Relative Invasion Risk for Plankton across Marine and Freshwater Systems: Examining Efficacy of Proposed International Ballast Water Discharge Standards

Understanding the implications of different management strategies is necessary to identify best conservation trajectories for ecosystems exposed to anthropogenic stressors. For example, science-based risk assessments at large scales are needed to understand efficacy of different vector management approaches aimed at preventing biological invasions associated with commercial shipping. We conducted a landscape-scale analysis to examine the relative invasion risk of ballast water discharges among different shipping pathways (e.g., Transoceanic, Coastal or Domestic), ecosystems (e.g., freshwater, brackish and marine), and timescales (annual and per discharge event) under current and future management regimes. The arrival and survival potential of nonindigenous species (NIS) was estimated based on directional shipping networks and their associated propagule pressure, environmental similarity between donor-recipient ecosystems (based on salinity and temperature), and effects of current and future management strategies (i.e., ballast water exchange and treatment to meet proposed international biological discharge standards). Our findings show that current requirements for ballast water exchange effectively reduce invasion risk to freshwater ecosystems but are less protective of marine ecosystems because of greater environmental mismatch between source (oceanic) and recipient (freshwater) ecoregions. Future requirements for ballast water treatment are expected to reduce risk of zooplankton NIS introductions across ecosystem types but are expected to be less effective in reducing risk of phytoplankton NIS. This large-scale risk assessment across heterogeneous ecosystems represents a major step towards understanding the likelihood of invasion in relation to shipping networks, the relative efficacy of different invasion management regimes and seizing opportunities to reduce the ecological and economic implications of biological invasions.     

Domestic ships as a potential pathway of nonindigenous species from the Saint Lawrence River to the Great Lakes

Ballast water moved by transoceanic vessels has been recognized globally as a predominant vector for the introduction of aquatic nonindigenous species (NIS). In contrast, domestic ships operating within confined geographic areas have been viewed as low risk for invasions, and are exempt from regulation in consequence. We examined if the St. Lawrence River could serve as a source of NIS for the Laurentian Great Lakes by surveying ballast water carried by domestic vessels and comparing biological composition in predominant St. Lawrence River—Great Lakes port-pairs in order to determine the likelihood that NIS could be transported to, and survive in, the Great Lakes. Thirteen potential invaders were sampled from ballast water, while 26 taxa sampled from St. Lawrence River ports are not reported from the Great Lakes. The majority of NIS recorded in samples are marine species with low potential for survival in the Great Lakes, however two euryhaline species (copepod Oithona similis, and amphipod Gammarus palustris) and two taxa reported from brackish waters (copepod Microsetella norvegica and decapod Cancer irroratus) may pose a risk for invasion. In addition, four marine NIS were collected in freshwater samples indicating that at least a subset of marine species have potential as new invaders to the Great Lakes. Based on results from this study, the ports of Montreal, Sorel, Tracy and Trois Rivières appear to pose the highest risk for new ballast-mediated NIS from the St. Lawrence River to the Great Lakes.     

Supply-side invasion ecology: characterizing propagule pressure in coastal ecosystems

The observed rates and deleterious impacts of biological invasions have caused significant alarm in recent years, driving efforts to reduce the risk (establishment) of new introductions. Characterizing the supply of propagules is key to understanding invasion risk and developing effective management strategies. In coastal ecosystems, ships' ballast water is an important transfer mechanism (vector) for marine and freshwater species. Commercial ships exhibit a high degree of variation in ballast water operations that affect both the quantity and quality of propagule supply, and thereby invasion risk. The per-ship inoculation size from ballast water depends upon both the volume discharged and the organism density. Moreover, propagule quality will vary among source regions (ports) and voyage routes, due to differences in species composition and transport conditions, respectively. We show that significant differences exist in (i) the frequency and volume of ballast water discharge among vessel types, (ii) the frequency of vessel types and routes (source regions) among recipient ports, and (iii) the transit success (survivorship) of zooplankton in ballast tanks among voyage routes. Thus, propagule supply is not a simple function of total ship arrivals. For ships, as well as other vectors, variation in propagule quantity and quality must be explicitly considered to estimate invasion risk and advance predictive ability.     

