Download The Impact of Maritime Commerce on Marine

The Impact of Maritime Commerce on
Marine Biodiversity
James T. Carlton
Professor
Williams College
The need to move people, and the food and other goods that support them by ships
along coastlines, across oceans, and between the seas, has resulted in profound environmental modifications to the world’s coastal systems. As ocean-going vessels proliferated
to support exploration, colonization, and commerce, there was a concomitant need to
convert (beginning in ancient times) river mouths, bays, and estuaries into ports and harbors. While shipping has long served a benevolent and fundamental role in many human
societies, the environmental consequences of shipping have been equally important.1
I focus here on a select subset of the environmental impacts of global shipping—the
transport and introduction of non-native species—and ask what pressing policy issues
related to marine bio-invasions have emerged in the twenty-first century.
Shipping-Mediated Environmental Impacts on the Ocean
Ship building to ship destruction, and all that lies between the birth and death of a
vessel, alters the marine environment. There is no one scholarly treatment that brings
together all of the environmental threads that are intertwined with the long history of
global shipping, one of the few enterprises that has touched every shore of the world.
In addition to the more obvious impacts (fuel spills, engine emissions, antifouling
paints, marine mammal collisions, shipwrecks and ship demolition, among others), a
fascinating combination of the voyages of the vessels themselves and the infrastructure
to support ships—specifically the building of harbors and canals—has led, perhaps
somewhat unexpectedly, to a profound alteration of the world’s marine biodiversity.
James Carlton is Professor of Marine Sciences at Williams College and Director of the Williams College
Mystic Seaport Maritime Studies Program. His research focuses on the history of marine environments,
including modern-day invasions and extinctions in the world’s oceans. He is the founder and editor-inchief of Biological Invasions.
Copyright © 2010 by the Brown Journal of World Affairs
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James T. Carlton
As ships sail the seas, they carry a plethora of marine life as fouling organisms
attached to the hull, including animals and plants such as barnacles, mussels, hydroids,
sponges, bryozoans, seaweeds, and many other species. Other species, such as shipworms
and gribbles, bored into wooden hulls. Ships also require ballast, which is “any solid or
liquid placed in a ship to increase the draft, to change the trim, to regulate the stability, or to maintain stress loads within acceptable limits.”2 Along with solid ballast and
water ballast come hundreds of species, only to be discharged at a distant port as the
vessel loads cargo. A well-laden ship can carry hundreds of different species. In due
course, thousands of non-native species would spread around the world in ship-mediated dispersal that continues today.3
As a result of global shipping and other human-associated vectors, harbors, bays,
and shores around the world now support large numbers of non-native species. These
species have had extensive ecological, environmental, economic, and other societal
impacts.4
The Development of Ports and Harbors: New Shores for New Invaders
132
Coincident with increased shipping was the vastly expanded development of
harbors.5 While non-native species invade habitats other than those created by ports,
harbors have long served as one of the great epicenters of invasions, which can then
spread to adjacent environments, even open oceans. Ports and harbors created out
of bays and estuaries required the construction of coastal flatlands (out of what were
once intertidal marshes and mudflats) and the creation of navigable channels and
deep-draft docks (by dredging out the estuary). In between the dredged channels and
the flatlands are the wooden, steel, or concrete columns (pilings) used to support the
piers to host the ships. With the exception of tropical mangrove forests, there is no
naturally occurring fixed, vertical wood in the oceans. With the development of ports,
vast forests of pilings began to appear, along with other structures that provided moreor-less permanent hard surfaces in what was formerly a world of soft mud. With the
widespread twentieth-century flourishing of recreational sailing came a further world
of floating piers in the form of “marinas:” pontoons made of wood, plastic, styrofoam,
concrete, and other materials that rise and fall with the tides, but do not drift away. In
essence, ports and marinas thus created a seascape of hard, fixed structures permitting
the transfer of fouling communities from ship to shore. At the same time, water quality
deteriorated as ports developed, due to pollution both from the ships themselves and
from the burgeoning seaport cities.
