Catch my drift? Between-farm dispersal of biofouling waste from salmon pen net cleaning: Potential risks for fish health.

Biofouling is a serious challenge for global salmon aquaculture and farmers have to regularly clean pen nets to avoid impacts on stock health and farms' structural integrity. The removed material is released into the surrounding environment. This includes cnidarian species such as hydroids, whose nematocyst-bearing fragments can impact gill health and fish welfare. There is also increasing evidence of the association of parasites and pathogens with biofouling organisms and cleaning fragments. It is unknown whether and how far local current regimes disperse biofouling material and whether this material reaches and interacts with adjacent pens or even neighbouring farms downstream, or wild fish populations in surrounding environments. We focussed on the cnidarian hydroid Ectopleura larynx, one of the most abundant biofouling species on Norwegian aquaculture installations. Using a 3D hydrodynamic model parameterised with physical and biological properties of hydroid particles (derived via field and laboratory studies), we simulated the dispersal of net cleaning waste from two Norwegian salmon farms. Our results demonstrate that net cleaning waste is extensively dispersed throughout neighbouring pens, and even to adjacent aquaculture facilities. Salmon were exposed to concentrations of biofouling particles up to 41-fold elevated compared to background concentrations, and for up to 30.5 h. Maximum dispersal distance of hydroid particles was 5.5 km from the point of release, achieved largely within 48 h. Least-cost distance calculations show that this distance exceeds the nearest-neighbour distance of 70 % of Norway's salmon farms (654 farms). Our study provides some evidence that actions taken to manage biofouling at salmon farms may affect neighbouring farms and surrounding natural environments. The results highlight the potential risks associated with net cleaning: the dispersal of harmful cnidarian particles, associated pathogens, and non-indigenous species, thus underlining the need for novel farming or net cleaning technologies that prevent the release of potentially harmful cleaning waste.

Quantifying the probability of a successful marine bioinvasion due to source-destination risk factors.

The increasing spread of marine non-indigenous species (NIS) due to the growth in global shipping traffic is causing widespread concern for the ecological and economic impacts of marine bioinvasions. Risk management authorities need tools to identify pathways and source regions of priority concern to better target efforts for preventing NIS introduction. The probability of a successful NIS introduction is affected by the likelihood that a marine species entrained in a transport vector will survive the voyage between origin and destination locations and establish an independently reproducing population at the destination. Three important risk factors are voyage duration, range of environmental conditions encountered during transit and environmental similarity between origin and destination. In this study, we aimed for a globally comprehensive approach to assembling quantifications of source-destination risk factors from every potential origin to every potential destination. To derive estimates of voyage-related marine biosecurity risk, we used computer-simulated vessel paths between pairs of ecoprovinces in the Marine Ecoregions Of the World biogeographic classification system. We used the physical length of each path to calculate voyage duration risk and the cross-latitudinal extent of the path to calculate voyage path risk. Environmental similarity risk was based on comparing annual average sea surface temperature and salinity within each ecoprovince to those of other ecoprovinces. We derived three separate sets of risk quantifications, one each for voyage duration, voyage path and environmental similarity. Our quantifications can be applied to studies that require source-destination risk estimates. They can be used separately or combined, depending on the importance of the types of source-destination risks that might be relevant to particular scientific or risk management questions or applications.

Hurdles and opportunities in implementing marine biosecurity systems in data-poor regions.

Managing marine nonindigenous species (mNIS) is challenging, because marine environments are highly connected, allowing the dispersal of species across large spatial scales, including geopolitical borders. Cross-border inconsistencies in biosecurity management can promote the spread of mNIS across geopolitical borders, and incursions often go unnoticed or unreported. Collaborative surveillance programs can enhance the early detection of mNIS, when response may still be possible, and can foster capacity building around a common threat. Regional or international databases curated for mNIS can inform local monitoring programs and can foster real-time information exchange on mNIS of concern. When combined, local species reference libraries, publicly available mNIS databases, and predictive modeling can facilitate the development of biosecurity programs in regions lacking baseline data. Biosecurity programs should be practical, feasible, cost-effective, mainly focused on prevention and early detection, and be built on the collaboration and coordination of government, nongovernment organizations, stakeholders, and local citizens for a rapid response.

Application of multi-region input-output analysis to examine biosecurity risks associated with the global shipping network.

