Marine ecosystem health and biological pollution: Reconsidering the paradigm.

Our study re-evaluates a fundamental paradigm in marine invasion ecology - whether introduced species are considered as contaminants, i.e. just present in the system, or whether they are pollutants per se, i.e. they cause biological harm. This re-evaluation includes the concepts of marine ecosystem health and biological pollution using the European Marine Strategy Framework Directive (MSFD) as an example. Hence, we clarify the distinction between "biological contamination" (pertaining to Non-Indigenous Species (NIS) introductions) and "biological pollution" (associated with Invasive Alien Species - IAS). We emphasize the need for comprehensive indicators that consider their ecological, economic, and societal impacts. The MSFD Descriptor D2 NIS is analysed using the "biocontamination-biopollution" gradient to better reflect the complexities of ecosystem health. We discuss limitations in current monitoring and evaluation criteria, such as the absence of unified NIS/IAS monitoring, challenges in interpreting ecological impacts, and context-dependent assessment results. We emphasize the importance of context-specific management measures, considering the origin of pressures, whether endogenic (caused within a management area such a regional sea) or exogenic (with causes from outside a management area). Ultimately, we underscore the importance of a holistic and adaptable approach to address the diverse challenges posed by biocontamination and biopollution, protecting both marine ecosystems and human well-being in an ever-changing environment.

Horizon scanning of potential threats to high-Arctic biodiversity, human health and the economy from marine invasive alien species: A Svalbard case study.

The high Arctic is considered a pristine environment compared with many other regions in the northern hemisphere. It is becoming increasingly vulnerable to invasion by invasive alien species (IAS), however, as climate change leads to rapid loss of sea ice, changes in ocean temperature and salinity, and enhanced human activities. These changes are likely to increase the incidence of arrival and the potential for establishment of IAS in the region. To predict the impact of IAS, a group of experts in taxonomy, invasion biology and Arctic ecology carried out a horizon scanning exercise using the Svalbard archipelago as a case study, to identify the species that present the highest risk to biodiversity, human health and the economy within the next 10 years. A total of 114 species, currently absent from Svalbard, recorded once and/or identified only from environmental DNA samples, were initially identified as relevant for review. Seven species were found to present a high invasion risk and to potentially cause a significant negative impact on biodiversity and five species had the potential to have an economic impact on Svalbard. Decapod crabs, ascidians and barnacles dominated the list of highest risk marine IAS. Potential pathways of invasion were also researched, the most common were found associated with vessel traffic. We recommend (i) use of this approach as a key tool within the application of biosecurity measures in the wider high Arctic, (ii) the addition of this tool to early warning systems for strengthening existing surveillance measures; and (iii) that this approach is used to identify high-risk terrestrial and freshwater IAS to understand the overall threat facing the high Arctic. Without the application of biosecurity measures, including horizon scanning, there is a greater risk that marine IAS invasions will increase, leading to unforeseen changes in the environment and economy of the high Arctic.

The Waiting Stage, Prolonged Residency in Nursery Habitats by Juveniles of the Predatory Sea Star Marthasterias glacialis.

AbstractGrowth and recruitment of the sea star Marthasterias glacialis was followed over six years in Lough Hyne, southwest Ireland. Juveniles from a 2-mm radius were found on algae at <1-2-m depth following what appeared to be gregarious larval settlement. Data from Lough Hyne and Mulroy Bay (northwest Ireland) indicated that algal habitat serves as a nursery area for juveniles of M. glacialis. Successive size frequency modes of the juveniles at Lough Hyne indicated slow growth over 6 years, to a mean radius of 20 mm. The absence of additional recruitment allowed monitoring of a discrete population. Recruits in the nursery habitat over the six years remained as waiting stage juveniles, a Peter Pan group with delayed maturity subsisting on a diet of epibionts. An initial sharp decline in numbers indicated post-settlement mortality, with subsequent decline likely due to migration to the adjacent shelly habitat, where subadult M. glacialis (30-70-mm radius) lives. In this habitat, M. glacialis preys on small bivalves and eventually joins the adult (maximum radius = 280 mm) population on open sediment, where it feeds on large bivalves. Size frequency distributions of the juveniles and adults showed growth over the six years, with the waiting stage sea stars slowly merging in size with the adult population. It appears that the supply of new individuals into the adult population may take place six or more years following settlement. Strong connectivity between life stage habitats and prolonged recruitment into the adult population may contribute to balanced exploitation of infaunal prey.

Invasive non-native species likely to threaten biodiversity and ecosystems in the Antarctic Peninsula region.