The result was, in essence, the creation of what on land might be viewed as a
“weedy lot:” highly disturbed, transient, anthropogenic habitats that eliminated the
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The Impact of Maritime Commerce on Marine Biodiversity
native flora and fauna, and perhaps paved the way for new invasions, often selecting
amongst the latter for those species with a robust physiological repertoire. As ships
arrived with heavily fouled hulls, with insect-and-plant laden ballast stones and rocks,
and later with whole ecosystems contained in ballast water, estuarine species from
elsewhere in the world found new homes with relative ease.
Ship Canals: Bridging Ancient Barriers
The world’s oceans are strikingly isolated from each other, despite the great ocean currents that would appear to connect them. Historically, coastal species living in the Pacific
Ocean had little access to the Atlantic Ocean, and vice versa. Indian Ocean and Red
Sea species were isolated by land barriers from the Mediterranean Sea. Over millions
of years, these isolated seas developed rich endemic biotas.
Both sea-level and lock canals dramatically changed this isolation. Just as the
opening of the sea-level Suez Canal in 1869 and the locked Panama Canal in 1914
changed shipping traffic patterns forever, they also opened up biological corridors that
in the first instance connected the Red Sea and Indian Ocean with the Mediterranean
Sea, and in the second the Atlantic and Pacific oceans. The most dramatic ecological
impact of any canal in the world has been the Suez Canal: nearly 300 species have
flowed into the Mediterranean since the 1870s, and new species continue to arrive on
a regular basis.6 The Panama Canal, long thought to be an unviable corridor between
oceans because of its central freshwater Gatun Lake, has in fact permitted the two-way
colonization of marine species tolerant of short-term submersion in freshwater.7 Perhaps
more important was that the vastly shortened sea voyages permitted by these canals
likely significantly improved survival of species moving around the world.8 A vessel
travelling from Japan to the American Atlantic coast through the Panama Canal now
saves 19 days in transit and 6,600 nautical miles as opposed to the trip around Cape
Horn.9 Although the biotic flow from the Red Sea to the Mediterranean Sea did not
require ship assistance, the same holds true for the reduction of passage time around
the Cape of Good Hope: a voyage from Mumbai to Haifa via the Suez Canal is reduced
by 25 days and 8,500 nautical miles.10
Fouling organisms on the hulls of ships passing through the Suez Canal, and
ballast-entrained organisms (via both canals) were thus more likely to survive passage
because of these shorter voyages. Ballast would prove particularly important for the
Panama Canal: marine species passing through the Canal inside a ship were provided
a safe haven transit through the freshwater barrier that was theoretically preventing
species from transiting between the Atlantic and Pacific oceans.
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James T. Carlton
The Advent of Ballast Water: Changing the Scale of Global Shipping-Mediated
Invasions
134
For thousands of years, ships carried barnacles and many other species on their hulls,
and insects, plants, and other organisms amongst their ballast rocks and sand. By the
1900s, heavy metal—copper and tin—based antifouling paints had begun to reduce,
but by no means eliminate, ship fouling as a major mediator of invasions by exotic
species. The goal, of course, was not to reduce alien invasions, but to reduce the drag
on the hull caused by massive biological accumulations that would significantly lower
vessel speed and increase fuel consumption.11 But this reduction in external transport
was to be replaced by the internal transport of species. Beginning in the 1880s, with
the development of iron ships (replacing wooden ships) and steam engines (replacing
sail), bulk-headed compartments could be developed in increasingly larger vessels.
