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1Â SettingÂ theÂ InvasiveÂ SpeciesÂ ManagementÂ Stage INTRODUCTION Human activities have moved hundreds, perhaps thousands, of species around the world's oceans to regions they would never have reached by ocean currents or other natural vectors. Human-mediated mechanisms that have his- torically bridged the natural barriers of ocean basins and continents include the global transportation of a diverse range of organisms attached to shipsâ hulls, burrowing into wooden ships, and living on (and sometimes in) commercial oysters (Ruiz et al., 2000a; Carlton, 2007, 2011). While these mechanisms are still in play today, it is widely recognized that the uptake and release of ballast water and associated sediments by ships is now one of the predominant means by which new nonindigenous species are introduced around the world (Carlton, 1985; Carlton and Geller, 1993; Gollasch et al., 2002; Kasyan, 2010). Many of these invasions have caused extensive environmental, economic, and human health impacts (Carlton, 2001). The prospects for future invasions, and especial- ly associated large impacts, have precipitated world-wide efforts to reduce, if not eliminate, the transport and release of living organisms in ballast water. The desire to manage ballast is not new. In the 1890s workers in New Zealand considered at-sea disposal, chemical treatment, and quarantined on- shore disposal for solid ballast to control plant invasions (Kirk, 1893). In 1918, the International Joint Commission on the Pollution of Boundary Waters took up the matter of the discharge of contaminated ballast water near municipal water intakes in the Great Lakes, again considering chemical treatment (Ferguson, 1932). While concerns about ballast discharge continued to be voiced in subse- quent decades, the invasion in the 1980s of Japanese dinoflagellates (causing harmful algal blooms) in Australia (Hallegraeff, 1998) and of zebra and quagga mussels (leading to a plethora of economic and environmental issues) in the United States and Canada (DâItri, 1997), motivated the United Nationsâ Interna- tional Maritime Organization (IMO) to take up the introduction of nonindigen- ous species due to the release of shipsâ ballast as a serious marine environmental issue. Concomitantly, a diverse range of governmental organizations and pri- vate interests throughout the world have been advancing policy (regulations) and Â 11Â
12Â Â PropaguleÂ PressureÂ andÂ InvasionÂ RiskÂ inÂ BallastÂ WaterÂ Â approaches (treatment methods) to reduce ballast-mediated invasions (see Chap- ter 2). Approaches to ballast water treatment have evolved over the past 20 years. Initial emphasis has been on ballast water exchange (BWE) to reduce the densi- ties of coastal organisms transferred among global regions (see below). Recent regulations have focused on limiting the density of organisms that are permitted in the discharge of shipsâ ballast water (IMO, 2004; see also Chapter 2). This post-treatment load is referred to as a âdischarge standard.â For air and water quality, these discharge standards were constructed to reduce the potential harm of dissolved or particulate matter (as measured in ppt, ppm, or ppb) to human health. For ballast water, discharge standards reflect the potential (or probabili- ty) that living nonindigenous organisms, when released by ships, will become successfully established in geographic regions where they do not occur and to cause subsequent harm to the environment or human health. The magnitude, complexity, and truly global scale of shipping present some challenges in advancing ballast water treatment. Maritime commerce is esti- mated to carry 90 percent of world trade, traversing the globe and encompassing a wide range of environmental conditions and unique operational constraints (Figure 1-1; Kaluza et al., 2010). Thus, effective treatment options must consid- er the appropriate scale and diverse operating conditions of the shipping indus- try. Â Â Â Â Â Â Â Â Â Â Â Â Â Â Â Â Â FIGUREÂ 1â1Â Â RoutesÂ andÂ portsÂ ofÂ theÂ globalÂ cargoÂ shipÂ network.Â Â ShownÂ areÂ theÂ trajectoâ riesÂ ofÂ allÂ cargoÂ vesselsÂ largerÂ thanÂ 10,000Â grossÂ tonnageÂ duringÂ 2007.Â Â TheÂ colorÂ scaleÂ indicatesÂ theÂ numberÂ ofÂ journeysÂ alongÂ eachÂ route.Â Â SOURCE:Â Â Reprinted,Â withÂ permisâ sion,Â fromÂ KaluzaÂ etÂ al.Â (2010).Â Â Â©Â 2010Â byÂ RoyalÂ SocietyÂ Publishing.Â Â Â
SettingÂ theÂ InvasiveÂ SpeciesÂ ManagementÂ StageÂ 13Â Â THE NUMBER OF VESSELS AND THE VOLUME OF BALLAST WATER IN PLAY In the United States commercial ships arrive in hundreds of different ports. For commercial ships greater than 300 metric tons, there are over 90,000 arrival events per year to locations in U.S. coastal waters including the Great Lakes (Miller et al., 2010)2. Approximately half (48,000) of these are âforeignâ or âoverseasâ arrivals from a last port of call outside the U.S. and Canada. The residual (42,000) are âdomesticâ or âcoastwiseâ arrivals, which arrive directly from another port within North America. These data are for a two-year period (2006-2007) and highlight the general magnitude of vessel traffic, which exhi- bits some variation among years. For this same period, these vessels reported an average annual discharge of 196 million metric tons of ballast water in U.S. coastal waters, based on reports to the National Ballast Water Information Clearinghouse (NBIC; Miller et al., 2010). Ballast water that originated from outside of North America (i.e., that was taken on from a foreign source port) accounted for 28.5 percent of the total discharge volume, and the remainder came from other ports or