Salinity tolerance of Great Lakes invaders

1. The Laurentian Great Lakes are among the most invaded freshwater ecosystems in the world. Historically, the major vector for the introduction of non‐indigenous species (NIS) has been the release of contaminated ballast water via transoceanic ships. Despite regulations implemented in 1993, requiring vessels carrying fresh ballast water to exchange this water with saline ocean water, new reports of invasions have continued. 2. NIS often have a wide environmental tolerance allowing them to adapt to and invade a variety of habitats. It has been hypothesized that NIS with broad salinity tolerance may be able to survive ballast water exchange (BWE) and continue to pose an invasion risk to the Great Lakes. 3. We tested the short‐term salinity tolerance of eight recent invaders to the Great Lakes, specifically three cladocera (Bosmina coregoni, Bythotrephes longimanus, Cercopagis pengoi), two molluscs (Dreissena polymorpha, Dreissena rostriformis bugensis), and one species each of the families Gammaridae, Mysidae and Gobidae (Echinogammarus ischnus, Hemimysis anomala, Neogobius melanostomus) to determine if they could have survived salinities associated with BWE. 4. Overall, short‐term exposure to highly saline water dramatically reduced survival of all species. Two different methods of BWE tested, simultaneous and sequential, were equally effective in reducing survival. Species that survived the longest in highly saline water either possess behavioural characteristics that reduce exposure to adverse environments (valve closure; both Dreissena species) or are reported to have some degree of salinity tolerance in their native region (Echinogammarus). Given that exposure in our trials lasted a maximum of 48 h, and that species in ballast tanks would typically be exposed to saline water for c. 5 days, it appears that BWE is an effective method to reduce the survival of these NIS. These results provide impetus for tightening policy and monitoring of BWE, in particular for ships entering the Great Lakes from freshwater ports.     

Efficacy of ‘saltwater flushing’ in protecting the Great Lakes from biological invasions by invertebrate eggs in ships’ ballast sediment

1. Mid‐ocean exchange and saltwater flushing were implemented as management practices to reduce the likelihood of new biological invasions in the Laurentian Great Lakes associated with ships’ ballast water and sediments. Despite this, there has been no formal assessment of the efficacy of these procedures. Here, we conduct a comparative analysis of community composition of dormant taxa transported by ballast sediment before and after regulations came into effect in 2006. 2. Ballast sediment samples were collected from 17 ships during the post‐regulation interval of 2007 and 2008. Invertebrate eggs were counted, hatched and species identified in the laboratory. Results were compared to similar samples collected from 39 ships between 2000 and 2002, prior to implementation of saltwater flushing regulations. 3. The estimated amount of residual ballast sediment transported by vessels was significantly lower during the post‐regulation period, ranging from <1 to 45 tonnes per ship, with an average of 5 tonnes. Mean density and number of dormant viable eggs per ship declined 91 and 81%, respectively. 4. Community composition also changed through time, with Rotifera accounting for 78% of taxa transported prior to regulation, whereas Cladocera and Copepoda each accounted for 38% of abundance post‐regulation. Although the number of non‐indigenous species (NIS) declined 73% per ship after 2006, the reduction was not statistically significant; however, the number of freshwater NIS – which pose the greatest risk of invasion for the Great Lakes – was significantly lowered. 5. Our comparative analysis suggests that ballast management regulations enacted in 2006 markedly reduced the probability of introduction of NIS via dormant eggs carried in ballast sediments.     

Is vessel hull fouling an invasion threat to the Great Lakes?