These vessels could, in turn, be ballasted almost instantaneously with seawater or river
water, rather than with rocks, which required much more intensive, drawn-out manual
labor.12 By the early 1900s, the first ballast water-mediated invasions were being detected,
including Asian diatoms and crabs appearing in Western Europe that could only have
made the voyage in ballast water.13
The potential for ballast water, instead of hull fouling or ballast rocks, to facilitate
the transport and release of exotic species much more effectively was thus huge, and
foreshadowed a potentially dramatic rise in invasions of exotic species. Ships were now
pumping aboard, or gravitating in, virtually entire marine communities—hundreds
of species of plankton, and sometimes fish—which would be safely carried across the
inhospitable ocean from one distant estuary to the next, without being washed away or
dislodged from the surface of the ship. Surprisingly, however, few invasions were laid at
the doorstep of this mechanism for the first half of the twentieth century, and, indeed,
ballast water-mediated invasions were not commonly reported until the last quarter
of the twentieth century. Rather, it appears that classical rock-and-sand-ballast, used
by ships for millennia, was regarded as a much greater mechanism for the dispersal of
coastal insects and plants.14
On the one hand, it may be that invasions were proceeding and were simply not
being recognized. Throughout the twentieth century, as ballast water was increasing
in use, the number of naturalists, bio-geographers, and taxonomists, those who had
their fingers on the pulse of marine biodiversity, were, coincidentally, rapidly declining,
replaced in part by new generations of biologists who were focusing on the molecular,
cellular, and neurological nature of life.15
However, it may also be that it was the environmental surge of the 1960s that
ironically led to increased invasions by ships’ ballast water. Environmental movements
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The Impact of Maritime Commerce on Marine Biodiversity
in the 1960s resulted in a series of major pieces of conservation and environmental
legislation in the United States in the early 1970s: the Marine Mammal Protection
Act of 1972, the Endangered Species Act of 1973, and the Clean Water Act (CWA) of
1972. It had been long observed that ballast water was often foul, as a result of being
derived from highly polluted urban harbors.16 Indeed, it was widely believed—and
in hindsight perhaps rightly so—that ballast water from sewage-filled ports was too
foul to regularly support the transport of viable macro-organisms.17 As early as 1918,
relative to the contamination of the Great Lakes, the International Joint Commission
on the Pollution of Boundary Waters had identified polluted ballast water as a serious
environmental issue. Ferguson, in a rarely-cited paper, experimented with ballast water
chlorination, a treatment approach not to be revisited in the ballast management field
for another 60 and more years.18
It is thus compelling to note the correlation between the advent of the Clean
Water Act (CWA) of 1972 (along with parallel legislation that then evolved elsewhere
around the world) and the steady increase in ballast-mediated invasions. Port and harbor
waters were becoming significantly cleaner in the 1970s and 1980s, and this may have
had two major consequences: ballast water from donor ports was now more likely to
be both biologically more diverse and also capable of sustaining life in transit, while at
the same time the receiving ports—in which the water was released—were becoming
more hospitable to new colonists. In the 1980s, international regulations also moved
toward requiring segregated tanks for ballast water aboard petroleum tankers, rather
than boarding ballast that would be mixed with oil residues. Thus tanker traffic was now
also transporting cleaner ballast water capable of supporting marine life. Complicating
this correlation is that the 1970s and the following decades have seen a vast increase
in the number, size, and speed of ships, and the number of voyages, all potentially
translating into the movement of an increased number of species, increased inoculations of larval and adult animals, and increased survival of those species transported.
In reality, cleaner port waters—ironically initiated in part by greater environmental
concern—and increased traffic likely conspired together to bring ballast water onto
the global policy stage in the 1980s.
Japanese Dinoflagellates in Australia and Eurasian Mussels in America
Although common enough in ships to appear in Lloyd’s Register in 1880, ballast water
did not come onto the global policy stage until the 1980s. It was not that ballast-mediated invasions, whether by solid ballast or by water ballast, were unknown, nor that
ballast was not recognized as an environmental issue before the 1980s. In a paper with
remarkable similarities to modern discussions of invasive species management, Kirk
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James T. Carlton
(1893) argued strongly for the control of the discharge of earthen ballast. Working in
New Zealand, Kirk observed that a ship from Buenos Aires, Brazil, had discharged a
large quantity of ballast ashore in Wellington. A few months later, Kirk found 17 species
of plants growing in the ballast heap, including nuisance weeds such as the cocklebur,
Xanthium strumarium, a North American native. He discussed a number of management
strategies, including the suggestion that such ballast, potentially laden with the seed of
foreign plants, should “be taken out to sea by lighters and thrown overboard.” Lighters
are typically smaller vessels used to lighten the load of larger vessels. Kirk observed,
however, that since seeds of some plants may remain viable in salt water, this action
would only serve to provide “for the wholesale distribution of noxious weeds all along
the coast,” an observation matching a concern 100 years later with exchanging ballast
water at sea.19 Kirk noted the possibility of chemical treatment of ballast, but favored
a secure site for onshore disposal (a “ballast depot”), where any weeds that manifested
themselves could then be dispatched (he also suggested that the ballast could then be
used for ballasting other vessels). Finally, Kirk even touched upon biocontrol, noting
that garden slugs appeared to be an effective agent of eliminating the plants, based
upon his transplanting some of the ballast-heap species to his own garden. The themes
of open ocean disposal, chemical treatment, secure onshore depots, the use of previous ballast to ballast other vessels, and biocontrol, did not, in general, reappear in the
136
literature until the 1990s.