locations within the U.S. and Canada. These values represent minimum estimates of ballast wa- ter discharge, since data were not available for all of the vessel arrivals to U.S. ports.3 The number of arrivals and ballast water discharge volume are not evenly distributed among recipient port systems; likewise, the relative contribution of the geographic sources to the number of arrivals and discharge volume is varia- ble (Carlton et al., 1995). The variation in relative importance of different reci- pient ports is illustrated in Figures 1-2 and 1-3, showing the number of arrivals and volume of ballast discharged across the U.S. that originated from foreign- only sources for 2006-2007, respectively. A similarly high level of spatial varia- tion also exists for âdomestic-sourceâ arrivals and ballast discharge in the U.S. (Miller et al., 2010). While these figures quickly convey the scope of commercial shipping for overseas arrivals, several other key points are highlighted. First, there is tre- mendous variation among U.S. ports in vessel arrivals and ballast volume. Second, there is a lack of concordance between arrivals and ballast volume for these ports (Figures 1-2 and 1-3). For example, there n are a relatively large number of arrivals in Florida, but this did not translate into a large ballast dis- charge volume. This reflects the large number of passenger vessels (cruise ships) and container vessels arriving to Florida, and these vessel types routinely 2 Â ThisÂ estimateÂ excludesÂ inlandÂ trafficÂ (e.g.,Â MississippiÂ River),Â andÂ someÂ typesÂ ofÂ vesselsÂ areÂ underâ representedÂ (seeÂ MillerÂ etÂ al.,Â 2007,Â 2010).Â 3 Â AnÂ estimatedÂ 85%Â ofÂ coastwiseÂ arrivalsÂ andÂ 86%Â ofÂ foreignÂ arrivalsÂ submittedÂ ballastÂ waterÂ reâ ports.Â Â AllÂ vesselsÂ areÂ requiredÂ toÂ submitÂ ballastÂ waterÂ reportsÂ underÂ U.S.Â CoastÂ GuardÂ regulations,Â andÂ thereÂ areÂ additionalÂ vesselsÂ (militaryÂ andÂ certainÂ commercialÂ ships,Â suchÂ asÂ crudeÂ oilÂ tankersÂ engagedÂ inÂ coastwiseÂ trade)Â thatÂ areÂ notÂ requiredÂ toÂ provideÂ thisÂ information.Â
14Â Â PropaguleÂ PressureÂ andÂ InvasionÂ RiskÂ inÂ BallastÂ WaterÂ Â FIGUREÂ 1â2Â Â NumberÂ ofÂ vesselÂ arrivalsÂ toÂ U.Â S.Â portsÂ inÂ 2006â2007Â thatÂ originatedÂ fromÂ overseasÂ locationsÂ (portsÂ ofÂ originÂ outsideÂ theÂ U.S.Â andÂ Canada).Â Â SOURCE:Â MillerÂ etÂ al.Â (2010).Â Â Â Â FIGUREÂ 1â3Â Â AmountÂ ofÂ ballastÂ waterÂ dischargedÂ inÂ U.Â S.Â portsÂ inÂ metricÂ tonsÂ (mt)Â fromÂ overseasÂ sourcesÂ (outsideÂ ofÂ U.S.Â andÂ Canada),Â regardlessÂ ofÂ lastÂ portÂ ofÂ callÂ orÂ route,Â Â inÂ 2006â2007.Â Â SOURCE:Â MillerÂ etÂ al.Â (2010).Â
SettingÂ theÂ InvasiveÂ SpeciesÂ ManagementÂ StageÂ 15Â Â discharge very little ballast water. Conversely, the Pacific Northwest and Che- sapeake Bay have relatively few arrivals but a large ballast discharge volume, resulting from a large proportion of bulk carriers, which carry and discharge more ballast water than many other vessel types (NBIC; Carlton et al., 1995). One critical feature that results from these data is that the number of vessel arrivals is not a good predictor or proxy for the volume of ballast water dis- charged in a port. This is illustrated in Figure 1-4, which shows the total num- ber of arrivals and total ballast water discharged (cumulative across these ves- sels) for U.S. ports. The weak relationship between these variables has signifi- cant consequences for the use of vessel arrivals as an indicator of propagule supply (organisms discharged) via ballast water, as will be discussed later. Another important dimension of commercial shipping concerns the geo- graphic source of arrivals and the history of ballast water aboard. Figure 1-5 shows the last port of call for foreign arrivals to the U.S. from 2006 to 2007, indicating the relative contribution of different source ports to the arrivals shown in Figure 1-2. This serves to quickly and simply convey the global nature of shipping, which creates connectivity between source and recipient ports, for the transfer of organisms by vessels (associated with ballast water, underwater sur- faces, and cargo). Similar projections are available to show the volume of bal- last water by source region that is delivered to the U.S. (Miller et al., 2010). The relative contribution of source regions for total ballast to the country differs from that for vessel arrivals, because (1) there are strong differences among ships and routes in the amount of ballast water carried and (2) vessels can simul- taneously carry ballast water sourced from multiple ports. Thus, as for recipient ports (Figures 1-2 and 1-3), the number of vessel arrivals may be a poor proxy for relative ballast volume from source regions. THE DIVERSITY OF ORGANISMS IN BALLAST WATER ENTERING U. S. COASTAL WATERS Ballast water is typically drawn into tanks from surrounding port water without treatment and thus routinely contains diverse assemblages, from viruses and bacteria to macroinvertebrates (e.g., Carlton, 1985; Carlton and Geller, 1993; Drake et al., 2001). In some cases, organisms as large as medium-sized fish are also drawn into tanks, depending on the size and state of screens used in the sea chest cover or the size of the openings of the gravitation ports (Wonham et al., 2000). Table 1-1 provides a brief summary of the organisms collected from unexc- hanged ballast water and sediments arriving in North American coastal waters, which span orders of magnitude in size. The animals collected from ballast wa- ter range from fishes (30 cm) down to diapausing eggs (~100 Âµm); protists, bac- teria, and viruses are even smaller in size and more numerous in ballast water.
