Role of commercial harbours and recreational marinas in the spread of non-indigenous fouling species

The role of commercial harbours as sink and source habitats for non-indigenous species (NIS) and the role of recreational boating for their secondary spread were investigated by analysing the fouling community of five Italian harbours and five marinas in the western Mediterranean Sea. It was first hypothesised that NIS assemblages in the recreational marinas were subsets of those occurring in commercial harbours. However, the data did not consistently support this hypothesis: the NIS pools of some marinas significantly diverged from harbours even belonging to the same coastal stretches, including NIS occurring only in marinas. This study confirms harbours as hotspots for marine NIS, but also reveals that numbers of NIS in some marinas is higher than expected, suggesting that recreational vessels effectively facilitate NIS spread. It is recommended that this vector of NIS introduction is taken into account in the future planning of sustainable development of maritime tourism in Europe.     

A hitchhiker’s guide to the Maritimes: anthropogenic transport facilitates long‐distance dispersal of an invasive marine crab to Newfoundland

Aim To determine timing, source and vector for the recent introduction of the European green crab, Carcinus maenas (Linnaeus, 1758), to Newfoundland using multiple lines of evidence. Location Founding populations in Placentia Bay, Newfoundland, Canada and potential source populations in the north‐west Atlantic (NWA) and Europe. Methods We analysed mitochondrial and microsatellite genetic data from European and NWA populations sampled during 1999–2002 to determine probable source locations and vectors for the Placentia Bay introduction discovered in 2007. We also analysed Placentia Bay demographic data and shipping records to look for congruent patterns with genetic analyses. Results Demographic data and surveys suggested that C. maenas populations are established and were in Placentia Bay for several years (c. 2002) prior to discovery. Genetic data corroboratively suggested central/western Scotian Shelf populations (e.g., Halifax) as the likely source area for the anthropogenic introduction. These Scotian Shelf populations were within an admixture zone made up of genotypes from both the earlier (early 1800s) and later (late 1900s) introductions of the crab to the NWA from Europe. Placentia Bay also exhibited this mixed ancestry. Probable introduction vectors included vessel traffic and shipping, especially vessels carrying ballast water. Main conclusions Carcinus maenas overcame considerable natural barriers (i.e., coastal and ocean currents) via anthropogenic transport to become established and abundant in Newfoundland. Our study thus demonstrates how non‐native populations can be important secondary sources of introduction especially when aided by human transport. Inference of source populations was possible owing to the existence of an admixture zone in central/western Nova Scotia made up of southern and northern genotypes corresponding with the crab’s two historical introductions. Coastal vessel traffic was found to be a likely vector for the crab’s spread to Newfoundland. Our study demonstrates that there is considerable risk for continued introduction or reintroduction of C. maenas throughout the NWA.     

Secondary spread of invasive species: historic patterns and underlying mechanisms of the continuing invasion of the European rockweed Fucus serratus in eastern North America

Post-establishment spread of invasive species is a major determinant of their impact, but the spatial pattern and temporal rhythm of secondary spread are often poorly known or understood. Here we examine the spread of the European rockweed Fucus serratus over 1,500 km of shoreline after its initial discovery in Pictou, Nova Scotia (Canada) in 1868. Building upon earlier periodic surveys, we document the current distribution of this invader and provide a historic analysis of the invasion, including the integration of the recently-detected multiple introductions from Europe. The initial spread was rapid in the southern Gulf of St. Lawrence (6.0 km year⁻¹), likely due to both natural spread in a favorable environment and the extensive regional shipping traffic at the time which linked Pictou to several key ports in eastern Canada and northeast USA. Later spread, especially along the Atlantic coast of Nova Scotia, was slower (recently 0.9 km year⁻¹), but included several major jumps (~50–500 km), undoubtedly due to human-mediated transport. Although the spatial extent of the invasion has increased over the past 140 years, it has experienced several remarkable events: apparent local extinctions of northern satellite populations, a major retraction (100–150 km) along the northwestern limits of its continuous range, and stalled invasions at several points and times during its southward progression. Distributional data suggest that this invader is excluding congeners in shallow zones and possibly kelp species in deeper zones. Genetic data from one contact zone showed hybridization with native F. distichus but no evidence for introgression in migrating F. serratus. Hybridization and several other reproductive traits likely contribute to the competitive dominance of the invader in this environment.     