Aim  Hull fouling is a leading vector for the introduction of marine, non‐indigenous species (NIS) worldwide, yet its importance to freshwater habitats is poorly understood. We aimed to establish the complement of NIS transported via this vector to the Great Lakes and to determine if they pose an invasion risk. Location  Laurentian Great Lakes. Methods  During 2007 and 2008, we collected scrapings from exterior surfaces as well as underwater video‐transects from 20 vessels shortly after their arrival in Great Lakes’ ports. Invertebrates present were sorted and identified in the laboratory. Results  Total estimated abundance averaged > 170,000 invertebrates per ship belonging to 109 taxa. Most (72%) of these taxa were freshwater species already present in the Great Lakes, whereas 11 and 31% were native to estuarine and marine habitats respectively, and would not be expected to survive in this habitat. Abundance was dominated by barnacles (51%), cladocerans (19%), bivalves (12%) and amphipods (11%). Sea‐chest grating and the rudder were hot‐spots for biofouling. Invertebrate diversity and total abundance were positively associated with total time spent in port during the last year and time in Pacific South American ports and negatively related to time in high latitudes and sailing speed. Although we found some live, established invaders such as Gammarus tigrinus and Dreissena rostriformis bugensis, only one individual of a freshwater NIS (Alexandrovia onegensis, Oligochaeta) not yet reported in the Great Lakes was detected. The animal’s poor condition and seemingly low population abundance indicated the risk of live introduction by this vector was likely quite low. Main conclusion  Our results indicate that hull fouling appears to pose a low risk of introductions of new species capable of surviving in the Great Lakes, unlike foreign‐sourced freshwater ballast water that historically was discharged by these transoceanic vessels.     

Population attenuation in zooplankton communities during transoceanic transfer in ballast water

Successful biological invasion requires introduction of a viable population of a nonindigenous species (NIS). Rarely have ecologists assessed changes in populations while entrained in invasion pathways. Here, we investigate how zooplankton communities resident in ballast water change during transoceanic voyages. We used next‐generation sequencing technology to sequence a nuclear small subunit ribosomal DNA fragment of zooplankton from ballast water during initial, middle, and final segments as a vessel transited between Canada and Brazil. Operational taxonomic unit (OTU) diversity decreased as voyage duration increased, indicating loss of community‐based genetic diversity and development of bottlenecks for zooplankton taxa prior to discharge of ballast water. On average, we observed 47, 26, and 24 OTUs in initial, middle, and final samples, respectively. Moreover, a comparison of genetic diversity within taxa indicated likely attenuation of OTUs in final relative to initial samples. Abundance of the most common taxa (copepods) declined in all final relative to initial samples. Some taxa (e.g., Copepoda) were represented by a high number of OTUs throughout the voyage, and thus had a high level of intraspecific genetic variation. It is not clear whether genotypes that were most successful in surviving transit in ballast water will be the most successful upon introduction to novel environments. This study highlights that population bottlenecks may be common prior to introduction of NIS to new ecosystems.     

Invasion risks posed by the aquarium trade and live fish markets on the Laurentian Great Lakes

International trade is an important mechanism for global non-indigenous species introductions, which have had profound impacts on the biodiversity of aquatic ecosystems including the Laurentian Great Lakes. The best-documented vector by which non-indigenous species have entered the Great Lakes is ballast water discharged by transoceanic ships. A variety of potential alternative vectors exist, including the intentional release of aquarium or food organisms. To assess whether these vectors pose a significant invasion risk for the Great Lakes, we surveyed fish sold live in markets and fish, mollusks and macrophytes sold in pet and aquarium stores within the Great Lakes watershed. We evaluated invasion risk using information on species’ thermal tolerance, history of invasion elsewhere, and potential propagule loads as indicated by frequency of occurrence in shops. Our research suggests that both the aquarium industry and live fish markets represent potential sources of future invaders to the Great Lakes, including several aquarium fishes and macrophytes, as well as Asian carp species sold in fish markets. Currently, few regulatory mechanisms exist to control these potential vectors.     

Assessing introduction risk using species’ rank-abundance distributions

Mixed-species assemblages are often unintentionally introduced into new ecosystems. Analysing how assemblage structure varies during transport may provide insights into how introduction risk changes before propagules are released. Characterization of introduction risk is typically based on assessments of colonization pressure (CP, the number of species transported) and total propagule pressure (total PP, the total abundance of propagules released) associated with an invasion vector. Generally, invasion potential following introduction increases with greater CP or total PP. Here, we extend these assessments using rank-abundance distributions to examine how CP : total PP relationships change temporally in ballast water of ocean-going ships. Rank-abundance distributions and CP : total PP patterns varied widely between trans-Atlantic and trans-Pacific voyages, with the latter appearing to pose a much lower risk than the former. Responses also differed by taxonomic group, with invertebrates experiencing losses mainly in total PP, while diatoms and dinoflagellates sustained losses mainly in CP. In certain cases, open-ocean ballast water exchange appeared to increase introduction risk by uptake of new species or supplementation of existing ones. Our study demonstrates that rank-abundance distributions provide new insights into the utility of CP and PP in characterizing introduction risk.     