16Â Â PropaguleÂ PressureÂ andÂ InvasionÂ RiskÂ inÂ BallastÂ WaterÂ Â 8 2 r = 0.558 n = 231 7 log10 (Discharge + 1 mt ) 3 6 5 4 3 2 1 0 0 1 2 3 4 log10 (No. reported arrivals) FIGUREÂ 1â4Â Â RelationshipÂ betweenÂ theÂ cumulativeÂ numberÂ ofÂ overseasÂ vesselÂ arrivalsÂ andÂ totalÂ volumeÂ ofÂ ballastÂ waterÂ dischargedÂ forÂ portsÂ inÂ theÂ U.S.Â forÂ 2006â2007.Â Â mtÂ =Â metricÂ ton.Â Â SOURCE:Â NationalÂ BallastÂ InformationÂ Clearinghouse.Â Â Â FIGUREÂ 1â5Â Â LastÂ portÂ ofÂ callÂ (LPOC)Â forÂ vesselÂ arrivalsÂ toÂ U.S.Â portsÂ inÂ 2006â2007Â thatÂ originatedÂ fromÂ overseasÂ locations.Â Â BallastÂ waterÂ aboardÂ shipsÂ isÂ notÂ limitedÂ toÂ theÂ LPOCÂ asÂ itsÂ origin.Â Â SOURCE:Â MillerÂ etÂ al.Â (2010).Â
SettingÂ theÂ InvasiveÂ SpeciesÂ ManagementÂ StageÂ 17Â Â Although this is not meant to represent an exhaustive list, Table 1-1 serves to underscore the taxonomic range associated with shipsâ ballast tanks that is transported around the globe. Over 15 animal phyla are included (with especial- ly common taxa being mollusks, crustaceans, worms, hydromedusae and flat- worms) in addition to algae, seagrasses, viruses, bacteria, and other microorgan- isms (such as diatoms, dinoflagellates, and other protists; see Table 1-1 for ref- erences). Many of the animals in ballast water are in planktonic stages (from larvae to adult), while those in ballast sediments may be adults as well as their diapause (resting) forms. There are additional analyses of ballast water in other parts of the world that demonstrate the same general picture and add species-level information to stu- dies in North America, but they do not add additional phyla [e.g., Williams et al., 1988 (Australia); Chu et al., 1997 (Hong Kong); Radziejewska et al., 2006 (Russia; sediments); David et al., 2007 (Mediterranean); and Zvyagintsev et al., 2009 (Russia)]. Overall, the size range of ballast-entrained organismsâranging from 20 nanometers to 30 cmâpresents fundamental technical and management challenges in designing control strategies. Thousands of species may be transported across and between oceans in bal- last water on a daily basis (Carlton, 1999), and the cumulative number of species over years to decades is undoubtedly enormous. Most of our understanding comes from studies which have sampled ballast tanks of ships arriving to a dis- crete location (port) over a period of one to several years, providing only a snap- shot of diversity (for a small fraction of discharged ballast water). For example, over 400 species were found in about 150 Japanese wood chip cargo vessels arriving in the Port of Coos Bay, Oregon (Carlton and Geller, 1993). McCarthy and Crowder (2000) reported 342 phytoplankton taxa from only nine ships arriv- ing from a variety of overseas and domestic ports in the Port of Morehead City, North Carolina; one vessel from Europe had over 130 species of diatoms alone. More than 221 species were found in 60 vessels sampled in the Chesapeake Bay (Smith et al., 1999), and 147 species were gathered from 38 shipsâ samples in the Great Lakes (Duggan et al., 2005). The community composition (species diversity) associated with unexchanged or untreated ballast water will vary tre- mendously as a function of source, season, and voyage characteristics (e.g., LaVoie et al., 1999; Wonham et al., 2001; Verling et al., 2005). This makes it especially challenging to predict with any confidence the ballast assemblage present in any one ship. In general, most organisms available in the water col- umn and bottom sediments of bays and coastal waters, as well as open-ocean waters, are entrained at some frequency in ballast tanks, unless ships never en- counter them or the organisms exceed some size threshold (e.g., marine mam- mals). In contrast to what is known about the diversity of metazoans and protists transported by shipsâ ballast water, very little is known about the corresponding diversity of bacteria and viruses in ballast water. Instead, studies have empha- sized their enumeration (e.g., Ruiz et al., 2000; Drake et al., 2001, 2002; Sun et
18Â Â PropaguleÂ PressureÂ andÂ InvasionÂ RiskÂ inÂ BallastÂ WaterÂ Â Â TABLEÂ 1â1Â Â DiversityÂ ofÂ OrganismsÂ CollectedÂ inÂ UnmanagedÂ BallastÂ WaterÂ andÂ SedimentÂ inÂ VesselsÂ ArrivingÂ inÂ NorthÂ AmericanÂ CoastalÂ andÂ InlandÂ Waters.Â Â (TheÂ listÂ ofÂ microâ organismsÂ isÂ notÂ comprehensive.)Â GroupÂ CommonÂ name CoastalÂ InlandÂ AnimalsÂ + + CnidariaÂ jellyfish,Â anemones,Â hydroids + CtenophoraÂ combÂ jelliesÂ (seaÂ gooseberries) + + ArthropodaÂ barnaclesÂ + + Â copepodsÂ + + Â decapodsÂ (shrimps,Â crabs,Â andÂ others) + + Â otherÂ crustaceans,Â includingÂ euphausids,Â stomatopods,Â cumaceans,Â mysids,Â isopods,Â amphipods,Â ostracods,Â cladoceransÂ + Â insectsÂ + + Â mitesÂ + TardigradaÂ waterÂ bears + + NematodaÂ threadÂ worms + ChaetognathaÂ arrowÂ worms + + MolluscaÂ bivalvesÂ (clams,Â mussels,Â oysters) + + Â gastropodsÂ (snails) + Â chitonsÂ + + AnnelidaÂ segmentedÂ worms + NemerteaÂ ribbonÂ worms + PlatyhelminthesÂ flatwormsÂ + PhoronidaÂ horseshoeÂ worms + + BryozoaÂ bryozoansÂ (mossÂ animals) + + RotiferaÂ rotifersÂ + GastrotrichaÂ gastrotrichs + EchinodermataÂ seaÂ starsÂ + Â brittleÂ stars + Â seaÂ urchins + Â seaÂ cucumbers + Â crinoidsÂ + HemichordataÂ acornÂ worms + UrochordataÂ ascidians,Â larvaceans + + PiscesÂ fishesÂ PlantsÂ + AngiospermsÂ seaÂ grasses + RedÂ andÂ greenÂ seaweedÂ algaeÂ tableÂ continuesÂ Â Â