Recreational boating: a large unregulated vector transporting marine invasive species

Aim Recreational boating is arguably the largest unregulated vector for the introduction and spread of marine invasive species. Hull fouling communities have been recognized to harbour non‐indigenous species (NIS), but presence should not be equated with transport. In this study, we characterize the presence of NIS in hull fouling communities, determine if host vessels transport these species and evaluate the importance of recreational boating as a vector for introduction and spread. Location Coastal British Columbia (BC), Canada. Methods Dive surveys in BC marinas were conducted to record the presence of NIS and to estimate their per cent cover. In addition, a boater questionnaire survey was used to determine common travel and maintenance practices. These results were combined to investigate the potential for recreational boats to transport NIS. Results Nine NIS, including the highly invasive ascidians Styela clava and Botrylloides violaceus, and the macroalga Sargassum muticum, were found in hull fouling communities on recreational boats. Overall, per cent cover was generally low; however, niche areas were commonly fouled, even on active and otherwise clean boats. Fouling of niche areas was not related to either antifouling paint age or travel frequency, and fouling levels were highly variable among individual boats both within marinas and across regions. Main conclusions Recreational boating is a major vector contributing to the spread of marine invasive species. Our results indicate that recreational boats represent a high‐risk vector both for primary introduction and secondary spread of marine NIS and should be subject to vector management regulations.     

A microsatellite-based estimation of clonal diversity and population subdivision in Zostera marina, a marine flowering plant

We examined the genetic population structure in eelgrass (Zostera marina L.), the dominant seagrass species of the northern hemisphere, over spatial scales from 12 km to 10 000 km using the polymorphism of DNA microsatellites. Twelve populations were genotyped for six loci representing a total of 67 alleles. Populations sampled included the North Sea (four), the Baltic Sea (three), the western Atlantic (two), the eastern Atlantic (one), the Mediterranean Sea (one) and the eastern Pacific (one). Microsatellites revealed substantial genetic variation in a plant group with low allozyme diversity. Average expected heterozygosities per population (monoclonal populations excluded) ranged from 0.32 to 0.61 (mean = 0. 48) and allele numbers varied between 3.3 and 6.7 (mean = 4.7). Using the expected frequency of multilocus genotypes within populations, we distinguished ramets from genetic individuals (i.e. equivalent to clones). Differences in clonal diversity among populations varied widely and ranged from maximal diversity (i.e. all ramets with different genotype) to near or total monoclonality (two populations). All multiple sampled ramets were excluded from further analysis of genetic differentiation within and between populations. All but one population were in Hardy-Weinberg equilibrium, indicating that Zostera marina is predominantly outcrossing. From a regression of the pairwise population differentiation with distance, we obtained an effective population size Ne of 2440-5000. The overall genetic differentiation among eelgrass populations, assessed as rho (a standardized estimate of Slatkin's RST) was 0.384 (95% CI 0.34-0.44, P < 0.001). Genetic differentiation was weak among three North Sea populations situated 12-42 km distant from one another, suggesting that tidal currents result in an efficient exchange of propagules. In the Baltic and in Nova Scotia, a small but statistically significant fraction of the genetic variance was distributed between populations (rho = 0.029-0. 053) at scales of 15-35 km. Pairwise genetic differentiation between European populations were correlated with distance between populations up to a distance of 4500 km (linear differentiation-by-distance model, R2 = 0.67). In contrast, both Nova Scotian populations were genetically much closer to North Sea and Baltic populations than expected from their geographical distance (pairwise rho = 0.03-0.08, P < 0.01). A biogeographical cluster of Canadian with Baltic/North Sea populations was also supported using a neighbour-joining tree based on Cavalli-Sforza's chord distance. Relatedness between populations may be very different from predictions based on geographical vicinity.     

Regional connectivity and coastal expansion: differentiating pre‐border and post‐border vectors for the invasive tunicate Styela clava

The dramatic increase in marine bio‐invasions, particularly of non‐indigenous ascidians, has highlighted the vulnerability of marine ecosystems and the productive sectors that rely on them. A critical issue in managing invasive species is determining the relative roles of ongoing introductions, versus the local movement of propagules from established source populations. Styela clava (Herdman, 1882), the Asian clubbed tunicate, once restricted to the Pacific shores of Asia and Russia, is now abundant throughout the northern and southern hemispheres and has had significant economic impact in at least one site of incursion. In 2005 S. clava was identified in New Zealand. The recent introduction of this species, coupled with its restricted distribution, provided an ideal model to compare and contrast the introduction and expansion process. In this study, the mitochondrial DNA cytochrome oxidase subunit I gene (COI) gene and 11 microsatellite markers were used to test the regional genetic structure and diversity of 318 S. clava individuals from 10 populations within New Zealand. Both markers showed significant differentiation between the northern and southern populations, indicative of minimal pre‐ or post‐border connectivity. Additional statistics further support pre‐ and post‐border differentiation among Port and Harbour populations (i.e. marinas and aquaculture farms). We conclude that New Zealand receives multiple introductions, and that the primary vector for pre‐border incursions and post‐border spread is most likely the extensive influx of recreational vessels that enter northern marinas independent of the Port. This is a timely reminder of the potential for hull‐fouling organisms to expand their range as climates change and open new pathways.     

