Sarah A. Bailey

Invasion risk posed by macroinvertebrates transported in ships’ ballast tanks

Invasions by non-indigenous macroinvertebrates often cause ecological and economic problems, and commercial ships have been implicated as a principal mechanism for their dispersal. We explored the presence and species diversity of adult macroinvertebrates transported by transoceanic and coastal vessels arriving to ports on the Atlantic coast of Canada. We sampled 67 ballast tanks from 62 ships operating along discrete geographic pathways and tested whether mid-ocean exchange or voyage length affects the probability for translocation of macroinvertebrates. Additionally, we assessed the relationship between macroinvertebrate presence and the amount of sediment in ballast tanks. We document the presence of highly invasive European green crab (Carcinus maenas), mud crab (Rhithropanopeus harrisii), common periwinkle (Littorina littorea), soft shell clam (Mya arenaria) and blue mussel (Mytilus galloprovincialis) in ballast tanks of surveyed ships. Mid-ocean exchange did not affect macroinvertebrate occurrence, suggesting that current ballast water management regulations are ineffective for this taxonomic group. Viable individuals were recorded in vessels undertaking shorter voyages (average and maximum of 4.5 and 15xa0days, respectively) and presence was not related to the amount of sediment in tanks. While presence and densities of macroinvertebrates were low, invasion risk may nonetheless be significant during reproductive seasons owing to high fecundity of some taxa. The highest risk may be posed by decapods since gravid females may carry thousands to several million eggs per clutch, and after several weeks of brooding, two or more subsequent clutches may be fertilized by retained sperm from an earlier mating.

Performance comparison of genetic markers for high-throughput sequencing-based biodiversity assessment in complex communities

Metabarcode surveys of DNA extracted from environmental samples are increasingly popular for biodiversity assessment in natural communities. Such surveys rely heavily on robust genetic markers. Therefore, analysis of PCR efficiency and subsequent biodiversity estimation for different types of genetic markers and their corresponding primers is important. Here, we test the PCR efficiency and biodiversity recovery potential of three commonly used genetic markers – nuclear small subunit ribosomal DNA (18S), mitochondrial cytochrome c oxidase subunit I (COI) and 16S ribosomal RNA (mt16S) – using 454 pyrosequencing of a zooplankton community collected from Hamilton Harbour, Ontario. We found that biodiversity detection power and PCR efficiency varied widely among these markers. All tested primers for COI failed to provide high‐quality PCR products for pyrosequencing, but newly designed primers for 18S and 16S passed all tests. Furthermore, multiple analyses based on large‐scale pyrosequencing (i.e. 1/2 PicoTiter plate for each marker) showed that primers for 18S recover more (38 orders) groups than 16S (10 orders) across all taxa, and four vs. two orders and nine vs. six families for Crustacea. Our results showed that 18S, using newly designed primers, is an efficient and powerful tool for profiling biodiversity in largely unexplored communities, especially when amplification difficulties exist for mitochondrial markers such as COI. Universal primers for higher resolution markers such as COI are still needed to address the possible low resolution of 18S for species‐level identification.

An overview of thirty years of research on ballast water as a vector for aquatic invasive species to freshwater and marine environments

Ballast water has been widely used by commercial vessels to control trim, draft and stability since the late 1870s. While the global transport of ballast water (and associated sediments) was first recognized as a potential dispersal mechanism for plankton in the late 1890s, quantitative research on the issue does not appear in the primary scientific literature until the mid-1980s. Following James T. Carltons comprehensive review of the biology of ballast water in 1985, there was an explosion in research effort, with nearly 400 papers published in the last thirty years. This article provides a brief overview of the role that ballast water has played as a global vector for aquatic invasive species, summarizing the current state of ballast water research and emerging topics for future study, based on a review of articles in the primary scientific literature. Initially, the main research focus was to document the community composition of ballast water in ships arriving to ports around the world. In the late 1990s, risk ssessments examining shipping traffic patterns and environmental tolerances of species likely transported in ballast water dominated. By 2000, ballast water studies examining efficacy of various treatment strategies dominated, and papers exploring new tools and methods for more accurate/representative sampling and analysis of ballast water emerged as an important research topic. There is currently insufficient data to confidently quantify the probability of invasion associated with any particular inoculum density (or discharge standard), as a result, laboratory, field and modeling studies examining the relationship between invasion risk and the size of the initially released population (the ‘risk-release relationship’) are an emerging, high priority field of study.

