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.     

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.     

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.     

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.     

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.     

A Spatial Modeling Approach to Predicting the Secondary Spread of Invasive Species Due to Ballast Water Discharge

Ballast water in ships is an important contributor to the secondary spread of invasive species in the Laurentian Great Lakes. Here, we use a model previously created to determine the role ballast water management has played in the secondary spread of viral hemorrhagic septicemia virus (VHSV) to identify the future spread of one current and two potential invasive species in the Great Lakes, the Eurasian Ruffe (Gymnocephalus cernuus), killer shrimp (Dikerogammarus villosus), and golden mussel (Limnoperna fortunei), respectively. Model predictions for Eurasian Ruffe have been used to direct surveillance efforts within the Great Lakes and DNA evidence of ruffe presence was recently reported from one of three high risk port localities identified by our model. Predictions made for killer shrimp and golden mussel suggest that these two species have the potential to become rapidly widespread if introduced to the Great Lakes, reinforcing the need for proactive ballast water management. The model used here is flexible enough to be applied to any species capable of being spread by ballast water in marine or freshwater 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.     

Transoceanic ships as vectors for nonindigenous freshwater bryozoans

Aim The transport of organisms in ships’ ballast tanks is a dominant vector for aquatic invasions worldwide. Until recently, efforts to manage this vector have overlooked the potential transport of invertebrate resting stages in the residual waters and sediments within emptied ballast tanks, i.e. NOBOB (‘No Ballast On Board’) tanks. The resting stages (statoblasts) of freshwater bryozoans are often buoyant and locally abundant and thus can be taken up easily during ballasting operations. They are also resistant to extreme environmental conditions and can generate new colonies after being dormant for decades; as such, they would likely remain viable propagules after lengthy transport in ship ballast tanks. This study quantified the occurrence of freshwater bryozoan statoblasts in ballast tank sediments of transoceanic ships. Location North American Great Lakes. Methods We quantified the frequency of occurrence, abundance and diversity of bryozoans (as statoblasts) in residual sediment samples taken from 51 NOBOB tanks of 33 transoceanic ships visiting the Great Lakes from 2000 to 2002. Results Our study identified 11 species, comprising nearly 12% of the total number of freshwater bryozoans known worldwide. These include two exotic species unrecorded in the Great Lakes (Fredericella sultana and Lophopus crystallinus), an exotic species already established in the region (Lophopodella carteri) and three cosmopolitan species (Plumatella casmiana, P. fungosa and P. repens). Our estimates suggest that a ship with NOBOB tanks may carry up to 10⁶ statoblasts. Main conclusions The discovery of species unrecorded in the Great Lakes and the potentially large numbers of statoblasts being transported in ship ballast tanks indicate a significant risk of new species introductions. Furthermore, the presence of cosmopolitan species and an exotic species already established in the Great Lakes suggests the strong possibility of cryptic invasions via the introduction of exotic genotypes.     

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.     

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.     

Dynamics and short-term survival of toxic cyanobacteria species in ballast water from NOBOB vessels transiting the Great Lakes—implications for HAB invasions

We measured the presence, viability and potential toxicity of cyanobacteria in ships’ ballast tanks during three domestic voyages through the North American Great Lakes. Using molecular methods, the toxin-producing forms of Microcystis and Anabaena were monitored in ballast water after ships’ ballast tanks were filled at their first port of call, and at subsequent ports as ships transited the Great Lakes. Microcystis was detected in ballast water at intermediate and final ports of call in all three experiments, but the presence of Anabaena was more variable, suggesting low abundance or patchy distribution in ballast tanks. Both species were detected in ballast water up to 11 days old. Detection of the microcystin synthetase gene, mcyE, in ballast tanks indicated entrained cells were capable of producing microcystin, and further analyses of RNA indicated the toxin was being expressed by Microcystis, even after 11 days in dark transit. These data demonstrate within-basin transport and delivery of planktonic harmful algal bloom (HAB) species to distant ports in the world's largest freshwater reservoir, with potential implications for drinking water quality. These implications are discussed with respect to management of microbial invasions and the fate of introduced phytoplankton in their receiving environment.     

