Ballast Water Exchange Plus Treatment Lowers Species Invasion Rate in Freshwater Ecosystems
- Johanna N. BradieJohanna N. BradieGreat Lakes Laboratory for Fisheries and Aquatic Sciences, Fisheries and Oceans Canada, 867 Lakeshore Road, Burlington, Ontario L7S 1A1, CanadaMore by Johanna N. Bradie
- ,
- David Andrew R. DrakeDavid Andrew R. DrakeGreat Lakes Laboratory for Fisheries and Aquatic Sciences, Fisheries and Oceans Canada, 867 Lakeshore Road, Burlington, Ontario L7S 1A1, CanadaMore by David Andrew R. Drake
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- Dawson OgilvieDawson OgilvieGreat Lakes Laboratory for Fisheries and Aquatic Sciences, Fisheries and Oceans Canada, 867 Lakeshore Road, Burlington, Ontario L7S 1A1, CanadaMore by Dawson Ogilvie
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- Oscar Casas-MonroyOscar Casas-MonroyGreat Lakes Laboratory for Fisheries and Aquatic Sciences, Fisheries and Oceans Canada, 867 Lakeshore Road, Burlington, Ontario L7S 1A1, CanadaMore by Oscar Casas-Monroy
- , and
- Sarah A. Bailey*Sarah A. Bailey*Email: [email protected]Great Lakes Laboratory for Fisheries and Aquatic Sciences, Fisheries and Oceans Canada, 867 Lakeshore Road, Burlington, Ontario L7S 1A1, CanadaMore by Sarah A. Bailey
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Abstract
The movement of ballast water by commercial shipping is a prominent pathway for aquatic invasions. Ships’ ballast water management is now transitioning from open ocean exchange to a ballast water performance standard that will effectively require use of onboard treatment systems. Neither strategy is perfect, therefore, combined use of ballast water exchange plus treatment has been suggested to provide greatest protection of aquatic ecosystems. This study compared the performance of exchange plus treatment against treatment alone by modeling establishment rates of nonindigenous zooplankton introduced by ballast water across different habitat types (fresh, brackish, and marine) in Canada. Treatment was modeled under two efficacy scenarios (100% and 50% of ship trips) to consider the possibility that treatment may not always be successful. The model results indicate that exchange plus treatment will be more effective than treatment alone at reducing establishments when recipient ports are freshwater (58 140 vs 11 338 trips until ≥1 establishment occurs, respectively). Exchange plus treatment also serves as an important backup strategy if treatment systems are partially effective (50% of trips), primarily for freshwater recipient ecosystems (1442 versus 585 trips until ≥1 establishment occurs, respectively).
Introduction
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The movement of ballast water by commercial shipping is one of the most prominent pathways for the introduction of nonindigenous aquatic species. (1,2) In response, the International Convention for the Control and Management of Ships’ Ballast Water and Sediments (the Convention) was introduced, which sets a ballast water performance standard limiting the concentration of viable organisms in discharged ballast water (Regulation D-2). (3) More specifically, Regulation D-2 states that discharged ballast water must contain <10 viable organisms ≥50 μm in minimum dimension per m3, < 10 viable organisms <50 μm in minimum dimension and ≥10 μm in minimum dimension per mL, and also specifies maximum concentrations for indicator microbes. (3) After entering into force in September 2017, (4) the Convention is gradually being implemented around the world, with the expectation that reductions in biological introductions will be achieved by limiting the number of viable organisms in ballast water discharge.
Most ships will achieve the D-2 standard using an onboard ballast water management system (hereafter known as treatment), which usually consists of a filtration process (e.g., disc or screen filters) followed by one or more disinfection processes (e.g., electrolysis or ultraviolet radiation). (5) When equipment is functioning and operated properly, treatment systems can effectively reduce the concentration of viable organisms in ballast water. (6,7) However, species establishment risk may not be completely eliminated by achieving D-2, since the upper limit of this performance standard may equate to >100 000 viable zooplankton in ballast discharge from a single ship (assuming ballast capacity of at least 11 500 m3). In addition, shipboard studies have determined that treatment systems do not always function as expected, resulting in failure to meet the D-2 standard. (8,9) For example, in three shipboard trials examining treatment efficacy under operational conditions, only one appeared to meet D-2 limits for zooplankton, while one had abundances close to the limit and one had gross exceedance of the limit. (8) While failure to meet the D-2 standard may occur regularly during the early years of implementation of the Convention, the performance of treatment systems is expected to improve in the future with advancements in treatment technologies and as experience with their use is gained.
To protect aquatic systems, countries retain the right to introduce stronger regulations than those set by the Convention (Article 2.3). (3) Therefore, the Canadian Government has proposed the combined use of ballast water exchange plus treatment to potentially provide greater protection for fresh or brackish water ecosystems. (10) Ballast water exchange involves discharging ballast water at sea to expel organisms from ballast tanks and filling tanks with open ocean water to expose any residual organisms to saline water—if the initial ballast water originated from a freshwater or brackish port, the abrupt salinity change can be lethal to most freshwater and some coastal species. (11−13) Any open ocean species entrained during exchange are expected to have lower probability of survival if released into recipient fresh or brackish water ecosystems. (13) Given that exchange efficacy is partially dependent on environmental mismatch (e.g., changes in salinity and temperature), it is highly dependent on the degree of environmental correspondence between the source, exchange, and destination localities. (13,14) Ballast water exchange is considered to be most protective of freshwater ecosystems where the environmental mismatch effect is greatest, (11−13) and less protective of coastal ecosystems where the salinity mismatch is low. (14,15) It is thus expected that the benefit of an exchange plus treatment management strategy may not be consistent across regions.
Land-based and shipboard research on exchange plus treatment determined that the combined approach may benefit freshwater ecosystems by reducing the abundance of high-risk freshwater and euryhaline organisms in discharged ballast water. (8,16) Additionally, exchange plus treatment may provide greater reduction in the total abundance and diversity of certain taxonomic groups compared to treatment alone. (9,17) This past work focused on specific cause-and-effect relationships without assessing the linked, system-wide effects of a management measure. Estimating the species establishment rate under different ballast water management measures is a useful approach to evaluate the costs and benefits of management measures at scales suitable for decision-making.
