The known extent of biological invasions exhibits strong variation with respect to space, time, taxonomic group, and vector. Using a synthesis of nonindigenous species (NIS) occurrences in North America, we characterized the invasion history for coastal marine ecosystems by invertebrates and algae through 2010, to evaluate variation and existing patterns at a continental scale. This study updates a previous analysis of invasions for the same taxonomic groups in North America, providing a first assessment of changes in the last 11 year period (2000–2010). Overall, we documented 450 marine and estuarine NIS that are considered to have established populations in tidal waters of North America, representing a 51% increase in NIS richness compared to the earlier analysis. Of the 152 species added, 71 species (47%) have first documented records since the year 1999, and 81 species (53%) were additions attributed to earlier time periods due to recent reports and further analysis. Across all time periods, taxonomic groups with the largest contribution were Crustaceans (112 species) and Molluscs (80 species), together providing 43% of the total species richness for North America. Species richness was unevenly distributed among coasts, with most documented on the Pacific Coast (310 species) and fewer on the Atlantic Coast (189 species) and Gulf Coast (88 species). Commercial ships have contributed between (a) 44–78% of the initial (primary) invasions of all nonindigenous species to North America and (b) 52–82% of NIS in the last 30-year time interval, being driven by transfers associated with ballast water and hull biofouling. Importantly, invasion dynamics are a shifting landscape, where the past may not predict the future, especially with emerging trade patterns and global to local environmental changes. Thus, effective management to reduce future invasions requires a dynamic and multi-vector approach, instead of single vector strategies based on past history alone.

Introduction

Over the past several decades, a major body of scientific research has emerged that indicates biological invasions by nonindigenous species (NIS) are a major force of change in coastal marine ecosystems, having significant ecological, economic, and human health effects (Grosholz, 2002; Galil, 2007). The effects of NIS are thought to be increasing over time, because (a) new invasions continue to accumulate in many global regions, (b) existing NIS often expand their geographic range and (c) the cumulative impact of invasions is likely a function of both number of species and area occupied (Parker et al., 1999). While the types of impacts occurring are understood and illustrated by a diverse range of studies, these underestimate the full scope of invasion effects for two reasons. First, the impacts of most marine NIS have not been assessed (Ruiz et al., 1999, 2011a; Williams et al., 2013). Second, the actual number of NIS is poorly resolved for most geographic regions.

In this article, we examine the current state of knowledge about the number of marine NIS established in North America, as a model system for which invasions are relatively well-studied. This updates previous analyses at the continental scale (Ruiz et al., 2000a; Fofonoff et al., 2003) and provides a review of more recent literature on invasion dynamics for this global region. In particular, we report on the spatial, temporal, and taxonomic distribution of NIS in coastal marine habitats of North America. We also examine the human-mediated transfer mechanisms (vectors) responsible for initial invasions to the continent, exploring how this has changed through time. Finally, we focus particular attention on shipping as a dominant source of new invasions and provide an overview of the current state of management and policy efforts in the United States to reduce the risk of future invasions and associated impacts.

Methodology

We examined patterns of invasions in coastal marine and estuarine habitats in North America, using records of NIS that were compiled in an extensive database, the National Marine and Estuarine Species Information System (NEMESIS), which we have created over the past 15 years. NEMESIS collects and characterizes NIS records for marine and tidal waters of the continental United States and Canada. The information is collected as an on-going effort from a diverse range of sources, including published literature, reports, museum collections, field-based surveys, and personal communication. For each putative NIS, we evaluate the taxonomic identification, invasion status (native, nonindigenous, or crytogenic), population status (whether established, extinct/failed, or unknown), date and location of first record at the level of bay, state, coast, and continent. For each species and location, we also assess possible vectors of introduction, based upon life-history and habitat information as well as the location and time of arrival. For further details of classification of species see Ruiz et al. (2000a, 2011b).

More specifically, we assessed the extent and characteristics of NIS in North America through 2010, including only invertebrates, algae, and microorganisms. We excluded vascular plants and vertebrates from this analysis. For NIS with occurrence records up to 2010, we assessed whether the species were considered to have established populations or not, based on repeated records or observations of reproduction and/or persistence, following Ruiz et al. (2011b). We included in our analyses all NIS considered established in tidal waters (bays and estuaries) and marine waters for the three coasts of North America (Figure 1). Furthermore, we focused primarily on the initial records of introduction at the continental scale to characterize the extent and characteristics of NIS, providing some discussion of secondary spread.