Population genetic structure of the round goby in Lake Michigan: implications for dispersal of invasive species

Understanding subsequent dispersal of non-native species following introduction is important for predicting the extent and speed of range expansion and is critical for effective management and risk assessment. Post-introduction dispersal may occur naturally or via human transport, but assessing the relative contribution of each is difficult for many organisms. Here, we use data from seven microsatellite markers to study patterns of dispersal and gene flow among 12 pierhead populations of the round goby (Neogobius melanostomus) in Lake Michigan. We find significant population structure among sampling sites within this single Great Lake: (1) numerous populations exhibited significant pairwise F _ST and (2) a Bayesian assignment analysis revealed three distinct genetic clusters, corresponding to different pierhead locations, and genetic admixture between these clusters in the remaining populations. Genetic differentiation (F _ST) is generally related to geographic distance (i.e., isolation by distance), but is periodically interrupted at the scale of Lake Michigan due to gene flow among geographically distant sites. Moreover, average genetic differentiation among populations exhibit a significant, negative correlation with the amount of shipping cargo at ports. Our results, therefore, provide evidence that genetic structure of the round goby in Lake Michigan results from limited natural dispersal with frequent long-distance dispersal through anthropogenic activities such as commercial shipping. Our study suggests that while round gobies can undoubtedly disperse and found new populations through natural dispersal mechanisms, their spread within and among the Great Lakes is likely aided by transport via ships. We, therefore, recommend that ballast-water treatment and management may limit the spread of non-native species within the Great Lakes after the initial introduction in addition to preventing the introduction of non-native species to the Great Lakes.     

Straddling the divide: invasive aquatic species in Illinois and movement between the Great Lakes and Mississippi basins

The Laurentian Great Lakes and the Mississippi River are two of the largest freshwater ecosystems in North America, and each contains large numbers of non-native species. In 1900 the Great Lakes and Mississippi were permanently connected with the opening of the Chicago Sanitary and Ship Canal in the US state of Illinois. More recently, movement of trailered boats, bait, and other overland vectors have increased and further enabled movement of non-native aquatic species. To investigate the role of Illinois in continent-wide species spread we assembled a comprehensive database of recorded occurrences of aquatic non-native species in Illinois inland waters. For each species we determined vector, location, current stage in the invasion sequence (introduced or established), and ecological impacts. The arrival of non-native species has accelerated over time. Sixty species are now established, and a further 39 have been recorded. The Great Lakes have been a stronger source of species to Illinois and the Mississippi River basin than the reverse. Over the last two decades the most important vectors delivering non-native aquatic species have been unintentional release and shipping. Through a survey of Illinois aquatic ecologists we found that established species exhibit a continuous range of ecological impacts and that almost a third have high or very high ecological impacts. Local, national, and continental approaches will be required to mitigate the threat of further invasive species spreading into Illinois and between the Great Lakes and Mississippi basins.     

Modelling the Arrival of Invasive Organisms via the International Marine Shipping Network: A Khapra Beetle Study

Species can sometimes spread significant distances beyond their natural dispersal ability by anthropogenic means. International shipping routes and the transport of shipping containers, in particular are a commonly recognised pathway for the introduction of invasive species. Species can gain access to a shipping container and remain inside, hidden and undetected for long periods. Currently, government biosecurity agencies charged with intercepting and removing these invasive species when they arrive to a county's border only assess the most immediate point of loading in evaluating a shipping container's risk profile. However, an invasive species could have infested a container previous to this point and travelled undetected before arriving at the border. To assess arrival risk for an invasive species requires analysing the international shipping network in order to identify the most likely source countries and the domestic ports of entry where the species is likely to arrive. We analysed an international shipping network and generated pathway simulations using a first-order Markov chain model to identify possible source ports and countries for the arrival of Khapra beetle (Trogoderma granarium) to Australia. We found Kaohsiung (Taiwan) and Busan (Republic of Korea) to be the most likely sources for Khapra beetle arrival, while the port of Melbourne was the most likely point of entry to Australia. Sensitivity analysis revealed significant stability in the rankings of foreign and Australian ports. This methodology provides a reliable modelling tool to identify and rank possible sources for an invasive species that could arrive at some time in the future. Such model outputs can be used by biosecurity agencies concerned with inspecting incoming shipping containers and wishing to optimise their inspection protocols.     

