by the volume of water
sampled per replicate (9).
14. R. D. Barnes, Invertebrate Zoology (Saunders,
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16. Organisms with a short larval phase can be
entrained in ballast water and then settle. We
found metamorphosed ascidians (1 to 2 mm)
settled on floating wood chips, and, in five ships
that had completed voyages of 13 to 16 days, we
found unattached ascidian tadpoles but no
adults. Although we found few fish in our samples,
more than 20 ship's captains in the Great Lakes,
and on the U.S. Atlantic, Gulf, and Pacific coasts,
have reported to us live fish in ballast water tanks.
17. Freshwater ballast transferred to other freshwater
endpoints (such as from Europe to the Laurentian
Great Lakes, or vice versa) may transfer encysted
stages of many taxa (such as sponge gemmules
and bryozoan statoblasts). Such stages remaining
in ship's ballast sediments after open ocean
exchange may resist saltwater immersion.
18. The recent increase in invasions caused by ballast
water may be due to a variety of factors,
including increases in the size, number, and
speed of ships (4, 5).
19. We expect that several of the six species of Asian
copepods now recognized on the Pacific coast of
North America will also be found in eastern Australia,
a region that receives large volumes of
ballast water from the same sources in Japan and
China as does the North American Pacific coast.
20. Over 50 examples are now known where introduced
species were mistakenly described as
"new" species, some several times from different
places around the world (J. T. Cariton, in San
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mediated through ballast water. Federal regula-
28.
29.
30.
31.
32.
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mechanisms to reduce the number of living
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and sediments. The United Nations International
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59. We are very grateful to D. Cariton for laboratory
and field assistance throughout every stage of
this work. We thank J. Chapman and S. Cohen for
critical comments on the manuscript, T. Johnson
for phytoplankton identification, and T. Stevens,
K. Kiefer, 0. Williams, and C. Hewitt for laboratory
and field support. Laboratory support was provided
by the Oregon Institute of Marine Biology.
Supported by National Oceanic and Atmospheric
Administration Sea Grant (Oregon) R/EM-21.
16 February 1993; accepted 5 May 1993
Regulation of Lymphoid-Specific Immunoglobulin ,
Heavy Chain Gene Enhancer
by ETS-Domain Proteins
Barbara Nelsen, Gang Tian, Batu Erman, Jacqueline Gregoire,
Richard Maki, Barbara Graves, Ranjan Sen*
The enhancer for the immunoglobulin g. heavy chain gene (IgH) activates a heterologous
gene at the pre-B cell stage of B lymphocyte differentiation. A lymphoid-specific element,
p.B, is necessary for enhancer function in pre-B cells. A p.B binding protein is encoded by
the PU. 1/Spi-1 proto-oncogene. Another sequence element, pA, was identified in the
enhancer that binds the product of the ets-1 proto-oncogene. The pA motif was required
for p.B-dependent enhancer activity, which suggests that a minimal B cell-specific enhancer
is composed of both the PU.1 and Ets-1 binding sites. Co-expression of both PU.1
and Ets-1 in nonlymphoid cells trans-activated reporter plasmidsthat contained the minimal
enhancer. These results implicate two members of the Ets family in the activation of IgH
gene expression.
Transcription of the immunoglobulin (Ig)
heavy chain gene (IgH) is activated at the
pre-B cell stage of B cell differentiation.
The g. enhancer ([LE), residing in the IgH
B. Nelsen, G. Tian, B. Erman, R. Sen, Rosenstiel
Research Center and Department of Biology, Brandeis
University, Waltham, MA 02254.
J. Gregoire and B. Graves, Department of Cellular,
Viral, and Molecular Biology, University of Utah School
of Medicine, Salt Lake City, UT 84132.
R. Maki, Cancer Research Center, La Jolla Cancer
Research Foundation, La Jolla, CA 92037.
*To whom correspondence should be addressed.
gene, is a lymphocyte-specific regulatory
element (1, 2) that enhances transcription
in transfection assays but is also sufficient to
activate a heterologous gene in the pre-B
cells of transgenic mice (3-7). Thus, the p.
enhancer may regulate IgH locus activation
during B cell ontogeny, perhaps by inducing
sterile p. transcripts that may be required
for the initiation of gene rearrangements
(8-10).
The p. enhancer is a composite of multiple
positive- and negative-acting sequence
SCIENCE * VOL. 261 * 2 JULY 1993
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