The objective of this study was to compare the efficacy of exchange plus treatment to treatment alone across different recipient habitat types (i.e., fresh, brackish, and marine environments) in Canada. This study also considered the possibility that the desired level of treatment efficacy may not be achieved on a proportion of ship trips and determined the effect of using exchange as a backup strategy. The effectiveness of each management scenario was measured by estimating species establishment rates of nonindigenous zooplankton using a multistage mechanistic model. This model incorporated three main components of the invasion process: (1) estimating the number of nonindigenous zooplankton species and their concentrations (individuals/m3) in ballast water under each management scenario; (2) calculating the survival probability of these species in the recipient port; and, (3) predicting species establishment rates based on initial population sizes and per-capita establishment probabilities.
Methods
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Management Scenarios and Establishment Rate Metrics
This analysis compared the outcome of six ballast water management scenarios, including (1) no management, (2) exchange, (3) partially effective treatment (meeting the D-2 limit on 50% of trips), (4) exchange plus partially effective treatment, (5) fully effective treatment (meeting the D-2 limit on 100% of trips), and (6) exchange plus fully effective treatment (see Modeling the Management Scenarios for details). We applied the management methods to trips of ships with ballast water arriving to fresh, brackish, or marine ports in Canada (Supporting Information (SI) Figure S1). Ports were classified as fresh (≤5.0 g/kg), brackish (5.1–18.0 g/kg), or marine (≥18.1 g/kg), depending on their mean annual salinity. The salinity thresholds were selected based on observed changes in community composition across a salinity gradient. (18) Salinity and temperature data were sourced from Keller et al. (19) and World Ocean Atlas 2013 Vol. 2, (20,21) with adjustments to correct salinity values of fresh and brackish water ports when calculated values did not match known measured values.
The effectiveness of each management scenario was measured as the estimated species establishment rate of nonindigenous zooplankton. Results were summarized using two relevant metrics of species establishment: (i) mean probability that ≥1 species establishes per trip; and, (ii) mean number of species establishing per year. To simplify the interpretation of the results, the probability of establishment per trip was converted to the number of trips until ≥1 species establishes. The number of trips until ≥1 species establishes reflects the species establishment risk of individual trips and is independent of shipping traffic volume. This metric was used to assess the establishment risk across fresh, brackish, and marine habitat types, since ship traffic volume varied across these habitat types. On the other hand, the species per year metric considers the cumulative effect of ship traffic volume on total establishments and was used to compare the model results to historical species discovery data in the Great Lakes-St. Lawrence region.
Simulation of Shipping Traffic
Using available region-specific shipping data from 2006, 2008, or 2015, (22,23) we constructed a 1 year iteration of shipping activity at Canadian ports to quantify the frequency and spatial distribution of ballast water discharge events (n = 2980 trips; SI Table S1); while there can be fluctuations in the number of trips year to year, a 1 year iteration of shipping activity provides a standard time frame to model establishment rates across different regions. The shipping data included international ship transits to Canadian ports in the Pacific, Atlantic, Great Lakes-St. Lawrence River, and Arctic, as well as domestic ship transits to Canadian Arctic ports from Canadian ports in the Atlantic or Great Lakes-St. Lawrence River (SI Figure S1). The combinations of ship traffic types (international or domestic) and geographical regions are hereafter referenced as shipping pathways. The domestic pathway was considered only for the Arctic because exchange can be performed by ships traveling to Arctic ports, whereas ships traveling between other Canadian regions cannot perform open ocean exchange due to limited distance-from-shore. Additionally, there is concern about resource development in the Arctic and the associated increase in shipping traffic and ballast water discharge. (23)
Species Arrival
Pathway-specific empirical biological data were used to estimate the number of nonindigenous zooplankton species and their individual concentrations in ballast water for each ship trip, following four steps. Zooplankton data were obtained from previous ballast water studies conducted across Canada, collected opportunistically throughout multiple seasons representing a range of source ports and corresponding transits (n = 213 samples; SI Table S2). (23−27) Due to limited biological data for the Arctic domestic pathway, pathway-specific data were supplemented with that from internal Great Lakes-St. Lawrence River transits. (28,29)
First, the total zooplankton concentration (indigenous and nonindigenous; individuals per m3) among ship trips was characterized by fitting a negative binomial distribution to empirical sample count data within each pathway using maximum likelihood estimation (SI Table S3 and Figure S2). A probability distribution was generated for each pathway, and a random draw was made from these distributions to determine the total concentration of zooplankton on each ship trip.
Second, a conditional variable—Cp | Cs (population concentration | sample concentration)—was used to account for sampling error in organism counts and the spatial distribution of organisms in a tank were assumed to be distributed according to a Poisson process (SI Figure S3), such that the actual population concentration may vary from the obtained sample. (30,31)
Third, the proportion of nonindigenous individuals out of the total population was estimated by summarizing the proportion of zooplankton in empirical samples that were nonindigenous to each region. (22) Then, a beta distribution was fit to the proportion of nonindigenous zooplankton for each shipping pathway using maximum likelihood (SI Table S3 and Figure S4). A random draw was made from these pathway-specific distributions to determine the total concentration of nonindigenous individuals on each ship trip.
Fourth, once the concentration of nonindigenous zooplankton on a single trip was determined, a single species abundance distribution was randomly selected from empirical ballast water sample data from the same shipping pathway (SI Table S2). The species abundance distribution determined the number of nonindigenous species and their relative concentrations out of the total concentration of nonindigenous individuals on a given ship trip. (32)
With this overall approach, for each ship trip, a random value was drawn from the sample concentration distribution to determine the total sample concentration of zooplankton (indigenous and nonindigenous). Then, a random value was selected from the Cp | Cs distribution to determine the population concentration given the sample concentration. A random draw was made from the nonindigenous distribution to determine the concentration of nonindigenous individuals out of the total zooplankton concentration (i.e., total zooplankton concentration × proportion of nonindigenous individuals). Lastly, a species abundance distribution was randomly selected to quantify the number of nonindigenous species and their concentrations, distributed among the total concentration of nonindigenous individuals on a given trip.