Molecular detection of invasive species in heterogeneous mixtures using a microfluidic carbon nanotube platform

Screening methods to prevent introductions of invasive species are critical for the protection of environmental and economic benefits provided by native species and uninvaded ecosystems. Coastal ecosystems worldwide remain vulnerable to damage from aquatic species introductions, particularly via ballast water discharge from ships. Because current ballast management practices are not completely effective, rapid and sensitive screening methods are needed for on-site testing of ships in transit. Here, we describe a detection technology based on a microfluidic chip containing DNA oligonucleotide functionalized carbon nanotubes. We demonstrate the efficacy of the chip using three ballast-transported species either established (Dreissena bugensis) or of potential threat (Eriocheir sinensis and Limnoperna fortuneii) to the Laurentian Great Lakes. With further refinement for on-board application, the technology could lead to real-time ballast water screening to improve ship-specific management and control decisions.     

Is <Emphasis Type="Italic">Gammarus tigrinus</Emphasis> (Crustacea,Amphipoda) becoming cosmopolitan through shipping? Predicting its potential invasive range using ecological niche modeling

While the intensity of global shipping has increased dramatically over the last decades, species exchange between continents has likewise intensified. Ballast water of ships is recognized playing a major role in this process. Many of the larger sea ports have become bridgeheads for invasions. Ecological niche modeling is used to investigate the potential invasive range and high invasive risk ports of the North American amphipod Gammarus tigrinus. Sixty-two occurrences of G. tigrinus in its native range (North America) and 34 environmental data sets were compiled. Data on dispersal distances were used via ecological niche modeling to analyze the invasive potential of G. tigrinus. The invasive risk of large ports was analyzed according to modeling result, as well as their salinity in the main oceanic routes of the world. G. tigrinus had a rapid range extension on the British Isles and in the rest of Western Europe. Now it is invading the countries surrounding the Baltic Sea. Worldwide it has a vast potential invasive range. It has a high invasive risk for many large ports along the main oceanic routes, among which the ports of Shanghai, Buenos Aires and Montevideo have the highest invasive risk. G. tigrinus may become cosmopolitan through shipping, and this possibility is increasing. Particular emphasis should be placed on preventing human-mediated dispersal. Ports may be the first places G. tigrinus invades. This study can identify high invasive risk ports, especially those at risk of introduced North America species. More importantly, the water of large ports should be monitored regularly for exotic aquatic organisms that may survive temporarily or permanently.     

International dissemination of epidemic Vibrio cholerae by cargo ship ballast and other nonpotable waters.

In 1991 and 1992, toxigenic Vibrio cholerae O1, serotype Inaba, biotype El Tor, was recovered from nonpotable (ballast, bilge, and sewage) water from five cargo ships docked in ports of the U.S. Gulf of Mexico. Four of these ships had taken on ballast water in cholera-infected countries; the fifth took on ballast in a noninfected country. Isolates examined by pulsed-field gel electrophoresis were indistinguishable from the Latin American epidemic strain, C6707; however, they differed significantly from the endemic Gulf Coast strain (VRL 1984), the sixth-pandemic strain (569-B), and a V. cholerae non-O1 strain isolated from a ship arriving from a foreign port. On the basis of our findings, the Food and Drug Administration recommended that the U.S. Coast Guard issue an advisory to shipping agents and captains requesting that ballast waters be exchanged on the high seas before entry of ships into U.S. ports.     

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.