SettingÂ theÂ InvasiveÂ SpeciesÂ ManagementÂ StageÂ 19Â Â TABLEÂ 1â1Â Â ContinuedÂ GroupÂ CommonÂ name CoastalÂ InlandÂ MicroorganismsÂ + + VirusesÂ Â virusesÂ + + CyanobacteriaÂ blueÂ greenÂ algae + + OtherÂ bacteriaÂ Â Â + + BacillariophyceaeÂ diatomsÂ + + DinoflagellataÂ Â dinoflagellates + CiliophoraÂ ciliatedÂ protists + + ForaminiferaÂ ForamsÂ + + OtherÂ "protists"Â Â SourcesÂ forÂ coastalÂ taxa:Â SmithÂ etÂ al.Â (1999);Â McCarthyÂ andÂ CrowderÂ (2000);Â RuizÂ etÂ al.Â (2000b;Â ChesapeakeÂ Bay);Â CordellÂ etÂ al.Â (2008;Â PugetÂ Sound);Â LevingsÂ etÂ al.Â (2004;Â Vancouver);Â CarltonÂ andÂ GellerÂ (1993;Â CoosÂ Bay).Â Â InlandÂ taxa:Â LockeÂ etÂ al.Â (1993;Â GreatÂ Lakes);Â DugganÂ etÂ al.Â (2005;Â GreatÂ Lakes).Â Â GastrotrichÂ dataÂ fromÂ CarltonÂ (1985).Â Â SourcesÂ forÂ microbialÂ taxa:Â DrakeÂ etÂ al.Â (2001,Â 2005);Â BurkholderÂ etÂ al.Â (2007);Â KleinÂ etÂ al.Â (2010);Â ReidÂ etÂ al.Â (2007).Â Â al., 2010), sometimes with a taxonomic focus on selected groups (e.g., Ruiz et al., 2000; Drake et al., 2005; Burkholder et al., 2007; Doblin et al. 2007). To the Committeeâs knowledge, no one has undertaken a metagenomics study (cf. AgoguÃ© et al., 2011) of bacteria or viruses in a ballast water context. ORGANISM CONCENTRATION IN BALLAST WATER As with community composition, the concentration of organisms present within a shipâs ballast water exhibits temporal and spatial variation. This is dri- ven in part by differences in the organism abundances among sources and sea- sons, but there can also be significant differences in the ballast assemblages of two nearly identical vessels, when sailing from the same port and time period, reflecting the patchy distribution of plankton during ballast operations. Fur- thermore, even if vessels begin with similar communities, these may diverge through time, as a result of particular voyage conditions and duration or charac- teristics of the ships themselves (e.g., antifouling coatings). Finally, the nature of any ballast water management practices will influence the concentration of organisms in discharged ballast water. Past studies provide some estimates of abundances for various types of or- ganisms in ballast tanks. Table 1-2 indicates concentrations of particular organ- ism types found in the ballast water of vessels that were sampled upon arrival to various ports (in the regions indicated). All of these studies were done before ballast water exchange was implemented, providing insight into concentrations
20Â Â PropaguleÂ PressureÂ andÂ InvasionÂ RiskÂ inÂ BallastÂ WaterÂ Â TABLEÂ 1â2Â Â ConcentrationÂ ofÂ VariousÂ OrganismÂ TypesÂ ReportedÂ inÂ BallastÂ WaterÂ SampledÂ UponÂ ArrivalÂ ofÂ ShipsÂ toÂ ParticularÂ RegionsÂ Â Â Â Â ConcentrationsÂ inÂ unexchangedÂ ballastÂ waterÂ Â Â Â Â Â Â Â Â Â Â Â Â Â Â Â meanÂ Â Â Â Â Â Â Â Â Â Â Â Â SEÂ nÂ Â Â ZooplanktonÂ (organisms/m3)Â Â Â Â Â Â 3 10Â ÃÂ 101Â 113Â Â Â ChesapeakeÂ BayÂ (overseas)Â 1.94Â ÃÂ 10 Â Â 4 3 Â ChesapeakeÂ BayÂ (domestic)Â 1.75Â ÃÂ 10 Â 1.5Â ÃÂ 10 Â 37Â Â Â 4 3 Â PrinceÂ WilliamÂ Sound,Â AlaskaÂ 1.26Â ÃÂ 10 Â 5.53Â ÃÂ 10 Â 169Â Â Â PhytoplanktonÂ (cells/liter)Â Â Â Â Â Â 5 1.84Â ÃÂ 105Â 273Â Â Â EuropeÂ 2.99Â ÃÂ 10 Â Â BacteriaÂ (cells/liter)Â Â Â Â Â Â 8 8 Â ChesapeakeÂ BayÂ 8.3Â ÃÂ 10 Â 1.7Â ÃÂ 10 Â 9Â Â Â 8 8 Â ChesapeakeÂ BayÂ 8.03Â ÃÂ Â 10 Â 1.88Â ÃÂ 10 Â (sd)Â 53Â Â Â VirusâlikeÂ ParticlesÂ (vlp/liter)Â Â Â Â Â Â 9 2.3Â ÃÂ 109Â Â ChesapeakeÂ BayÂ 7.4Â ÃÂ 10 Â 7Â Â Â 10 10 Â ChesapeakeÂ BayÂ 1.39Â ÃÂ 10 Â 1.57Â ÃÂ 10 Â (sd)Â 31*Â Â Â SOURCES:Â DataÂ forÂ ChesapeakeÂ BayÂ areÂ fromÂ MintonÂ etÂ al.Â (2005;Â zooplankton),Â RuizÂ etÂ al.Â (2000a),Â andÂ DrakeÂ etÂ al.Â (2007;Â bacteriaÂ andÂ virusâlikeÂ particles);Â dataÂ forÂ AlaskaÂ areÂ fromÂ HinesÂ etÂ al.Â (2000;Â zooplankton);Â dataÂ forÂ phytoplanktonÂ areÂ fromÂ InternationalÂ MaritimeÂ OrganizationÂ (2004).Â Â InÂ general,Â zooplanktonÂ refersÂ toÂ organismsÂ collectedÂ onÂ netsÂ >50Â ïmÂ inÂ meshÂ size,Â andÂ phytoplankâ tonÂ includesÂ diatoms,Â dinoflagellates,Â andÂ otherÂ photosyntheticÂ protists.Â *ItÂ isÂ unclearÂ whetherÂ theseÂ 31Â samplesÂ representÂ exchangedÂ orÂ unexchangedÂ ballastÂ water.Â Â Â SEÂ =Â isÂ theÂ standardÂ error,Â nÂ =Â numberÂ ofÂ ballastÂ tanksÂ sampledÂ forÂ concentrationÂ estimates.Â in unexchanged or untreated ballast water as was common before the mid-1990s. These data may not be representative of certain regions or the country as a whole or predictive of future densities as exchanged and/or treated ballast water becomes more common. Nevertheless, when scaled to the volume of ballast discharged into U.S. waters (196 million metric tons in recent years), these esti- mates underscore the approximate magnitude of historic biotic transfers due to shipsâ ballast. While most past research on organisms in ballast tanks has focused on wa- terborne assemblages, it is also clear that bottom communities can develop with- in ballast tanks that can include a diverse range of biota, including adults, larvae, eggs, and resting stages. Very high densities of resting stages can accumulate within ballast tanks. In a survey of 343 vessels in Australia, Hallegraeff and Bolch (1992) found that 65 percent had sediments, all of which contained di- atom resting spores. Further, they detected resting stages (cysts) of toxic dinof- lagellates in the tanks of 16 vessels and estimated > 300 million cysts of one such species in a single tank. Based on this research and further studies of rest-
SettingÂ theÂ InvasiveÂ SpeciesÂ ManagementÂ StageÂ 21Â Â ing stages for a variety of taxa in the Great Lakes and elsewhere (e.g., McCarthy and Crowder, 2000; Bailey et al., 2005; Fahnenstiel et al., 2009), it is clear that such bottom sediments serve as âseed banksâ with viable organisms that can be released from ballast tanks during operations. Effect of Ballast Water Management Ships arriving to U.S. waters from overseas are currently required to âman- ageâ their ballast water before discharge into waters of the U.S., and some ves- sels on coastwise domestic routes are also required to manage their ballast be- fore discharge (Chapter 2). At the current time, ballast water exchange is the only method that is readily available to most vessels. As outlined in Chapter 2, ballast water exchange is being replaced by treatment to specific discharge stan- dards, which are considered more stringent for some organism types (Minton et al., 2005). In general, ballast water exchange operates to reduce the concentration of coastal organisms that are transferred among global regions, by transferring wa- ter from a shipâs ballast system to the environment, with concomitant or subse- quent uptake of water. Coastal