Species Establishment
The establishment of each species released in each recipient port was determined based on (i) the temperature and salinity match between source and recipient environments; and, (ii) each species’ concentration and reproductive capacity. Temperature match was incorporated by estimating the environmental distance between source and recipient environments, calculated as the Euclidean distance between standardized temperature variables (maximum, minimum, mean). (33) The relationship between environmental distance and survival probability was determined using a binomial generalized-linear model fitted with presence-presence distances versus presence-background distances for 603 aquatic animal and plant species that have established in at least one novel region. Presence data was obtained in 2014 from the Global Invasive Species Information Network, excluding species with fewer than three unique occurrence points. The species data was split into 80% for fitting and 20% for training, and model performance was evaluated using the area under the curve (AUC = 0.90). (34) The resultant environmental distance curve is available in SI Figure S5. Once the environmental distance was calculated for a given ship trip, a random draw was made from the logistic function (SI Figure S5) to determine whether each released species survived the environmental temperature in the recipient port.
Surviving species were assessed to determine whether they would establish viable populations based on their concentration and reproductive capacity. Species establishment probabilities (1–probability of extinction) were determined using the following equation adapted from Leung et al.: (35)
where Pe is the probability of establishment, α is the probability that a single propagule will establish a viable population, N is the concentration of organisms (individuals/m3), and c is a shape parameter to accommodate an Allee effect (where c > 1). We assumed no Allee effect (c = 1), following results from Bradie et al. (36) that showed c = 1 to be a reasonable assumption when modeling multiple species within a pathway. Examples of establishment probability curves are presented in SI Figure S6; the probability of establishment is high when α is large, even with low organism concentrations, whereas higher organism concentrations are necessary to attain high establishment probabilities when α is small.
Since the α parameter is expected to vary by species, an α value was drawn for each surviving species from a beta distribution with shape parameters α = 0.005 and β = 5 (SI Figure S7). This distribution was designed to include a wide range of aquatic species and their per-capita establishment probabilities under diverse biological, chemical, and physical conditions. The lower range of α representing sexually reproducing species is unknown. The upper limit of α was based on Bailey et al.’s (37) estimate of the upper limit of establishment probability for parthenogenetic zooplankton in the Great Lakes, which was fitted to align with the 97.5th percentile of the curve. The per-capita establishment probability distribution was assumed to be identical across all shipping pathways.
The α parameter was then adjusted based on the salinity match between ports. When the salinity difference between the source and recipient environments was either marine-brackish or brackish-freshwater (or vice versa), α values were halved. When the salinity difference was marine-freshwater or vice versa, α values were divided by 10. As the true effect of salinity on species’ α values is unknown, the adjustments in α were chosen following the rationale that most species would experience highest establishment probability in environments matching their donor region, and lower establishment probability in environments that do not match their donor region. (11,12,38) With this approach, the life history processes governing establishment are also constrained when a species has been introduced to an environment with poor survival potential.
Based on the outcome of the establishment probability equation, a binary outcome of establishment (1) or extinction (0) was determined for each surviving species per trip using a Bernoulli trial. Simulations were repeated 1000 times to determine the mean establishment rate. Model simulations were run in the R statistical programming language. (39) The 95% confidence interval for the mean was determined by bootstrapping with replacement 5000 times using the boot package in R. (40)
Modeling the Management Scenarios
Ballast water exchange was assumed to alter both the temperature and salinity match for species resident in tanks, but not affect the concentration of organisms or number of species on a given ship trip. This assumption was based on conflicting empirical data from ships conducting exchange, with some studies showing a strong influence of exchange on organism abundance, (41−43) while others did not observe a reduction in abundance following exchange. (23) Therefore, the approach assuming no change in the abundance or proportion of nonindigenous zooplankton introduced the fewest assumptions to the model. As a result, the modeled effect of exchange was a change in species establishment probabilities reflective of the temperature and salinity match between the location of exchange and recipient port. (13) The location of exchange was randomly selected from population data of midpoints of exchange for ships arriving to each Canadian region in 2015.
The model incorporated the efficacy of exchange at purging organisms from ballast tanks given the method of performing exchange. The mean efficacy of exchange was assumed to be 70.1% for flow-through and 97.9% for empty-refill, (44) and the prevalence of each method for each pathway was based on observed empirical data for one year of ship transits to Canada. Therefore, following exchange, the total population concentration remained the same, with a percentage of this total comprised of the open ocean community (70.1 or 97.9%) and the remainder comprised of the original ballast source community. The establishment probability of the residual pre-exchange community was based on the temperature and salinity match between the source and recipient ports.
Ballast water treatment was modeled by changing the organism concentration for a trip to levels observed in “successful” or “failed” treatments from a study of treated ballast water samples obtained from international ships arriving to Canada during 2017 and 2018; (45) “successful” treatment refers to treated ballast water samples with numbers of viable organisms within the limits of the D-2 standard, while “failed” treatment samples had numbers of viable organisms exceeding the limits of the D-2 standard. For successful treatments, zooplankton concentrations were drawn from a Poisson distribution with a mean of 1.58 zooplankton organisms per m3. (45) For failed treatments, zooplankton concentrations were drawn from a log-normal distribution with a mean of 1155 individuals per m3. (45) The post-treatment probability distributions were the best fitting distributions using maximum likelihood. Post-treatment concentrations were restricted to being equal to or less than pretreatment concentrations. The treated ballast water sample data were not pathway specific due to the limited number of samples (n = 32) collected in Canada to date.
Both fully and partially effective treatment scenarios were considered, where successful treatment occurred on 100% and 50% of trips, respectively. The 50% rate for partially effective treatment was based on empirical evidence to date, (8,45) noting that treatment efficacy may vary depending on water conditions during ballast loading (e.g., turbidity), treatment system type, or operational experience. (8,9,16) The simulated effect of treatment was applied to the same ship trips in the no management and exchange only scenarios to produce the treatment only and exchange plus treatment scenarios, respectively.
Model Sensitivity
The sensitivity of the model was evaluated by increasing or decreasing (by 25%) the total organism concentration, proportion of nonindigenous species or number of trips, and observing the proportional response in outcomes. Additionally, the source and recipient port combinations were randomized to simulate a change in ship traffic patterns, all species’ α values were set to 0.005 to assess the effect if all species reproduced clonally, and an Allee effect was included in the establishment equation (c = 2). (36) The response variable for sensitivity analysis was the mean number of species establishments per year among all Canadian ports (fresh, brackish, and marine).