In the 1980s, two events occurred that brought ballast water to the attention of
port and flag states as well as to the United Nations International Maritime Organization (IMO), an agency focused on, among other mandates, environmental issues
associated with shipping.
These small, two centimeter–long mussels form Species of planktonic dimassive fouling aggregations that shut down noflagellates capable of
water supply systems, foul navigation buoys, and exploding in huge numbers to form what are
coat beaches with millions of razor-sharp shells. known as HABs (harmful
algal blooms), or toxic phytoplankton blooms (and more colloquially as “red tides”)
appeared in Australia with immediate impacts on the shellfish industry.20 Their source
was Japan, and the means of their appearance was quickly linked to transportation in
ballast water. Also in the 1980s, two species of freshwater bivalves, the zebra mussels
(Dreissena polymorpha and D. bugensis), native to rivers flowing into the Black Sea, appeared in the Great Lakes, an event also linked to ballast water discharge. These small,
two centimeter–long mussels form massive fouling aggregations that shut down water
supply systems, foul navigation buoys, and coat beaches with millions of razor-sharp
shells. First encountered by industry and the public in 1985, and first detected by the
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The Impact of Maritime Commerce on Marine Biodiversity
scientific community in 1988, zebra mussels colonized much of the eastern half of the
United States by the early 1990s.
Australia, Canada, and the Unites States responded to these invasions by bringing
the need to control ballast water discharge to the Marine Environmental Protection
Committee (MEPC) of the IMO, in London, which initially assigned the problem to
small subgroups for discussion and development. Throughout the 1990s, scores of additional groups (academic, industrial, governmental, and environmental) in the United
States, Canada, Japan, Australia, New Zealand, and a number of European countries,
also met to discuss ballast water management, producing thousands of pages on potential control strategies. Nearly 20 years of this work are summarized by Dobroski,
who reviewed the physical, chemical, biological, and other strategies that have been
suggested to reduce or eliminate living organisms in ballast water.21
International, National, and State Responses to Ballast Water Management
In 1991, the IMO’s MEPC adopted “Guidelines for Preventing the Introduction of
Unwanted Organisms and Pathogens from Ships’ Ballast Water and Sediment Discharges.” Two years later, ballast water was taken up at the Assembly (full) level of IMO,
and a similar resolution (of the same title) was adopted; four years later, in 1997, the
Assembly adopted a revised and expanded version, “Guidelines for the Control and
Management of Ships’ Ballast Water to Minimize the Transfer of Harmful Aquatic
Organisms and Pathogens.” All of these actions were voluntary and non-binding. It
took until February 2004, more than 15 years after Australia and North America had
been invaded by economically damaging exotic species, for the IMO to adopt a formal
convention on ballast management with the release of the “International Convention
for the Control and Management of Ships’ Ballast Water and Sediments.”
The long delay in producing this convention was due to a painfully extended timeline (often assigned to such deliberations); the need to involve an increasing number of
port and flag states as the issue rose closer to the top of the MEPC agenda; numerous
industrial and political agendas; and, as with all UN conventions, the extended analysis
and debate of almost every word in the Convention.
The 2004 convention identified ballast water management procedures, particularly focusing on exchanging ballast water at sea, a strategy which had been in place
for more than a decade, and adopted so-called “discharge standards”—the number and
size of organisms that could be discharged in ballast water following at-sea exchange or
other water treatment methods. At-sea exchange involves the deballasting of as much
water as is safe to do so and then reballasting. Deballasting coastal water in mid-ocean
would result in the death of estuarine and harbor species; reciprocally, releasing open
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James T. Carlton
138
ocean species (which had been taken up in the mid-ocean reballasting process) in bays
and estuaries would not cause invasions, as oceanic species would die in the enclosed
coastal waters.