A preliminary examination of genetic variation in a peripheral population of Blanding's turtle, Emydoidea blandingii

Random amplified polymorphic DNA (RAPD) was used to compare the Nova Scotia population of Blanding's turtle (Emydoidea blandingii) with several populations from the species' main range. The Nova Scotia population is believed to have been isolated from the main range for 4000-8000 years. Cluster analysis using a neighbour-joining algorithm produced a dendrogram showing the Nova Scotia population clustering separately from those populations in the main range. Analysis of molecular variance shows 34.28% of total variance to be accounted for between the Nova Scotia population and populations in the main range. While this study is preliminary, the results suggest that the Nova Scotia population of Blanding's turtle may be important to the maintenance of genetic diversity in the species.     

Genetic diversity and relatedness in aquaculture and marina populations of the invasive tunicate Didemnum vexillum in the British Isles

Introductions of invasive, non-native species in the marine environment are increasing as human activity within coastal areas rises. Genetic datasets are useful tools to identify source populations, track routes of invasions, and illuminate the role of genetic variation in the establishment and subsequent spread of novel introductions. Here, a microsatellite dataset is used to estimate the genetic diversity and population structure of 7 introduced Didemnum vexillum populations in Britain and Ireland, 4 of which are associated with aquaculture and 3 with marinas. Genetic differentiation observed between these populations indicates human-mediated transport as the main mechanism underlying the population structure of D. vexillum in Britain and Ireland. In addition to elucidating patterns of population structure we found that aquaculture sites showed significantly higher genetic diversity (measured as allelic richness) in comparison to the marina sites. We discuss these findings in relation to the history of each invasion, the complex life history of D. vexillum, and available evidence of the relative invasiveness of these populations. Our results show numerous interesting patterns which highlight further research avenues to elucidate the complex factors underlying the global spread of this successful invader.

     

Predicting and mapping the risk of introduction of marine non-indigenous species into Great Britain and Ireland

Non-indigenous species (NIS) can have adverse environmental, economic and social impacts. Their management is now incorporated into key legislation, including the European Union (EU) Marine Strategy Framework Directive and the EU Regulation on the prevention and management of the introduction and spread of invasive alien species. Prevention of NIS introductions and the early detection of NIS following their introduction are recognised as the most effective approaches for reducing the potential impacts of NIS. This is true for most aquatic environments but especially so for the marine environment, where control and/or eradication are often not achievable. By assessing introduction vector activity, it is possible to identify coastal areas and specific locations where marine NIS may be more likely to be introduced. This study uses data relating to the activity of key introduction vectors; shipping, recreational boating and live animal aquaculture import, to estimate the relative risk of introduction of NIS around coastal regions of Great Britain and Ireland. Spatial analysis was used to create “heat” maps indicating coastal areas of increased relative risk of introduction of NIS by these vectors. The results of the present study will be crucial for the implementation of targeted vector management plans, supporting preventive strategies, and will facilitate a risk analyses of NIS threats to inform monitoring and surveillance programmes.     

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

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

Population genetics of an invasive species,Heracleum mantegazzianum: implications for the role of life history,demographics and independent introductions

The population genetic structure of an invasive, nonindigenous riparian weed (Heracleum mantegazzianum) in the northeast of England was investigated using microsatellite DNA markers. Data were used to assess the size and frequency of introductions into three catchments and the subsequent spread. We sampled 13 populations, including a remote population (Perivale, London) for comparison. Five loci were screened and considerable variation was found. Results revealed greater overall variation between populations from different catchments than those in the same catchment, and suggested the generation of population structure in the relatively short time since the initial introduction. Between-catchment variation may reflect population structure generated by local founders as the species spread and may indicate a large initial founder population at the time of the introduction into Britain, or multiple introductions. Within-catchment variation was consistent with expectations based on the water-borne dispersal of seeds in this species, and the relatively small dispersal range of likely pollinators. Independent introductions stand out in some cases as exceptions to the general pattern. Taken together the results are consistent with a relatively large initial founder population, and the subsequent spread of the species in local founder populations, followed by some level of inbreeding within local populations and novel introductions in some localities.     

