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.     

Selectivity in vector management: an investigation of the effectiveness of measures used to prevent transport of non-indigenous species

Measures taken to control the spread of non-indigenous species by human vectors may act selectively by providing effective protection against some (but not all) species. Toxic antifouling paints are used by boat owners to prevent the development of fouling assemblages on the hulls of their boats, which reduce vessel speed and maneuverability. By reducing fouling, these paints also prevent transport of non-indigenous species. Using experimental surfaces mimicking boat hulls, we evaluated the effectiveness and selectivity of (1) antifouling paints, and (2) manual, in-water hull cleaning for preventing the transport of marine sessile invertebrates by recreational vessels. Different types of antifouling paints provided effective protection only against barnacles and bivalves. Other fouling taxa occurred on experimental surfaces after a period of only 2 months. Manual hull cleaning did not remove fouling completely, and even enhanced the risk of subsequent recruitment by some fouling organisms. Up to six times more individuals and colonies recruited to boat surfaces from which the existing fouling organisms had been removed manually than to surfaces that had been sterilized or contained intact fouling assemblages. Bivalves, colonial and solitary ascidians, encrusting bryozoans, hydroids, tubiculous polychaetes, and sponges consistently recruited in greatest abundance to manually cleaned surfaces. Individual taxa responded in complex, but predictable ways to the biogenic cues left by manual cleaning, so that different suites of organisms colonized surfaces that had originally contained fouling assemblages of local or non-local origin. Our study shows that widely adopted measures to control the spread of non-indigenous species by human vectors are often highly selective and, while effective for some taxa, do not prevent the transport of others.     

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.     

Benthic assemblages,biodiversity and invasiveness in marinas and commercial harbours: an investigation using a bioindicator group

Fouling communities on artificial marine structures are generally different from benthic communities in natural rocky habitats. However, they may also differ among different types of artificial structures. Two artificial structures in direct contact with arriving vessels were compared: floating pontoons within recreational marinas, and sea-walls within commercial harbours. Natural rocky habitats were used as a reference, and the genus Eudendrium (Cnidaria, Hydrozoa) was chosen as a bioindicator. The assemblages were different among the three types of habitat studied, with different species characterising each habitat. The probability of finding an invasive Eudendrium species was significantly higher on pontoons. Diversity was the lowest on pontoons, but it was not significantly different between sea-walls and natural rocks. In general, a barrier to the spread of exotic species exists between harbours and natural rocky habitats. Floating pontoons seem to be a less suitable habitat for native fauna and a key element in marine biological invasions.     

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.     

Animal trade and non-indigenous species introduction: the world-wide spread of squirrels

Aim  In this study, a dataset on world-wide squirrel introductions has been used to locate the relative pathways and to determine the factors correlated with species establishment.
Location  The world.
Methods  The analysis includes a chronological table of introductions, a biogeographical analysis and an assessment of the likelihood of establishment according to species, propagule pressure, area of origin and characteristics of the recipient area.
Results  The main vector of such introductions was the intentional importation of live animals. Introductions increased in developed countries and proportionately to the volume of imported mammals. Moreover, areas characterized by higher numbers of native squirrels were more invaded. Squirrels were often introduced deliberately and only to a smaller extent escaped from captivity. The likelihood of their establishment increased proportionately to the number of animals released and decreased proportionately to the increase of the latitudinal distance between the recipient area and the native range of the species. The likelihood that the release of one pair of either Sciurus or Callosciurus species would establish a new population was higher than 50%.
Main conclusion  Squirrels proved to be successful invaders and their importation should be restricted so as to prevent further introductions.     

Comparison of methods for estimating the spread of a non-indigenous species

Aim  To compare different quantitative approaches for estimating rates of spread in the exotic species gypsy moth, Lymantria dispar L., using county-level presence/absence data and spatially extensive trapping grids.
Location  USA
Methods  We used county-level presence/absence records of the gypsy moth's distribution in the USA, which are available beginning in 1900, and extensive grids of pheromone-baited traps, which are available in selected areas beginning in 1981. We compared a regression approach and a boundary displacement approach for estimating gypsy moth spread based on these sources of data.
Results  We observed relative congruence between methods and data sources in estimating overall rates of gypsy moth spread through time, and among regions.
Main conclusions  The ability to estimate spread in exotic invasive species is a primary concern in management programmes and one for which there is a lack of information on the reliability of methods. Also, in most invading species, there is generally a lack of data to explore methods of estimating spread. Extensive data available on gypsy moth in the USA allowed for such a comparison. We show that, even with spatially crude records of presence/absence, overall rates of spread do not differ substantially from estimates obtained from the more costly deployment of extensive trapping grids. Moreover, these methods can also be applied to the general study of species distributional changes, such as range expansion or retraction, in response to climate change or other environmental effects.     

