Ecological Applications, 23(2), 2013, pp. 289–300

2013 by the Ecological Society of America

Ballast water regulations and the move toward concentration-based

numeric discharge limits

RYAN J. ALBERT,

1 JOHN M. LISHMAN, AND JUHI R. SAXENA

U.S. Environmental Protection Agency, Office of Water, Office of Wastewater Management, Permits Division,

1200 Pennsylvania Avenue, N.W., Washington, D.C. 20460 USA

Abstract. Ballast water from shipping is a principal source for the introduction of

nonindigenous species. As a result, numerous government bodies have adopted various ballast

water management practices and discharge standards to slow or eliminate the future

introduction and dispersal of these nonindigenous species. For researchers studying ballast

water issues, understanding the regulatory framework is helpful to define the scope of research

needed by policy makers to develop effective regulations. However, for most scientists, this

information is difficult to obtain because it is outside the standard scientific literature and

often difficult to interpret. This paper provides a brief review of the regulatory framework

directed toward scientists studying ballast water and aquatic invasive species issues. We

describe different approaches to ballast water management in international, U.S. federal and

state, and domestic ballast water regulation. Specifically, we discuss standards established by

the International Maritime Organization (IMO), the U.S. Coast Guard and U.S. Environmental Protection Agency, and individual states in the United States including California,

New York, and Minnesota. Additionally, outside the United States, countries such as

Australia, Canada, and New Zealand have well-established domestic ballast water regulatory

regimes. Different approaches to regulation have recently resulted in variations between

numeric concentration-based ballast water discharge limits, particularly in the United States,

as well as reliance on use of ballast water exchange pending development and adoption of

rigorous science-based discharge standards.

To date, numeric concentration-based discharge limits have not generally been based upon

a thorough application of risk-assessment methodologies. Regulators, making decisions based

on the available information and methodologies before them, have consequently established

varying standards, or not established standards at all. The review and refinement of ballast

water discharge standards by regulatory agencies will benefit from activity by the scientific

community to improve and develop more precise risk-assessment methodologies.

Key words: aquatic nuisance species (ANS); ballast water; International Maritime Organization

(IMO); invasive species; National Invasive Species Act (NISA); propagule pressure; Vessel General Permit

(VGP).

INTRODUCTION

Ballast water discharges have been a major source of

nonindigenous species introductions to marine, estuarine, and freshwater ecosystems (Ruiz et al. 1997,

2000a). When organisms in ballast tanks are transported

between waterbodies and discharged, they have the

potential to establish new populations of species in

waterbodies to which they are not native (Ruiz et al.

2000b, Bolch and de Salas 2007, Drake and Lodge 2007,

Kipp et al. 2010). The introduction of nonnative aquatic

nuisance species (ANS) via ballast water discharge can

cause significant economic and ecological damage

(Lovell and Drake 2009).

Ballast water is necessary for the safe operation of the

vast majority of larger vessels to assist with draft, trim,

and stability. Depending on the ship type and cargo

operations, vessels may discharge anywhere from less

than 100 cubic meters of ballast to tens of thousands of

cubic meters (American Bureau of Shipping 2010). Best

management practices can help reduce the potential

impacts of ballast water discharges. Such practices

include ballast water exchange and saltwater flushing

for certain vessels/voyages (collectively referred to as

ballast water exchange, or BWE). Ballast water exchange refers to the replacement of the water in a ballast

tank with ocean water through either flow-through

exchange or empty/refill exchange (Gregg et al. 2009).

Saltwater flushing refers to the addition of ocean water

Manuscript received 23 April 2012; revised 15 August 2012;

accepted 16 August 2012. Corresponding Editor (ad hoc): H. J.

MacIsaac. For reprints of this Invited Feature, see footnote 1,

p. 287. 1 E-mail: albert.ryan@epa.gov

289

March 2013 MANAGING BALLAST WATER DISCHARGES
to empty ballast water tanks, where it is mixed with

residual ballast water and sediment through the motion

of the vessel, and then discharged (Briski et al. 2010).

These practices have been shown to help mitigate the

transfer and potential introduction of many potential

invasive species (Gray et al. 2007, McCollin et al. 2007,

Ruiz and Reid 2007, Bailey et al. 2011). However, the

practices have also been shown to provide limited

removal efficacy in some cases, such as for invertebrate

dormant eggs in sediments or macroinvertebrates for

certain voyages (Briski et al. 2011, 2012). Additionally,

BWE and saltwater flushing are not feasible for all

vessels (e.g., vessels that cannot voyage offshore or that

are engaged in coastal voyages), or in all circumstances

due to vessel safety concerns (e.g., rough weather and

high seas) (Miller et al. 2011, U.S. EPA 2011, Cohen et

al. 2012).

One way to address the limitations associated with

BWE is to require treatment of ballast water discharges

to meet an established standard for the concentration of

living organisms. The establishment of concentrationbased ballast water standards, implemented with effective ballast water treatment technologies, will reduce the

number of organisms discharged from most vessels and

will allow more vessels to effectively treat ballast water

than under current BWE practices. The reduction in

propagule pressure (i.e., the reduction in the quality,

quantity, and frequency with which living organisms are

introduced into the aquatic environment), in turn, will

reduce the probability of invasions, when controlling for

all other variables (NRC 2011). A general consensus has

emerged among policy makers that concentration-based

ballast water discharge standards should be stringent

enough to substantially reduce the risk of ANS

establishment in aquatic ecosystems, with some policy

makers believing the risk should be eliminated. However, in the absence of robust scientifically based risk

assessment methodologies, policy makers do not always

agree on the most appropriate discharge standards to

achieve these goals, resulting in inaction or a variety of

ballast water discharge standards.

For researchers studying ballast water issues, an

understanding of the regulatory framework is helpful

to define the scope of research needed by policy makers

to develop effective regulations. For example, the early

reliance on ballast water exchange as the primary

management practice spurred researchers to explore its

effectiveness in reducing the concentration of organisms

in ballast discharge (e.g., Ruiz and Reid 2007, Bailey et

al. 2011). The implementation of concentration-based

discharge standards will also drive future research and

funding. Critical questions associated with development

and implementation of such discharge standards include

how well the existing or more stringent limits prevent or

reduce the risk of invasion (Lee et al. 2013, Reusser et al.

2013); and how to implement effective compliance

monitoring and treatment system testing (Frazier et al.

2013). An understanding of the regulatory framework

will also help researchers parameterize risk models so

they are most relevant to policy makers. One limitation

of some of the models that were initially used to inform

the development of discharge limits was that invasion

probability was modeled using parameters other than

the concentration of organisms in discharge (i.e.,

volume, for example; Lee et al. [2011]). In these cases,

the utility of these models to policy makers was reduced

because the data were difficult to evaluate in the context

of the current regulatory framework. Despite the

importance of having a working knowledge of ballast

regulations, for most scientists this information is

difficult to obtain because it is outside the standard

scientific literature and often difficult to interpret. To

meet this need, we provide a brief review of several

regulatory frameworks for ballast water discharge

standards, including those at the international and

domestic levels, that is specifically directed at scientists

studying ballast water issues. We also discuss how

establishment of discharge standards might benefit from

improved risk-assessment methodologies. We do not

discuss issues related to the effectiveness of ballast water

treatment technologies, which has been addressed elsewhere (Dobroski et al. 2011, Lloyds Register 2011, U.S.

