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.     

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

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

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

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

Detection of a colonizing, aquatic, non-indigenous species

Detecting the presence of rare species has interested ecologists and conservation biologists for many years. A particularly daunting application of this problem pertains to the detection of non-indigenous species (NIS) as they colonize new ecosystems. Ethical issues prevent experimental additions of NIS to most natural systems to explore the relationship between sampling intensity and the detection probability of a colonizing NIS. Here we examine this question using a recently introduced water flea, Cercopagis pengoi , in Lake Ontario. The species has biphasic population development, with sexually-produced 'spring morphs' developing prior to parthenogenetically-produced 'typical' morphs. Thus, this biphasic morphology allows distinction between new colonists (spring morphs) from subsequent generations. We repeatedly sampled Hamilton Harbour, Lake Ontario for the presence of both spring and typical morphs. Probability of detection was positively related to both the number of samples taken and animal density in the lake; however, even highly intensive sampling (100 samples) failed to detect the species in early spring when densities were very low. Spatial variation was greatest when densities of Cercopagis were intermediate to low. Sub-sampling, which increased space between adjacent samples, significantly decreased the number of samples required to reach greater, calculated detection probabilities on these dates. Typical sampling protocols for zooplankton have a low probability (< 0.2) of detecting the species unless population density is high. Results of this study suggest that early detection of colonizing, aquatic NIS may be optimized through use of a risk-based sampling design, combined with high sampling intensity in areas deemed most vulnerable to invasion, rather than less intensive sampling at a wider array of sites.     

Relative risk assessment for ballast-mediated invasions at Canadian Arctic ports

Vector-based risk assessment is a powerful and efficient management approach for nonindigenous species (NIS). By managing a vector, an entire assemblage of associated NIS is simultaneously considered. The majority of current risk assessment frameworks have been conducted for a single, or selected few, target species and thus are not useful for managing vectors transporting a large number of potentially unknown species. Here we develop a predictive framework to assess relative invasion risk for a vector (ballast water) transporting an unknown species assemblage, using the Canadian Arctic as a case study. Ballast water discharge is a known high-risk vector globally, but its magnitude in the Arctic has not been well characterized. Our framework determined relative invasion risks between different transit pathways by quantifying the probability of NIS successfully transiting all stages of the invasion process and the magnitude of consequences of introduction to those ports. Churchill, Manitoba was ranked at ‘higher’ invasion risk via ballast water discharged by international merchant vessels than any other recipient port studied. The overall pattern of ballast water discharge suggests that water originating from coastal domestic sources carried by international merchant vessels may be important for dispersal of NIS. In addition, ballast-mediated NIS are more likely to arrive to the Hudson Bay region during summer months. These results can be useful for developing prevention and early detection programs for the region. Our risk assessment framework is not limited to ballast water and could be applied to other vectors for effective management of NIS.     

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.     

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

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

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.     

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.     

Paradox lost: genetic diversity and the success of aquatic invasions

There is mounting evidence that reduced genetic diversity in invasive populations is not as commonplace as expected. Recent studies indicate that high propagule vectors, such as ballast water and shellfish transplantations, and multiple introductions contribute to the elimination of founder effects in the majority of successful aquatic invasions. Multiple introductions, in particular, can promote range expansion of introduced populations through both genetic and demographic mechanisms. Closely related to vectors and corridors of introduction, propagule pressure can play an important role in determining the genetic outcome of introduction events. Even low-diversity introductions have numerous means of avoiding the negative impact of diversity loss. The interaction of high propagule vectors and multiple introductions reveal important patterns associated with invasion success and deserve closer scrutiny.     

Post-exchange zooplankton in ballast water of ships entering the San Francisco Estuary

The San Francisco Estuary in California (CA), USA, has beenheavily altered by invasions of nonnative zooplankton and benthicorganisms, presumably by the discharge of ships’ ballastwater. Since 2000, ships entering CA have been required to exchangeballast water with oceanic water during the voyage to decreasethe number of organisms discharged into the Estuary that hadpreviously been taken aboard at foreign ports. We examined abundanceof zooplankton in ballast water of 18 container ships and 48bulk carriers. Asia dominated the sources of ballast water,which contained multiple nonnative zooplankton including speciesthat have invaded and since become common residents in the Estuary.The abundance of zooplankton was significantly lower in ballastwater that had been emptied and refilled with oceanic waterthan those that had continuously been flushed with oceanic water(about three times the volume of ballast water), suggestingthat empty–refill is more effective in removing exoticzooplankton.     

