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1  Setting the Invasive Species Management 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 ships’ 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 (D’Itri, 1997), motivated the United Nations’ Interna- tional Maritime Organization (IMO) to take up the introduction of nonindigen- ous species due to the release of ships’ 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   11 

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12    Propagule Pressure and Invasion Risk in Ballast Water    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 ships’ ballast water (IMO, 2004; see also Chapter 2). This post-treatment load is referred to as a “discharge standard.” 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.                                   FIGURE 1‐1  Routes and ports of the global cargo ship network.  Shown are the trajecto‐ ries  of  all  cargo  vessels  larger  than  10,000  gross  tonnage  during  2007.   The  color  scale  indicates  the  number  of  journeys  along  each  route.   SOURCE:   Reprinted,  with  permis‐ sion, from Kaluza et al. (2010).  © 2010 by Royal Society Publishing.   

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Setting the Invasive Species Management Stage  13    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 “foreign” or “overseas” arrivals from a last port of call outside the U.S. and Canada. The residual (42,000) are “domestic” or “coastwise” 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 “domestic-source” 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  This estimate excludes inland traffic (e.g., Mississippi River), and some types of vessels are under‐ represented (see Miller et al., 2007, 2010).  3   An  estimated  85%  of  coastwise  arrivals  and  86%  of  foreign  arrivals  submitted  ballast  water  re‐ ports.   All  vessels  are  required  to  submit  ballast  water  reports  under  U.S.  Coast  Guard  regulations,  and  there  are  additional  vessels  (military  and  certain  commercial  ships,  such  as  crude  oil  tankers  engaged in coastwise trade) that are not required to provide this information. 

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14    Propagule Pressure and Invasion Risk in Ballast Water    FIGURE  1‐2   Number  of  vessel  arrivals  to  U.  S.  ports  in  2006‐2007  that  originated  from  overseas  locations  (ports  of  origin  outside  the  U.S.  and  Canada).   SOURCE:  Miller  et  al.  (2010).      FIGURE  1‐3   Amount  of  ballast  water  discharged  in  U.  S.  ports  in  metric  tons  (mt)  from  overseas sources (outside of U.S. and Canada), regardless of last port of call or route,  in  2006‐2007.  SOURCE: Miller et al. (2010). 

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Setting the Invasive Species Management Stage  15    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 µm); protists, bac- teria, and viruses are even smaller in size and more numerous in ballast water.

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16    Propagule Pressure and Invasion Risk in Ballast Water    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) FIGURE  1‐4    Relationship  between  the  cumulative  number  of  overseas  vessel  arrivals  and  total  volume  of  ballast  water  discharged  for  ports  in  the  U.S.  for  2006‐2007.   mt  =  metric ton.  SOURCE: National Ballast Information Clearinghouse.    FIGURE  1‐5    Last  port  of  call  (LPOC)  for  vessel  arrivals  to  U.S.  ports  in  2006‐2007  that  originated  from  overseas  locations.    Ballast  water  aboard  ships  is  not  limited  to  the  LPOC as its origin.  SOURCE: Miller et al. (2010). 

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Setting the Invasive Species Management Stage  17    Although this is not meant to represent an exhaustive list, Table 1-1 serves to underscore the taxonomic range associated with ships’ 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 organisms—ranging from 20 nanometers to 30 cm—presents 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 ships’ 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 ships’ 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

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18    Propagule Pressure and Invasion Risk in Ballast Water      TABLE  1‐1   Diversity  of  Organisms  Collected  in  Unmanaged  Ballast  Water  and  Sediment  in  Vessels  Arriving  in  North  American  Coastal  and  Inland  Waters.    (The  list  of  micro‐ organisms is not comprehensive.)  Group  Common name Coastal  Inland  Animals  + + Cnidaria  jellyfish, anemones, hydroids + Ctenophora  comb jellies (sea gooseberries) + + Arthropoda  barnacles  + +   copepods  + +   decapods (shrimps, crabs, and others) + +   other crustaceans, including euphausids, stomatopods,  cumaceans, mysids, isopods, amphipods, ostracods,  cladocerans  +   insects  + +   mites  + Tardigrada  water bears + + Nematoda  thread worms + Chaetognatha  arrow worms + + Mollusca  bivalves (clams, mussels, oysters) + +   gastropods (snails) +   chitons  + + Annelida  segmented worms + Nemertea  ribbon worms + Platyhelminthes  flatworms  + Phoronida  horseshoe worms + + Bryozoa  bryozoans (moss animals) + + Rotifera  rotifers  + Gastrotricha  gastrotrichs + Echinodermata  sea stars  +   brittle stars +   sea urchins +   sea cucumbers +   crinoids  + Hemichordata  acorn worms + Urochordata  ascidians, larvaceans + + Pisces  fishes  Plants  + Angiosperms  sea grasses + Red and green  seaweed  algae  table continues     