Results and Discussion
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When treatment systems were effective on 50% of trips, exchange plus treatment was more effective than treatment alone for trips arriving to freshwater ports, more than doubling the mean number of trips until ≥1 species establishes from 585 (effective treatment on 50% trips) to 1442 (exchange plus treatment, with effective treatment on 50% of trips; Figure 1a). A similar, but smaller, positive effect was found for brackish water recipient ports, with the mean number of trips until ≥1 species establishes increasing from 2007 to 2948 (Figure 1b). In contrast, there was no apparent benefit to using exchange plus treatment versus treatment alone for marine recipient ports (1169 vs 1287 trips until ≥1 species establishes, respectively; Figure 1c). These results indicate that exchange may serve as an important backup strategy most protective of fresh or brackish recipient ports, at least until treatment can be applied successfully across all ship trips.
Figure 1
Figure 1. Mean number of trips until ≥1 nonindigenous zooplankton species establishes by ballast water discharge in fresh, brackish, or marine water recipient ports in Canada. The ballast water management methods assessed are no management (NM), exchange only (E), treatment only (T), and exchange plus treatment (E+T). Ballast water treatment was either partially effective (meeting D-2 limit on 50% of ship trips) (PE) or fully effective (meeting D-2 limit on 100% of ship trips) (FE). The error bars represent the bootstrapped 95% confidence intervals of the mean across 1000 single year iterations. Upper confidence intervals with infinite number of trips until ≥1 species establishment occurs are denoted by *. The y-axis is on a logarithmic scale.
Fully effective treatment extended the time frame required until ≥1 nonindigenous zooplankton species establishes compared to partially effective treatment for all recipient ports (all salinities; Figure 1). Still, even with fully effective treatment, exchange plus treatment was more effective at preventing nonindigenous zooplankton establishments than treatment alone in freshwater ports, increasing the mean number of trips until ≥1 species establishes from 11 338 to 58 140, respectively (Figure 1a). On the other hand, exchange plus treatment provided no additional benefit compared to treatment alone in recipient ports that were brackish (141 443 trips until ≥1 species establishes for both scenarios; Figure 1b) or marine (42 553 vs 58 824 trips until ≥1 species establishes, respectively; Figure 1c). Summarily, exchange plus treatment was most effective at mitigating establishment risk in freshwater ports, regardless of whether treatment was successful on 50% or 100% of ship trips.
These results highlight the importance of considering environmental context when designing and implementing management plans and demonstrate that additional benefit (reduced establishment rate) can be achieved with a multidimensional management approach. Since the combined approach of exchange plus treatment entails additional costs (in terms of crew effort and operational costs), this study can inform a more targeted management approach that maximizes the cost-benefit ratio.
Correlation with Historical Observations
Evaluating the model output to determine whether it is empirically reasonable is an important, yet difficult, task, due to incomplete data on successful and failed establishments of nonindigenous species. Nonetheless, we compared model results for the Great Lakes–St. Lawrence region with observed species discovery data for ship-mediated nonindigenous species assembled by Sturtevant and colleagues. (46) We ran the model for the Great Lakes–-St. Lawrence River international shipping pathway with the mean species per year metric, and compared the results for the baseline scenarios (no management and exchange only) against observed species discovery rate during related time periods.
The estimated establishment rate of nonindigenous invertebrates during the 25-year period prior to 1993 (no management) of 0.32 species per year, based on species discovery data, (46) is similar to the 0.55 species per year produced by this model. There have been seven confirmed invertebrate establishments in the Great Lakes attributed to ballast water in the 25 years since exchange became mandatory under U.S. law in 1993. (25,46) The discovery rate of 0.28 invertebrates per year from 1994 to 2019 corresponds well with model results of 0.33 species per year for the exchange only scenario. Ultimately, the encouraging correlation between the model results and historical observations indicates that the scenarios provide sound representation of the risk of ballast-mediated invasions to fresh, brackish, and marine ecosystems in Canada.
Sources of Uncertainty and Model Sensitivity
The true per-capita establishment probabilities of species may have been under- or overestimated, given widespread uncertainty about the relationship between propagule pressure and establishment. (47) To examine the potential effect of underestimating alpha values, we considered the case where alpha for all species was 0.005, which is equivalent to a parthenogenetic species having establishment probability greater than 50% with an initial concentration of at least 150 individuals per m3. Results showed this would increase the number of establishments, but not influence the relative performance of the different management options (SI Table S4). Additional research evaluating appropriate alpha values across species and environments would help shape the per-capita establishment probability distribution, improving estimates of species establishment.
The alteration of alpha values based on salinity matching (to give effect of ballast water exchange) is another source of uncertainty. While the premise of species having a lower establishment risk in recipient environments that do not match the source environment’s salinity is founded on past research, (11,12,38) the actual value associated with this decrease is unknown. To examine the implications of this assumption, the model was also run with the salinity variable built into the fitted environmental distance curve rather than including it as a separate factor affecting establishment. Model predictions were similar, which implied that the estimated numeric effect of environment on establishment is in the right vicinity. This model also assumed no Allee effect (c = 1), as recommended for pathway-level models, (36) but we examined the influence of this assumption on the results by running the model with the Allee effect set to c = 2. This caused a 67% increase in establishment rate on average (SI Table S4), but the relative differences between the management scenarios remained the same. While other biotic and abiotic variables can influence species survival or establishment (e.g., nutrient availability, competition, or predation), (48) they were beyond the scope of this analysis, though they may contribute uncertainty to the model results.
The transit frequency, total sample organism concentration, and proportion of nonindigenous individuals were also shifted by 25% to evaluate the model’s sensitivity to changes in propagule pressure. The model was not particularly sensitive to deviations in these parameters, with each parameter shift typically resulting in a less than 10% change in species per year (SI Table S4). This could be due to the summation of unique species establishments (rather than species predicted to establish more than once) but, nonetheless, the model was robust to changes in these input parameters. In some cases, the scenarios involving 100% successful treatment had wider fluctuations in the percentage change in species establishment rate relative to the null (e.g., a 25% increase in mean proportion of nonindigenous zooplankton resulted in a 35% increase in establishment rate; SI Table S4). However, fully successful treatment had fewer initial establishments, resulting in larger percentage changes corresponding to relatively small deviations in species establishments.