EPA SAB 2011).

REGULATORY BACKGROUND

Ballast water discharges from vessels are presently

subject to regulation at the international and domestic

levels.

International regime

At the international level, ballast water discharges are

primarily addressed under the auspices of the International Maritime Organization (IMO) and its subsidiary

body, the Marine Environment Protection Committee

(MEPC) (Gollasch et al. 2007, Gregg et al. 2009). The

IMO first adopted a resolution in 1991 that contained

guidelines calling for mid-ocean ballast water exchange

and other ballast water management practices (MEPC

1991). Those guidelines were subsequently updated and

replaced in 1997 (IMO 1997). Following adoption of

that resolution, a working group under IMO’s MEPC

was given the charge of developing legally binding

requirements for a ballast water management treaty.

Over the course of deliberation, there was a gradual

evolution away from BWE to the adoption of ballast

water discharge standards in the form of concentrations

of organisms per unit of volume of ballast water

discharged. The culmination of this effort was a

Diplomatic Conference held at the IMO in 2004, which

adopted the text of the International Convention for the

Control and Management of Ships’ Ballast Water and

Sediments (hereinafter referred to as ‘‘the BWM

Convention’’ [IMO 2004]). The BWM Convention will

not enter into force until 12 months after ratification by

30 states, representing 35% of world merchant shipping

tonnage. As of 31 July 2012, the United States is not a

290 INVITED FEATURE Ecological Applications

Vol. 23, No. 2
signatory, nor has the BWM Convention entered into

force internationally; although 35 states have ratified the

BWM Convention, they represent only 27.95% of world

merchant shipping tonnage (IMO 2012).

The provisions of the BWM Convention will apply to

Parties’ commercial ships that engage in international

voyages (BWM Convention Article 3). Subject to certain

exceptions, these vessels must conduct ballast water

exchange, and over time, comply with the Convention’s

concentration-based ballast water discharge standards

according to a schedule dependent on vessel build date

and ballast water capacity (BWM Convention Regulation B-3). Those discharge standards address allowable concentrations of three size groupings of organisms:

(1) organisms 50 lm (to address macrofauna and

zooplankton) at less than 10 viable organisms per cubic

meter; (2) organisms .10 lm but ,50 lm (to address

phytoplankton) at less than 10 viable organisms per

milliliter; and (3) specified indicator bacteria (to address

pathogens), standards typically expressed in terms of

number of colony-forming units (CFU) per 100 milliliters (BWM Convention Regulation D-2; see Table 1).

The BWM Convention also preserves the ability of

Parties to adopt more stringent standards as necessary

(BWM Convention Regulation C-1; BWM Convention

Article 2(3)).

Under the Treaty, ballast water treatment systems

are subject to a review and approval process (BWM

Convention Regulation D-3). The ability of a treatment system to meet the Convention’s discharge

standards is evaluated by Administrations (typically

the Flag State) under guidelines developed by the

MEPC (the ‘‘G8 Guidelines’’) (MEPC 2008a). In

addition to this type-approval process, systems using

‘‘active substances’’ (e.g., biocidal agents) are also

reviewed by the MEPC in regard to environmental and

safety aspects under a technical procedure commonly

referred to as the ‘‘G9 Guidelines’’ or ‘‘G9 Procedure’’

(MEPC 2008b). Although the BWM Convention is not

in force as of 31 July 2012, a number of systems have

been reviewed and approved under the processes

described above (Albert et al. 2010, IMO 2011). As of

14 March 2012, there are 21 type-approved ballast

water management systems (MEPC 2012), although

two of these systems were removed from the market by

their manufacturers.

Examples of domestic regulation

United States federal regulation.—At the U.S. federal

level, ballast water management is principally addressed

by two statutes: (1) the Nonindigenous Aquatic Nuisance Prevention and Control Act (NANPCA) of 1990,

as amended (16 U.S. Code [U.S.C.] §§ 4701 et seq.); and

(2) the Federal Water Pollution Control Act (commonly

referred to as the Clean Water Act or CWA, 33 U.S.C.

§§ 1251 et seq.; see Fig. 1). Both NANPCA and the

CWA preserve the authority of the individual U.S. states

to more stringently regulate ballast water discharges that

occur in their waters (16 U.S.C. § 4725, NANPCA; 33

U.S.C. § 1370, CWA). For the states that currently

regulate ballast water discharges, there is substantial

variation in their requirements (Table 1).

Congress enacted NANPCA in November 1990

(Public Law 101-646; 104 STAT 4761) to authorize the

U.S. Coast Guard (USCG) to issue regulations to

prevent the introduction and spread of ANS into the

Great Lakes through the ballast water of vessels. In

1996, Congress enacted the National Invasive Species

Act (NISA), which amended and reauthorized NANPCA (Public Law 104 -332; 110 STAT 4073). Among

other things, the amendments made by NISA directed

the USCG to develop a national ballast water management program for U.S. waters besides the Great Lakes.

The USCG ballast water management requirements

specific to the Great Lakes are codified in regulations at

33 U.S. Code of Federal Regulations [C.F.R.] Part 151,

Subpart C, and the requirements applicable to all U.S.

waters are codified at 33 C.F.R. Part 151, Subpart D. As

initially issued, both sets of regulations were consistent

with the existing ballast water management resolutions

adopted by IMO and placed primary emphasis on use of

mid-ocean BWE to manage ballast water. Recognizing

the significant limitations of a BWE-based regulatory

framework, the USCG issued for public comment a

proposed rule in August 2009 to gradually replace

reliance on BWE with a regime requiring treatment of

ballast water to meet a concentration-based discharge

standard. The initial USCG proposed rule would first

have required ballast water discharges to meet a

standard consistent with the BWM Convention’s

Regulation D-2 standard (referred to in the USCG

proposal as the ‘‘Phase 1’’ standard). The proposed rule

would have subsequently required compliance with a

discharge standard 1000 times more stringent than

Phase 1 for the two larger size classes of organisms

(the ‘‘Phase 2’’ standard) (74 Federal Register 44632).

Following consideration of the public comments

received on its proposed rule, the USCG issued a final

ballast water discharge standard rule on 23 March 2012

(77 Federal Register 17254). The final rule adopts the

proposed Phase 1 standard but defers final action on a

Phase 2 standard. The final rule applies the Phase 1

standard to two groups of vessels: (1) those already

subject to the USCG’s BWE requirements (essentially,

vessels discharging in U.S. waters that take on ballast

water outside the United States and Canadian Exclusive

Economic Zone [EEZ]) and (2) certain coastwise vessels

over 1600 gross register tons discharging in U.S. waters,

but that do not operate beyond the U.S. and Canadian

EEZ.