The Antarctic is considered to be a pristine environment relative to other regions of the Earth, but it is increasingly vulnerable to invasions by marine, freshwater and terrestrial non-native species. The Antarctic Peninsula region (APR), which encompasses the Antarctic Peninsula, South Shetland Islands and South Orkney Islands, is by far the most invaded part of the Antarctica continent. The risk of introduction of invasive non-native species to the APR is likely to increase with predicted increases in the intensity, diversity and distribution of human activities. Parties that are signatories to the Antarctic Treaty have called for regional assessments of non-native species risk. In response, taxonomic and Antarctic experts undertook a horizon scanning exercise using expert opinion and consensus approaches to identify the species that are likely to present the highest risk to biodiversity and ecosystems within the APR over the next 10 years. One hundred and three species, currently absent in the APR, were identified as relevant for review, with 13 species identified as presenting a high risk of invading the APR. Marine invertebrates dominated the list of highest risk species, with flowering plants and terrestrial invertebrates also represented; however, vertebrate species were thought unlikely to establish in the APR within the 10 year timeframe. We recommend (a) the further development and application of biosecurity measures by all stakeholders active in the APR, including surveillance for species such as those identified during this horizon scanning exercise, and (b) use of this methodology across the other regions of Antarctica. Without the application of appropriate biosecurity measures, rates of introductions and invasions within the APR are likely to increase, resulting in negative consequences for the biodiversity of the whole continent, as introduced species establish and spread further due to climate change and increasing human activity.

A comparison of impact and risk assessment methods based on the IMO Guidelines and EU invasive alien species risk assessment frameworks.

A comparative analysis of two risk assessment (RA) frameworks developed to support the implementation of the international Ballast Water Management Convention (BWMC) and European Regulation on Invasive Alien Species (IAS) was performed. This analysis revealed both differences and similarities between the IMO Risk Assessment Guidelines (IMO, 2007) and EU Regulation supplement on RA of IAS (EU, 2018) in RA approaches, key principles, RA components and categories of IAS impacts recommended for assessment. The results of this analysis were used to produce a common procedure for the evaluation of the bioinvasion risk and impact assessment methods intended to support international, regional and/or national policy on IAS. The procedure includes a scoring scheme to assess compliance with the key principles, RA components and categories of bioinvasion impacts taken into account by the methods. In these methods the categories of impacts on human health and economy are underrepresented comparing with impacts on environment.

What is really out there? Review of the genus Okenia Menke, 1830 (Nudibranchia: Goniodorididae) in the Mediterranean Sea with description of two new species.

The precise number of Okenia taxa inhabiting the Mediterranean Sea, as well as their general taxonomy, varies according to different specialists. So far, eight valid species have been reported from the area: Okenia aspersa (Alder & Hancock, 1845), Okenia cupella (Vogel & Schultz, 1970), Okenia elegans (Leuckart, 1828), Okenia hispanica Valdés & Ortea, 1995, Okenia impexa Er. Marcus, 1957, Okenia leachii (Alder & Hancock, 1854), Okenia mediterranea (Ihering, 1886), and Okenia zoobotryon (Smallwood, 1910). Of these, only three (O. elegans, O. hispanica, and O. mediterranea) have their type localities in the Mediterranean Sea, whereas the others were described from different biogeographic areas and later included in the Mediterranean biota. We carried out a review on Mediterranean Okenia species through an integrative approach, based on a wide literature search and a morphological and molecular analysis of available type material and samples collected recently. The present study confirmed the presence of O. aspersa, O. elegans, O. hispanica, and O. mediterranea in the Mediterranean Sea, although leaving remaining questions about some of those taxa. The distribution of O. cupella, O. impexa, and O. zoobotryon is limited to the western Atlantic, and of O. leachii to the eastern Atlantic. All specimens previously identified as O. cupella, O. impexa, and O. zoobotryon by different authors in the Mediterranean Sea were repeatedly misidentified. Thus, we describe Okenia problematica sp. nov. and Okenia longiductis sp. nov., from the "Mediterranean" Okenia cupella/impexa and O. zoobotryon. We also consider here Okenia pusilla Sordi, 1974 a nomen dubium and include a redescription of the holotype of O. cupella. A molecular phylogeny, including all the sequenced Okenia species, was performed in order to evaluate the evolutionary relationships of the newly described species with the other congeneric taxa.

Climate change opens new frontiers for marine species in the Arctic: Current trends and future invasion risks.

Climate change and increased anthropogenic activities are expected to elevate the potential of introducing nonindigenous species (NIS) into the Arctic. Yet, the knowledge base needed to identify gaps and priorities for NIS research and management is limited. Here, we reviewed primary introduction events to each ecoregion of the marine Arctic realm to identify temporal and spatial patterns, likely source regions of NIS, and the putative introduction pathways. We included 54 introduction events representing 34 unique NIS. The rate of NIS discovery ranged from zero to four species per year between 1960 and 2015. The Iceland Shelf had the greatest number of introduction events (n = 14), followed by the Barents Sea (n = 11), and the Norwegian Sea (n = 11). Sixteen of the 54 introduction records had no known origins. The majority of those with known source regions were attributed to the Northeast Atlantic and the Northwest Pacific, 19 and 14 records, respectively. Some introduction events were attributed to multiple possible pathways. For these introductions, vessels transferred the greatest number of aquatic NIS (39%) to the Arctic, followed by natural spread (30%) and aquaculture activities (25%). Similar trends were found for introductions attributed to a single pathway. The phyla Arthropoda and Ochrophyta had the highest number of recorded introduction events, with 19 and 12 records, respectively. Recommendations including vector management, horizon scanning, early detection, rapid response, and a pan-Arctic biodiversity inventory are considered in this paper. Our study provides a comprehensive record of primary introductions of NIS for marine environments in the circumpolar Arctic and identifies knowledge gaps and opportunities for NIS research and management. Ecosystems worldwide will face dramatic changes in the coming decades due to global change. Our findings contribute to the knowledge base needed to address two aspects of global change-invasive species and climate change.