Figure 1.

Map of North America. Shown are the locations for the three coasts (West, East and Gulf) included in this study.

Figure 1.

Map of North America. Shown are the locations for the three coasts (West, East and Gulf) included in this study.

A list of NIS included in our analyses is available from the authors. In addition, these data and more extensive information are being made available publically on the website for NEMESIS (http://invasions.si.edu/nemesis/browseDB/intro.html).

Results

We documented a total of 450 NIS of invertebrates and algae that are considered established in marine and estuarine waters of North America, excluding an additional 77 NIS that have been recorded but are not known to have established populations. Since 1999, this represents a 51% increase for the total NIS richness documented at the continental scale, when compared to the 298 species reported previously for the same geographic region (Ruiz et al., 2000a). Importantly, only 47% of the additional 152 NIS added since 1999 were reported as new occurrences in the last 11 years, whereas the other 53% were detected initially prior to 2000 and were included only later due to (a) a delay in reporting or publication, (b) further analysis on taxonomic or biogeographic status or (c) overlooked records. Thus, addition of the latter group of NIS reflects the lag-time in reporting and analysis that exists in available data.

The number of documented NIS is unevenly distributed among taxonomic groups and geographic regions in North America (Figures 2 and 3). The largest number of NIS are known for Crustaceans (112 species) and Molluscs (80 species), which together contributed 43% of total NIS richness. In contrast, few NIS are documented for Protozoans and Platyhelminths (flatworms), which are relatively small and inconspicuous organisms compared to crustaceans and molluscs. When comparing among the three coasts, the largest number of NIS is known from the West Coast (310 species) compared to the East or Gulf Coasts (189 and 88 species, respectively). As shown in Figure 3, the number of documented NIS increased from 16–25% per coast between 1999 and 2010.

Figure 2.

Taxonomic distribution of established NIS. Shown are the numbers of NIS (invertebrates and algae) documented to occur in coastal waters of North America through 2010 by taxonomic group.

Figure 2.

Taxonomic distribution of established NIS. Shown are the numbers of NIS (invertebrates and algae) documented to occur in coastal waters of North America through 2010 by taxonomic group.

Figure 3.

Rate of detection for established NIS. Shown are the numbers of NIS (invertebrates and algae) detected in each 30-year time interval for coastal waters of North America through 2010.

Figure 3.

Rate of detection for established NIS. Shown are the numbers of NIS (invertebrates and algae) detected in each 30-year time interval for coastal waters of North America through 2010.

On a continental scale, the rate of NIS detection for coastal marine ecosystems in North America has increased exponentially over the past two centuries, with more new occurrences reported with each successive 30-year interval from 1800 to 2010 (Figure 4). Forty two percent of all documented NIS (450 species) were first reported in the last 30-year interval, and 16% of NIS were reported in the last 11 years since 1999.

Figure 4.

Comparison of established NIS richness by coast. Shown are the numbers of NIS (invertebrates and algae) documented to occur per coast of North America through 2010; the gray bar indicates the number detected after 1999.

Figure 4.

Comparison of established NIS richness by coast. Shown are the numbers of NIS (invertebrates and algae) documented to occur per coast of North America through 2010; the gray bar indicates the number detected after 1999.

Commercial shipping has been a dominant source of initial introductions for the 450 NIS we documented in North America (Figure 5). Two hundred species (44% of the total) were attributed solely to ships, including species transferred primarily with ballast water or hull biofouling. The second largest category shown in Figure 5 was “multiple,” which indicates that multiple mechanisms were possible for the time period and location where these NIS were first detected. For example, the Chinese mitten crab (Eriocheir sinensis) was first introduced to San Francisco Bay, California, and it may have arrived in the ballast water of a ship or in live trade as food from Asia (Cohen and Carlton, 1995). The shaded portion of this multiple category indicates the number of NIS for which commercial ships were a possible mechanism. Thus, when considering those species attributed solely to ships and those for which ships were a possible mechanism, shipping has contributed from 44–78% of the 450 initial NIS introductions into North America.