Under the CWA, the U.S. Environmental Protection

Agency (EPA) regulates the discharge of pollutants

into U.S. waters. However, under a regulation first

promulgated by EPA in 1973, discharges incidental to

the normal operation of a vessel, including ballast

water, were excluded from the Act’s National Pollutant

March 2013 MANAGING BALLAST WATER DISCHARGES 291
Discharge Elimination System (NPDES) permitting

regime (38 Federal Register 13528, 40 C.F.R. 122.3(a)).

That exclusion from NPDES permitting was challenged

in court, and the U.S. District Court for the Northern

District of California issued an order that vacated

(struck down) the exclusion of vessel discharges from

NPDES permitting as of 6 February 2009 (see,

generally, Northwest Environmental Advocates et

al. v. EPA, 573 F.3d 1006 (9th Cir 2008); available

online).2

In light of the court’s decision, EPA issued the Vessel

General Permit (VGP) in December 2008, which

TABLE 1. Selected ballast water discharge standards for organisms (current as of 31 July 2012).

Standard Size 50 lmSize , 50 lm but 10 lm

IMO BWM Convention (Reg. D-2) ,10 ‘‘viable’’ organisms per m3 ,10 ‘‘viable’’ organisms per mL

U.S. negotiating position (BWM/

CONF/13 and 14)

,0.01 ‘‘living’’ organisms per m3 ,0.01 ‘‘living’’ organisms per mL

USCG final rule ,10 ‘‘living’’ organisms per m3 ,10 ‘‘living’’ organisms per mL

EPA proposed 2013 VGP same as USCG final rule same as USCG final rule

California (VGP 401 cert/State regulations)

Interim standard 0 detectable ‘‘living’’ organisms U.S. negotiating position

Final standard 0 detectable ‘‘living’’ organisms 0 detectable ‘‘living’’ organisms

Illinois, Indiana, Ohio (VGP 401

cert), and Minnesota (VGP 401

cert/State permit)

,10 ‘‘viable’’ organisms per m3

(as daily average)

,10 ‘‘viable’’ organisms per mL

Michigan (MI)(VGP 401 cert/State

permit)

use a treatment process approved

by MI DEQ

use a treatment process approved

by MI DEQ

New York (VGP 401 cert)}

Interim standard ,1 ‘‘living’’ organism per 10 m3 ,1 ‘‘living’’ organism per 10 mL

Final standard Same as California levels U.S. negotiating position

Wisconsin (State Permit)|| ,10 ‘‘viable’’ organisms per m3

(as daily average)

,10 ‘‘viable’’ organisms per mL (as

daily average)

Notes: Note that some U.S. states have indicated that they plan to delay implementation dates for system installation.

Abbreviations: Reg., regulation; CFU, colony-forming unit; cert, certificate. Other abbreviations are defined in Fig. 1.

For some standards, the groupings actually are stated as organisms .50 lm and organisms 50 lm but .10 lm. For sake of

simplicity, this table uses the IMO groupings throughout as the default column header.

 Indiana, Minnesota, Ohio, and Wisconsin have defined ‘‘viable’’ as living AND able to reproduce. IMO G8 (type-approval)

Guidelines (paragraph 3.12) simply define viable as ‘‘living.’’

§ Indicator microbes specified by State do not include Vibrio cholerae.

} Pennsylvania provided limits generally consistent with New York’s limits on its CWA section 401 certification for the VGP but

modified its certification on 1 October 2010 to delete conditions with numeric ballast water treatment limits. Pennsylvania currently

has no state numeric ballast water discharge standards

# The State of New York subsequently ‘‘extended its implementation date to midnight, December 19, 2013’’ (J. M. Tierney,

unpublished letter).

jj Wisconsin finalized its first ballast water permit on 18 November 2009 with limits 100 times more stringent than IMO. On 1

April 2011, Wisconsin announced it had modified its general permit to require ballast water treatment to standards consistent with

the IMO BWM Convention limits based on a review that determined that BWT technology was not available to meet the WI 100

times IMO standards.

2 http://archive.ca9.uscourts.gov/ca9/newopinions.nsf/

1B1275291668F0348825748F00481607/$file/0374795.pdf?

openelement

292 INVITED FEATURE Ecological Applications

Vol. 23, No. 2
regulates discharges incidental to the normal operation

of vessels and includes provisions requiring BWE. The

2008 VGP includes, among other things, technologybased effluent limits (based on what technologies can

achieve) that are similar to the mandatory ballast water

management and exchange requirements in the thenexisting USCG regulations implementing NANPCA. In

addition, the 2008 VGP includes water quality-based

effluent limits to control discharges as stringently as

necessary to meet applicable water quality standards

(VGP § 2.3).

The existing VGP will expire on 19 December 2013.

EPA released the next VGP for public comment on 30

November 2011, and it included numeric concentrationbased ballast water discharge standards equivalent to

the IMO Regulation D-2 standards and the proposed

USCG regulations’ Phase 1 standard (U.S. EPA 2011).

When developing the new VGP, EPA sought the advice

of the National Academy of Sciences National Research

Council (NRC) on the identification and application of

relevant risk assessment methodologies (NRC 2011).

The resulting NRC report concluded that the risk

associated with a variety of regulatory discharge limits

could not be evaluated because of ‘‘a profound lack of

data and information to develop and validate models’’

and ‘‘it was not possible with any certainty to determine

the risk of nonindigenous species establishment under

existing discharge limits’’ (NRC 2011). Nonetheless, the

NRC report noted that a concentration-based ballast

water discharge standard that is consistent with the

BWM Convention’s Regulation D-2 standard would

significantly reduce organism concentrations relative to

ballast water exchange. The NRC report proposed a

coordinated, large scale research program that would

take between 3–10 years to complete, consisting

primarily of a ship discharge sampling program to

estimate propagule supply and a mesocosm-based

approach to calibrate models (NRC 2011).

Provided some or all of the identified data gaps are

filled, efforts to derive environmentally protective ballast

TABLE 1. Extended.