organisms are considered less likely to survive under oceanic conditions, and oceanic organisms are considered less likely to colonize coastal and inland waters, due to habitat and environmental mismatch. A diverse range of studies, mainly for the greater than 50 Âµm size class, demonstrate the effect of ballast water exchange on the original contents of bal- last tanks. Available data suggest the process of ballast water exchange removes on average 88 to 99 percent of waterborne contents of ballast tanks when per- formed properly (see review by Ruiz and Reid, 2007). For freshwater and estua- rine biota, exposure to high salinity waters often also results in osmotic shock and mortality, further increasing the efficacy of ballast water exchange (Santa- gata and Ruiz, 2007; Santagata et al., 2008). This combined effect is demon- strated in shipboard experiments, which exposed ballast tanks (either initially ballasted or not ballasted, considered âno ballast on boardâ or NOBOB) to salt- water (Gray et al., 2007; Bailey et al., 2011). As shown in Figure 1-6, the mean abundance of freshwater invertebrates, measured as the number of individuals per cubic meter, was significantly reduced (>99.99 percent) following salt-water flushing. In addition, the variation (standard error) was reduced greatly follow- ing exchange, further indicating the removal of high density discharges, both for total abundance and freshwater species alone. While ballast water exchange and salt-water flushing (in the case of NO- BOB tanks) have a strong effect in reducing original organisms, including spe- cies considered high-risk in the case of the Great Lakes, residual biota are still present in exchanged ballast tanks. For example, Table 1-3 summarizes a sub- stantial amount of empirical data on the abundance of planktonic organisms in ships that have exchanged ballast water prior to entering the Great Lakes. It
22Â Â PropaguleÂ PressureÂ andÂ InvasionÂ RiskÂ inÂ BallastÂ WaterÂ Â Â FIGUREÂ 1â6Â MeanÂ (+S.E.)Â abundanceÂ ofÂ invertebratesÂ recordedÂ fromÂ ânoÂ ballastÂ onÂ boardâÂ (aÂ andÂ bÂ panels)Â andÂ ballastedÂ (cÂ andÂ dÂ panels)Â shipsÂ beforeÂ (blackÂ bars)Â andÂ afterÂ (whiteÂ bars)Â theÂ introductionÂ ofÂ saltâwaterÂ flushingÂ andÂ ballastÂ waterÂ exchange,Â respecâ tively.Â Â MedianÂ valuesÂ areÂ indicatedÂ byÂ horizontalÂ whiteÂ orÂ blackÂ linesÂ superimposedÂ onÂ bars.Â Â LeftÂ panelsÂ includeÂ dataÂ forÂ allÂ taxa;Â rightÂ panelsÂ presentÂ dataÂ onlyÂ forÂ highÂ riskÂ taxaÂ knownÂ toÂ inhabitÂ freshâÂ orÂ brackishâwaterÂ habitats.Â *Â =Â P<0.05.Â Â SOURCE:Â Â Reâ printed,Â withÂ permission,Â fromÂ BaileyÂ etÂ al.Â (2011).Â Â Â©Â 2011Â byÂ AmericanÂ ChemicalÂ Socieâ ty.Â Â Â
SettingÂ theÂ InvasiveÂ SpeciesÂ ManagementÂ StageÂ 23Â Â shows that total abundance tends to be slightly higher for invertebrates and dinoflagellates in ballast from coastal vessels, while transoceanic vessels have higher abundances of diatoms and bacteria. For benthic organisms, total abun- dance was higher in coastal exchanged vessels. In the case of vessels arriving to the Great Lakes, with tanks having been exposed to seawater by ballast water exchange, many (most) of the waterborne organisms are likely to be marine species instead of freshwater biota that can colonize if discharged. However, many species produce resting stages (e.g., cysts, resting eggs, ephippia) that may survive ballast water exchange and be present in ballast sediments (e.g., Fahnenstiel et al., 2009; Gray and MacIsaac, 2010). Likewise, some diatoms can live for decades or longer in anoxic sedi- ments and are unlikely to be affected by osmotic shock associated with salt- water flushing or ballast water exchange (E. Stoermer, personal communication, October 25, 2010). Although ballast water exchange serves to reduce the transfer of coastal or- ganisms, there are still residual biota that can colonize coastal recipient ports upon ballast discharge. The efficacy of ballast water exchange is likely lowest when it involves source and recipient ports of high salinity, as there is no added benefit of âosmotic shockâ to residual organisms. In such cases, without added mortality, Minton et al. (2005) estimated that vessels implementing ballast water exchange would still deliver a mean of > one million coastal zooplankton alone from the original source per discharge event from the original source. The num- bers are greater for smaller organisms, simply because their densities in ballast tanks are much greater than those for zooplankton (Table 1-2). A final consideration is that much ballast water in the future will be treated, and it is this water that will be the primary target of ballast discharge standards. Though routine treatment by most vessels may be years off (see Chapter 2), ear- ly data from land-based testing of ballast treatment systems using ambient source water provide insight into the likely characteristics of treated discharge. First, densities of live organisms can be expected to range within a few orders of magnitude around the discharge standard. Compositionally, rather than a spars- er version of the diverse untreated intake assemblage, the post-treatment assem- blage may be dominated by species which prove resilient to the specific treat- ment process and which find the post-treatment environment favorable for sur- vival or re-growth. Treatment by filtration, for example, yields asymmetrical reductions in organisms across taxa largely due to size, but also because of mor- phology (Cangelosi et al., 2007). Similarly, biocidal processes will affect spe- cies differently. Tests of a chlorine treatment system at the Great Ships Initia- tive land-based Ballast Water Treatment testing facility have shown large shifts in assemblages due to treatment (Cangelosi et al., 2010). Thus, biota in treated water may become much simpler to characterize in terms of variation in concen- tration and composition, especially as only a limited number of treatment processes will prove effective, safe, and operationally feasible.