This convention enters into force one year after ratification by 30 countries that
represent not less than 35 percent of the gross tonnage of the world’s merchant shipping.
As of 28 February 2010, 22 countries have become contracting states to the Convention, together representing 22.65 percent of the merchant fleet’s gross shipping tonnage
(tonnage calculations are based upon Lloyd’s Register/Fairplay World Fleet Statistics as
of 31 December 2008). None of the original parties—Australia, Canada, or the United
State—that brought ballast to the IMO have yet ratified the treaty.
One of the obstacles to ratification is agreement on what should be the acceptable standard for the amount of life discharged in ballast water. Such standards will be
fundamental to approving the onboard use and installation of ballast water treatment
methods. At the IMO convention, the United States lobbied for more stringent standards than those that were adopted. The proposed IMO standard, as tabled in 2004,
is that for organisms larger than 50 micrometers in size, discharge must be less than 10
individuals per cubic meter. For organisms equal to or smaller than 50 micrometers,
but larger than 10 micrometers, discharge must be less than 10 individuals per milliliter of water. Additional standards were formulated for the discharge of toxigenic
cholera bacteria and Enterococcus bacteria. The United States Coast Guard (USCG)
regards these IMO standards as likely to yield only “minor to moderate reduction” in
marine bio-invasions.
United States Federal Government
Ballast water came to the attention of the United States Congress in late 1988 and
early 1989 as a result of the appearance of zebra mussels in the Great Lakes, as noted
above. Early reports of the mussels in both the Senate and House of Representatives
were first greeted as a typical environmental issue best addressed locally (or not at all),
or as some workers in Washington, D.C. refer to as a MEGO (“my eyes glaze over”)
matter. When the seriousness of the invasion became clear, legislation was written to
address ballast water and exotic species invasions. The first hearings on proposed bills
to address ballast water and “aquatic nuisance species” were held in the 101st Congress
on 14 June, 1990 in the House and on 15 June, 1990 in the Senate.
Prior to 1990, the question of invasions of non-native species in U.S. fresh and
marine waters had rarely come before Congress. One of the more famous exchanges
during the first testimony occurred in the Senate hearing. After a United States Fish
and Wildlife Service official had outlined the history and potentially dire economic
consequences of the zebra mussel invasion in the Great Lakes, a senior senator leaned
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The Impact of Maritime Commerce on Marine Biodiversity
forward into his microphone, and, departing from the questions prepared by his aides,
asked if the zebra mussel was an endangered species. After a 10 second pause filled the
chamber with silence, the witness replied that he was pleased to report that it was not.
The hearing continued, and these remarks never appeared in the published record of
that day. While only a minor note in legislative history, this incident illustrates the
challenges scientists faced early on in bringing invasive species issues to the “three
P’s”—public, press, and politicians.
A critical piece of legislation was passed that fall, the National Aquatic Nuisance
Prevention and Control Act of 1990 (NANPCA), which was reauthorized and renamed
in 1996 as NISA, the National Invasive Species Act. As a result of authorization by
NANPCA and NISA, and
While only a minor note in legislative history, this
of too-limited voluntary
actions by the shipping in- incident illustrates the challenges scientists faced
dustry to exchange ballast early-on in bringing invasive species issues to the
water called for by NISA,
the USCG established in “three P’s”—the public, the press, and politicians.
2004 a mandatory Ballast Water Management program, requiring foreign ships to
conduct mid-ocean exchange when safe to do so, before entering a U.S. port-of-call.
The USCG also required all ships, regardless of whether they exchanged water or not,
139
to file a ballast water management report with the National Ballast Information Clearinghouse located at the Smithsonian Environmental Research Center in Edgewater,
Maryland.
In August 2009, the USCG, partly in response to the IMO Convention of 2004,
issued a long-awaited “Draft Programmatic Environmental Impact Statement for Standards for Living Organisms in Ship’s Ballast Water Discharged in U.S. Waters.” Under
these standards, ships would have to meet the IMO targets by 2016. Future federal
targets would set allowable concentrations significantly lower than the IMO’s standards:
for organisms larger than 50 micrometers, concentrations would be required to be less
than one per cubic meter; for organisms greater than 10 but less than or equal to 50
micrometers, discharge concentrations would be less than one per milliliter of water. A
number of U. S. states (to the dismay of shipping organizations desiring one national
standard) have already invoked these stronger standards. In a curious denouement, the
Clean Water Act (CWA) returned to the ballast water stage again in 2009. In 2003, a
consortium of environmental groups sued the Environmental Protection Agency (EPA)
for failure to regulate ballast water discharge as point source pollution under the CWA.