Bacteria Viruses Compliance date

Vibrio cholerae ,1 CFU/100 mL, E. coli

,250 CFU/100 mL, intestinal

enterococci ,100 CFU/ 100 mL

2009–2019 (varies by vessel

construction date/BW capacity/

survey date as per Reg. B-3)

Vibrio cholerae ,1 CFU/100 mL, E. coli

,126 CFU/100 mL, intestinal

enterococci ,33 CFU/100 mL

as soon as possible

Vibrio cholerae ,1 CFU/100 mL, E. coli

,250 CFU/100 mL, intestinal

enterococci ,100 CFU /100 mL

on delivery for all vessels constructed

on or after 1 Dec 2013, all other

vessels: varies by BW capacity and

drydock cycle with latest compliance

date of first drydock after 1 Jan 2016

same as USCG final rule on delivery for all vessels constructed

on or after 1 Jan 2012, same as

USCG final rule for all other vessels

Vibrio cholerae, IMO Reg D-2 levels; E.

coli, U.S. negotiating position;

intestinal enterococci, U.S. negotiating

position, ,103 bacteria/100 mL

,104 viruses/100 mL 1 Jan 20101 Jan 2016 (varies by

vessel construction date/BW

capacity)

0 detectable ‘‘living’’ organisms 0 detectable ‘‘living’’ organisms 1 Jan 2020

Vibrio cholerae§; E. coli, IMO Reg D-2

levels (as daily average); intestinal

enterococci, IMO Reg D-2 levels (as

daily average)

constructed before 1 Jan 2012, 1 Jan

2016; constructed after 1 Jan 2012,

prior to operation

use a treatment process approved by MI

DEQ

use a treatment process approved by

MI DEQ

1 Jan 2007

Vibrio cholerae, IMO Reg D-2 levels; E.

coli, U.S. negotiating position,

intestinal enterococci, U.S. negotiating

position

1 Jan 2012 (subject to case-by-case

time extension)

Vibrio cholerae, IMO Reg D-2 levels; E.

coli, U.S. negotiating position,

intestinal enterococci, U.S. negotiating

position; other bacteria, same as CA

interim levels

Same as California interim levels constructed on or after 1 Jan 2013

(subject to case-by-case time

extension)#

E. coli, IMO Reg D-2 levels; intestinal

enterococci, IMO Reg D-2 levels

constructed after 1 Jan 2012,

immediate; constructed before 1

Jan 2012, 1 Jan 2014

March 2013 MANAGING BALLAST WATER DISCHARGES 293
FIG. 1. Flow chart describing regulation of ballast water discharges at international and domestic levels. Oval boxes indicate

regulations based primarily on ballast water exchange; shaded square boxes are regulations based primarily on concentration of

organisms.

294 INVITED FEATURE Ecological Applications

Vol. 23, No. 2
water discharge limits will benefit from an improved

understanding of how to assess the risk of establishment

of ANS given the concentrations of living organisms in

ballast water discharges. As a basic principle, the risk of

successful invasions increases with propagule pressure

(Simberloff 2009, NRC 2011, Lee et al. 2013), and ballast

water discharge standards are established to reduce

propagule pressure. However, standards historically

considered or adopted have had a range of more than

three orders of magnitude for organisms of a given size

class (Albert et al. 2010). Additionally, past efforts to

develop standards generally have not been based upon

rigorous scientific analysis of what would be appropriately protective of aquatic ecosystems (Lee et al. 2011).

United States regulation by individual states.—Four

U.S. states (California, Michigan, Minnesota, and

Wisconsin) have independent laws, regulations, or

permits establishing numeric ballast water discharge

standards or treatment requirements. Four other states

without specific ballast water related laws have included

numeric ballast water discharge limits as part of their

Clean Water Act (CWA) section 401 certifications of the

VGP (Illinois, Indiana, Ohio, and New York); a fifth

state, Pennsylvania, included those conditions but

subsequently deleted them in November 2010. See Table

1 for a list of U.S. state standards.

Under CWA section 401, when the U.S. federal

government issues a permit such as the VGP, it must

seek certification from the state in which the discharge

originates (i.e., the location(s) where the ballast water is

discharged) to ensure that the discharge will comply with

the applicable provisions of the CWA, including water

quality standards, and other appropriate requirements of

state law. As a result, the VGP contains a number of

section CWA 401 certifications with ballast water-related

conditions, which vary in their stringency, schedules for

implementation, and types of vessels covered (Table 1).

By way of example, we briefly discuss three states’

concentration-based standards for organisms in ballast

discharge and summarize their publicly stated rationale.

California enacted legislation establishing ballast

water discharge standards for state waters and a

schedule for compliance with those standards based on

recommendations of the California State Lands Commission in order to ‘‘approach a protective zero

discharge standard’’ (CSLC 2010, Dobroski et al.

2011). The interim standard (those in force starting in

2010) for organisms greater than 50 lm is zero

detectable living organisms, and for organisms between

10 and 50 lm is less than 0.01 organisms/mL. Final

standards, currently set to start in 2020, are zero

detectable organisms for all size classes of organisms,

including viruses and bacteria (Table 1). California also

included these standards in its CWA section 401

certification of the VGP by reference.

New York’s mechanism for regulating ballast water

discharges is through its CWA section 401 certification

of the VGP. As part of its certification, the New York

Department of Environmental Conservation (DEC)

requires, for vessels constructed on or after 1 January

2013, the same concentrations as California’s interim

standards for organisms greater than or equal to 50 lm

(zero detectable living organisms) and organisms between 10 and 50 lm (less than 0.01 living organisms/

mL). In its certification, New York stated that the IMO

standards ‘‘are not sufficiently protective’’ and more

stringent concentration-based standards were necessary

to ‘‘prevent further impairment of the state’s water

quality’’ (New York 2008). Due to implementation

difficulties and other factors, New York extended the

compliance date until the end of the VGP’s five-year

term (J. M. Tierney, unpublished letter). As part of the

VGP five-year renewal, the state is currently evaluating

what, if any, conditions to apply to the next issuance of

the VGP; however, as of 31 July 2012, New York has

not proposed conditions similar in stringency to those

contained in their 2008 certification.

In 2008, the Minnesota Pollution Control Agency

(MPCA), under Minnesota state law, issued a State

Disposal System (SDS) permit for ballast water discharges into Minnesota waters. According to MPCA,

the discharge standards contained in the permit ‘‘are

based on the Performance Standards contained in

Section D-2 of the BWM Convention, with the

exception of the standard for Vibrio cholerae. The

general permit does not include a limit on Vibrio

cholerae because analytical methods to enumerate that

organism in ballast water have not been validated’’

(Minnesota Pollution Control Agency 2008).

Domestic regulation outside the United States.—

Several other countries and regional organizations have

established ballast water regulatory programs. We

briefly discuss the approaches of three of those countries

below (Australia, Canada, and New Zealand) as well as

recent activity by the OSPAR and Helsinki (HELCOM)

Commissions with respect to ballast water management.

None of these entities have numeric ballast water

discharge standards currently in effect, and are looking

at the February 2004 IMO BWM Convention to

establish numeric ballast water discharge standards for

vessels on international voyages.

Australia is an active participant in ballast water and

other ANS matters at the IMO and is a signatory to the

BWM Convention (though they have not yet ratified

that Convention) (Hewitt et al. 2009, IMO 2012). Like

the United States, Australia currently regulates ballast

water at the national level, via the Australian Government Department of Agriculture, Fisheries, and Forestry (ADAFF), formerly the Australian Quarantine

and Inspection Service (AQIS) under the Authority of

the Quarantine Act 1908, and at the regional level by

state and territory government agencies (ADAFF 2011).