24Â Â PropaguleÂ PressureÂ andÂ InvasionÂ RiskÂ inÂ BallastÂ WaterÂ Â TABLEÂ 1â3Â Â DensitiesÂ ofÂ PlanktonicÂ InvertebratesÂ (inÂ Water),Â BenthicÂ InvertebratesÂ (inÂ Sediment),Â Dinoflagellates,Â Diatoms,Â andÂ BacteriaÂ inÂ ShipsÂ ArrivingÂ toÂ TheÂ GreatÂ Lakes.Â Â AbundancesÂ inÂ WaterÂ areÂ perÂ 1000Â L,Â AbundancesÂ inÂ SedimentÂ areÂ perÂ m3.Â Â TransoceanicÂ exchangedÂ shipsÂ CoastalÂ exchangedÂ shipsÂ TaxaÂ TotalÂ meanÂ NISÂ meanÂ TotalÂ meanÂ NISÂ meanÂ abundanceÂ abundanceÂ abundanceÂ abundanceÂ (S.E.)Â (S.E.)Â (S.E.)Â (S.E.)Â WaterÂ InvertebratesÂ 522.7 421.6 2742.6 2414.7Â (170.4)Â (173.3)Â (1071.6)Â (912.3)Â 2.8Â xÂ 104 4 4 4 DinoflagellatesÂ 2.4Â xÂ 10 6.4Â xÂ 10 6.4Â xÂ 10 Â 4 4 4 4 (1.2Â xÂ 10 )Â (1.1Â xÂ 10 )Â (3.3Â xÂ 10 )Â (3.3Â xÂ 10 )Â 1.8Â xÂ 106 8.1Â xÂ 104 1.4Â xÂ 105 9.0Â xÂ 104Â DiatomsÂ 6 4 4 4 (1.1Â xÂ 10 )Â (4.7Â xÂ 10 )Â (8.1Â xÂ 10 )Â (7.9Â xÂ 10 )Â 11 11 BacteriaÂ 7.5Â xÂ 10 N/AÂ 8.2Â xÂ 10 N/AÂ (5.6Â xÂ 1010)Â (9.2Â xÂ 1010)Â 9.4Â xÂ 1012 6.8Â xÂ 1012 VirusesÂ N/AÂ N/AÂ 12 (1.1Â xÂ 1012)Â (1.5Â xÂ 10 )Â SedimentÂ 8.9Â xÂ 105 1.4Â xÂ 104 1.2Â xÂ 106 1.8Â xÂ 103Â InvertebratesÂ 5 4 5 3 (2.6Â xÂ 10 )Â (1.1Â xÂ 10 )Â (2.8Â xÂ 10 )Â (1.8Â xÂ 10 )Â 4 4 4 9.7Â xÂ 104Â DinoflagellatesÂ 6.4Â xÂ 10 6.4Â xÂ 10 9.7Â xÂ 10 4 4 4 (2.9Â xÂ 104)Â (1.2Â xÂ 10 )Â (1.2Â xÂ 10 )Â (2.9Â xÂ 10 )Â 9 6 DiatomsÂ 3.2Â xÂ 10 9.5Â xÂ 10 N/AÂ N/AÂ (1.9Â xÂ 109)Â (5.7Â xÂ 106)Â BacteriaÂ N/AÂ N/AÂ N/AÂ N/AÂ VirusesÂ N/AÂ N/AÂ N/AÂ N/AÂ N=15,Â 15,Â 14,Â 12,Â andÂ 12Â shipsÂ processedÂ forÂ invertebrates,Â dinoflagellates,Â diatoms,Â bacteria,Â andÂ viruses,Â respectively,Â inÂ waterÂ ofÂ transoceanicÂ shipsÂ thatÂ exchangedÂ theirÂ waterÂ ("transoceanicÂ exchanged").Â Â N=13,Â 6,Â andÂ 9Â shipsÂ processedÂ forÂ invertebrates,Â dinoflagellates,Â andÂ diatoms,Â reâ spectively,Â inÂ sedimentÂ ofÂ transoceanicÂ shipsÂ thatÂ exchangedÂ theirÂ waterÂ ("transoceanicÂ exâ changed").Â Â N=4Â forÂ waterÂ andÂ 5Â forÂ sedimentÂ forÂ coastalÂ exchangedÂ vessels.Â Â Â NISÂ =Â NonindigenousÂ Species.Â N/AÂ =Â dataÂ notÂ available.Â DataÂ collectedÂ betweenÂ 2007â2009Â inclusive.Â Â Â SOURCE:Â DataÂ CourtesyÂ ofÂ E.Â BriskiÂ andÂ H.Â MacIsaac,Â CanadianÂ AquaticÂ InvasiveÂ SpeciesÂ Network.Â Â
SettingÂ theÂ InvasiveÂ SpeciesÂ ManagementÂ StageÂ 25Â Â U.S. INVASIONS FROM BALLAST WATER A diverse range of studies have evaluated invasion history of North Ameri- can waters, examining the patterns in terms of date of first detection, mechan- isms of introduction (or vector), native region, and source region (e.g., Carlton, 1979; Mills et al., 1993; Cohen and Carlton, 1995; Ruiz et al., 2000a; Holeck et al., 2004; Wonham and Carlton, 2005; Fofonoff et al., 2009; Kelly et al., 2009). In general, these analyses involved synthesis of occurrence records, which are gleaned from the literature and a diverse range of research programs, instead of an organized field-based research (monitoring) program designed explicitly to detect invasions as they occur. For this reason, it is important to recognize that (1) the resulting knowledge about invasions represents an underestimate of the total number of nonindigenous species that have colonized and (2) only the date of detection is certain, as the lag-time from invasion to detection is unknown (Ruiz et al., 2000a; Solow and Costello, 2004). The Laurentian Great Lakes are among the best studied freshwater ecosys- tems in North America, if not the world, with a documented invasion history that dates back to at least 1830 (Mills et al., 1993). More than 180 invaders are now known to be established in the Great Lakes (Ricciardi, 2006). The tax- onomic composition of invaders has changed dramatically over time, reflecting changes in different vectors over time. In particular, the switch from solid to liquid ballast in commercial cargo vessels resulted in a wholesale change in non- indigenous species (NIS) composition (Mills et al., 1993). Plants dominated early ship-mediated NIS, while invertebrates and phytoplankton have dominated post-1900 (Holeck et al., 2004). Conservatively, 55 percent of the nonindigen- ous species that established populations in the Great Lakes during the period following expansion of the St. Lawrence Seaway (from 1959 onward) are attri- buted to ballast water release (Kelly et al., 2009), although this number could be as high as 70 percent (Holeck et al., 2004). For coastal marine ecosystems, California and western North America have received the most in-depth analyses of aquatic invasions (Carlton, 1979; Cohen and Carlton, 1995). Over 250 nonindigenous species of invertebrates, algae, and microorganisms (excluding vertebrates and vascular plants) are considered es- tablished in tidal (marine and estuarine) waters of California (Ruiz et al., 2011). Of these, only about 10 percent are attributed solely to ballast water as a vector. However, greater than 50 percent include ballast water as a possible vector. This is because many species have life stages and invasion histories that make it possible for the initial introduction to occur by one of several mechanisms, in- cluding ballast water, biofouling of vesselsâ hulls, and transfer of shellfish.