Finally, the effectiveness of exchange may have been underestimated by this model due to the assumption that exchange did not alter organism concentrations in ballast tanks. More information on pre- versus postexchange organism concentrations could improve the modeled effect of exchange. Although a number of parameters driving this model were based on best available data, due to the high degree of uncertainty associated with predicting establishment rates given current scientific knowledge, management decisions should be based on the relative differences in establishment risk between management strategies rather than numerical outputs.
Final Considerations
Exchange plus treatment can be conducted by either (1) loading untreated port water and using a treatment system only during exchange (E+T); or, (2) using a treatment system to treat incoming water during both initial ballast loading and exchange (T+E+T). A third combination, using a treatment system during initial ballast loading and no treatment during exchange (T+E), though operationally possible, would be unlikely to meet the D-2 standard required by the Convention. E+T places less stress on treatment systems during challenging port conditions (e.g., turbid water due to seasonal flooding) thereby potentially reducing maintenance and repairs, and has lower associated effort due to fewer required treatment steps. However, E+T only manages source port ballast water using exchange, thus posing a potential threat to ocean ecosystems when unmanaged ballast water is expelled. Furthermore, residual ballast water and sediments following exchange may contain a substantial number of viable organisms from the initial unmanaged ballast uptake, posing invasion risks to recipient ecosystems. In contrast, T+E+T ensures no unmanaged water enters ballast tanks, and in cases where it is unsafe to perform exchange due to poor weather conditions, at least the treatment system will have been utilized.
Supporting Information
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The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.0c05238.
Information on the Canadian regions examined in this study, model parameter values, probability distributions, sensitivity analysis results, and supplementary model results (PDF)
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Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.
Author Information
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- Sarah A. Bailey - Great Lakes Laboratory for Fisheries and Aquatic Sciences, Fisheries and Oceans Canada, 867 Lakeshore Road, Burlington, Ontario L7S 1A1, Canada;
http://orcid.org/0000-0003-3635-919X;
Acknowledgments
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This study was funded by Fisheries and Oceans Canada and Transport Canada.
References
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- 6de Lafontaine, Y.; Despatie, S.; Veilleux, É.; Wiley, C. Onboard ship evaluation of the effectiveness and the potential environmental effects of PERACLEAN® Ocean for ballast water treatment in very cold conditions. Environ. Toxicol. 2009, 24, 49– 65, DOI: 10.1002/tox.20394[Crossref], [PubMed], [CAS], Google Scholar6https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD1MXisVWmtrw%253D&md5=6915c21c81fc47760e30ba5b8bc3190eOnboard ship evaluation of the effectiveness and the potential environmental effects of PERACLEAN Ocean for ballast water treatment in very cold conditionsde Lafontaine, Y.; Despatie, S.-P.; Veilleux, E.; Wiley, C.Environmental Toxicology (2009), 24 (1), 49-65CODEN: ETOXFH; ISSN:1520-4081. (John Wiley & Sons, Inc.)This study verified the effectiveness and the potential toxic impact of PERACLEAN Ocean ballast water treatment for very cold freshwater (0.1-0.5°) in real ballast tank (750 M3) conditions aboard a ship and in large-vol. (4.5 M3) polyethylene tanks. Concns. of peracetic acid (PAA) and hydrogen peroxide (H2O2) gradually dropped by 41-59% over 5 days. The treatment altered the quality of the treated waters by causing a pH drop of 0.9-1.3 units and a fourfold to sevenfold increase in dissolved org. carbon and organophosphates concns. More than 90% of the biomass of free-floating microorganisms and viable phytoplankton were eliminated within 48 h after treatment. The treatment resulted in 100% mortality in caged fish exposed to treated waters but was totally ineffective against adult zebra mussels and some nematodes living in tank sediments. Toxic response from ecotoxicol. assays indicated that treated waters after 5 days should be dild. by a factor of 1:2 to 1:200 to reduce toxicity below selected endpoints of acute lethality tests. On the basis of PAA degrdn. rate, fresh waters treated with 100-ppm PERACLEAN Ocean should be kept in ballast tanks for 15-20 days after treatment to reduce toxicity. It is concluded that the treatment can be an effective biocide to rapidly eliminate organisms of the water column inside the ballast tanks over a wide range of environmental conditions, but that the discharge of the toxic treated waters should be property managed to minimize potential environmental impact.