However, unlike the United States, where both the

federal and state governments can generally regulate

ballast water discharges, ADAFF is currently responsible for regulating ballast water from international

March 2013 MANAGING BALLAST WATER DISCHARGES 295
vessels while the state and territory governments are

responsible for ballast water taken up in Australian

ports and territorial seas (Hewitt et al. 2009). ADAFF

prohibits the discharge of unmanaged ‘‘high risk’’ ballast

water, which it considers ‘‘all salt water from ports and

coastal waters outside Australia’s territorial sea’’ (Dunstan and Bax 2008, ADAFF 2011). These vessels must

currently manage this water through ballast water

exchange, internal tank-to-tank transfers, not discharging, or by seeking case-by-case permission to use a typeapproved ballast water treatment system. As one of the

Australian states/territories active in ballast water

management, Victoria has additional requirements for

the management of Australian-sourced domestic ballast

water, which are enforced under the Environment

Protection Act 1970, and requires that vessels taking

up and discharging ballast water from Australian

domestic sources must maintain a ballast water log,

obtain written permission to discharge ballast water,

and report when that water is discharged (regulations

available online).3 Notably, both the Australian national

and state level regulations do not yet include any

requirements that vessels must meet numeric ballast

water treatment limits.

Voluntary Canadian ballast water exchange requirements for vessels entering the Great Lakes were first

introduced in 1989 (Transport Canada 2007, Bailey et

al. 2011) and were expanded to all Canadian waters in

2000 (Transport Canada 2007). Mandatory ballast

water management and sediment disposal requirements

for all Canadian waters were established in 2006

(Canadian Department of Justice [2006], pursuant to

the Canada Shipping Act). These Canadian regulations,

which received an administrative update in 2011

(Canadian Department of Justice 2011) provide several

management options for vessels to meet their ballast

water management obligations. Vessels subject to the

requirements may conduct ballast water exchange, use

onshore treatment, not discharge their ballast within

Canadian waters, or treat water to the BWM Convention Regulation D-2 standard (see Section 4 of

Ballast Water Control and Management Regulations

[Canadian Department of Justice 2011]). In addition,

vessels bound for the Great Lakes that have only

residual amounts of ballast water (NOBOBs) that was

not exchanged or treated are generally required to

conduct saltwater flushing. There are exceptions to the

requirements for ballast water management, including

vessels that operate exclusively in Canadian waters,

vessels that operate exclusively within the Great Lakes,

small search and rescue vessels, vessels with permanent

ballast, and government vessels. Additionally, in cooperation with the United States, Canada established a binational program under which all vessels entering the St.

Lawrence Seaway from outside Canada’s exclusive

economic zone are inspected before they enter the Great

Lakes (report available online).4 Bailey et al. (2011)

stated that this program appears effective in reducing

invasions and recommended it for other freshwater

ecosystems around the world.

The Canadian regulations have not replaced ballast

water exchange with a concentration-based standard

such as those that will be required by the BWM

Convention Regulation D-2. However, as of March

2012, Canada is in the process of revising its regulations

to implement the BWM Convention (Colin Henein,

personal communication), which Canada acceded to in

2010 (IMO 2012). The Canadian government has

expressed support for the concept of ballast water

exchange plus ballast water treatment to the D-2

standard for vessels entering the Great Lakes (D. Lebel,

unpublished letter). Hence, though not currently implementing or supporting numeric limits more stringent

than the IMO discharge standard, the Canadian government is supporting alternate measures to further reduce

risk of ANS introduction to the Great Lakes.

New Zealand’s ballast water exchange requirements,

established in 1998, were among the first national

requirements mandating that vessels conduct ballast

water exchange. In June 2005, New Zealand published

updated ballast water requirements issued under the

authority of Section 22 of the Biosecurity Act 1993 (New

Zealand Ministry of Agriculture and Forestry 2005).

These requirements mandate that vessels that take on

ballast water outside New Zealand waters, only discharge in New Zealand waters with the approval of an

inspector. An inspector may approve the discharge if the

vessel has conducted ballast water exchange, the ballast

tank contains freshwater, or the vessel uses a shipboard

or onshore ballast water treatment system approved by

the New Zealand Ministry of Agriculture and Forestry.

Most international arriving vessels must currently

conduct ballast water exchange (Murphy et al. 2009).

Additionally, as in the United States, sediment from the

cleaning of ballast tanks may not be discharged into

New Zealand’s waters (New Zealand Ministry of

Agriculture and Forestry 2010). Potentially unique to

New Zealand, vessels having taken on ballast water in

areas deemed particularly high risk are not allowed to

discharge ballast water for any reason. As in the United

States and Australia, the New Zealand requirements

allow for a safety exemption from the ballast water

exchange requirement and authorize substantial financial penalties for noncompliance (New Zealand Ministry

of Agriculture and Forestry 2005). Though New

Zealand has not yet ratified the BWM convention as

of 31 July 2012 (IMO 2012), they have been an active 3 http://www.legislation.vic.gov.au/Domino/Web_Notes/

LDMS/PubStatbook.nsf/93eb987ebadd283dca256e92000e40

69/C4CEE91AA20A2D51CA25717E00185C57/$FILE/06-059sr.

pdf

4 http://www.greatlakes-seaway.com/en/pdf/2011_BW_

Rpt_EN.pdf

296 INVITED FEATURE Ecological Applications

Vol. 23, No. 2
participant at IMO and a strong supporter of the BWM

Convention (Hewitt et al. 2009).

Numerous other countries have national, mandatory,

ballast water exchange requirements including Argentina (Boltovskoy et al. 2011), Brazil (IMO 2005), and

Norway (Norwegian Ministry of the Environment

2009). Additionally, several countries have taken affirmative steps toward implementing programs which will

ultimately allow for effective ballast water treatment,

despite not having formal ballast water treatment

regulatory programs. For example, though not yet a

party to the BWM Convention (IMO 2012), Germany

has invested significant resources into type-approving

ballast water treatment systems by the Federal Maritime

and Hydrographic Agency (BSH).

International cooperation also takes place through

the auspices of Regional treaties, such as The Convention for the Protection of the Marine Environment of

the North-East Atlantic (the OSPAR Convention) and

the Convention on the Protection of the Marine

Environment of the Baltic Sea Area (the Helsinki

Convention). While those Conventions themselves do

not directly address ballast water management, the

parties to these Conventions have jointly agreed to

voluntary application of the ballast water exchange

requirements contained in Regulation D-1 of the IMO

BWM Convention in the North-East Atlantic and Baltic

Sea (IMO 2008). However, as the IMO BWM Convention has not yet entered into force, despite regional

agreement and cooperation, a European-wide approach

to ballast water discharge standards has not yet emerged

(David and Gollasch 2008).