After the EPA fought for years, the courts ruled in favor of the plaintiffs in 2008, and
the EPA was required to regulate ballast water discharge in U.S. waters. In response, in
2009, the EPA issued permits paralleling the USCG standing regulations.
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The Challenges Ahead
140
Numerous challenges attend the development of policy and management scenarios
relative to shipping-mediated invasions. What remains unclear is the actual timing of
the development and installation on tens of thousands of vessels of ballast treatment
technology and what that technology would be. In the meantime, extensive biological
monitoring to determine what ships have been able to achieve by ballast water exchange
or other treatments remains beyond the funding capacity of most oversight agencies.
Equally challenging is that ballast water is not the sole mediator of exotic species invasions by ocean-going vessels. Remaining in play, despite the advancement of
antifouling paints, are hull fouling organisms (growing where the ship was not painted
or where the paint has worn away), including the appearance of populations of certain fouling species that have become resistant to such paints. Also continuing to be
transported by ships are species carried in other areas of the vessel, such as seachests
(compartments where ballast water is first drawn into the ship before being pumped to
tanks or cargo holds), seawater pipe systems, and anchors and anchor chains.
Finally, in the bigger picture, maritime commerce is not simply restricted to ships.
Numerous living marine organisms are now moving around the world everyday—but
on planes and not ships—in the live seafood trade, the aquaculture/mariculture industries, the live bait trade, and the aquarium/pet trade.22 The historical precedents for this
modern-day active trade in marine life are many, prominent among them a century of
global movements of commercial oysters, between the 1860s and 1970s, that led to
the introduction of far more species than the oysters themselves.23
Considering the tens of thousands of ships at sea, the entrained species in their
ballast, hulls, and other systems—along with the intentional international trade moving living marine plants and animals—there is little doubt that the number of marine
species in global bioflow on a daily basis must number in the thousands; it is possible
that more than 10,000 species of marine life may be in motion daily by means of seagoing vessels.24 As a result, it is reasonable to conclude that new invasions occur daily,
somewhere in the world’s oceans.
Conclusion
Beginning in 2006, the A. P. Moller-Maersk shipping group began launching the
largest container ships ever constructed, including the Emma Maersk, at 1,305 feet
(397.7 meters) in length, and with a gross tonnage of over 170,000. Larger ships mean
greater surface areas for fouling organisms, and the need for more ballast water as well.
As global commerce expands and as the desire and need to move more goods faster
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increase, environmental management scenarios will have to not only keep up with the
growth of the maritime industry, but also anticipate the direction and nature of growth
as well. Indeed, while both policy scholars and scientists tend to work within their own
disciplines, both groups would do well to study the business world to develop more
robust insight into what the future may hold. W
A
Notes
1. Ameer Abdulla and Olof Linden, eds, “Maritime Traffic Effects on Biodiversity,” Mediterranean
Sea: Review of Impacts, Priority Areas, and Mitigation Measures (Malaga: IUCN Centre for Mediterranean
Cooperation, 2008).
2. National Research Council, Stemming The Tide. Controlling Introductions of Nonindigenous Species by
Ships’ Ballast Water (Washington, D.C.: National Academy Press, 1996).
3. James Carlton, “The Scale and Ecological Consequences of Biological invasions in the World’s Oceans,”
Invasive Species and Biodiversity Management (Dordrecht: Kluwer Academic Publishers, 1999): 195-212;
James Carlton, “Deep Invasion Ecology and the Assembly of Communities in Historical Time,” Biological
Invasions in Marine Ecosystems (Berlin: Springer-Verlag, 2009): 13-56; Rilov, Gil, and Jeff Crooks, eds.,
Biological Invasions in Marine Ecosystems (Berlin: Springer-Verlag, 2009).