Figure 5.

Vector strength for established NIS. Shown are the numbers of NIS (invertebrates and algae) attributed to coarse vector categories through 2010, based on the initial introduction to North America; black bar indicates the number for which shipping is a sole or possible vector.

Figure 5.

Vector strength for established NIS. Shown are the numbers of NIS (invertebrates and algae) attributed to coarse vector categories through 2010, based on the initial introduction to North America; black bar indicates the number for which shipping is a sole or possible vector.

It is also the case that species transfers by commercial ships are driving the observed increase in number of NIS in North America over time (Figure 6). In the last 30 year interval (1981–2010), 52% of all new NIS occurrences were attributed solely to shipping, and an additional 31% of new NIS records include shipping as a possible mechanism for introduction. Thus, shipping contributed up to 83% of all initial introductions to North America that were detected in the last time interval of our analyses.

Figure 6.

Strength of shipping (top) and oyster (bottom) as vectors through time for established NIS. Shown are the numbers of NIS (invertebrates and algae) attributed to each vector per 30-year time interval through 2010, based on the initial introduction to North America; the black bar indicates the number attributed solely to that vector and the gray bar indicates the number for which that vector is possible (among multiple vectors).

Figure 6.

Strength of shipping (top) and oyster (bottom) as vectors through time for established NIS. Shown are the numbers of NIS (invertebrates and algae) attributed to each vector per 30-year time interval through 2010, based on the initial introduction to North America; the black bar indicates the number attributed solely to that vector and the gray bar indicates the number for which that vector is possible (among multiple vectors).

Both ballast water and hull biofouling have been the dominant vectors for shipping-related invasions, and their contributions to NIS richness have increased over time. When considering the 200 species attributed solely to shipping (bottom of Figure 5) for all time periods combined, 16% were attributed solely to ballast water, the water that is taken on from ports and oceans and used for stability during voyages (see Carlton, 1985 for discussion of associated species transfers). Another 30% of these 200 species were attributed solely to hull biofouling, or species transferred on the hulls and underwater surfaces of vessels. For nearly all of the remaining NIS (>50% of the 200 species), both ballast water and hull biofouling were possible vectors. This uncertainty about the relative importance of these two vectors results because many organisms have life stages that are associated with coastal waters (that can be taken on in ballast tanks) and also hard surfaces (such as the undersides of vessels).

Figure 7 shows the contribution of ballast water and hull fouling over time, for the 200 NIS attributed solely to shipping. Those species attributed solely to each vector are shown in black, and those for which the vector is possible are shown in gray. For both vectors, the total number of species has increased in recent time intervals, which is driving the overall increase of shipping-related transfers through time. Hull biofouling and ballast water were responsible solely for 12.5% and 10% of species, respectively, in the last time period (n = 99 NIS attributed solely to shipping). However, both were a possible vector for an additional 77.5% of the shipping-only invasions from 1981–2010. While each were important sources for NIS, there remains uncertainty about which of these two vectors was responsible for most shipping-related invasions.

Figure 7.

Strength of hull fouling (top) and ballast water (bottom) as vectors through time for established NIS. Shown are the numbers of NIS (invertebrates and algae) attributed to each vector per 30-year time interval through 2010, based on the initial introduction to North America. This includes only those species attributed solely to shipping (n = 200; see lowest bar in Figure 5); the black bar indicates the number attributed solely to the respective vector and the gray bar indicates the number for which that vector is possible.

Figure 7.

Strength of hull fouling (top) and ballast water (bottom) as vectors through time for established NIS. Shown are the numbers of NIS (invertebrates and algae) attributed to each vector per 30-year time interval through 2010, based on the initial introduction to North America. This includes only those species attributed solely to shipping (n = 200; see lowest bar in Figure 5); the black bar indicates the number attributed solely to the respective vector and the gray bar indicates the number for which that vector is possible.

