Ecological Applications , 23(2), 2013, pp. 289–3002013 by the Ecological Society of America



# Ballast water regulations and the move toward concentration-based numeric discharge limits

RYAN J. A LBERT , 1 J OHN M. L ISHMAN
, AND J UHI R. S AXENA

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 bythe 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)

.

I NTRODUCTION

Ballast water discharges have been a major source ofnonindigenous species introductions to marine, estuarine, and freshwater ecosystems (Ruiz et al. 1997,

2000 a). 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.

2000 b , 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 asballast 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 DISCHARGESto 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 ofliving 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 policymakers 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 watertreatment technologies, which has been addressed elsewhere (Dobroski et al. 2011, Lloyds Register 2011, U.S. EPA SAB 2011).

R EGULATORY B ACKGROUND
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 areprimarily 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 INVITED FEATURE 290 Ecological Applications Vol. 23, No. 2signatory, 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 dateand 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 ofnumber 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 (BWMConvention 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 Guid elines’’) (MEPC 2008 a ). 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 2008 b ). Although the BWM Convention is not in force as of 31 July 2012, a number of systems have been reviewed and appro ved 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 addressedby 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 SpeciesAct (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 wa ter 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 291 MANAGING BALLAST WATER DISCHARGESDischarge 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 Envi ronmental 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 T ABLE 1. Selected ballast water discharge standards for organisms (current as of 31 July 2012).

Standard Size 50 lm Size , 50 lm but 10 lm

IMO BWM Convention (Reg. D-2) , 10 ‘‘viable’’ organisms per m 3 , 10 ‘‘viable’’ organisms per mL

U.S. negotiating position (BWM/

CONF/13 and 14) , 0.01 ‘‘living’’ organisms per m 3 , 0.01 ‘‘living’’ organisms per mL

USCG final rule , 10 ‘‘living’’ organisms per m 3 , 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 m 3 (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 m 3 , 1 ‘‘living’’ organism per 10 mL

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

Wisconsin (State Permit)|| , 10 ‘‘viable’’ organisms per m 3 (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 INVITED FEATURE 292 Ecological Applications Vol. 23, No. 2regulates discharges incidental to the normal operation of vessels and includes provisions requiring BWE. The2008 VGP includes, among other things, technologybased effluent limits (based on what technologies can achieve) that are similar to the mandatory ballast watermanagement 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 30November 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 T ABLE 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, , 10 3 bacteria/100 mL , 10 4 viruses/100 mL 1 Jan 2010

 1 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 293 MANAGING BALLAST WATER DISCHARGESF IG . 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. INVITED FEATURE

294 Ecological Applications Vol. 23, No. 2water 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 uponrigorous 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 standar ds 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 StateDisposal 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 ballastwater 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 regulateballast water discharges, ADAFF is currently responsible for regulating ballast water from international March 2013 295 MANAGING BALLAST WATER DISCHARGESvessels 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 andcoastal waters outside Australia’s territorial sea’’ (Dunstan and Bax 2008, ADAFF 2011). These vessels must currently manage this water through ballast waterexchange, 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/territori es 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 withinCanadian 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 permanentballast, 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 stringentthan 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 onballast 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 arrivin g 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 waterexchange 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/Domin o/Web_Notes/ LDMS/PubStatbook.nsf/93eb987eb add283dca256e92000e40 69/C4CEE91AA20A2D51CA25717E00185C57/$FILE/06-059sr. pdf 4 http://www.greatlakes-sea way.com/en/pdf/2011_BW_ Rpt_EN.pdf INVITED FEATURE 296 Ecological Applications Vol. 23, No. 2participant 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 Environment2009). 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 throughthe 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 BalticSea (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 domesticlegislation 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.

D ISCUSSION
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 tohave 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 moreprotective 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 otheranthropogenic 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 297 MANAGING BALLAST WATER DISCHARGESmore 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 riskassessment 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 inballast 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 waterdischarges. 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 readilyincrease 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.

A CKNOWLEDGMENTS

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.

L ITERATURE C ITED
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 anenvironmental 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 INVITED FEATURE 298 Ecological Applications Vol. 23, No. 2Lakes 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 inCalifornia waters. Produced for the California State Legislature, Sacramento, California, USA. Canadian Department of Justice. 2006. Ballast water control

and management regulations. SOR/2006-129. CanadianDepartment of Justice, Ottawa, Ontario, Canada. http://lawslois.justice.gc.ca/eng/regu lations/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 ameans 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 managementoptions 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 regulatoryframeworks 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_id 1⁄4 13081&filename 1⁄4 1.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 ProtectionAgency 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. 2008 a . Resolution MEPC.174(58). Guidelines for

approval of ballast water management systems (G8). International Maritime Organization, Marine Environment Protection Committee, London, UK.
MEPC. 2008 b . 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 DisposalSystem (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 299 MANAGING BALLAST WATER DISCHARGESeastern 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 sh ips’ ballast water from allcountries. 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 bynon-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. 2000 a . 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. 2000 b . 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.htmU.S. Coast Guard. 2012. USCG ballast water discharge standard final programmatic environmental impact statement. http://www.regulations .gov/#!documentDetail;D 1⁄4

USCG-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 INVITED FEATURE 300 Ecological Applications Vol. 23, No. 2