Other than plans to implement the IMO BWM

Convention, we are unaware of independent domestic

legislation that prescribes numeric ballast water treatment limits other than in the United States and

therefore, the patchwork of numeric ballast water

discharge limits currently found in the United States is

not currently found internationally. Though recent

trends have resulted in less variability between U.S.

states and the U.S. federal government’s ballast water

discharge limits, uncertainty about the risk posed by

discharges of ballast water at various numeric discharge

limits leaves open the possibility for continued regional

differentiation in these standards. In addition, while

much of the international community looks toward

entry into force of the IMO BWM Convention

Regulation D-2 discharge standards, as previously

noted, that Convention (e.g., Regulation C-1) preserves

the right of Parties to adopt more stringent measures

when determined necessary to prevent, reduce, or

eliminate the transfer of ANS.

DISCUSSION

There are considerable policy questions as to what

constitutes a ‘‘sufficiently protective’’ ballast water

discharge standard; for example, is the goal to prevent

all future invasions, or to reduce the risk of future

invasions to some level deemed ‘‘acceptable’’ by policy

makers? In addition, some regulatory bodies appear to

have placed greater emphasis on international consensus, practicability, and cost of treatment, while others

have emphasized the need to establish limits they believe

will be least likely to result in invasion. While such

policy issues and choices are beyond the scope of this

paper, we believe that the absence of a rigorous, widely

accepted, risk-based scientific framework complicates

the ability to objectively discuss and agree on such

fundamental issues. In particular, development of such a

framework will enable a better understanding of what

degree of ecological protection is afforded by various

proposed discharge standards.

As a basic principle, the risk of successful invasions

increases with propagule pressure (Simberloff 2009,

NRC 2011, Lee et al. 2013), and at present, there is

general agreement that ballast water discharge standards

comparable to or more stringent than the BWM

Convention’s Regulation D-2 standards will be more

protective than simply employing current BWE measures. However, there does not appear to be consensus

on whether more stringent limits than are in the BWM

Convention are warranted, and if so, what those more

stringent limits should be. Developing ‘‘sufficiently

protective’’ ballast water discharge standards to reduce

or prevent invasions from ballast water becomes even

more complex when one considers that there are other

anthropogenic pathways for ANS, such as hull biofouling, aquaculture releases, the aquarium trade, recreational boating activities, and manmade water diversions

connecting previously distinct hydrologic units etc.

While most countries active in ballast water management are pushing toward implementation of the IMO

standard, in the United States, a number of states and

environmental groups have questioned whether that

standard is adequately protective for all discharges in all

waters (comments available online).5,6,7,8,9

Additionally, both the U.S. EPA and the U.S. Coast

Guard have indicated they would go beyond the IMO

standard if necessary to protect the aquatic environment

(U.S. EPA 2011, 77 Federal Register 17254). Many

countries and international regional regulatory bodies

are looking to implementation of the IMO BWM

Convention’s regulation D-2 standard, and there is

scientific recognition that this standard ‘‘is a good first

step’’ (NRC 2011). However, as Regulation C-1 of the

BWM Convention preserves the right of Parties to adopt

5 http://www.regulations.gov/#!documentDetail;D1⁄4EPAHQ-OW-2011-0150-0413 6 http://www.regulations.gov/#!documentDetail;D1⁄4EPAHQ-OW-2011-0141-0577 7 http://www.regulations.gov/#!documentDetail;D1⁄4EPAHQ-OW-2011-0141-0497 8 http://www.regulations.gov/#!documentDetail;D1⁄4EPAHQ-OW-2011-0141-0446 9 http://www.regulations.gov/#!documentDetail;D1⁄4EPAHQ-OW-2011-0141-0723

March 2013 MANAGING BALLAST WATER DISCHARGES 297
more stringent measures when determined necessary to

prevent, reduce, or eliminate the transfer of ANS, even

in the context of that Convention, development of a

widely accepted robust risk-assessment framework will

remain important to better understand whether the

Regulation D-2 standard provides adequate protection

or more stringent standards are appropriate.

In the absence of widely accepted and robust risk

assessment methodologies, the current regulatory framework has resulted in varying ballast water regulations

and varying numeric concentration-based discharge

limits, particularly in the United States. Industry groups

are concerned as to how to meet the most stringent of

the proposed limits, while other interests are concerned

that current discharge limits may not be adequately

protective. In addition, the varying standards may be

impeding development and installation of treatment

technologies due to uncertainty in the efficacy that

treatment equipment will ultimately have to achieve.

Furthermore, the continued absence of robust, validated

risk assessment methodologies may result in numeric

ballast water treatment limit variability becoming more

of a global issue as Parties to the IMO BWM

Convention could adopt more stringent measures if

they deem it necessary.

Views of what constitutes a ‘‘sufficiently protective’’

standard can vary due to differences in underlying

assumptions, analytical methods, and risk tolerance.

Such differences are based, in part, on not having

sufficient data and validated risk assessment methods

that enable a fuller understanding of the risks associated

with differing low-level concentrations of organisms in

ballast water discharges. Efforts to derive environmentally protective ballast water discharge limits will

benefit from an improved understanding of how to

assess the risk of establishment of ANS given the

concentrations of living organisms in ballast water

discharges. However, this will not resolve all uncertainty, and we acknowledge that application of such a

risk assessment framework may still yield variable

results when applied by a particular risk assessor. In

addition, the acceptance of a given discharge standard

will also vary due to policy choices involving factors

such as economic cost and risk tolerance.

Although variability and uncertainty is inherent in

environmental decision making, we believe use of a

widely accepted risk-assessment framework would help

reduce such variability, and, at a minimum, more readily

increase the transparency and productivity of discussions as to how the risk assessment was performed.

Hence, validated risk assessment methodologies can

reduce uncertainty such that risk management decisions

are more clearly linked to the actual risk posed by

managed ballast water discharges, which in turn can

help inform the policy choice of whether a given

discharge standard is sufficiently protective.

It is our opinion that there are several promising

approaches for estimating risk associated with ballast

water discharges at various discharge limits (Lee et al.

2011, U.S. Coast Guard 2012, Reusser et al. 2013).

While application of risk assessment methodologies,

such as those suggested by Lee at al. (2011), can help

inform regulatory agencies as to whether the IMO limit

is sufficiently protective, the NRC (2011) identified

several long-term data gaps that should be filled to

better calibrate and validate these risk assessment

methodologies. Efforts are currently underway by

several entities, including U.S. federal agencies, to

develop strategies and identifying ongoing and future

research that can be used to fill these data gaps. Where

those gaps are filled, risk assessment methodologies may

provide higher confidence and precision, such that, even

though policy choices may continue to differ, policy

makers will be able to make better informed risk

management decisions.

In conclusion, effective, science-based risk analyses

could result in more confidence that the regulatory limits

provide adequate protection against ballast water

mediated introductions of invasive species. This could,

in turn, help foster more consistent ballast water

regulations among U.S. state, federal, and international

regulators and reduce the potential for varying discharge

standards.