Discussion

Total richness and taxonomic distribution

While 450 NIS of invertebrates and algae were reported as established in marine and estuarine waters of North America, this represents only a minimum estimate of established species richness, and the actual number of NIS is undoubtedly larger for multiple reasons. First, detection of species requires surveys and analyses, which identify and document occurrences, and such effort is limited (historically and currently) for many regions, habitats, and taxonomic groups, resulting in an incomplete inventory. Even for well-studied groups within North America, extensive surveys may be decades or longer in the past and would therefore not include (detect) recent invasions. Second, recognition of NIS requires knowledge of both taxonomic and biogeographic status of species which is not available in many cases. As a result, while some species are recognized as NIS upon detection, a large number of species are now considered cryptogenic, reflecting the uncertainty about historical distributions (Cohen and Carlton, 1995; Carlton, 1996). Third, our analysis ends in 2010, and additional invasions have been recorded since this time (Ruiz et al., unpublished data).

This study also provides a minimum estimate of NIS richness within each taxonomic group, for the same reasons. Moreover, the quality of the data is variable among taxonomic groups and may result in a strong bias in the observed distribution of NIS (Figure 2). As discussed previously (Ruiz et al., 2000a; Wyatt and Carlton, 2002; Gibbons et al., 2005), taxonomic and biogeographic knowledge is positively associated with organism size, being relatively high for the large, conspicuous organisms such as many molluscs and crustaceans (which also often have hard parts and fossil records compared to soft-bodied organisms). It is also noteworthy that the concentration and species richness of organisms in general is inversely related to size in coastal marine environments and associated with some major vectors responsible for invasions (Drake et al., 2001; Minton et al., 2005). Together, these attributes suggest that (a) the likelihood of transfer and establishment may actually be greatest for microorganisms, due to high species richness and density of propagules transferred by human activities, and (b) many invasions by microorganisms may go undetected compared to larger organisms. An alternative hypothesis is that some groups of microorganisms are different than larger organisms in terms of biogeography and therefore invasion potential, affecting actual NIS richness (for discussion, see Ruiz et al., 2000b; Dobbs and Rogerson, 2005). There are examples of microorganism invasions, which include pathogens that cause diseases in marine systems (Hallegraeff, 2015; Burreson et al., 2000), demonstrating that some small organisms are NIS, but there is a critical gap in understanding about the biogeography and scope of invasions for small organisms.

Temporal distribution

Our results show an exponential increase in the detection rate of new invasions at a continental scale, and previous analyses have also documented exponential increases of NIS for each of the three coasts as well as specific bays in North America (Cohen and Carlton, 1998; Ruiz et al., 2000a, 2011; Fofonoff et al., 2009). A similar pattern of increased detection through time has been observed in studies of many other marine systems around the world, suggesting this is a broad-based phenomenon (Hewitt et al., 2004; Galil et al., 2014). Some caution is required in interpreting these results, because detection rate can deviate from that actual invasion rate. As outlined previously (Ruiz et al., 2000a), the search effort and resolution (due to improved understanding and tools) has changed through time and almost certainly has increased the probability of detection (and recognition) of NIS in more recent time. One expected outcome of such changes is that more NIS would be detected later in time, even if the exact same number of actual invasions occurred in two time intervals (e.g. 1800–1830 versus 1981–2010). However, it is also likely that the rate of delivery of propagules has increased dramatically over time, as the magnitude and speed of global trade has increased, which would be expected to increase the probability and number of invasions.

There is no doubt that the cumulative number of NIS in North America and elsewhere is increasing over time and that new invasions continue to occur. Increases observed in the detection rate of NIS for large and conspicuous organisms, which are not easily overlooked (such as shelled molluscs and crabs), provide strong evidence that invasion rates have increased through time (Ruiz et al., 2000a). While there is consensus that invasion rates are increasing in many regions, the actual rate function of invasions remains uncertain and challenging to assess.

Geographic and habitat distribution

There are several geographic patterns in marine NIS richness that are evident from a synthesis of reported invasions for North America. First, the number or detected NIS differs among the three coasts (Figure 4, this study). Second, there are conspicuous differences in the number of NIS reported at different latitudes in North America, with relatively few species reported at high latitudes compared to more temperate regions. This latitudinal pattern is best documented along the West Coast, from Alaska to southern California (Ruiz and Hewitt, 2009; Ruiz et al., 2011b), but it is also more generally the case that relatively few marine invasions are reported from high latitude or polar regions of the world (Ruiz and Hewitt, 2009) as well as tropical regions (Ruiz et al., 2009a; Freestone et al., 2013).