Lake Superior: an invasion coldspot?

Lake Superior receives a disproportionate number of ballast water discharges from transoceanic ships operating on the Laurentian Great Lakes. Although this provides dispersal opportunities for nonindigenous species (NIS), relatively few NIS were initially discovered in this lake prior to being recorded elsewhere in the basin. A lack of NIS records from this lake may be an artefact of sampling bias. We tested this hypothesis by sampling benthos and plankton from littoral and deepwater habitats around the perimeter of Lake Superior during June and August 2001. Using morphological analysis techniques, we identified a total of 230 invertebrate taxa representing planktonic, benthic and nektonic lifestyles. Five species with invasion histories in the lower Great Lakes, the bivalves Sphaerium corneum, Pisidium amnicum and P. moitessierianum, gastropod Potamopyrgus antipodarum and amphipod Echinogammarus ischnus, were identified for the first time in Lake Superior. In addition, records of expanded distributions within this lake are presented for the amphipod Gammarus fasciatus and oligochaetes Ripistes parasita and Vejdovskyella intermedia. Recently introduced NIS in Lake Superior were found near international ports, implicating shipping as the vector of their introduction. Intrinsic physical-chemical aspects of Lake Superior may account for the scarcity of NIS in this lake as compared to the lower Great Lakes.     

Biosecurity risk factors presented by international vessels: a statistical analysis

Invasive non-indigenous species are among the greatest threats to global biodiversity. Shipping is the principal vector for international dispersal of nonindigenous species, and shipping rates are increasing globally. The Australian government performs a range of regulatory actions to mitigate biosecurity risks associated with marine vessels, and in so doing has amassed a large volume of operational inspection data. This data can be used to quantitatively examine risk factors of vessels failing biosecurity procedures after arriving from international ports, the nature of biosecurity failures, and the types and seizure rates of biosecurity risk material (BRM). Classification trees with gradient boosting were used to assess characteristics that predict high risk vessels (n = 93,006) for carrying BRM, across 7 years of inspection data. Undeclared vessels and suspected irregular entry vessels posed the highest risk, but both were rare. Vessels that visit infrequently (<20 visits in 7 years) were common and had almost three times greater odds of failing inspection than vessels visiting frequently. On statistical analysis, yachts appeared to pose less risk than commercial vessels. In operational terms, a tentative profiled 20% fraction would contain 57% of genuine failures, and the concomitant non-screened group would contain 82% of passes. The most common reason for inspection failures was ballast water non-compliance (2.53%) and plant or insect detections (1.77%); biofouling was less common (0.13%) but testing for biofouling is not exhaustive. Invertebrate species comprised almost 90% of invasive organisms detected and seized from vessels failing biosecurity inspections. This study targets an entire transportation vector, which includes many pathways. Understanding the characteristics of transport vectors is pivotal to characterising the risk of biological invasions and applying adequate controls and prevention strategies. Our results show that biosecurity risk is not uniform on maritime pathways, so there is considerable scope for biosecurity regulators to impose risk-based intervention.     

Marine introductions in the Shark Bay World Heritage Property, Western Australia: a preliminary assessment

The presence and impacts of non‐indigenous species (NIS) in marine areas of high conservation or World Heritage significance have rarely been examined. Case studies worldwide suggest that the potential exists for the introduction of NIS to significantly impact conservation values in regions conserved for the uniqueness and diversity of native assemblages. In this study, a preliminary investigation was conducted to provide information essential for managing marine introductions in the Shark Bay World Heritage Property. A focused fouling plate survey sampled a total of 112 encrusting taxa, of which 10 (11.2%) were classified as introduced and 10 others as cryptogenic. Eight introduced bryozoans: Aetea anguina (Linnaeus, 1758), Bugula neritina (Linnaeus, 1758), Bugula stolonifera Ryland, 1960, Conopeum seurati (Canu, 1928), Savignyella lafontii (Audouin, 1826), Schizoporella errata (Waters, 1878), Watersipora subtorquata (d’Orbigny, 1842) and Zoobotryon verticellatum della Chiaje, 1828; one tunicate, Styela plicata Lesueur, 1823; and an introduced hydroid, Obelia dichotoma (Linnaeus, 1758) were frequent, and in some cases dominant, components of encrusting communities. Of the 20 most frequently occurring species detected in the Bay, four were introduced and of the 20 species with highest average percent cover per plate, six were introduced. At one site, space occupation by NIS averaged 71.6% ± 7.4 of plate live cover. Space occupation by an individual NIS was as high as 62.4% of plate area (mean 7.82% ± 1.8). NIS were detected at sites lacking commercial traffic and ballast water discharge and isolated by distance and physical environment, suggesting that hull fouling of recreational craft may be the most important vector in the region. Seventy‐five percent of NIS detected in Shark Bay are established in Australian ports to the south of Shark Bay, while 33% are established to the north, tentatively implicating temperate affinity NIS and the movement of vessels from Australian ports south of Shark Bay as a greater risk to the region.     