26Â Â PropaguleÂ PressureÂ andÂ InvasionÂ RiskÂ inÂ BallastÂ WaterÂ Â A FURTHER CHALLENGE: THE POLYVECTIC WORLD The above challenges noted, it is critical to set the role of ballast water and sediment release into the larger vector picture. Ballast water is one of many potential vectors that now transport marine, estuarine, and freshwater species between continents and oceans. These additional vectors form what is known as a polyvectic world (Carlton and Ruiz, 2005) and include vessel fouling (on and in many regions of a ship), aquaculture, live bait industries, aquarium and pet industries, the live seafood industry, and the availability of hundreds if not thou- sands of species on the Internet for unregulated purchase and distribution to the public at large (Lodge et al., 2006). As a result, it is often a challenge to deter- mine which vector or vectors, from a sea of dispersal mechanisms, has led to a particular invasion. Failure to address this multiplicity of vectors with the same intensity and funding that have been applied to ballast water management will result in continued invasions. In short, even when robust and enforced ballast management is achieved, the management community should be prepared for, and not be surprised when, invasions continue. Coupled with polyvectism is the reality that virtually all management scena- rios apply regulatory filters rather than complete barriers to any vector. A su- perb example of this is the work of the United States Department of Agricul- tureâs Animal and Plant Health Inspection Service (APHIS), whose responsibili- ties for the interception of unwanted nonindigenous species date back to 1854 (note that U.S. interests in managing ballast water formally commenced in 1990). Despite the monitoring (inspection, interception, and quarantine) sys- tems in place, and despite the extensive statutory authority wielded by APHIS, new pestiferous insect and plant invasions (for example) occur annually. This is because the holes in the management filtration matrix expand (or contract) over time and space and are at the mercy of the frequency and intensity of inspection, the volume of cargo inspected, human behavior that seeks to circumvent inspec- tion and interception, and yet other factors. Despite all of the challenges and lacunae outlined above, the enduring value of pursuing vector management is that control decreases invasions. In the ab- sence of APHIS and similar federal and state agencies, it is staggering to im- agine what the economic, environmental, and societal impacts of terrestrial plant and insect invasions would be in the United States. It is for this reason that bal- last water (and other vector) control, restraint, and supervision are critical, and will prove of inestimable value in protecting and preserving the beneficial uses and the indigenous populations of fish, shellfish, and other wildlife in the na- tionâs waters. REQUEST FOR THE STUDY AND REPORT ROADMAP There are two main federal programs for regulating ballast water in the United StatesâEPAâs Vessel General Permit under the Clean Water Act and the
SettingÂ theÂ InvasiveÂ SpeciesÂ ManagementÂ StageÂ 27Â Â U.S. Coast Guardâs authority under the National Invasive Species Act (described in detail in Chapter 2). Both programs are undergoing revision and analyses in the near future, which prompted the EPA Office of Wastewater Management and the USCG to request the National Research Councilâs (NRC) Water Science and Technology Board (WSTB) to undertake a study to provide technical advice to help inform the derivation of numeric limits for living organisms in ballast water for the next Vessel General Permit and for regulatory programs of the USCG. Both EPA and the USCG desire a federal ballast water management pro- gram that will be more effective than ballast water exchange-based requirements in preventing the establishment of new aquatic nonindigenous species through the discharge of shipsâ ballast water. To improve the regulation of ballast water, the agencies seek to better understand and relate the concentration of living or- ganisms in ballast water discharges (inoculum density) to the probability of non- indigenous organisms successfully establishing populations in U.S. waters. Al- though the scientific understanding of this relationship is limited, several organ- izations have created or are in the process of creating numeric standards for bal- last water discharges, expressed as limits on the concentrations of living organ- isms per unit volume. This report focuses on the initial survival of aquatic nonindigenous species upon release from ballast water and subsequent establishment of a reproducing population, because it is thought that lowering the total concentration of organ- isms in ballast water is critical to reducing the risk of a successful invasion. Other factors that affect the overall successful establishment of nonindigenous speciesâsuch as their interface with a transport vector, such as a ship; vector uptake of specific species; survival of the nonindigenous species during trans- port events; ballast water treatment to reduce NIS numbers; and release of non- indigenous species from the vectorâare not the focus. It should be noted that the NRC was not asked to propose specific ballast water discharge limits, as that is a risk management decision, nor was it asked to evaluate matters related to the technical and engineering aspects of testing, installing, and using ballast water treatment systems on board vessels. The latter topic would include what types of technologies exist and are available for use in the on-board treatment of bal- last water discharges, what discharge standards can be reliably achieved by the ballast water treatment systems currently on the market or under development, and what are the technological constraints or other impediments to the develop- ment of ballast water treatment technologies. These topics are being considered by a Science Advisory Board committee of the EPA. The statement of task reads âEPA and the USCG request the NRC to con- duct a study that will significantly inform their efforts to derive environmentally protective numeric ballast water discharge limits in the next Vessel General Permit and other programs. The study will take into account estuarine and freshwater systems, including the Great Lakes and other inland navigable wa- ters, as well as the waters of the three-mile territorial sea, considering what im- plications their differing environmental and ecological conditions might have for