‘Flying barnacles’: implications for the spread of non-indigenous species

The presence of adult barnacles of Fistulobalanus pallidus (Darwin) and Fistulobalanus albicostatus (Pilsbry) attached to field-readable plastic leg rings on the Lesser Black-backed Gull Larus fuscus in Northern Europe is reported. L. fuscus is a long-distance palaearctic migrant, breeding in temperate areas spreading widely over inland and marine habitats outside the breeding season. The species is known to perform long-distance migration to Africa and the Middle East. Combining present knowledge on the birds' migratory pattern and the home range of the barnacle species, it is concluded that the cypris larvae of F. pallidus must have settled in African waters, whereas the area where F. albicostatus settled on the bird leg rings is less certain. The barnacles were of adult size and must thus have been attached for a period of no less than 2 months. More than 30 individual barnacles could occur together on a single field-readable plastic leg ring. The barnacles could therefore, if ported alive to a new area, reproduce successfully and thus either introduce the species or genetically affect other native populations. This may pose a new and wholly unexpected transportation pathway for barnacles as invasive species.     

The potential for translocation of marine species via small-scale disruptions to antifouling surfaces

Vessel hull fouling is a major vector for the translocation of nonindigenous species (NIS). Antifouling (AF) paints are the primary method for preventing the establishment and translocation of fouling species. However, factors such as paint age, condition and method of application can all reduce the effectiveness of these coatings. Areas of hull that escape AF treatment (through limited application or damage) constitute key areas that may be expected to receive high levels of fouling. The investigation focused on whether small-scale (mm² to cm²) areas of unprotected surface or experimental ‘scrapes’ provided sufficient area for the formation of fouling assemblages within otherwise undamaged AF surfaces. Recruitment of fouling taxa such as algae, spirorbids and hydroids was recorded on scrapes as narrow as 0.5 cm wide. The abundance and species richness of fouling assemblages developing on scrapes ≥1 cm often equalled or surpassed levels observed in reference assemblages totally unprotected by AF coatings. Experiments were conducted at three sites within the highly protected and isolated marine park surrounding Lady Elliott Island at the southernmost tip of the Great Barrier Reef, Australia. Several NIS were recorded on scrapes of AF coated surfaces at this location, with 1-cm scrapes showing the greatest species richness and abundance of NIS relative to all other treatments (including controls) at two of the three sites investigated. Slight disruptions to newly antifouled surfaces may be all that is necessary for the establishment of fouling organisms and the translocation of a wide range of invasive taxa to otherwise highly protected marine areas.     

A preliminary assessment of biofouling and non-indigenous marine species associated with commercial slow-moving vessels arriving in New Zealand

Vessel traffic is the primary pathway for non-indigenous marine species introductions to New Zealand, with hull fouling recognised as being an important mechanism. This article describes hull fouling on seven slow-moving commercial vessels sampled over a 1 year period. Sampling involved the collection of images and fouling specimens from different hull locations using a standardised protocol developed to assess vessel biofouling in New Zealand. A total of 29 taxa was identified by expert taxonomists, of which 24% were indigenous to New Zealand and 17% non-indigenous. No first records to New Zealand were reported, however 59% of species were classified as ‘unknown’ due to insufficient taxonomic resolution. The extent of fouling was low compared to that described for other slow-movers. Fouling cover, biomass and richness were on average 17.1% (SE = 1.8%), 5.2 g (SE = 1.1 g) and 0.8 (SE = 0.07) per photoquadrat (200 × 200 mm), respectively. The fouling extent was lowest on the main hull areas where the antifouling paint was in good condition. In contrast, highest levels of fouling were associated with dry-docking support strips and other niche areas of the hull where the paint condition was poor. Future studies should target vessels from a broader range of bioregions, including vessels that remain idle for extended periods (ie months) between voyages, to increase understanding of the biosecurity risks posed by international commercial slow-movers.     