Environmental and ecological changes associated with a marina

Anthropogenic modifications to waterways are common and their ecological consequences must be understood to effectively conserve local biodiversity. The facilitation of recreational boating activities often requires substantial alteration of natural areas, however the environmental and ecological consequences of such alterations are rarely described in the scientific literature. In this study, ecological and physico-chemical conditions were investigated in a recreational boating marina, located inside a marine park on the south-east coast of Australia. Recruitment panels were deployed for 8?weeks both inside and outside the marina, and differences in the composition of the developing fouling communities were observed. The recruitment of taxa, which often have short-lived larvae, was increased inside the marina (bryozoans, spirorbids and sponges) while the recruitment of taxa, which often have longer-lived larvae, was reduced or absent (barnacles, solitary ascidians and non-spirorbid polychaetes). Differences were also observed in environmental conditions inside the marina cf. directly outside. The marina environment had higher turbidity, temperature and pH along with higher concentrations of lead and copper in suspended sediments, while flow rates and trapped sediment loads were reduced inside the marina. The differences observed in the study suggest that there may be marked environmental changes associated with marina developments. The potential ecological consequences of these changes should be a primary consideration during the planning process, particularly for developments in locations of notable ecological value.     

Starting the invasion pathway: the interaction between source populations and human transport vectors

Human transport hubs, such as shipping ports, airports and mail centers are important foci for the spread of non-indigenous species. High relative abundance in a transport hub has been proposed as a correlate of invasion success, since abundant species are thought more likely to colonize vectors and to be transported more frequently. We here evaluate the relative importance of vector characteristics and local source assemblages in determining the pool of species that is transported by hull fouling on recreational boats. We compared the resident fouling communities of three recreational boat harbors in Australia with the assemblages on the hulls of boats that travel between them. We used data on the recent travel and maintenance history of the boats to evaluate correlates of transport probability and the potential for intra-coastal spread of fouling organisms. Invertebrate assemblages on heavily fouled vessels reflected the composition of biotic assemblages within the marina in which they were moored, but by itself, relative abundance in the source port was not a reliable predictor of transport probability. More important was the age of the antifouling paint on the vessels’ hulls, which acted selectively on some groups of organisms. Movements of vessels were characterized by “fidelity” (vessels remaining close to homeport) interspersed with “promiscuity” (vessels traveling to a diverse pool of destinations). In an infested harbor, measures taken to increase the resistance of vectors to colonization by the invader should be effective in slowing the rate of spread to other locations, by decreasing the overall frequency of transport.     

Parasitism and predation as agents of mortality of winter moth populations in neglected apple orchards in Nova Scotia

Abstract.

• 1 This study compared the roles of pupal mortality and parasitism in winter moth (Operophtera brumata) population dynamics in Nova Scotian apple orchards and assessed the importance of beetles as pupal predators.
• 2 The component of pupal mortality termed predation accounted for greater stage-specific mortality of winter moth than parasitism by Cyzenis albicans in four neglected orchards.
• 3 Parasitism by Cyzenis albicans was not spatially density-dependent in any orchard, whereas the predation component of pupal mortality was spatially density-dependent in the two orchards most densely populated by winter moth.
• 4 Field experiments indicated that over 60% of pupal predation may be attributed to beetles, and that about 46% of pupal predation occurred within 4 weeks after pupal drop.
• 5 Mortality of introduced populations of winter moth in Nova Scotia resembles that of native populations in England where density-dependent predation regulates the winter moth population and reduces the parasitoid population to minimal levels. The situation in Nova Scotia appears to have changed appreciably since the establishment of parasitoids into the system in the 1950s.

     

Effects of two marinas on the composition of fouling assemblages

The composition of fouling assemblages was surveyed inside and near two fully enclosed marinas using settlement plates. The location of a plate, inside or outside the marina, influenced the abundances of four functional groups of fouling organisms (solitary ascidians, arborescent bryozoans, encrusting bryozoans and colonial ascidians). Transplantation of mature assemblages revealed that reductions in the abundance of arborescent bryozoans inside marinas might be explained by increased growth and recruitment of these bryozoans outside the marina. Surveys of settlement revealed decreased recruitment of encrusting bryozoans inside the marinas, a result consistent with patterns of adult abundance. It is proposed that an increased abundance of solitary ascidians inside marinas may be due to decreased competition. A second survey of adult assemblages was performed with multiple ‘Outside’ sites per marina. Effects of location consistent with the first survey were found for arborescent bryozoans, and in one marina area for solitary ascidians and encrusting bryozoans, but not in the other. Although mechanisms can be proposed to explain the effects of the marina (inside or outside) on the abundances of solitary ascidians, arborescent bryozoans and encrusting bryozoans, the second survey revealed that the effects may vary among marinas.     