Changes and drivers of zooplankton diversity patterns in the middle reach of Yangtze River floodplain lakes,China

Anthropogenic habitat alteration interferes the natural aquatic habitats and the system''s hydrodynamics in the Yangtze River floodplain lakes, resulting in a serious decline in freshwater biodiversity. Zooplankton communities possess major position in freshwater ecosystems, which play essential parts in maintaining biological balance of freshwater habitats. Knowledge of processes and mechanisms for affecting variations in abundance, biomass, and diversity of zooplankton is important for maintaining biological balance of freshwater ecosystems. Here, we analyzed that the temporal and spatial changes in the structure of zooplankton community and their temporal and spatial variations respond to changes in environmental factors in the middle reach of Yangtze River floodplain lakes. The results showed that zooplankton samples were classified into 128 species, and Rotifera was the most common taxa. Significant seasonal differences were found among the abundance and diversity of zooplankton. Similarly, we also found significant seasonal differences among the biomass of zooplankton functional groups. The spatial turnover component was the main contributor to the β diversity pattern, which indicated that study areas should establish habitat restoration areas to restore regional biodiversity. The NMDS plot showed that the structure of zooplankton community exhibited significant seasonal changes, where the community structure was correlated with pH, water temperature, water depth, salinity, total nitrogen, chlorophyll‐a, and total phosphorus based on RDA. This study highlights that it is very important to ensure the floodplain ecosystem''s original state of functionality for maintaining the regional diversity of the ecosystem as a whole.     

A biological survey of ballast water in container ships entering Hong Kong

The role of ballast water in the introduction of exotic species has recently received extensive attention. The aim of this study is to assess the importance of ballast water discharge as a vector for the introduction of exotic species into Hong Kong waters. Twelve ballast water samples were collected from 5 container ships entering Hong Kong between June1994 and October 1995. The ballast water originated from ports on both sides of the Pacific Ocean. At least 81 species from 8 animal phyla and 5 protist phyla were found. Most of the major marine taxonomic groups were represented and many planktonic larval stages were included. Species richness in the ballast tanks decreased with the age of ballast water. Copepoda was the most diverse and abundant taxonomic group. The density of calanoid and cyclopoid copepods decreased with the age of ballast water, but that of harpacticoid copepods did not change significantly with time. Bivalve, crustacean, polychaete and ascidian larvae from ballast water samples were observed to settle in laboratory culture tanks. The mussel Mytilopsis sallei which was introduced to Hong Kong in 1980, was one of the bivalves that settled readily. Results of this study indicate that ballast water can be a major source for the introduction of exotic species to Hong Kong waters. Regulatory guidelines on the discharge of ballast water should be established. This revised version was published online in August 2006 with corrections to the Cover Date.     

Genetic diversity is positively associated with fine‐scale momentary abundance of an invasive ant

Many introduced species become invasive despite genetic bottlenecks that should, in theory, decrease the chances of invasion success. By contrast, population genetic bottlenecks have been hypothesized to increase the invasion success of unicolonial ants by increasing the genetic similarity between descendent populations, thus promoting co‐operation. We investigated these alternate hypotheses in the unicolonial yellow crazy ant, Anoplolepis gracilipes, which has invaded Arnhem Land in Australia's Northern Territory. We used momentary abundance as a surrogate measure of invasion success, and investigated the relationship between A. gracilipes genetic diversity and its abundance, and the effect of its abundance on species diversity and community structure. We also investigated whether selected habitat characteristics contributed to differences in A. gracilipes abundance, for which we found no evidence. Our results revealed a significant positive association between A. gracilipes genetic diversity and abundance. Invaded communities were less diverse and differed in structure from uninvaded communities, and these effects were stronger as A. gracilipes abundance increased. These results contradict the hypothesis that genetic bottlenecks may promote unicoloniality. However, our A. gracilipes study population has diverged since its introduction, which may have obscured evidence of the bottleneck that would likely have occurred on arrival. The relative importance of genetic diversity to invasion success may be context dependent, and the role of genetic diversity may be more obvious in the absence of highly favorable novel ecological conditions.     

Multiple introductions and invasion pathways for the invasive ctenophore Mnemiopsis leidyi in Eurasia

The introduction and spread of non-indigenous species (NIS) in marine ecosystems accelerated during the twentieth century owing to human activities, notably international shipping. Genetic analysis has proven useful in understanding the invasion history and dynamics of colonizing NIS and identifying their source population(s). Here we investigated sequence variation in the nuclear ribosomal Internal Transcribed Spacer region of the ctenophore Mnemiopsis leidyi, a species considered one of the most invasive globally. We surveyed four populations from the native distribution range along the Atlantic coasts of the United States and South America, as well as six populations in the introduced range from the Black, Azov, Caspian and Baltic seas. Allelic and nucleotide diversity of introduced populations were comparable to those of native populations from which they were likely drawn. Introduced populations typically exhibited lower genetic differentiation (F _ST = ?0.014?C0.421) than native populations (F _ST = 0.324?C0.688). Population genetic analyses supported the invasion of Eurasia from at least two different pathways, the first from the Gulf of Mexico (e.g., Tampa Bay) to the Black Sea and thence to the Caspian Sea, the second from the northern part of the native distribution range (e.g., Narragansett Bay) to the Baltic Sea. The relatively high genetic diversity observed in introduced populations is consistent with large inocula and/or multiple invasions, both of which are possible given ballast water transport and the extensive native distribution of the ctenophore in the Atlantic Ocean.     