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Setting the Invasive Species Management Stage  19    TABLE 1‐1  Continued  Group  Common name Coastal  Inland  Microorganisms  + + Viruses   viruses  + + Cyanobacteria  blue green algae + + Other bacteria     + + Bacillariophyceae  diatoms  + + Dinoflagellata   dinoflagellates + Ciliophora  ciliated protists + + Foraminifera  Forams  + + Other "protists"    Sources  for  coastal  taxa:  Smith  et  al.  (1999);  McCarthy  and  Crowder  (2000);  Ruiz  et  al.  (2000b;  Chesapeake  Bay);  Cordell  et  al.  (2008;  Puget  Sound);  Levings  et  al.  (2004;  Vancouver);  Carlton  and  Geller  (1993;  Coos  Bay).   Inland  taxa:  Locke  et  al.  (1993;  Great  Lakes);  Duggan  et  al.  (2005;  Great  Lakes).  Gastrotrich data from Carlton (1985).  Sources for microbial taxa: Drake et al. (2001, 2005);  Burkholder et al. (2007); Klein et al. (2010); Reid et al. (2007).    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 Committee’s knowledge, no one has undertaken a metagenomics study (cf. Agogué 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 ship’s 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

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20    Propagule Pressure and Invasion Risk in Ballast Water    TABLE 1‐2  Concentration of Various Organism Types Reported in Ballast Water Sampled  Upon Arrival of Ships to Particular Regions        Concentrations in unexchanged ballast water                   mean              SE  n      Zooplankton (organisms/m3)            3 10 × 101  113      Chesapeake Bay (overseas)  1.94 × 10     4 3   Chesapeake Bay (domestic)  1.75 × 10   1.5 × 10   37      4 3   Prince William Sound, Alaska  1.26 × 10   5.53 × 10   169      Phytoplankton (cells/liter)           5 1.84 × 105  273      Europe  2.99 × 10     Bacteria (cells/liter)           8 8   Chesapeake Bay  8.3 × 10   1.7 × 10   9      8 8   Chesapeake Bay  8.03 ×  10   1.88 × 10  (sd)  53      Virus‐like Particles (vlp/liter)           9 2.3 × 109    Chesapeake Bay  7.4 × 10   7      10 10   Chesapeake Bay  1.39 × 10   1.57 × 10  (sd)  31*      SOURCES: Data for Chesapeake  Bay are from Minton  et al. (2005; zooplankton), Ruiz et al. (2000a),  and Drake et al. (2007; bacteria and virus‐like particles); data for Alaska are from Hines et al. (2000;  zooplankton);  data  for  phytoplankton  are  from  International  Maritime  Organization  (2004).    In  general,  zooplankton  refers  to  organisms  collected  on  nets  >50  m  in  mesh  size,  and  phytoplank‐ ton includes diatoms, dinoflagellates, and other photosynthetic protists.  *It is unclear whether these 31 samples represent exchanged or unexchanged ballast water.    SE = is the standard error, n = number of ballast tanks sampled for concentration estimates.  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 ships’ 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-

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Setting the Invasive Species Management Stage  21    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 “seed banks” 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 “man- age” 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 ship’s 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 µm 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 ‘no ballast on board’ 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