The documented marine and estuarine NIS in North America are unevenly distributed among habitats. When considering invertebrates and algae, most NIS are restricted to bays and estuaries, and very few NIS occur on the more exposed outer coasts (Wasson et al., 2005; Ruiz et al., 2009b). Those on outer coasts are also known from bays and estuaries, indicating that the latter are the focal point for invasions. In addition, while these NIS occur across a wide range of habitats, the majority are associated with hard substrata for some portion of their life histories (Ruiz et al., 2009b). This latter distribution has implications in considering the mechanisms of introduction, as discussed below.

As with taxonomic and temporal patterns, some caution is required in interpreting the cause of observed spatial and habitat distributions for NIS. In general, there are three general hypotheses that may explain these each of these patterns, including (a) biases in the data, due to differences in search effort, taxonomic knowledge, or biogeographic information, (b) differences in propagule supply, such as the numbers or sources of NIS, concentrations delivered, frequency or duration of introductions, physiological condition of propagules and (c) differences in susceptibility to invasion, resulting from biological and environmental resistance. There is a considerable and growing literature that explores these various hypotheses and associated mechanisms (Ruiz et al., 2000a, 2011b; Fofonoff et al., 2009; Briski et al., 2012; Wonham et al., 2013). All three of these contribute to the observed patterns, but there is uncertainty about the relative importance of each.

This study provides a retrospective analysis of historical data, and we wish to underscore that invasion processes are dynamic, such that future patterns may deviate from those observed to date, especially when considering geographic and habitat distributions. In particular, some component of differences among coasts and latitudes reflect historical trade patterns, which are undergoing changes that affect propagule delivery characteristics. For example, both the Panama Canal and Suez Canal are undergoing major expansions, which are scheduled for completion in 2015–2016 and are expected to significantly alter the dynamics of global shipping and propagule supply (Ruiz et al., 2009a; Galil et al., 2015; Muirhead et al., 2015). On a longer time horizon, shipping and other human activities are expected to expand greatly in the Arctic, which will further alter global trade routes and propagule delivery patterns (Ruiz and Hewitt, 2009; Miller and Ruiz, 2014). These changes will affect greatly the future patterns of invasions across coasts and latitudes, if variation in propagule delivery (b, above) has contributed strongly to historical patterns of invasion. Moreover, expansion of Arctic shipping and other activities are a response to retreating sea ice under climate change, which itself can alter the susceptibility to invasions (c, above; see Hellman et al., 2008).

It is also possible that invasion to outer coast habitats may change in the future, as a consequence of infrastructure development associated with mineral extraction, wind and wave energy, aquaculture, and marine terminals. This may result from any combination of increased propagule supply and increased susceptibility (Lonsdale, 1999; Wasson et al., 2005; Glasby et al., 2007; Ruiz et al., 2009b). Specifically, increased site-based activities offshore may increase propagule delivery, and especially propagule from other offshore regions that serve to increase habitat matching. Increased infrastructure in the form of artificial structure may also create more suitable substrata for colonization and spread of NIS, compared to natural substrata. A further consequence of an increase in offshore human activities may be increases in physical disturbance or chemical pollution, which it thought to increase susceptibility to invasions (Ruiz et al., 1999; Piola and Johnston, 2008).

Vector strength

Our analyses of vector strength at the continental scale for North America provide an update of a previous study Fofonoff et al. (2003). Although the total number of NIS has increased greatly in our current analyses, the overall pattern and conclusions are largely unchanged: (a) shipping has been historically a dominant source of invasions for the initial introduction to North America, (b) the relative importance (strength) of shipping has increased over time and (c) ballast water and hull biofouling each have contributed strongly to this signal, but the relative importance of these two vectors is not clear. Within North America, similar results have been reported also at regional and local scales (Cohen and Carlton, 1995; Fofonoff et al., 2009; Ruiz et al., 2011b; Williams et al., 2013).

While we have focused on the initial introduction into North America, it is also important to recognize that many (if not most) species spread coastwise, following this initial introduction (Ruiz et al., 2011b; NEMESIS 2014). Given that most occurrences are in bays and estuaries, and that many NIS are unlikely to disperse on their own over such distances, human-aided dispersal is implicated in the spread of many such species. Although commercial ships may contribute to this coastwise (secondary) spread in North America and elsewhere, there is increasing evidence that small recreational and fishing vessels may play a significant role in this regard (Murray et al., 2011, 2014; Ashton et al., 2014; Zabin et al., 2014).