Marine range shifts and species introductions: comparative spread rates and community impacts

Aim Shifts in species ranges are a predicted and realized effect of global climate change; however, few studies have addressed the rates and consequence of such shifts, particularly in marine systems. Given ecological similarities between shifting and introduced species, we examined how our understanding of range shifts may be informed by the more established study of non‐native species introductions. Location Marine systems world‐wide. Methods Database and citation searches were used to identify 129 marine species experiencing range shifts and to determine spread rates and impacts on recipient communities. Analyses of spread rates were based on studies for which post‐establishment spread was reported in linear distance. The sizes of the effects of community impacts of shifting species were compared with those of functionally similar introduced species having ecologically similar impacts. Results Our review and meta‐analyses revealed that: (1) 75% of the range shifts found through the database search were in the poleward direction, consistent with climate change scenarios, (2) spread rates of range shifts were lower than those of introductions, (3) shifting species spread over an order of magnitude faster in marine than in terrestrial systems, and (4) directions of community effects were largely negative and magnitudes were often similar for shifters and introduced species; however, this comparison was limited by few data for range‐shifting species. Main conclusions Although marine range shifts are likely to proceed more slowly than marine introductions, the community‐level effects could be as great, and in the same direction, as those of introduced species. Because it is well‐established that introduced species are a primary threat to global biodiversity, it follows that, just like introductions, range shifts have the potential to seriously affect biological systems. In addition, given that ranges shift faster in marine than terrestrial environments, marine communities might be affected faster than terrestrial ones as species shift with climate change. Regardless of habitat, consideration of range shifts in the context of invasion biology can improve our understanding of what to expect from climate change‐driven shifts as well as provide tools for formal assessment of risks to community structure and function.     

Down under the southeastern Pacific: marine non-indigenous species in Chile

This article presents the first compilation of marine non-indigenous species (NIS) of algae and macro-invertebrates invading Chilean waters. A total of 32 cosmopolitan and non-cosmopolitan species are reported. Among them there are six species considered as extending their southern range of distribution in connection with El Niño events. The article highlights negative and positive impacts caused by marine NIS invasions. Among the first are Codium fragile var. tomentosoide, considered as a pest in Gracilaria chilensis aquaculture facilities in northern Chile, and Ciona intestinalis, a pest in scallop aquaculture installations. Among the second are bio-engineers species, such as the ascidian Pyura praeputialis and the sea grass Heterozostera tasmanica, which have caused an increase in local biodiversity and enhancement of nursery grounds via the creation of new habitats. Further more, invaders such as the algae Mastocarpus papillosus, Porphyra linearis and P. pseudolinearis represent new exploitable resources, extracted by coastal food gatherers along the coast (M. papillosus) or potential species to develop aquaculture. Additional information is presented on the anemone Anemonia alicemartinae, which appears to be a native species (?), having shown in the past 40–50 years, a geographical southward range extension of approximately 1900 km. The number of NIS reported for Chile is compared with those published for the southwestern Atlantic, South Africa, North America (Atlantic and Pacific coasts) and New Zealand. It is suggested that probably the low number of Chilean NIS is due to the fact that the Chilean coasts are environmentally less stressed than other coasts in the world, due to the scarcity of estuaries, gulfs, enclosed bays, lagoons and low human populations. These kinds of sheltered areas have been suggested as centers for bio-invasions, due to the high rate of human-mediated transfer and increase of pollutants. Furthermore, none of NIS reported from Chile show a fast geographical expansion rate (exception of A. alicemartinae), nor invading strategies such as those described for marine NIS in other latitudes, where notorious ecological unbalances following invasions have been observed. An alternative hypothesis is that the low number of marine NIS invading Chile is underestimated, since the modern list of species generated through specific taxonomically intensive port and harbor surveys is still lacking. Fifteen species (five invertebrate and 10 fish) have been deliberately imported to Chile for aquaculture. The invertebrates appear to be controlled within aquaculture facilities and have not established naturalized populations or caused direct ecological impacts on local communities. On the contrary, several millions of salmoniforms (and rainbow trout) have escaped from farming facilities in southern Chile and established naturalized populations. Studies on ecological impacts are lacking. These escapees are also playing a role in the enhancement of artisanal and sport fishery activities.     