- 7Casas-Monroy, O.; Linley, R. D.; Chan, P.; Kydd, J.; Byllaardt, J. V.; Bailey, S. Evaluating efficacy of filtration UV-C radiation for ballast water treatment at different temperatures. J. Sea Res. 2018, 133, 20– 28, DOI: 10.1016/j.seares.2017.02.001
- 8Briski, E.; Gollasch, S.; David, M.; Linley, R. D.; Casas-Monroy, O.; Rajakaruna, H.; Bailey, S. A. Combining ballast water exchange and treatment to maximize prevention of species introductions to freshwater ecosystems. Environ. Sci. Technol. 2015, 49, 9566– 9573, DOI: 10.1021/acs.est.5b01795[ACS Full Text
], [CAS], Google Scholar8https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC2MXhtFKhtr7P&md5=c20afcab21f58f82d8eaf9dfcc146bfdCombining Ballast Water Exchange and Treatment To Maximize Prevention of Species Introductions to Freshwater EcosystemsBriski, Elizabeta; Gollasch, Stephan; David, Matej; Linley, R. Dallas; Casas-Monroy, Oscar; Rajakaruna, Harshana; Bailey, Sarah A.Environmental Science & Technology (2015), 49 (16), 9566-9573CODEN: ESTHAG; ISSN:0013-936X. (American Chemical Society)The most effective way to manage species transfers is to prevent their introduction via vector regulation. International ships will be required to meet numeric ballast discharge stds. using ballast water treatment (BWT) systems, and ballast water exchange (BWE), currently required by several countries, will be phased out. However, there are concerns that BWT systems may not function reliably in fresh and/or turbid water. A land-based evaluation of simulated BWE plus BWT vs. BWT alone demonstrated potential benefits of combining BWE with BWT for protection of freshwater ecosystems. We conducted ship-based testing to compare the efficacy of BWE plus BWT vs. BWT alone on voyages starting with freshwater ballast. We tested the hypotheses that there is an addnl. effect of BWE plus BWT compared to BWT alone on the redn. of plankton, and that taxa remaining after BWE plus BWT will be marine (low risk for establishment at freshwater recipient ports). Our study found that BWE has significant addnl. effect on the redn. of plankton, and this effect increases with initial abundance. As per expectations, BWT alone tanks contained higher risk freshwater or euryhaline taxa at discharge, while BWE plus BWT tanks contained mostly lower risk marine taxa unlikely to survive in recipient freshwater ecosystems. - 9Paolucci, E. M.; Hernandez, M. R.; Potapov, A.; Lewis, M. A.; Macisaac, H. J. Hybrid system increases efficiency of ballast water treatment. J. Appl. Ecol. 2015, 52 (2), 348– 357, DOI: 10.1111/1365-2664.12397[Crossref], [CAS], Google Scholar9https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC2MXpvFahtb4%253D&md5=cdb7243270d33614a92e6048997a7e44Hybrid system increases efficiency of ballast water treatmentPaolucci, Esteban M.; Hernandez, Marco R.; Potapov, Alexei; Lewis, Mark A.; MacIsaac, Hugh J.Journal of Applied Ecology (2015), 52 (2), 348-357CODEN: JAPEAI; ISSN:0021-8901. (Wiley-Blackwell)Summary : Ballast water has been a principal pathway of non-indigenous species introduction to global ports for much of the 20th century. In an effort to reduce the scale of this pathway, and recognizing forthcoming global regulations that will supplant ballast water exchange (BWE) with ballast water treatment (BWT), we explore whether a combined hybrid treatment of BWE and chlorination (Cl) exceeds individual effects of either BWE or chlorination alone in reducing densities of bacteria, microplankton and macroplankton. Five full-scale trials were conducted on an operational bulk carrier travelling between Canada and Brazil. The hybrid treatment generally had the lowest final densities among all treatments for putative enterococci, Escherichia coli and coliform bacteria, as well as microplankton and macroplankton, with the former two being synergistically lower than individual treatments alone. Microplankton abundance in the hybrid treatment was significantly but antagonistically reduced relative to individual treatments alone. Macroplankton final d. was lowest in the hybrid treatment, though the interaction between treatments was not significant. Synthesis and applications. In most cases, the combined hybrid treatment of ballast water exchange (BWE) and chlorination reduced population densities of indicator organisms in ballast water below those proposed by the International Maritime Organization's D-2 performance stds. BWE alone was often ineffective at reducing bacterial and macroplankton densities. Even when performance stds. are implemented globally, continued use of BWE could further reduce risk of invasions to freshwater ecosystems that receive ballast water from foreign sources by accentuating the decline in propagule pressure and enhancing demog. constraints for putative invaders.
- 10Canada. Proposal to Utilize Ballast Water Exchange in Combination with a Ballast Water Management System to Achieve an Enhanced Level of Protection. Submitted to 15th session of the Sub-Committee on Bulk Liquids and Gases as BLG 15/5/7. International Maritime Organization, London, England, 2010.Google ScholarThere is no corresponding record for this reference.
- 11Santagata, S.; Gasiu̅naite, Z.; Verling, E.; Cordell, J.; Eason, K.; Cohen, J.; Bacela, K.; Quilez-Badia, G.; Johengen, T. H.; Reid, D. F.; Ruiz, G. Effect of osmotic shock as a management strategy to reduce transfers of nonindigenous species among low-salinity ports by ships. Aquatic Invasions 2008, 3, 61– 76, DOI: 10.3391/ai.2008.3.1.10
- 12Ellis, S.; Macisaac, H. J. Salinity tolerance of Great Lakes invaders. Freshwater Biol. 2009, 54, 77– 89, DOI: 10.1111/j.1365-2427.2008.02098.x[Crossref], [CAS], Google Scholar12https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD1MXisVCrt7o%253D&md5=17a32bd46a09db9860009393d1622876Salinity tolerance of Great Lakes invadersEllis, Sandra; MacIsaac, Hugh J.Freshwater Biology (2009), 54 (1), 77-89CODEN: FWBLAB; ISSN:0046-5070. (Wiley-Blackwell)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. 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. 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 det. if they could have survived salinities assocd. with BWE. 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 behavioral 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 max. 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.
- 13Reid, D. F. The Role of Osmotic Stress (Salinity Shock) In Protecting the Great Lakes from Ballast-Associated Aquatic Invaders; submitted to the U.S. Saint Lawrence Seaway Development Corporation, U.S. Department of Transportation, 2012.Google ScholarThere is no corresponding record for this reference.
- 14Cordell, J. R.; Lawrence, D. J.; Ferm, N. C.; Tear, L. M.; Smith, S. S.; Herwig, R. P. Factors influencing densities of nonindigenous species in the ballast water of ships arriving at ports in Puget Sound, Washington, United States. Aquatic Conserv: Mar. Freshw. Ecosyst. 2009, 19 (3), 322– 343, DOI: 10.1002/aqc.986
- 15McCollin, T.; Shanks, A. M.; Dunn, J. Changes in zooplankton abundance and diversity after ballast water exchange in regional seas. Mar. Pollut. Bull. 2008, 56, 834– 844, DOI: 10.1016/j.marpolbul.2008.02.004[Crossref], [PubMed], [CAS], Google Scholar15https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD1cXlvVKks7k%253D&md5=7df083127814d0eb91a63633d4d24558Changes in zooplankton abundance and diversity after ballast water exchange in regional seasMcCollin, Tracy; Shanks, Aileen M.; Dunn, JohnMarine Pollution Bulletin (2008), 56 (5), 834-844CODEN: MPNBAZ; ISSN:0025-326X. (Elsevier B.V.)A study of the efficiency of ballast water exchange (BWE) in regional seas was carried out to assess this management method in reducing the risk of introducing non-native species. Zooplankton samples were taken before and after exchange on ten voyages where BWE took place (North Sea, English Channel, Irish Sea and Bay of Biscay). Zooplankton abundance was always reduced after exchange, but diversity increased on eight occasions. The greatest changes occurred when the source port water was of low salinity and when exchange took place in deeper waters further from land. However, it was clear that BWE did not remove all the source port taxa and this method is unlikely to provide a consistent and effective method of managing ballast water in regional seas.