Vector management: Ballast water

On a global scale, ships' ballast water has been a major focus of management and policy to reduce the rate of new coastal invasions. This has resulted from an understanding of the role of ships in driving increased invasions and also the occurrence of several high-impact invasions that had significant economic and health effects, including the zebra mussel invasion of North America and toxic dinoflagellates in Australia (National Research Council [NRC], 1996). Ballast water management gained momentum in the 1980s, advancing at international, national, and regional (including state and provincial) levels. The history, status, and effectiveness of both management and policy are the focus of many articles over the past several decades. This landscape is still highly dynamic and continues to evolve in a punctuated fashion, driven by new regulations that emerge in different global regions.

This evolution is illustrated by the history of ballast water management in the United States that was initiated in the 1980s, resulting in a stepwise series of regulations at national, regional, and state levels (for reviews, see NRC 1996, 2008, 2011; Albert et al., 2013). A primary focus has been on reducing the concentration of organisms delivered in ballast water, especially by ships that arrive with water from overseas sources, although there is also some effort to accomplish this for coastwise traffic in some regions. The rationale is that reducing the concentration of organisms from other coastal areas will reduce the number of new invasions to U.S. coasts, especially surrounding bays and estuaries (and ports) where shipping is concentrated, because the probability of establishment is density-dependent.

At the present time, ships that arrive to the U.S. with ballast water from overseas (outside the U.S. and Canada) are required to manage this water in one of multiple ways, including: (a) retain ballast water on board with no discharge, (b) undertake ballast water exchange (BWE), by flushing tanks in open-ocean ≥200 nautical miles from shore, to reduce concentrations of coastal organisms or (c) use an approved treatment technology. Recent studies indicate that BWE routinely can remove 88–99% of the original coastal water and planktonic organisms, when conducted properly (Ruiz and Reid, 2007; Bailey et al., 2011; Simard et al., 2011), but residual coastal organisms are still present. In addition, there are some routes and safety conditions that do now allow BWE in open-ocean, as discussed below.

Most ballast water discharged to the U.S. from overseas sources is now treated by BWE, as a result of regulations. For example, based on required reporting by vessels to U.S. Coast Guard, 119.6 million metric tons (MT) of ballast water was discharged to the U.S. from overseas sources in 2012, and 101.6 million MT (85%) was treated with BWE (Minton et al., 2013). This discharge differed among coasts in several respects (Figure 8). First, most (54%) of the total was discharged to the Gulf Coast. Second, the use of BWE was lowest on the Gulf Coast (80.5% of total volume) compared to the East Coast and West Coast (89.8% and 93.7%, respectively). Moreover, the use of BWE appears relatively stable since at least 2005, as a percentage of total volume discharged at a national level and for the individual coasts (Miller et al., 2011), suggesting widespread application of this management strategy for the past 10 years.

Figure 8.

Ballast water discharged from overseas sources arriving to the continental U.S. in 2013. Shown for each coast is the total volume discharge that was treated (black) and untreated (grey) with BWE. (Data from Minton et al., 2013.)

Figure 8.

Ballast water discharged from overseas sources arriving to the continental U.S. in 2013. Shown for each coast is the total volume discharge that was treated (black) and untreated (grey) with BWE. (Data from Minton et al., 2013.)

As Miller et al. (2011) point out, the source regions and voyage routes constrain opportunities for BWE by some vessels arriving to the U.S. Gulf Coast. In particular, the Gulf Coast receives a relatively large fraction of overseas vessel traffic and ballast water from the Americas, compared to the West Coast. Many vessels on this Pan American route do not have sufficient time or opportunity to conduct BWE at open-ocean, as they are often close to land, in contrast to transoceanic vessel routes. As a result, many of these vessels forgo BWE, and others performed BWE closer (<200 miles) to shore than desired.