Modelling the introduction and spread of non‐native species: international trade and climate change drive ragweed invasion

Biological invasions are a major driver of global change, for which models can attribute causes, assess impacts and guide management. However, invasion models typically focus on spread from known introduction points or non‐native distributions and ignore the transport processes by which species arrive. Here, we developed a simulation model to understand and describe plant invasion at a continental scale, integrating repeated transport through trade pathways, unintentional release events and the population dynamics and local anthropogenic dispersal that drive subsequent spread. We used the model to simulate the invasion of Europe by common ragweed (Ambrosia artemisiifolia), a globally invasive plant that causes serious harm as an aeroallergen and crop weed. Simulations starting in 1950 accurately reproduced ragweed's current distribution, including the presence of records in climatically unsuitable areas as a result of repeated introduction. Furthermore, the model outputs were strongly correlated with spatial and temporal patterns of ragweed pollen concentrations, which are fully independent of the calibration data. The model suggests that recent trends for warmer summers and increased volumes of international trade have accelerated the ragweed invasion. For the latter, long distance dispersal because of trade within the invaded continent is highlighted as a key invasion process, in addition to import from the native range. Biosecurity simulations, whereby transport through trade pathways is halted, showed that effective control is only achieved by early action targeting all relevant pathways. We conclude that invasion models would benefit from integrating introduction processes (transport and release) with spread dynamics, to better represent propagule pressure from native sources as well as mechanisms for long‐distance dispersal within invaded continents. Ultimately, such integration may facilitate better prediction of spatial and temporal variation in invasion risk and provide useful guidance for management strategies to reduce the impacts of invasion.     

Genetic structure of the star sea squirt, Botryllus schlosseri, introduced in southern European harbours

The introduction of new genetic variants or species is often caused by maritime transport between harbours. Botryllus schlosseri is a cosmopolitan ascidian species that is found in both harbours and open shore habitats. In order to determine the influence of ship traffic on the genetic structure and phylogeography of B. schlosseri in southern Europe, we analyzed the variability of a fragment of the mitochondrial gene cytochrome c oxidase subunit I (COI). We sampled seven Atlanto-Mediterranean harbour populations and three open-shore populations. In addition, we sequenced some colonies from the US-Atlantic coast and from other Mediterranean localities to perform phylogenetic analyses. Although the number of polymorphic sites recorded (25.8%) was within the range observed in other population studies based on ascidian COI sequences, the haplotypic diversity (16 haplotypes out of 181 sequences) was much lower. Moreover, a lack of intermediate haplotypes was observed. This pattern of high nucleotide diversity and low haplotype diversity was consistent with introduction events of a few divergent haplotypes. We found a strong genetic structure in the study populations. Gene flow was only appreciable between some harbour populations. Harbour- and open-shore populations were well differentiated, although there was no evidence for isolation by distance. A nested clade analysis pointed to long-distance colonization, possibly coupled with subsequent fragmentation, as the underlying process. Our results suggest that B. schlosseri entered the study area via harbour-hopping, possibly through recurrent introduction events. The haplotypes from North America and most of the European ones were grouped in the same phylogenetic clade. This suggests occasional gene flow between both continents, probably through ship transport.     

Worldwide genetic differentiation in the common fouling barnacle,Amphibalanus amphitrite

Amphibalanus amphitrite is a common fouling barnacle distributed globally in tropical and subtropical waters. In the present study, the genetic (mitochondrial cytochrome oxidase subunit I) and morphological differentiation in A. amphitrite from 25 localities around the world were investigated. The results revealed three clades within A. amphitrite with a genetic divergence of ~ 4% among clades, whereas there were no diagnostic morphological differences among clades. Clade 1 is widely distributed in both temperate and tropical waters, whereas Clade 3 is currently restricted to the tropical region. The deep divergence among clades suggests historical isolation within A. amphitrite; thus, the present geographical overlaps are possibly a result of the combined effects of rising sea level and human-mediated dispersals. This study highlights the genetic differentiation that exists in a common, widely distributed fouling organism with great dispersal potential; future antifouling research should take into account the choice of lineages.     