- 16Briski, E.; Allinger, L. E.; Balcer, M.; Cangelosi, A.; Fanberg, L.; Markee, T. P.; Mays, N.; Polkinghorne, C. N.; Prihoda, K. R.; Reavie, E. D.; Regan, D. H.; Reid, D. M.; Saillard, H. J.; Schwerdt, T.; Schaefer, H.; TenEyck, M.; Wiley, C. J.; Bailey, S. A. Multidimensional approach to invasive species prevention. Environ. Sci. Technol. 2013, 47, 1216– 1221, DOI: 10.1021/es3029445[ACS Full Text], [CAS], Google Scholar16https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC3sXkt12jsw%253D%253D&md5=d8b14803b74705b994f3464c8068331dMultidimensional Approach to Invasive Species PreventionBriski, Elizabeta; Allinger, Lisa E.; Balcer, Mary; Cangelosi, Allegra; Fanberg, Lana; Markee, Tom P.; Mays, Nicole; Polkinghorne, Christine N.; Prihoda, Kelsey R.; Reavie, Euan D.; Regan, Deanna H.; Reid, Donald M.; Saillard, Heidi J.; Schwerdt, Tyler; Schaefer, Heidi; TenEyck, Matthew; Wiley, Chris J.; Bailey, Sarah A.Environmental Science & Technology (2013), 47 (3), 1216-1221CODEN: ESTHAG; ISSN:0013-936X. (American Chemical Society)Nonindigenous species (NIS) cause global biotic homogenization and extinctions, with com. shipping being a leading vector for spread of aquatic NIS. To reduce transport of NIS by ships, regulations requiring ballast water exchange (BWE) have been implemented by numerous countries. BWE appears to effectively reduce risk for freshwater ports, but provides only moderate protection of marine ports. In the near future, ships may be required to undertake ballast water treatment (BWT) to meet numeric performance stds., and BWE may be phased out of use. However, there are concerns that BWT systems may not operate reliably in fresh or turbid water, or both. Consequently, it has been proposed that BWE could be used in combination with BWT to maximize the pos. benefits of both management strategies for protection of freshwater ports. We compared the biol. efficacy of "BWE plus BWT" against "BWT alone" at a ballast water treatment exptl. test facility. Our comparative evaluation showed that even though BWT alone significantly reduced abundances of all tested organism groups except total heterotrophic bacteria, the BWE plus BWT strategy significantly reduced abundances for all groups and furthermore resulted in significantly lower abundances of most groups when compared to BWT alone. Our study clearly demonstrates potential benefits of combining BWE with BWT to reduce invasion risk of freshwater organisms transported in ships' ballast water, and it should be of interest to policy makers and environmental managers.
- 17Paolucci, E. M.; Ron, L.; Macisaac, H. J. Combining ballast water treatment and ballast water exchange: Reducing colonization pressure and propagule pressure of phytoplankton organisms. Aquat. Ecosyst. Health Manage. 2017, 20 (4), 369– 377, DOI: 10.1080/14634988.2017.1404419
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- 20Locarnini, R. A.; Mishonov, A. V.; Antonov, J. I.; Boyer, T. P.; Garcia, H. E.; Baranova, O. K.; Zweng, M. M.; Paver, C. R.; Reagan, J. R.; Johnson, D. R.; Hamilton, M.; Seidov, D. World Ocean Atlas 2013, Vol. 1: Temperature; Levitus, S., Mishonov, A., Eds.; NOAA Atlas NESDIS, 2013; Vol. 73.Google ScholarThere is no corresponding record for this reference.
- 21Zweng, M. M; Reagan, J. R.; Antonov, J. I.; Locarnini, R. A.; Mishonov, A. V.; Boyer, T. P.; Garcia, H. E.; Baranova, O. K.; Johnson, D. R.; Seidov, D.; Biddle, M. M. World Ocean Atlas 2013, Vol. 2: Salinity; Levitus, S., Mishonov, A., Eds; NOAA Atlas NESDIS, 2013, Vol. 74.Google ScholarThere is no corresponding record for this reference.
- 22Casas-Monroy, O.; Linley, R. D.; Adams, J. K.; Chan, F. T.; Drake, D. A. R.; Bailey, S. A. National risk assessment for introduction of aquatic nonindigenous species to Canada by ballast water. PLoS One 2015, 10, 2013/128, DOI: 10.1371/journal.pone.0118267
- 23Chan, F. T.; Macisaac, H. J.; Bailey, S. A. Relative importance of vessel hull fouling and ballast water as transport vectors of nonindigenous species to the Canadian Arctic. Can. J. Fish. Aquat. Sci. 2015, 72 (8), 1230– 1242, DOI: 10.1139/cjfas-2014-0473
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- 25Bailey, S. A.; Deneau, M. G.; Jean, L.; Wiley, C. J.; Leung, B.; Macisaac, H. J. Evaluating efficacy of an environmental policy to prevent biological invasions. Environ. Sci. Technol. 2011, 45 (7), 2554– 2561, DOI: 10.1021/es102655j[ACS Full Text], [CAS], Google Scholar25https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC3MXivFSqsrg%253D&md5=af41827f3e76bad54bf1f1cacade2af6Evaluating Efficacy of an Environmental Policy to Prevent Biological InvasionsBailey, Sarah A.; Deneau, Matthew G.; Jean, Laurent; Wiley, Chris J.; Leung, Brian; MacIsaac, Hugh J.Environmental Science & Technology (2011), 45 (7), 2554-2561CODEN: ESTHAG; ISSN:0013-936X. (American Chemical Society)Enactment of any environmental policy should be followed by an evaluation of its efficacy to ensure optimal utilization of limited resources, yet measuring the success of these policies can be a challenging task owing to a dearth of data and confounding factors. We examine the efficacy of ballast water policies enacted to prevent biol. invasions in the Laurentian Great Lakes. We utilize four criteria to assess the efficacy of this environmental regulation: (1) Is the prescribed management action demonstrably effective (2) Is the management action effective under operational conditions (3) Can compliance be achieved on a broad scale (4) Are desired changes obsd. in the environment. The four lines of evidence resulting from this anal. indicate that the Great Lakes ballast water management program provides robust, but not complete, protection against ship-mediated biol. invasions. Our anal. also indicates that corresponding inspection and enforcement efforts should be undertaken to ensure that environmental policies translate into increased environmental protection. Similar programs could be implemented immediately around the world to protect the biodiversity of the many freshwater ecosystems which receive ballast water discharges by international vessels. This general framework can be extended to evaluate efficacy of other environmental policies.