Due partly to constraints of voyage routes and safety for using BWE, ballast water treatment is transitioning to treatment technologies that can be applied more broadly to most (if not all) vessels. In addition, even where feasible, there is uncertainty about the level of efficacy for BWE. While there is no doubt that BWE reduces the probability of invasions and is reducing the number of new invasions, there is uncertainty about the magnitude of this reduction and the latent risk (likelihood) of new invasions that remains. This uncertainty exists because (a) the exact shape of the quantitative relationship between propagule supply and invasion outcome is not known (NRC, 2011; Wonham et al., 2013) and (b) the actual response of invasion rate to BWE is poorly resolved, due to uneven measures over time and lag-times in reporting (see previous sections). Treatment technologies are expected to meet particular discharge standards for organism concentrations, which are often lower than the levels achieved by BWE and are expected to further reduce invasion probability (Minton et al., 2005).

Ships that discharge ballast water from overseas to the U.S. are required currently to meet specific discharge standards to be phased-in on a defined timetable, as specified in recently-adopted national regulations (United States Department of Homeland Security, 2012; United States Environmental Protection Agency, 2013). In the future, this will have the effect of decreasing propagule supply per volume of ballast water discharged, compared to today, but some uncertainty remains about the impact of these standards on invasion dynamics for three reasons. First, despite a specified timetable for implementation, it is not clear the extent to which existing technologies can meet consistently the required discharge standards. For example, there are no technologies that have received approval for use in the U.S. as meeting the standards. Second, once technologies are approved, it will take additional time to install treatment systems on the fleet of commercial ships that visit U.S. waters from overseas. Finally, when fully implemented, the efficacy of discharge standards is not known. While it is clear that treatment technologies (with discharge standards) will reduce the future number of ballast-mediated invasions beyond the current situation (with BWE), the residual rate of new invasions under this scenario is not yet known and should be expected to vary in space and time, especially given climate change and other forces (e.g. disturbances, pollutants, and habitat modification at local to regional scales) that can modify existing environmental conditions and susceptibility to invasions.

Due to the complex nature and uncertainty of invasion dynamics, understanding the efficacy of ballast water management requires an adaptive approach and framework for examining changes over time. While a variety of approaches can be considered to predict or estimate the likely outcome of current and future management strategies (NRC, 2011), only direct measures of invasion rates over time can provide confidence and demonstrate that expected outcomes are achieved (Ruiz and Carlton, 2003). This argues for repeated measures of the number of new NIS over time, as the key dependent variable and ultimate measure of efficacy.

Vector management: Hull biofouling

Despite a similar historical magnitude and temporal increase of vector strength for both hull biofouling and ballast water (Figure 7), only the latter has been a focus of substantial vector management activities to date. There have been significant economic incentives in play for a long time to reduce vessel biofouling, due the drag and associated increases in fuel consumption and travel time (Schultz et al., 2011). This has resulted in widespread use of various coatings and hull husbandry practices, which have undoubtedly served also to reduce the scale of NIS transfers through time. However, a key point is that biofouling is not being managed as a vector, with a goal for reducing invasions, but to reduce drag. There are still large numbers of NIS transferred even with existing economic incentives, especially in “niche areas” (e.g. rudders, intakes, thrusters) that often do not affect drag (Minchin and Gollasch, 2003; Coutts and Taylor, 2004; Davidson et al., 2009), and hull biofouling remains a dominant vector for invasions around the globe.

On an international scale, the International Maritime Organization only recently adopted voluntary guidelines for managing hull biofouling as a vector (International Maritime Organization, 2011), and most countries have no regulations that limit the extent of biofouling or NIS associated with arriving commercial vessels. For example, we are not aware of any regulations or restrictions for biofouling on commercial vessels (or recreational, fishing, military, or other types of vessels) for U.S. ports or jurisdictions, with one exception: the Northwestern Hawaiian Islands Marine National Monument prohibits release of NIS associated with vessels (United States Department of Commerce and United States Department of Interior, 2006). In addition, the state of California now requires reporting on hull husbandry practices, and several western U.S. states are considering possible regulations for hull biofouling (Scianni et al., 2013).

By comparison, management of the ballast water vector began with voluntary guidelines at both the national and international levels over 20 years ago, eventually becoming mandatory requirements in some regions that have continued to evolve in stepwise fashion under multiple regulations (NRC, 1996, 2011). It appears that management of the hull biofouling vector has begun a similar trajectory, but it is currently not possible to predict the rate and extent of implementation for any future requirements for commercial or other types of vessels. Nonetheless, even if ballast water management continues to advance and has a high efficacy in reducing new invasions, it is evident that a substantial ship-mediated influx on NIS will continue to occur unless effective management of the hull biofouling vector also occurs.