Invasion Pressure to a Ballast-flooded Estuary and an Assessment of Inoculant Survival

The relationships between invasion pressure, post-transport inoculant survival, and regional susceptibility to invasion are poorly understood. In marine ecosystems, the movement and release of ballast water from ocean-going ships provides a model system by which to examine the interplay among these factors. One of the largest estuaries in North America, the Chesapeake Bay, receives tremendous amounts of foreign ballast water annually and thus should be at high invasion risk. To date, however, few introductions in Chesapeake Bay have been attributed to ballast release. To understand better the dynamics of this invasion process, we (1) characterized and quantified the biota arriving to Chesapeake Bay in foreign ballast water, (2) compared temperatures and salinities of ballast water and harbor water in upper Chesapeake Bay, and (3) tested experimentally survival of organisms collected from ballast water in temperatures and salinities characteristic of the region. From 1993 to 1994, we sampled planktonic and benthic organisms from 60 foreign vessels arriving to Chesapeake Bay. Our data show that the estuary is being inoculated by a diverse assemblage of aquatic organisms from around the world. Furthermore, the short transit time (15d) for most vessels ensured that substantial numbers of larval and post-larval organisms were being deballasted alive. Most of the ballast water discharged into the upper Chesapeake Bay, however, was significantly higher in salinity (>20) than that of the receiving harbor. In laboratory tolerance experiments, ballast water organisms perished under such conditions. Thus, a mismatch in physical conditions between donor and receiver regions may explain the dearth of invasions in the upper Bay. It is likely that the lower Chesapeake Bay, which is more saline, remains at higher risk to ballast water invasion. Recognition of such intraregional differences should allow more focused predictions for monitoring and management.     

Patterns of invasion in the Laurentian Great Lakes in relation to changes in vector activity

The Laurentian Great Lakes basin has been invaded by at least 182 non-indigenous species. A new invader is discovered every 28 weeks, which is the highest rate recorded for a freshwater ecosystem. Over the past century, invasions have occurred in phases linked to changes in the dominant vectors. The number of ship-vectored invaders recorded per decade is correlated with the intensity of vessel traffic within the basin. Ballast water release from ocean vessels is the putative vector for 65% of all invasions recorded since the opening of the St. Lawrence Seaway in 1959. As a preventive measure, ocean vessels have been required since 1993 to exchange their freshwater or estuarine ballast with highly saline ocean water prior to entering the Great Lakes. However, this procedure has not prevented ship-vectored species introductions. Most ships visiting the Great Lakes declare 'no ballast on board' (NOBOB) and are exempt from the regulation, even though they carry residual water that is discharged into the Great Lakes during their activities of off-loading inbound cargo and loading outbound cargo. Recently introduced species consist predominantly of benthic invertebrates with broad salinity tolerance. Such species are most likely to survive in a ballast tank following ballast water exchange, as well as transport in the residual water and tank sediments of NOBOB ships. Thus, the Great Lakes remain at risk of being invaded by dozens of euryhaline invertebrates that have spread into Eurasian ports from whence originates the bulk of foreign ships visiting the basin.     