Sediments in ships: Biota as biological contaminants

Global ports are hubs for industrial activities and trade. In consequence, sediments and water in these areas are often contaminated by an array of chemicals. Sediments also harbour both living, active stages and various diapausing or resting stages of biota. International shipping activities move sediments containing these biotic stages around the world, possibly resulting in biological contamination of port areas. In this study we assess active and resting stages of invertebrates contained in ballast sediment of transoceanic vessels operating on the North American Great Lakes to determine if ballast sediments could serve as a vector of nonindigenous species. A cumulative total of 160 species were identified, including 22 freshwater species not recorded from the Great Lakes basin. Hatch rates of resting stages are affected by thermal conditions, thereby affecting invasion success. Total abundance and species diversity of freshwater invertebrate animals hatched from resting stages were negatively related to salinity of residual water in ballast tanks from which the sediments were obtained, suggesting that ballasting a shallow lens of saltwater may provide some degree of risk reduction from freshwater species invasions.

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

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

Are genetic databases sufficiently populated to detect non-indigenous species?

Correct species identifications are of tremendous importance for invasion ecology, as mistakes could lead to misdirecting limited resources against harmless species or inaction against problematic ones. DNA barcoding is becoming a promising and reliable tool for species identifications, however the efficacy of such molecular taxonomy depends on gene region(s) that provide a unique sequence to differentiate among species and on availability of reference sequences in existing genetic databases. Here, we assembled a list of aquatic and terrestrial non-indigenous species (NIS) and checked two leading genetic databases for corresponding sequences of six genome regions used for DNA barcoding. The genetic databases were checked in 2010, 2012, and 2016. All four aquatic kingdoms (Animalia, Chromista, Plantae and Protozoa) were initially equally represented in the genetic databases, with 64, 65, 69, and 61xa0% of NIS included, respectively. Sequences for terrestrial NIS were present at rates of 58 and 78xa0% for Animalia and Plantae, respectively. Six years later, the number of sequences for aquatic NIS increased to 75, 75, 74, and 63xa0% respectively, while those for terrestrial NIS increased to 74 and 88xa0% respectively. Genetic databases are marginally better populated with sequences of terrestrial NIS of plants compared to aquatic NIS and terrestrial NIS of animals. The rate at which sequences are added to databases is not equal among taxa. Though some groups of NIS are not detectable at all based on available data—mostly aquatic ones—encouragingly, current availability of sequences of taxa with environmental and/or economic impact is relatively good and continues to increase with time.

Assessing introduction risk using species’ rank-abundance distributions

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

Brine-induced mortality of non-indigenous invertebrates in residual ballast water

All transoceanic vessels entering the Great Lakes are required to manage ballast water and ballast tank residuals with ballast water exchange and tank flushing, respectively. While these management procedures effectively reduce the density and richness of biota in ballast waters and thereby reduce the risk of transferring non-indigenous species, some ships are unable to uniformly manage all tanks. Laboratory experiments were conducted to evaluate sodium chloride brine as an emergency treatment for ballast tanks with non-compliant residuals. Invertebrate communities collected from i) Detroit River, ii) exchanged ballast tanks arriving in the Great Lakes, and iii) North Sea ports, were exposed to a range of brine concentrations (15-115‰) until complete mortality was reached. Results indicate that a 1-h exposure to 115‰ brine is a broadly effective treatment (>99.9% mortality) regardless of treatment temperature, taxonomic group, or species source habitat salinity. A median of 0.00% (range 0.00-5.33) of individuals are expected to survive treatment and the expected number of viable individuals released after treatment is within Canadian and proposed international discharge standards. Before implementation, validation with ship-scale trials is recommended.

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.

Survival of ship biofouling assemblages during and after voyages to the Canadian Arctic

Human-mediated vectors often inadvertently translocate species assemblages to new environments. Examining the dynamics of entrained species assemblages during transport can provide insights into the introduction risk associated with these vectors. Ship biofouling is a major transport vector of nonindigenous species in coastal ecosystems globally, yet its magnitude in the Arctic is poorly understood. To determine whether biofouling organisms on ships can survive passages in Arctic waters, we examined how biofouling assemblage structure changed before, during, and after eight round-trip military voyages from temperate to Arctic ports in Canada. Species richness first decreased (~70% loss) and then recovered (~27% loss compared to the original assemblages), as ships travelled to and from the Arctic, respectively, whereas total abundance typically declined over time (~55% total loss). Biofouling community structure differed significantly before and during Arctic transits as well as between those sampled during and after voyages. Assemblage structure varied across different parts of the hull; however, temporal changes were independent of hull location, suggesting that niche areas did not provide protection for biofouling organisms against adverse conditions in the Arctic. Biofouling algae appear to be more tolerant of transport conditions during Arctic voyages than are mobile, sessile, and sedentary invertebrates. Our results suggest that biofouling assemblages on ships generally have poor survivorship during Arctic voyages. Nonetheless, some potential for transporting nonindigenous species to the Arctic via ship biofouling remains, as at least six taxa new to the Canadian Arctic, including a nonindigenous cirripede, appeared to have survived transits from temperate to Arctic ports.