Conclusions

Understanding of biological invasions in coastal marine ecosystems has advanced greatly in the past three decades, due to a substantial body of scientific research (see References and citations therein; see also Bailey, 2015). While there is still uncertainty about the full extent of invasions and vector strength, we do have minimum estimates that underscore the importance of commercial shipping as the source of many initial introductions to a geographic region. In particular, ballast water and hull biofouling are known to be dominant vectors, driving the observed increases in new invasions over time in North America and other global regions. Moreover, the general operation of these vectors is also understood, in terms of (a) the types and abundances of organisms that are delivered and (b) processes that lead to NIS establishment.

For ballast water, this understanding has been applied to a truly global-scale campaign in vector management, with regulations and requirements advancing in a step-wise and punctuated fashion. Due to existing information gaps, the expected magnitude of reduction in new invasions (i.e. efficacy) is not known under current or future conditions. Understanding the actual efficacy of ballast water management requires field-based measures that are designed to detect new NIS occurrences and assess the extent to which this vector is still contributing to vector strength.

In contrast, a similar campaign has not emerged for the hull biofouling vector, despite clear evidence that this is a major driver of new NIS incursions and has vector strength on par with ballast water. Only recently is there some effort to focus on management of hull biofouling, albeit with voluntary guidelines. There is currently an uncertain path or rate for implementation of management and policies surrounding this vector. The different timelines for management of ballast water versus hull biofouling underscores the operation of a single vector management approach that exists today that can result in very different and uneven outcomes, independent of the relative importance (both in number of NIS and their impacts). Moreover, this dichotomy reflects political decisions based on past historical events, over 20 years ago, and may not be nimble in reflecting changes in vector operation or importance through time.

Recognizing that many different vectors contribute to invasions, and that the these are changing in space and time, Williams et al. (2013) have suggested that a multi-vector approach would be a much more effective and robust strategy to minimize the occurrence and impacts of future invasions. Such an approach should evaluate the operation and relative strength of existing vectors, as well as management strategies surrounding these, including both shipping and non-shipping transfer mechanisms. Moreover, this approach should be dynamic, to consider changes in the vector magnitude and operation as well as emergence of new vectors. Such a dynamic, multi-vector approach differs significantly from the current consideration of single vectors in isolation.

Finally, while our analysis has focused on invasion dynamics in coastal ecosystems of North America, it has broad relevance to many other global regions. First, we use a model system and approach to explore the current state of knowledge about invasion dynamics in coastal ecosystems. Second, we summarize the current operation and management for both ballast water and hull biofouling, two dominant vectors for marine invasions throughout the world. This synthesis provides a relevant background to evaluate and manage coastal marine invasions in any region, including especially tropical latitudes, which have received relatively little analysis compared to temperate regions (Ruiz and Hewitt, 2009; Freestone et al., 2013). Within tropical regions, locations with high levels of shipping activity warrant significant attention, given the potential magnitude of ship-mediate species transfers. Moreover, those regions that export bulk commodities (e.g. oil, coal, minerals, grains, and wood) may receive the greatest level of species transfers, due to the delivery of ballast water by arriving vessels, because (a) tankers and bulk cargo vessels deliver the greatest volumes of ballast water among vessels and (b) their discharge occurs primarily at export locations (Miller et al., 2011; Minton et al., 2013; Muirhead et al., 2015). We hope this article will provide a useful background to consider invasion dynamics and management in tropical systems and elsewhere.

Acknowledgements

We thank Gail Ashton, Ian Davidson, Richard Everett, A. Whitman Miller, Mark Minton and Chela Zabin for discussions on aspects of marine invasions and shipping. We also thank the Sultunate of Oman for the opportunity to contribute this article to the international conference on marine invasive species.

Funding

This research was supported by funding from the California Department of Fish and Wildlife, National Sea Grant Program and Smithsonian Institution. Updating information in NEMESIS was made possible through additional research applications sponsored by U.S. Coast Guard.

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