28Â Â PropaguleÂ PressureÂ andÂ InvasionÂ RiskÂ inÂ BallastÂ WaterÂ Â the development of allowable concentrations of living organisms in discharged ballast water. Specifics tasks are outlined below. 1. Evaluate the state of the science of various approaches that assess the risk of establishment of aquatic NIS given certain concentrations of living or- ganisms in ballast water discharges. ï· What are the advantages and disadvantages of the available ap- proaches? ï· Identify and discuss the merits and practical utility of other addi- tional approaches of which the NAS is aware. ï· How can the various approaches be combined or synthesized to form a model or otherwise more powerful approach? ï· What are the data gaps or other shortcomings of the various ap- proaches and how can they be addressed within the near and long term? ï· Can a ânatural invasion rateâ (invasion rates based on historic in- vasion rates), or other ânaturalâ baselines, be reliably established, and if so, how? What utility might such baselines have in informing EPAâs deriva- tion of allowable numeric limits for living organisms in ballast water dis- charges? Can such baselines be established on a national basis, or would this need to be done on a regional or ecosystem basis? 2. Recommend how these approaches can be used by regulatory agencies to best inform risk management decisions on the allowable concentrations of living organisms in discharged ballast water in order to safeguard against the establishment of new aquatic NIS and to protect and preserve existing indigen- ous populations of fish, shellfish, and wildlife and other beneficial uses of the nationâs waters. 3. Evaluate the risk of successful establishment of new aquatic NIS asso- ciated with a variety of ballast water discharge limits that have been used or suggested by the international community and/or domestic regulatory agen- cies.â Two documents that summarize an understanding of the risk of invasion for nonindigenous species from ballast water were critical to the work of the com- mittee. Lee et al. (2010) summarized and analyzed seven approaches that have been used or are proposed to either predict the probability of invasion or predict or establish an ecologically âacceptableâ concentration of living organisms in ballast water discharges. In addition, in April 2008 the U.S. Coast Guard com- pleted a Draft Programmatic Environmental Impact Statement (DPEIS) accom- panying its proposed ballast water discharge standards rulemaking under NANPCA. Chapter 2 of this report discusses the regulatory context surrounding ballast water management, including state, federal, and international guidelines and
SettingÂ theÂ InvasiveÂ SpeciesÂ ManagementÂ StageÂ 29Â Â regulations that are the foundation for the current ballast discharge standards. Chapter 3 discusses the many sources of variability that ultimately control the rate of invasion from organisms present in ballast water. The prospect of devel- oping a ballast water standard that can be applied to all ships is daunting because ships are coming from all over the world, with significant differences in source regions; in the diversity, abundance, and density of entrained organisms; and in the compatibility of source and recipient regions. Chapter 4 presents the theory underlying the relationship between ballast water organism concentration and the risk of NIS establishment, which is fo- cused on the role of propagule pressure. It analyzes the mathematical models that have been developed to express this relationship, discussing their data needs and other strengths and weaknesses. In this chapter, three of the methods for setting ballast water standards found in the Lee et al. (2010) report are dis- cussed, including the reaction-diffusion approach, the population viability analy- sis, and the per capita invasion probability approach. Chapter 5 analyzes and critiques the non-quantitative, expert-opinion-based methods for setting ballast water discharge standards presented in Lee et al. (2010), including the zero- detectable discharge standard and the natural invasion rate approach. The report paves a way forward in Chapter 6 with conclusions and recommendations for setting numeric ballast water discharge standards for the next iteration of the Vessel General Permit and USCG regulations. REFERENCES AgoguÃ©, H., D. Lamy, P. R. Neal, M. L. Sogin, and G. J. Herndl. 2011. Water mass- specificity of bacterial communities in the North Atlantic revealed by massively pa- rallel sequencing. Molecular Ecology 20:258â274. Bailey, S. A., I. C. Duggan, P. T. Jenkins, and H. J. MacIsaac. 2005. Invertebrate resting stages in residual ballast sediment of transoceanic ships. Canadian Journal of Fishe- ries and Aquatic Sciences 62:1090â1103. 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. En- vironmental Science and Technology 45:2554â2561. Burkholder, J. M., G. M. Hallegraeff, G. Melia, A. Cohen, H. A. Bowers, D. W. Oldach, M. W. Parrow, M. J. Sullivan, P. V. Zimba, E. H. Allen, C. A. Kinder, and M. A. Mallin. 2007. Phytoplankton and bacterial assemblages in ballast water of U.S. military ships as a function of port of origin, voyage time, and ocean exchange prac- tices. Harmful Algae 6:486â518. Cangelosi, A. A., N. L. Mays, M. D. Balcer, E. D. Reavie, D. M. Reid, R. Sturtevant, and X. Gao. 2007. The Response of Zooplankton and Phytoplankton from the North American Great Lakes to Filtration. Harmful Algae 6:547â566. Cangelosi, A., L. Allinger, M. Balcer, N. Mays, T. Markee, C. Polkinghorne, K. Prihoda, E. Reavie, D. Reid, H. Saillard, T. Schwerdt, H. Schaefer, and M. TenEyck. 2010. Report of the Land-Based Freshwater Testing by the Great Ships Initiative of the Siemens SiCURETM Ballast Water Management System for Type Approval Accord- ing to Regulation D-2 and the Relevant IMO Guidelines. Great Ships Initiative.
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