The vast majority of globally traded cargo is transported via maritime shipping. Whilst in port for loading and unloading, these ships can pick up local marine organisms with internal ballast water or as external biofouling assemblages and subsequently move these to destination far beyond their natural ranges. Over the past decades, this mechanism has led to the establishment of hundreds of non-indigenous species (NIS) around global coastlines. Marine NIS cause significant environmental, economic, cultural and human health impacts. Taking effective steps to preventing their dispersal and establishment is an enduring challenge for governments and conservation agencies around the world. Here we use international commodity trade data and a Nobel-Prize-winning economic analysis technique to develop a novel approach for assessing global marine NIS transfer risks. We show that by tracing the origins and destinations of seaborne trade connections, and the nature of the traded commodities, we can predict the strength of shipping vectors and associated marine biosecurity risks. We demonstrate the utility of our approach via a case-study, where we trace the spread of a hypothetical marine NIS from Japan and show the congruence of our model results with documented invasion histories from that region. Our study demonstrates that biosecurity risk can be assessed using established economic modelling frameworks on the basis of monetary transaction data alone, and without the need for detailed itineraries of the many thousand vessels making up the global commercial fleet. Novel, cost-effective tools are needed to mitigate biosecurity risks associated with maritime trade, and to meet conservation goals while enabling economic prosperity. The modelling framework presented here can be expanded to incorporate future risk factors, life-history traits of particular NIS of concern, and even adapted to simulate the dispersal of terrestrial pests or disease agents.

Testing of novel net cleaning technologies for finfish aquaculture.

To avoid the negative impacts caused by biofouling development, aquaculture nets around the world are periodically cleaned using high-pressure washers. Net cleaning is labour-intense and costly, can damage antifouling coatings on the nets, and pose contamination as well as fish health and welfare risks. To support the environmental sustainability of the growing aquaculture sector, novel net cleaning methods are needed. This study examined low-pressure-, cavitation-, and suction-based cleaning technologies as alternatives to conventional high-pressure cleaning. Using field experiments, cleaning efficacy, cleaning waste generation, and the impact of cleaning on coating integrity and net strength were evaluated. Cavitation and high-pressure cleaning achieved considerably higher cleaning efficacy than low-pressure and suction cleaning. However, a single high-pressure treatment caused up to 53% coating degradation, compared to 2% for cavitation. All technologies produced similar cleaning waste and neither reduced net strength significantly. This study identifies cavitation cleaning as promising technology for biofouling control on aquaculture nets.

The role of biofouling development in the loss of seed mussels in aquaculture.

The efficient seeding of juvenile mussels is critical to the sustainability and profitability of mussel aquaculture. However, seeding mussels is highly inefficient, with many juveniles being lost in the following few months. One possible cause of these losses could be the development of biofouling assemblages. Therefore, the relationships between biofouling accumulation and losses of juveniles were assessed. Losses of juvenile mussels were initially high (42.9-49.1% over approximately one to two weeks), with lower rates of loss over the following four to five months. Biofouling development followed a successional pattern beginning with colonisation by amphipods, subsequent establishment of macroalgae, and the formation of an assemblage dominated by mussels and sessile invertebrates. However, biofouling development did not play a major role in the loss of juveniles. Rather, large-scale losses of mussels occurred shortly after seeding when biofouling was scant, suggesting alternative causes of loss were in operation.

A portable thermal system for reactive treatment of biofouled internal pipework on recreational vessels.

Biofouled commercial and recreational vessels are primary vectors for the introduction and spread of marine non-indigenous species (NIS). This study designed and assessed a portable system to reactively treat biofouling in the internal pipework of recreational vessels - a high-risk 'niche area' for NIS that is difficult to access and manage. A novel thermal treatment apparatus was optimised in a series of laboratory experiments performed using scale models of vessel pipework configurations. Treatment effectiveness was validated using the Pacific oyster Magallana gigas, a marine NIS with known resilience to heat. In subsequent field validations on actual recreational vessels, treatment was successfully delivered to high-risk portions of pipework when an effective seal between delivery unit and targeted pipework was achieved and ambient heat loss was minimised. In addition to demonstrating the feasibility of in-water treatment of vessel pipework, the study highlights the importance of robust optimisation and validation of any treatment system intended for biosecurity purposes.

Urban impacts across realms: Making the case for inter-realm monitoring and management.

Burgeoning populations and the increasing concentration of humans in urban areas have resulted in extensive and increasing degradation and destruction of natural ecosystems. The multitude of impacts and their drivers in urban areas across realms are often studied at local scales, but there is regularly a mismatch between the spatial extent of the impacts and that of the pressures driving those impacts. For example, most human activities occur on land and therefore disturb terrestrial habitats (intrinsic impacts), but their impacts can also extend to the atmosphere and aquatic realms (extrinsic impacts). Management of urban impacts is often designed at local scales and aims to control local pressures, mostly overlooking pressures originating outside the 'managed' area. This is often due to jurisdictional barriers but can also result from the lack of knowledge and recognition among scientists and managers of larger scale pressures. With the aim to highlight the importance of ameliorating extrinsic impacts for holistic management of urban areas, this paper discusses the range and extent of extrinsic impacts produced by the most common pressures in urban environments. We discuss that the terrestrial realm is a 'net-donor' of impacts, as most human activities occur on land and the resulting impacts are transferred to aquatic and atmospheric realms. However, activities in aquatic realms can result in impacts on land. We conclude that, to achieve effective management strategies, greater collaboration is needed between scientists and managers focussing on different realms and regions and we present suggestions for approaches to achieve this.