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24    Propagule Pressure and Invasion Risk in Ballast Water    TABLE  1‐3    Densities  of  Planktonic  Invertebrates  (in  Water),  Benthic  Invertebrates  (in  Sediment),  Dinoflagellates,  Diatoms,  and  Bacteria  in  Ships  Arriving  to  The  Great  Lakes.   Abundances in Water are per 1000 L, Abundances in Sediment are per m3.    Transoceanic exchanged ships  Coastal exchanged ships  Taxa  Total mean  NIS mean  Total mean  NIS mean  abundance  abundance  abundance  abundance  (S.E.)  (S.E.)  (S.E.)  (S.E.)  Water  Invertebrates  522.7 421.6 2742.6 2414.7  (170.4)  (173.3)  (1071.6)  (912.3)  2.8 x 104 4 4 4 Dinoflagellates  2.4 x 10 6.4 x 10 6.4 x 10   4 4 4 4 (1.2 x 10 )  (1.1 x 10 )  (3.3 x 10 )  (3.3 x 10 )  1.8 x 106 8.1 x 104 1.4 x 105 9.0 x 104  Diatoms  6 4 4 4 (1.1 x 10 )  (4.7 x 10 )  (8.1 x 10 )  (7.9 x 10 )  11 11 Bacteria  7.5 x 10 N/A  8.2 x 10 N/A  (5.6 x 1010)  (9.2 x 1010)  9.4 x 1012 6.8 x 1012 Viruses  N/A  N/A  12 (1.1 x 1012)  (1.5 x 10 )  Sediment  8.9 x 105 1.4 x 104 1.2 x 106 1.8 x 103  Invertebrates  5 4 5 3 (2.6 x 10 )  (1.1 x 10 )  (2.8 x 10 )  (1.8 x 10 )  4 4 4 9.7 x 104  Dinoflagellates  6.4 x 10 6.4 x 10 9.7 x 10 4 4 4 (2.9 x 104)  (1.2 x 10 )  (1.2 x 10 )  (2.9 x 10 )  9 6 Diatoms  3.2 x 10 9.5 x 10 N/A  N/A  (1.9 x 109)  (5.7 x 106)  Bacteria  N/A  N/A  N/A  N/A  Viruses  N/A  N/A  N/A  N/A  N=15,  15,  14,  12,  and  12  ships  processed  for  invertebrates,  dinoflagellates,  diatoms,  bacteria,  and  viruses,  respectively,  in  water  of  transoceanic  ships  that  exchanged  their  water  ("transoceanic  exchanged").    N=13,  6,  and  9  ships  processed  for  invertebrates,  dinoflagellates,  and  diatoms,  re‐ spectively,  in  sediment  of  transoceanic  ships  that  exchanged  their  water  ("transoceanic  ex‐ changed").  N=4 for water and 5 for sediment for coastal exchanged vessels.    NIS = Nonindigenous Species. N/A = data not available.  Data collected between 2007‐2009 inclusive.    SOURCE: Data Courtesy of E. Briski and H. MacIsaac, Canadian Aquatic Invasive Species Network.  

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Setting the Invasive Species Management Stage  25    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 vessels’ hulls, and transfer of shellfish.

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26    Propagule Pressure and Invasion Risk in Ballast Water    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- ture’s 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- tion’s waters. REQUEST FOR THE STUDY AND REPORT ROADMAP There are two main federal programs for regulating ballast water in the United States—EPA’s Vessel General Permit under the Clean Water Act and the

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Setting the Invasive Species Management Stage  27    U.S. Coast Guard’s 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 Council’s (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 ships’ 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 species—such 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 vector—are 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 “EPA 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

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28    Propagule Pressure and Invasion Risk in Ballast Water    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.  What are the advantages and disadvantages of the available ap- proaches?  Identify and discuss the merits and practical utility of other addi- tional approaches of which the NAS is aware.  How can the various approaches be combined or synthesized to form a model or otherwise more powerful approach?  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?  Can a “natural invasion rate” (invasion rates based on historic in- vasion rates), or other “natural” baselines, be reliably established, and if so, how? What utility might such baselines have in informing EPA’s 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 nation’s 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.” 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 “acceptable” 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

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Setting the Invasive Species Management Stage  29    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 Agogué, 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 20:258–274. 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 62:1090–1103. 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 45:2554–2561. 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 6:486–518. 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 6:547–566. 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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