ACKNOWLEDGMENTS

We thank Richard Everett, Melanie Frazier, Shirley Fan,

Henry Lee, Katharine Marko, and Jamie Piziali for their

review, insightful suggestions, and editing on elements in this

paper. We also thank Matt Gregg, Colin Henein, and Paul

Topping for their thoughtful suggestions for the discussion on

their respective country regulations and three anonymous

reviewers for their valuable review and feedback on the

manuscript. The contents of this paper reflect the opinions of

the authors and do not necessarily reflect the views of the U.S.

Environmental Protection Agency.

LITERATURE CITED

Albert, R., R. Everett, J. Lishman, and D. Smith. 2010.

Availability and efficacy of ballast water treatment technology: background and issue paper. White paper. EPA Science

Advisory Board, Washington, D.C., USA.

American Bureau of Shipping. 2010. Ballast Water Treatment

Advisory. 8 June 2010. American Bureau of Shipping,

Houston, Texas, USA.

Australian Department of Agriculture, Fisheries, and Forestry

(ADAFF). 2011. Australian ballast water management requirements: version 5. http://www.daff.gov.au/__data/assets/

pdf_file/0004/713884/Ballast-Water-Mgmt-Requirements.pdf

Bailey, S. A., M. G. Deneau, L. Jean, C. J. Wiley, B. Leung,

and H. J. MacIsaac. 2011. Evaluating efficacy of an

environmental policy to prevent biological invasions. Environmental Science and Technology 45(7):2554–2561.

Bolch, C. J. S., and M. F. D. de Salas. 2007. A review of the

molecular evidence for ballast water introduction of the toxic

dinoflagellates Gymnodinium catenatum and the Alexandrium

‘‘tamarensis complex’’ to Australasia. Harmful Algae 6:465–

485.

Boltovskoy, D., P. Almada, and N. Correa. 2011. Biological

invasions: assessment of threat from ballast-water discharge

in Patagonian (Argentina) ports. Environmental Science and

Policy 14(5):578–583.

Briski, E., S. A. Bailey, M. E. Cristecu, and H. J. MacIsaac.

2010. Efficacy of ‘‘saltwater flushing’’ in protecting the Great

298 INVITED FEATURE Ecological Applications

Vol. 23, No. 2
Lakes from biological invasions by invertebrate eggs in ships’

ballast sediment. Freshwater Biology 55:2414–2424.

Briski, E., S. A. Bailey, and H. J. MacIsaac. 2011. Invertebrates

and their dormant eggs transported in ballast sediments of

ships arriving to the Canadian coasts and the Laurentian

Great Lakes. Limnology and Oceanography 56(5):1929–

1939.

Briski, E., S. Ghabooli, S. A. S.,Bailey, and H. J. MacIsaac.

2012. Invasion risk posed by macroinvertebrates transported

in ships’ ballast tanks. Biological Invasions 14:1843–1850.

California State Lands Commission (CSLC). 2010. 2010

assessment of the efficacy, availability, and environmental

impacts of ballast water treatment systems for use in

California waters. Produced for the California State Legislature, Sacramento, California, USA.

Canadian Department of Justice. 2006. Ballast water control

and management regulations. SOR/2006-129. Canadian

Department of Justice, Ottawa, Ontario, Canada. http://lawslois.justice.gc.ca/eng/regulations/SOR-2006-129/20060608/

P1TT3xt3.html

Canadian Department of Justice. 2011. Ballast water control

and management regulations. SOR/2011-237. Canadian

Department of Justice, Ottawa, Ontario, Canada. http://

laws-lois.justice.gc.ca/eng/regulations/SOR-2011-237/index.

html

Cohen, N. J., et al. 2012. Preventing maritime transfer of

toxigenic vibrio cholerae during an epidemic. Emerging

Infectious Diseases 18(10):1680–1682.

David, M., and S. Gollasch. 2008. EU shipping in the dawn of

managing the ballast water issue. Marine Pollution Bulletin

56:1966–1972.

Dobroski, N., C. Scianni, D. Gehringer, and M. Falkner. 2011.

Assessment of the efficacy, availability and environmental

impacts of ballast water treatment systems for use in

California. California State Lands Commission, Marine

Facilities Division, Sacramento, California, USA.

Drake, J. M., and D. M. Lodge. 2007. Rate of species

introductions in the Great Lakes via ships’ ballast water

and sediments. Canadian Journal of Fisheries and Aquatic

Sciences 64:530–538.

Dunstan, P. K., and N. J. Bax. 2008. Management of an

invasive marine species: defining and testing the effectiveness

of ballast-water management options using management

strategy evaluation. ICES Journal of Marine Science 6:841–

850.

Frazier, M., A. W. Miller, H. Lee II, and D. A. Reusser. 2013.

Counting at low concentrations: the statistical challenges of

verifying ballast water discharge standards. Ecological

Applications 23:339–351.

Gollasch, S., M. David, M. Voigt, E. Dragsund, C. Hewitt, and

Y. Fukuyo. 2007. Critical review of the IMO international

convention on the management of ships’ ballast water and

sediments. Harmful Algae 6:585–600.

Gray, D. K., T. H. Johengen, D. F. Reid, and H. J. MacIsaac.

2007. Efficacy of open-ocean ballast water exchange as a

means of preventing invertebrate invasions between freshwater ports. Limnology and Oceanography 52(6):2386–2397.

Gregg, M., G. Rigby, and G. M. Hallegraeff. 2009. Review of

two decades of progress in the development of management

options for reducing or eradicating phytoplankton, zooplankton and bacteria in ship’s ballast water. Aquatic

Invasions 4:521–565.

Hewitt, C. L., R. A. Everett, and N. Parker. 2009. Examples of

current international, regional and national regulatory

frameworks for preventing and managing marine bioinvasions. Pages 335–352 in G. Rilov and J. A. Crooks, editors.

Biological invasions in marine ecosystems: ecological, management, and geographic perspectives. Ecological Studies.

Volume 204. Springer, New York, New York, USA.

IMO. 1997. Assembly Resolution A.868 (20): Guidelines for the

control and management of ships’ ballast water to minimize

the transfer of harmful aquatic organisms and pathogens.

International Maritime Organization, London, UK.

IMO. 2004. International convention for the control and

management of ship’s ballast water and sediments. IMO

BWM/CONF/36. International Maritime Organization,

London, UK.

IMO. 2005. Communication received from the Administration

of Brazil. IMO circular BWM.2/Circ.1. International Maritime Organization, London, UK. http://www.imo.org/blast/

blastDataHelper.asp?data_id1⁄413081&filename1⁄41.pdf

IMO. 2008. Communication received from the Administration

of the United Kingdom. BWM.2/Circ. 14. International

Maritime Organization, London, UK.

IMO. 2011. International convention for the control and

management of ships’ ballast water and sediments. List of

ballast water management systems that make use of Active

Substances which received Basic and Final Approvals.