- 26Briski, E.; Bailey, S. A.; Casas-Monroy, O.; DiBacco, C.; Kaczmarska, I.; Levings, C.; MacGillivary, M. L.; McKindsey, C. W.; Nasmith, L. E.; Parenteau, M.; Piercey, G.; Rochon, A.; Roy, S.; Simard, N.; Villac, M. C.; Weise, A.; MacIsaac, H. J. Relationship between propagule pressure and colonization pressure in invasion ecology: A test with ships’ ballast. Proc. R. Soc. London, Ser. B 2012, 279, 2990– 2997, DOI: 10.1098/rspb.2011.2671
- 27DiBacco, C.; Humphrey, D. B.; Nasmith, L. E.; Levings, C. D. Ballast water transport of non-indigenous zooplankton to Canadian ports. ICES J. Mar. Sci. 2012, 69, 483– 491, DOI: 10.1093/icesjms/fsr133
- 28Briski, E.; Wiley, C. J.; Bailey, S. A. Role of domestic shipping in the introduction or secondary spread of nonindigenous species: Biological invasions within the Laurentian Great Lakes. J. Appl. Ecol. 2012, 49 (5), 1124– 1130, DOI: 10.1111/j.1365-2664.2012.02186.x
- 29Adebayo, A. A.; Zhan, A.; Bailey, S. A.; MacIsaac, H. J. Domestic ships as a potential pathway of nonindigenous species from the Saint Lawrence River to the Great Lakes. Biol. Invasions 2014, 16 (4), 793– 801, DOI: 10.1007/s10530-013-0537-5[Crossref], [PubMed], [CAS], Google Scholar29https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A280%3ADC%252BB3MzktlWmsw%253D%253D&md5=998e363e9466016001a5118b5bb0109bDomestic ships as a potential pathway of nonindigenous species from the Saint Lawrence River to the Great LakesAdebayo Abisola A; Zhan Aibin; MacIsaac Hugh J; Bailey Sarah ABiological invasions (2014), 16 (4), 793-801 ISSN:1387-3547.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 Rivieres appear to pose the highest risk for new ballast-mediated NIS from the St. Lawrence River to the Great Lakes.
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Abstract
Figure 1
Figure 1. Mean number of trips until ≥1 nonindigenous zooplankton species establishes by ballast water discharge in fresh, brackish, or marine water recipient ports in Canada. The ballast water management methods assessed are no management (NM), exchange only (E), treatment only (T), and exchange plus treatment (E+T). Ballast water treatment was either partially effective (meeting D-2 limit on 50% of ship trips) (PE) or fully effective (meeting D-2 limit on 100% of ship trips) (FE). The error bars represent the bootstrapped 95% confidence intervals of the mean across 1000 single year iterations. Upper confidence intervals with infinite number of trips until ≥1 species establishment occurs are denoted by *. The y-axis is on a logarithmic scale.
References
ARTICLE SECTIONSThis article references 48 other publications.
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- 26Briski, E.; Bailey, S. A.; Casas-Monroy, O.; DiBacco, C.; Kaczmarska, I.; Levings, C.; MacGillivary, M. L.; McKindsey, C. W.; Nasmith, L. E.; Parenteau, M.; Piercey, G.; Rochon, A.; Roy, S.; Simard, N.; Villac, M. C.; Weise, A.; MacIsaac, H. J. Relationship between propagule pressure and colonization pressure in invasion ecology: A test with ships’ ballast. Proc. R. Soc. London, Ser. B 2012, 279, 2990– 2997, DOI: 10.1098/rspb.2011.2671
- 27DiBacco, C.; Humphrey, D. B.; Nasmith, L. E.; Levings, C. D. Ballast water transport of non-indigenous zooplankton to Canadian ports. ICES J. Mar. Sci. 2012, 69, 483– 491, DOI: 10.1093/icesjms/fsr133
- 28Briski, E.; Wiley, C. J.; Bailey, S. A. Role of domestic shipping in the introduction or secondary spread of nonindigenous species: Biological invasions within the Laurentian Great Lakes. J. Appl. Ecol. 2012, 49 (5), 1124– 1130, DOI: 10.1111/j.1365-2664.2012.02186.x
- 29Adebayo, A. A.; Zhan, A.; Bailey, S. A.; MacIsaac, H. J. Domestic ships as a potential pathway of nonindigenous species from the Saint Lawrence River to the Great Lakes. Biol. Invasions 2014, 16 (4), 793– 801, DOI: 10.1007/s10530-013-0537-5[Crossref], [PubMed], [CAS], Google Scholar29https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A280%3ADC%252BB3MzktlWmsw%253D%253D&md5=998e363e9466016001a5118b5bb0109bDomestic ships as a potential pathway of nonindigenous species from the Saint Lawrence River to the Great LakesAdebayo Abisola A; Zhan Aibin; MacIsaac Hugh J; Bailey Sarah ABiological invasions (2014), 16 (4), 793-801 ISSN:1387-3547.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 Rivieres appear to pose the highest risk for new ballast-mediated NIS from the St. Lawrence River to the Great Lakes.
- 30Lee, H., II; Reusser, D. A.; Frazier, M. Approaches to setting organism-based ballast water discharge standards. Ecological Applications 2013, 23, 301– 310, DOI: 10.1890/11-1638.1
- 31Drake, D. A. R.; Casas-Monroy, O.; Koops, M. A.; Bailey, S. A. Propagule pressure in the presence of uncertainty: Extending the utility of proxy variables with hierarchical models. Methods in Ecology and Evolution 2015, 6 (11), 1363– 1371, DOI: 10.1111/2041-210X.12429
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Supporting Information
Supporting Information
ARTICLE SECTIONSThe Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.0c05238.
Information on the Canadian regions examined in this study, model parameter values, probability distributions, sensitivity analysis results, and supplementary model results (PDF)
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