Effects of cnidarian biofouling on salmon gill health and development of amoebic gill disease.

This study examines the potential implications of biofouling management on the development of an infectious disease in Norwegian farmed salmon. The hydroid Ectopleura larynx frequently colonises cage nets at high densities (thousands of colonies per m2) and is released into the water during regular in-situ net cleaning. Contact with the hydroids' nematocysts has the potential to cause irritation and pathological damage to salmon gills. Amoebic gill disease (AGD), caused by the amoeba Paramoeba perurans, is an increasingly international health challenge in Atlantic salmon farming. AGD often occurs concomitantly with other agents of gill disease. This study used laboratory challenge trials to: (1) characterise the gill pathology resulting from the exposure of salmon to hydroids, and (2) investigate if such exposure can predispose the fish to secondary infections-using P. perurans as an example. Salmon in tanks were exposed either to freshly 'shredded' hydroids resembling waste material from net cleaning, or to authentic concentrations of free-living P. perurans, or first to 'shredded' hydroids and then to P. perurans. Gill health (AGD gill scores, non-specific gill scores, lamellar thrombi, epithelial hyperplasia) was monitored over 5 weeks and compared to an untreated control group. Nematocysts of E. larynx contained in cleaning waste remained active following high-pressure cleaning, resulting in higher non-specific gill scores in salmon up to 1 day after exposure to hydroids. Higher average numbers of gill lamellar thrombi occurred in fish up to 7 days after exposure to hydroids. However, gill lesions caused by hydroids did not affect the infection rates of P. perurans or the disease progression of AGD. This study discusses the negative impacts hydroids and current net cleaning practices can have on gill health and welfare of farmed salmon, highlights existing knowledge gaps and reiterates the need for alternative approaches to net cleaning.

A review of three decades of research on the invasive kelp Undaria pinnatifida in Australasia: An assessment of its success, impacts and status as one of the world's worst invaders.

Marine invasive macroalgae can have severe local-scale impacts on ecological communities. The kelp Undaria pinnatifida is one of the most successful marine invasive species worldwide, and is widely regarded as one of the worst. Here, we review research on Undaria in Australasia, where the kelp is established throughout much of New Zealand and south-eastern Australia. The presence of Undaria for at least three decades in these locations makes Australasia one of the longest-invaded bioregions globally, and a valuable case study for considering Undaria's invasion success and associated impacts. In Australasia, Undaria has primarily invaded open spaces, turf communities, and gaps in native canopies within a relatively narrow elevation band on rocky shores. Despite its high biomass, Undaria has relatively few direct impacts on native species, and can increase community-wide attributes such as primary productivity and the provision of biogenic habitat. Therefore, Australasian Undaria research provides an example of a decoupling between the success and impact of an invasive species. Undaria will most likely continue to spread along thousands of kilometres of rocky coastline in temperate Australasia, due to its tolerance to large variations in temperature, ability to exploit disturbances to local communities, and the continued transfer among regions via vessel movements and aquaculture activities. However, the spread of Undaria remains difficult to manage as eradication is challenging and seldom successful. Therefore, understanding potential invasion pathways, maintaining native canopy-forming species that limit Undaria success, and effectively managing anthropogenic vectors of Undaria spread, should be key management priorities.

Factors influencing the en route survivorship and post-voyage growth of a common ship biofouling organism, Bugula neritina.

The likelihood that viable non-indigenous biofouling species will survive a voyage on a vessel is influenced by a range of factors, including the speed, duration, and route of the voyage and the amount of time the vessel spends in port. In this study, a land-based dynamic flow device was used to test the effect of recruit age, vessel speed and voyage duration on the survivorship and growth of the bryozoan Bugula neritina. In the experiment, one-week-old recruits had a higher likelihood (100%) of surviving voyages than older (one-month-old, 90%) or younger (one-day-old, 79%) recruits, but survival was not influenced by vessel speed (6 and 18 knots) or voyage duration (two and eight days). The results suggest that the non-indigenous species B. neritina can be effectively transferred at a range of ages but one-week-old recruits are more likely to survive the translocation process and survive in the recipient environment.

Metabarcoding improves detection of eukaryotes from early biofouling communities: implications for pest monitoring and pathway management.