Overview on introduced aquatic species in European navigational and adjacent waters

More than 1,000 non-indigenous aquatic species have been recorded, in total, from coastal Europe, i.e. navigational inland waterways for ocean-going vessels and adjacent water bodies in close proximity. Regions considered in this overview range from European Arctic waters to the Mediterranean Sea and Irish waters to the Black Sea. The majority of introduced taxa have been first recorded since the 1950s. Approximately 600 taxa (ranging from unicellular algae to vertebrates) are established with self-sustaining populations. The dominating group of exotic species across all seas is zoobenthos organisms. Introduction vectors are predominantly shipping (ballast water and hull fouling) and species movements for aquaculture or stocking purposes.     

The role of constructed reefs in non-indigenous species introductions and range expansions

Constructed reefs can contribute to non-indigenous species (NIS) introductions or range expansions in several ways. Reef materials that retain developed fouling communities or ballast, such as decommissioned petroleum platforms, inactive or derelict ships, and bridge rubble are potential NIS vectors. Habitat provided by reefs placed in areas devoid of natural hard bottom or structure may be colonized by NIS propagules dispersed from natural or anthropogenic sources. A network of reef structures may also create NIS corridors for linking previously unconnected areas. Due to its level of offshore habitat alteration, changing environmental conditions, volume of shipping and boating traffic, and subtropical location, the Gulf of Mexico may be particularly vulnerable to NIS introductions and has a number of documented NIS. Non-indigenous or invasive species concerns have delayed and increased costs for some recent reef construction projects. The linkages between NIS and constructed reefs are reviewed, and approaches for anticipating, assessing, and controlling introductions are recommended. Using basic information about NIS risks, reef planners can begin to evaluate unintended consequences and incorporate risk management measures to reduce future introductions. Prevention is the most effective risk reduction approach because controlling marine NIS after introduction is expensive and offers limited probability for success.     

Viability of invertebrate diapausing eggs exposed to saltwater: implications for Great Lakes’ ship ballast management

International shipping has been the dominant vector of nonindigenous species introductions to the Laurentian Great Lakes over the past century. Apparent ballast-mediated invasions have been recorded in recent years, despite the implementation of voluntary ballast water exchange regulations in 1989. Since unregulated no-ballast-on-board vessels currently dominate inbound traffic to the Great Lakes, it has been proposed that live or dormant organisms contained in residual ballast of these vessels may be partially responsible for recent invasions. Alternatively, euryhaline species may pose a significant invasion threat because they can potentially survive ballast exchange. In this study, we explored whether exposure to open-ocean water (32) reduced the viability of invertebrate diapausing eggs in ballast sediments. Sediments collected from three transoceanic ships and from three freshwater habitats were exposed to open-ocean seawater. Egg viability, assessed as the abundance of taxa hatched between exposed and unexposed sediments, was not affected by saltwater exposure in any experiment. Species richness of hatched diapausing eggs was reduced by saltwater exposure in only one of seven trials. Our results indicate that oligostenohaline zooplankton may pose an invasion risk because their diapausing eggs are largely resistant to exposure to open-ocean saltwater.     

In situ hatching of invertebrate diapausing eggs from ships' ballast sediment

Ships that enter the Great Lakes laden with cargo carry only residual ballast water and sediment in ballast tanks. These ships are designated ‘no ballast on board’ (NOBOB) and constitute > 90% of inbound traffic. We conducted in situ experiments using emergence traps to assess the viability and the introduction potential of invertebrate diapausing stages present in ships’ ballast sediment. All trials commenced while vessels operated on the lower lakes (Erie, Ontario) and were completed 6–11 days later at ports on the upper lakes (Michigan, Lake Superior). Eight trials were conducted on four ships using five different ballast sediments. Hatching was observed on every ship, although not from all sediments on all ships. Overall hatch rates were very low (0.5 individuals per 500 g sediment), typically involving activation of < 0.05% of total eggs present. Five species of rotifers and copepod nauplii were hatched from ballast sediments, although only one or two species typically hatched from any one sediment. Results of this study indicate that hatching of diapausing eggs contained in ballast sediment of NOBOB ships poses a relatively low risk of invasion to the Great Lakes. However, as reproduction may occur in tanks, and non‐indigenous species may be involved in numerous introduction events, the risk posed by this vector is small but potentially important. While dormancy is a characteristic enabling enhanced survival during transportation in ballast tanks, it becomes a hindrance for introduction.