BWM.2/Circ.34. International Maritime Organization, London, UK.

IMO. 2012. Status of multilateral conventions and instruments

in respect of which the International Maritime Organization

or its Secretary-General performs depositary or other

functions as of July 31, 2012. International Maritime

Organization, London, UK.

Kipp, R., S. A. Bailey, H. J. MacIsaac, and A. Ricciardi. 2010.

Transoceanic ships as vectors for nonindigenous freshwater

bryozoans. Diversity and Distributions 16(1):77–83.

Lee, H., II, D. A. Reusser, and M. Frazier. 2013. Approaches to

setting organism-based ballast water discharge standards.

Ecological Applications 23:301–310.

Lee, H., II, D. A. Reusser, M. Frazier, and G. Ruiz. 2011.

Density matters: review of approaches to setting organismbased ballast water discharge standards. EPA/600/R-10/031.

U.S. EPA, Office of Research and Development, National

Health and Environmental Effects Research Laboratory,

Western Ecology Division, Corvallis, Oregon, USA.

Lloyds Register. 2011. Ballast water treatment technology:

current status, London. June 2011. Lloyds Register, London,

UK.

Lovell, S. J., and L. A. Drake. 2009. Tiny stowaways: analyzing

the economic benefits of a U.S. Environmental Protection

Agency permit regulating ballast water discharges. Environmental Management 43:546–555.

McCollin, T., A. Shanks, and J. Dunn. 2007. The efficiency of

regional ballast water exchange: Changes in phytoplankton

abundance and diversity. Harmful Algae 6:531–546.

MEPC. 1991. MEPC Resolution 50 (31): International guidelines for preventing the introduction of unwanted aquatic

organisms and pathogens from ships’ ballast water and

sediment discharges. International Maritime Organization,

Marine Environment Protection Committee, London, UK.

MEPC. 2008a. Resolution MEPC.174(58). Guidelines for

approval of ballast water management systems (G8). International Maritime Organization, Marine Environment Protection Committee, London, UK.

MEPC. 2008b. Resolution MEPC.169(57). Procedure for

approval of ballast water management systems that make

use of active substances (G9). International Maritime

Organization, Marine Environment Protection Committee,

London, UK.

Miller, W. A., M. S. Minton, and G. M. Ruiz. 2011.

Geographic limitations and regional differences in ships’

ballast water management to reduce marine invasions in the

contiguous United States. BioScience 61(11):880–887.

Minnesota Pollution Control Agency. 2008. Ballast water

discharge general permit and fact sheet for State Disposal

System (SDS) Permit MNG300000. June 30, 2008. Minnesota Pollution Control Agency, Minneapolis, Minnesota,

USA.

Murphy, K., M. Doblin, J. Boehme, and G. Ruiz. 2009. Spatial

and temporal variation in CDOM and trace elements in

March 2013 MANAGING BALLAST WATER DISCHARGES 299
eastern Australian ports: implications for verifying ballast

water exchange by ships. MAF Biosecurity New Zealand

Technical Paper No: 2009/45. New Zealand Ministry of

Agriculture and Forestry, Wellington, New Zealand.

National Academy of Sciences National Research Council.

2011. Assessing the relationship between propagule pressure

and invasion risk in ballast water. NRC, Washington, D.C.,

USA.

New York Department of Environmental Conservation. 2008.

Clean Water Act Section 401 certification for commercial

vessel and large recreational vessel general permit. NYDEC,

Albany, New York, USA.

New Zealand Ministry of Agriculture and Forestry. 2005.

Import health standard ships’ ballast water from all

countries. New Zealand Ministry of Agriculture and Forestry, Wellington, New Zealand.

New Zealand Ministry of Agriculture and Forestry. 2010.

Guide to New Zealand ballast water controls. New Zealand

Ministry of Agriculture and Forestry, Wellington, New

Zealand.

Norwegian Ministry of the Environment. 2009. Regulation of 7

July 2009 No. 992 concerning the prevention of transfer of

alien organisms via ballast water and sediments from ships

(the Ballast Water Regulation). Norwegian Ministry of the

Environment, Oslo, Norway.

Reusser, D. A., H. Lee II, M. Frazier, G. M. Ruiz, P. Fofonoff,

M. S. Minton, and W. Miller. 2013. Per capita invasion

probabilities: an empirical model to predict rates of invasion

via ballast water. Ecological Applications 23:321–330.

Ruiz, G. M., J. T. Carlton, E. D. Grosholz, and A. H. Hines.

1997. Global invasions of marine and estuarine habitats by

non-indigenous species: mechanisms, extent, and consequences. American Zoologist 37(6):621–632.

Ruiz, G. M., P. W. Fofonoff, J. T. Carlton, M. J. Wonham, and

A. H. Hines. 2000a. Invasion of coastal marine communities

in North America: apparent patterns, processes, and biases.

Annual Review of Ecology and Systematics 31:481–531.

Ruiz, G. M., T. K. Rawlings, F. C. Dobbs, L. A. Drake, T.

Mullady, A. Huq, and R. R. Colwell. 2000b. Global spread

of microorganisms by ships. Nature 408:49–50.

Ruiz, G. M., and D. F. Reid. 2007. Current state of

understanding about the effectiveness of ballast water

exchange (BWE) in reducing aquatic nonindigenous species

(ANS) introductions to the Great Lakes Basin and Chesapeake Bay, USA: synthesis and analysis of existing

information. U.S. Department of Commerce, National

Oceanic and Atmospheric Administration, Ann Arbor,

Michigan, USA.

Simberloff, D. 2009. The role of propagule pressure in

biological invasions. Annual Review of Ecology, Evolution,

and Systematics 40:81–102.

Transport Canada. 2007. A guide to Canada’s ballast water

control and management regulations. TP 13617 E. Transport

Canada, Ottawa, Ontario, Canada. http://www.tc.gc.ca/eng/

marinesafety/tp-tp13617-menu-2138.htm

U.S. Coast Guard. 2012. USCG ballast water discharge standard final programmatic environmental impact statement.

http://www.regulations.gov/#!documentDetail;D1⁄4USCG-2001-

10486-0468

U.S. EPA. 2011. Proposed issuance of National Pollutant

Discharge Elimination System (NPDES) Vessel General

Permit (VGP) for discharges incidental to the normal

operation of vessels: draft fact sheet. U.S. EPA, Washington,

D.C., USA.

U.S. EPA SAB. 2011. Efficacy of ballast water treatment systems:

a report by the EPA Science Advisory Board. EPA-SAB-11-

009. U.S. EPA, Washington, D.C., USA. http://yosemite.epa.

gov/sab/sabproduct.nsf/0/6FFF1BFB6F4E09FD852578CB

006E0149/$File/EPA-SAB-11-009-unsigned.pdf

300 INVITED FEATURE Ecological Applications

Vol. 23, No. 2