In this experimental study the patterns in early marine biofouling communities and possible implications for surveillance and environmental management were explored using metabarcoding, viz. 18S ribosomal RNA gene barcoding in combination with high-throughput sequencing. The community structure of eukaryotic assemblages and the patterns of initial succession were assessed from settlement plates deployed in a busy port for one, five and 15 days. The metabarcoding results were verified with traditional morphological identification of taxa from selected experimental plates. Metabarcoding analysis identified > 400 taxa at a comparatively low taxonomic level and morphological analysis resulted in the detection of 25 taxa at varying levels of resolution. Despite the differences in resolution, data from both methods were consistent at high taxonomic levels and similar patterns in community shifts were observed. A high percentage of sequences belonging to genera known to contain non-indigenous species (NIS) were detected after exposure for only one day.

Amplified recruitment pressure of biofouling organisms in commercial salmon farms: potential causes and implications for farm management.

The development of biofouling on finfish aquaculture farms presents challenges for the industry, but the factors underlying nuisance growths are still not well understood. Artificial settlement surfaces were used to examine two possible explanations for high rates of biofouling in Norwegian salmon farms: (1) increased propagule release during net cleaning operations, resulting in elevated recruitment rates; and (2) potential reservoir effects of farm surfaces. The presence of salmon farms was associated with consistently and substantially (up to 49-fold) elevated recruitment rates. Temporal patterns of recruitment were not driven by net cleaning. Resident populations of biofouling organisms were encountered on all submerged farm surfaces. Calculations indicate that a resident population of the hydroid Ectopleura larynx, a major biofouling species, could release between 0.3 × 10(9) and 4.7 × 10(9) larvae per farm annually. Such resident populations could form propagule reservoirs and be one explanation for the elevated recruitment pressure at salmon farms.

Biosecurity risks associated with in-water and shore-based marine vessel hull cleaning operations.

The removal of biofouling from vessels during hull cleaning can pose a biosecurity threat if viable, non-indigenous organisms are released into the aquatic environment. However, the effect of cleaning on biofouling organism viability in different types of cleaning operations has been poorly studied. We compared the effects of hull cleaning on biofouling organisms removed from 36 marine vessels during in-water (without capture of cleaning waste) and shore-based (with capture, and treatment of cleaning waste) cleaning. In-water cleaning resulted in higher proportions of viable biofouling organisms surviving cleaning (62.3 ± 7.1% of all organisms examined) compared to dry dock (37.8 ± 8.6%) and haul-out (20.1 ± 5.3%) operations. For shore-based facilities with effluent treatment systems, concentrations of organisms and/or their propagules in cleaning effluent was reduced by ≥ 98.5% compared to initial hydro-blast effluent concentrations. These results can be used in guidance for hull cleaning operations to minimize associated biosecurity risk.

Potential ramifications of the global economic crisis on human-mediated dispersal of marine non-indigenous species.

The global economy is currently experiencing one of its biggest contractions on record. A sharp decline in global imports and exports since 2008 has affected global merchant vessel traffic, the principal mode of bulk commodity transport around the world. During the first quarter of 2009, 10% and 25% of global container and refrigerated vessels, respectively, were reported to be unemployed. A large proportion of these vessels are lying idle at anchor in the coastal waters of South East Asia, sometimes for periods of greater than 3 months. Whilst at anchor, the hulls of such vessels will develop diverse and extensive assemblages of marine biofouling species. Once back in service, these vessels are at risk of transporting higher-than-normal quantities of marine organisms between their respective global trading ports. We discuss the potential ramifications of the global economic crisis on the spread of marine non-indigenous species via global commercial shipping.

A risk-based predictive tool to prevent accidental introductions of nonindigenous marine species.

Preventing the introduction of nonindigenous species (NIS) is the most efficient way to avoid the costs and impacts of biological invasions. The transport of fouling species on ship hulls is an important vector for the introduction of marine NIS. We use quantitative risk screening techniques to develop a predictive tool of the abundance and variety of organisms being transported by ocean-going yachts. We developed and calibrated an ordinal rank scale of the abundance of fouling assemblages on the hulls of international yacht hulls arriving in New Zealand. Fouling ranks were allocated to 783 international yachts that arrived in New Zealand between 2002 and 2004. Classification tree analysis was used to identify relationships between the fouling ranks and predictor variables that described the maintenance and travel history of the yachts. The fouling ranks provided reliable indications of the actual abundance and variety of fouling assemblages on the yachts and identified most (60%) yachts that had fouling on their hulls. However, classification tree models explained comparatively little of the variation in the distribution of fouling ranks (22.1%), had high misclassification rates (approximately 43%), and low predictive power. In agreement with other studies, the best model selected the age of the toxic antifouling paint on yacht hulls as the principal risk factor for hull fouling. Our study shows that the transport probability of fouling organisms is the result of a complex suite of interacting factors and that large sample sizes will be needed for calibration of robust risk models.