4. James Carlton, Introduced Species in U.S. Coastal Waters: Environmental Impacts and Management
Priorities (Arlington, Virginia: Pew Oceans Commission, 2001); Rilov, Gil, and Jeff Crooks, eds., Biological
Invasions in Marine Ecosystems (Berlin: Springer-Verlag, 2009).
5. Robert Albion, The Rise of New York Port (1815-1860) (Boston: Northeastern University Press,
1939); Morgan, Frederick W. Ports and Harbours (London: Hutchinson’s University Library, 1952); L.E.
Klimm, “Man’s Ports and Channels,” Man’s Role in Changing the Face of the Earth (Chicago: University
of Chicago Press, 1956): 522-541; Bird, James. Seaports and Seaport Terminals (London: Hutchinson
University Library, 1971).
6. Bella Galil. “The Marine Caravan—the Suez Canal and the Erythrean Invasion,” Bridging Divides.
Maritime Canals as Invasion Corridors (Dordrecht, The Netherlands: Springer, 2006): 207-300; Bella Galil.
“Taking Stock: Inventory of Alien Species in the Mediterranean Sea.” Biological Invasions 11 (2008): 359372; Gil Rilov and Bella Galil. “Marine Bioinvasions in the Mediterranean Sea—History, Distribution,
and Ecology,” Biological Invasions in Marine Ecosystems (Berlin: Springer-Verlag, 2009): 549-575.
7. Andrew Cohen. “Species Introductions and the Panama Canal,” Bridging Divides, Maritime Canals
as Invasion Corridors (Dordrecht: Springer, 2006): 127-206.
8. L.E. Klimm, “Man’s Ports and Channels,” Man’s Role in Changing the Face of the Earth (Chicago:
University of Chicago Press, 1956): 522-541.
9. Dan Minchin, Bella Galil, Matej David, Stephan Gollasch, and Sergej Olenin, “Overall Introduction,”
Bridging Divides, Maritime Canals as Invasion Corridors (Dordrecht: Springer, 2006): 1-4.
10. Ibid.
11. Woods Hole Oceanographic Institution, Marine Fouling and its Prevention (Woods Hole: Woods
Hole Oceanographic Institution, 1952).
12. James Carlton, “Transoceanic and Interoceanic Dispersal of Coastal Marine Organisms: The Biology
of Ballast Water.” Oceanography and Marine Biology, An Annual Review 23 (1985): 313-371.
13. Ibid.
14. Carl Lindroth, The Faunal Connections Between Europe and North America (New York: John Wiley
and Sons, Inc., 1957).
15. Joel Hedgpeth, Robert Menzies, Cadet Hand, and Martin Burkenroad. “On Certain Problems of
Taxonomists.” Science 117 (1953): 17-18; David Ehrenfeld, “Is Anyone Listening?.” Conservation Biology
3 (1989): 415.
16. G. H. Ferguson, “The Chlorination of Ballast Water on Great Lakes Vessels,” Public Health Reports
47 (1932): 256-258.
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James T. Carlton
17. James Carlton, (1985): 313-371.
18. G.H. Ferguson, “The Chlorination of Ballast Water on Great Lakes Vessels,” Public Health Reports
47 (1932): 256-258.
19. James Carlton, David Reid, and Henry van Leeuwen, The Role of Shipping in the Introduction of
Non-Indigenous Aquatic Organisms to the Coastal Waters of the United States (other than the Great Lakes)
and an Analysis of Control Options (Washington, D.C.: Department of Transportation, United States
Coast Guard, 1995).
20. Gustav Hallegraeff, “Transport of Toxic Dinoflagellates via Ships’ Ballast Water: Bioeconomic Risk
Assessment and Efficacy of Possible Ballast Water Management Strategies,” Marine Ecology Progress Series
168 (1998): 297-309; J.S. Bolch, Christopher, and Miguel F. de Salas. “A Review of the Molecular Evidence
for Ballast Water Introductions of the Toxic Dinoflagellates Gymnodinium catenatum and Alexandrium
tamarensis Complex to Australasia,” Harmful Algae 6 (2007): 465-485.
21. Nicole Dobroski S. Scianni, D. Gehringer, and M. Falkner, 2009 Assessment of the Efficacy, Availability
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