Genomics reveals the history of a complex plant invasion and improves the management of a biological invasion from the South African–Australian biotic exchange

Many plants exchanged in the global redistribution of species in the last 200 years, particularly between South Africa and Australia, have become threatening invasive species in their introduced range. Refining our understanding of the genetic diversity and population structure of native and alien populations, introduction pathways, propagule pressure, naturalization, and initial spread, can transform the effectiveness of management and prevention of further introductions. We used 20,221 single nucleotide polymorphisms to reconstruct the invasion of a coastal shrub, Chrysanthemoides monilifera ssp. rotundata (bitou bush) from South Africa, into eastern Australia (EAU), and Western Australia (WAU). We determined genetic diversity and population structure across the native and introduced ranges and compared hypothesized invasion scenarios using Bayesian modeling. We detected considerable genetic structure in the native range, as well as differentiation between populations in the native and introduced range. Phylogenetic analysis showed the introduced samples to be most closely related to the southern‐most native populations, although Bayesian analysis inferred introduction from a ghost population. We detected strong genetic bottlenecks during the founding of both the EAU and WAU populations. It is likely that the WAU population was introduced from EAU, possibly involving an unsampled ghost population. The number of private alleles and polymorphic SNPs successively decreased from South Africa to EAU to WAU, although heterozygosity remained high. That bitou bush remains an invasion threat in EAU, despite reduced genetic diversity, provides a cautionary biosecurity message regarding the risk of introduction of potentially invasive species via shipping routes.     

遗传多样性与外来物种的成功入侵: 现状和展望

遗传多样性被认为是影响外来种入侵成功的重要因素之一。研究表明, 尽管外来种在入侵过程中可能受到奠基者效应的影响, 但是多次引种、种内或种间杂交等过程使得许多外来种在引入地的遗传多样性水平未必会显著低于原产地, 从而使得外来种可能通过快速进化来适应引入地的新生境。然而, 高水平的遗传多样性并非成功入侵的必要条件, 遗传变异的匮乏对一些外来种的入侵能力没有明显的影响, 甚至在一些生物入侵案例中, 遗传多样性的降低反而促进了入侵成功。针对遗传多样性与入侵成功之间的复杂关系, 本文在评述外来种遗传多样性的研究现状的基础上, 分析了遗传多样性对外来种的短期入侵成功和长期进化的影响机制, 从方法角度探讨了目前研究中存在的若干问题, 并对如何推进入侵生态学研究提出了一些看法。正如一些学者提出的, 入侵生态学需要与生态学其他分支整合起来, 才能加深对生物入侵及其相关的生态和进化过程的理解。     

Genetic diversity and population structure of invasive and native populations of Erigeron canadensis L.

小蓬草入侵地和原产地种群的遗传多样性和种群结构 外来入侵植物对全球生物多样性造成了危害。小蓬草(Erigeron canadensis L.)是危害最为严重的外来农业杂草之一,代表了洲际入侵的典型例子。本研究利用10个多态性SSR位点,分别对采自中国江苏和浙江省的入侵地和采自美国阿拉巴马州的原产地各5个种群、共计312个植株的基因型进行了遗传多样性和遗传结构分析。结果表明,江苏省和浙江省的入侵种群显示出与阿拉巴马州原产地种群相似的遗传多样性,表明入侵期间没有严重的遗传瓶颈。利用STRUCTURE对种群结构的分析结果显示,种群之间分化较低,在原产地和入侵范围内均只仅检测到两个基因群。在入侵种群中观察到的遗传多样性较高,表明在入侵初期可能存在多次引入或引入了遗传背景不同的繁殖体。上述研究为阐明小蓬草这一全球有害杂草在中国东部的入侵动态提供了新的证据。在防除实践中,应注意防范小蓬草入侵种群和本地种群之间的种子基因流传播,阻止除草剂抗性植株的引入和扩散。     

Does saltwater flushing reduce viability of diapausing eggs in ship ballast sediment?

Flushing of ballast tanks with seawater has been proposed to reduce the risk of invasion associated with residual ballast in 'no ballast on board' ships. The efficacy of this procedure, however, has not been determined. Using diapausing eggs isolated from ballast sediments — as well as from Lake Erie sediment — this study investigated the impact of salinity (0, 8 and 35‰) and temperature (10, 20 and 30 °C) on the cumulative abundance and species richness of hatched zooplankton taxa. The rate and amount of hatching varied dramatically between sediments and across salinity–temperature regimes. Although exposure to saline water inhibited emergence of freshwater taxa during the exposure phase of all trials, mixed results were evident after diapausing eggs were returned to freshwater. The efficacy of salinity as a ballast treatment method was temperature dependent, although the direction of the effect was case-specific. Exposure of eggs to saline water was less effective at 10 and 30 °C than at 20 °C. Although flushing ballast tanks with open ocean water is expected to significantly reduce the number of active invertebrates living in residual ballast water (a potentially larger source of invaders), our results indicate that the most effective treatment conditions for reduction of diapausing egg viability is 8‰ salinity at 20 °C.