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

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

Boat harbour design can exacerbate hull fouling

Abstract Hull fouling is a major cost for owners of small vessels and an important pathway for the spread of non‐indigenous aquatic species. The extent of fouling depends on a hull's susceptibility to recruitment by aquatic organisms and the local availability of competent planktonic propagules (‘propagule pressure’). Management strategies have typically been concerned with increasing resistance of the hull to recruitment through the use of toxic paints. Here we tested the hypothesis that fouling is influenced by the design of the harbour in which the boat is moored. We compared recruitment of sessile invertebrates to available surfaces in two types of recreational boat harbours: marinas that were partially enclosed by a permanent breakwall, and marinas that lacked breakwalls. Recruitment in the marinas was compared to coastal reference sites that were not used for mooring. At each location, recruitment tiles were deployed for 4 weeks on four separate occasions over a period of 2 years. Measurements of current velocities and spatial patterns of water flow at each location showed that permanent breakwalls created complex patterns of circulation that retained water within the marina basin for up to 12 h d^?1. Despite large regional and temporal variability in fouling over time, most organisms recruited in greatest numbers to surfaces in partially enclosed marinas, and were often several orders of magnitude more abundant in the enclosed marinas than in unenclosed marinas or coastal reference locations. Harbour design has an important influence on the rate at which fouling organisms recruit to available surfaces within marinas. Entrainment of water in enclosed marinas may limit the dispersal of planktonic propagules by advective currents but effectively increases propagule pressure to available surfaces, including resident boat hulls. This is likely to accelerate the development of hull‐fouling assemblages and increase the chances of transport of non‐indigenous species that establish populations in the harbour basin.     

Genetic diversity and colony breeding structure in native and introduced ranges of the Formosan subterranean termite, Coptotermes formosanus

The Formosan subterranean termite, Coptotermes formosanus is recognized as one of the most important invasive pest species. Originating from China, C. formosanus has spread to many tropical and subtropical regions around the globe in the last 400 years, including Japan, Hawaii and the continental USA. Although the current distribution is well documented, information about the patterns of invasion and effects of introduction on the population genetics of this species is largely lacking. We analyzed the genetic structure of populations from two native populations (Guangdong and Hunan provinces, China) and two introduced populations (Maui and Kauai, Hawaii) using microsatellite genotyping. We also reanalyzed published data of additional populations from China, Japan, Hawaii, and the continental USA. The population from Hunan, the earliest introduction outside of China (Japan) and the first introduction to the continental USA (South Carolina) showed little genetic similarity with any of the native or introduced populations investigated. However, populations from Oahu (HI), New Orleans (LA) and Rutherford County (NC) showed close similarity. In general, genetic patterns suggest multiple introductions to the USA, with, for example, two separate introductions to the island of Maui. Bottleneck effects were detected in almost all recent introductions (after 1940). All populations in the introduced range showed lower genetic diversity than those in the native range. However, this low genetic diversity did not result in the formation of polygynous supercolonies as has been described for other invasive termite and ant species.     

Linking environmental conditions and ship movements to estimate invasive species transport across the global shipping network

Aim Some nations, and the International Maritime Organization, are moving towards requirements for managing ballast water to reduce the number of alien species transported and released. These and other measures will be most efficient when targeted at ships posing the greatest risks. Here, we analyse world‐wide ship movements and port environmental conditions to explore how these risk components differ across arriving ships. Location Global, with a case study of the Laurentian Great Lakes. Methods We gathered salinity and temperature data for all global shipping ports, and data for all global ship movements during a 12 ‐month period. We applied these data to the Laurentian Great Lakes to determine which global ports may donate new species to the Great Lakes via ship traffic, and which are most environmentally similar to the Great Lakes. Results We show that ships regularly travel to the Great Lakes from all major coastal, and many inland, regions of the world. Most global ports, and thus the species in them, are separated from the Great Lakes by no more than two ship voyages. Combined with a measure of environmental similarity among global ports, we identify ship routes likely to transport species adapted for survival in the Great Lakes and global regions that may be the source of increasing future invasions. Main conclusions The Great Lakes account for a small fraction of global shipping yet are closely connected to all other ports, and the species in them, by the shipping network. Our methods and data allow risks from individual ships to be ranked so that management activities can be targeted at ships most likely to introduce new invaders. Because our data sets are global, they could be applied to ship arrivals at any global port.