Assessing the diversity and distribution of Cephalothrix species (Nemertea: Palaeonemertea) in European waters by comparing different species delimitation methods

Soft‐bodied marine taxa, like ribbon worms (Nemertea), often lack clear diagnostic morphological characters impeding traditional species delimitation. Therefore, recent studies concentrated on molecular genetic methods to solve taxonomic issues. Different delimitation methods were employed to explore species boundaries and the presence of cryptic species. However, the performance of the different delimitation methods needs to be tested. A particularly promising nemertean genus in this regard is the palaeonemertean genus Cephalothrix that is commonly found in European waters. In order to gain information on the number and distribution of European cephalotrichids and to test different tree‐based and non‐tree‐based delimitation methods, we analyzed a dataset comprising the barcoding region of the mitochondrial cytochrome c oxidase subunit I (COI) of 215 European Cephalothrix specimens, of which 78 were collected for this study. Our results show the presence of 12–13 European lineages of which several can be assigned to known European species. Analyzing a second dataset comprising 74 additional sequences from the Pacific and the Atlantic Oceans helped identify some of the unassigned European specimens. One resulting clade seems to represent a non‐native introduced Cephalothrix species, while another has never been recorded from Europe before. In our analysis, especially the tree‐based methods and the phylogenetic analysis proved to be a useful tool when delimiting species. It remains unclear whether the different identified clades result from cryptic speciation or from a high genetic variability of the COI gene.     

Occurrence and diversity of barnacles on international ships visiting Osaka Bay,Japan, and the risk of their introduction

Abstract

The occurrence and diversity of barnacles attached to the hulls of two intercontinental bulk carriers were studied at the port in Osaka Bay, Japan, to assess the potential risk of introduction of exotic species to the inner part of the bay. Barnacles were sampled from the bulbous bows, near the midship draft marks, and around the propeller posts and rudders. Twenty-two species were found, with 14 of these not previously recorded in Osaka Bay, including four species not previously recorded elsewhere in Japan. From an assessment of environmental similarity between Osaka Bay and native ranges, of the 14 species, Elminius modestus and Amphibalanus variegatus were considered to have the highest risk of introduction to the inner part of the bay.     

The ghost of fouling communities past: the effect of original community on subsequent recruitment

Biofouling on ships has been linked to the spread of invasive species, which has been identified as one of the current primary threats to the environment. Previous research on antifouling coatings suggested that the quantity of fouling, as well as community composition, on biocidal coatings was modified by prior fouling settlement. The experiment reported in this paper was designed to determine how preconditioning affected the rate and composition of subsequent fouling on transplanted silicone coatings. A series of 10 × 20?cm panels coated with Intersleek 700 or DC3140 were placed at three locations in Florida (Ponce Inlet, Sebastian Inlet, and Port of Miami), which were characterized by distinct fouling communities. Panels were immersed for four months, cleaned, and reciprocally transplanted among the three sites. Fouling community composition and coverage were characterized at bimonthly intervals both before and after transplantation. The original fouling community affected the subsequent fouling composition and recolonization by tunicates, sea anemones, barnacles, sponges, hydroids, and arborescent bryozoans. The community-level effects were short-term, lasting 2–4?months, but specific responses lasted up to 14?months post-transplant.     

Community context and the influence of non-indigenous species on juvenile salmon survival in a Columbia River reservoir

Non-indigenous species (NIS) have been called biological pollutants, which implies that reducing their numbers should reduce negative impacts. To test this hypothesis, we used food web models, parameterized with data from field studies, to ask how reducing the number of NIS co-occurring with endangered salmon would affect salmon mortality. Our analyses indicate that predation on Upper Columbia River spring chinook salmon Oncorhynchus tshawytscha and steelhead O. mykiss juveniles was affected very little by NIS reduction. The effects of removing NIS were partly or totally offset by indirect food web interactions, and were subtle compared to effects of native predator management. We predict that the most effective way of reducing predation on salmon smolts will involve managing native predators and targeted removals of specific NIS. Minimizing impact of established NIS thus entails not only reducing NIS prevalence, but also considering background management practices and community context.