Developing a list of invasive alien species likely to threaten biodiversity and ecosystems in the European Union.

The European Union (EU) has recently published its first list of invasive alien species (IAS) of EU concern to which current legislation must apply. The list comprises species known to pose great threats to biodiversity and needs to be maintained and updated. Horizon scanning is seen as critical to identify the most threatening potential IAS that do not yet occur in Europe to be subsequently risk assessed for future listing. Accordingly, we present a systematic consensus horizon scanning procedure to derive a ranked list of potential IAS likely to arrive, establish, spread and have an impact on biodiversity in the region over the next decade. The approach is unique in the continental scale examined, the breadth of taxonomic groups and environments considered, and the methods and data sources used. International experts were brought together to address five broad thematic groups of potential IAS. For each thematic group the experts first independently assembled lists of potential IAS not yet established in the EU but potentially threatening biodiversity if introduced. Experts were asked to score the species within their thematic group for their separate likelihoods of i) arrival, ii) establishment, iii) spread, and iv) magnitude of the potential negative impact on biodiversity within the EU. Experts then convened for a 2-day workshop applying consensus methods to compile a ranked list of potential IAS. From an initial working list of 329 species, a list of 66 species not yet established in the EU that were considered to be very high (8 species), high (40 species) or medium (18 species) risk species was derived. Here, we present these species highlighting the potential negative impacts and the most likely biogeographic regions to be affected by these potential IAS.

Rapid assessment of target species: Byssate bivalves in a large tropical port.

Rapid assessment sampling for target species is a fast cost-effective method aimed at determining the presence, abundance and distribution of alien and native harmful aquatic organisms and pathogens that may have been introduced by shipping. In this study, the method was applied within a large tropical port expected to have a high species diversity. The port of Kaohsiung was sampled for bivalve molluscan species that attach using a byssus. Such species, due to their biological traits, are spread by ships to ports worldwide. We estimated the abundance and distribution range of one dreissenid (Mytilopsis sallei) and four mytilids (Brachidontes variabilis, Arcuatula senhousa, Mytilus galloprovincialis, Perna viridis) known to be successful invaders and identified as potential pests, or high-risk harmful native or non-native species. We conclude that a rapid assessment of their abundance and distribution within a port, and its vicinity, is efficient and can provide sufficient information for decision making by port managers where IMO port exemptions may be sought.

Assessing exemptions under the ballast water management convention: preclude the Trojan horse.

The International Maritime Organization (IMO) Ballast Water Management Convention (BWMC) is a powerful instrument aimed at reducing spread of harmful aquatic organisms and pathogens (HAOPs). As BWMC is expected to enter into force soon, shipping companies will start seeking exemptions for ballast water management in accordance with BWMC Regulation A-4. However, without scientifically robust risk assessment (RA) and consistent rules, the exemptions may introduce a new form of risk within a convention generally designed to reduce risks. This paper describes an adaptive system for granting exemptions, consisting of six major components: target species selection procedure, port-to-port RA, monitoring, information support, administrative decision and review process. The system is based on key principles defined in the IMO guidelines for RA and is designed to continuously accumulate evolving experience on granting exemptions. The ultimate goal is to contribute to the control of the spread of HAOPs, without placing an unnecessary burden on the shipping industry.

Warming can enhance invasion success through asymmetries in energetic performance.

Both climate warming and biological invasions are prominent drivers of global environmental change and it is important to determine how they interact. However, beyond tolerance and reproductive thresholds, little is known about temperature dependence of invaders' performance, particularly in the light of competitive attributes of functionally similar native species. We used experimentally derived energy budgets and field temperature data to determine whether anticipated warming will asymmetrically affect the energy budgets of the globally invasive Ponto-Caspian mysid crustacean Hemimysis anomala and a functionally similar native competitor (Mysis salemaai) whose range is currently being invaded. In contrast to M. salemaai, which maintains a constant feeding rate with temperature leading to diminishing energy assimilation, we found that H. anomala increases its feeding rate with temperature in parallel with growing metabolic demand. This enabled the invader to maintain high energy assimilation rates, conferring substantially higher scope for growth compared to the native analogue at spring-to-autumn temperatures. Anticipated warming will likely exacerbate this energetic asymmetry and remove the winter overlap, which, given the seasonal limitation of mutually preferred prey, appears to underpin coexistence of the two species. These results indicate that temperature-dependent asymmetries in scope for growth between invaders and native analogues comprise an important mechanism determining invasion success under warming climates. They also highlight the importance of considering relevant spectra of ecological contexts in predicting successful invaders and their impacts under warming scenarios.

Classification of non-indigenous species based on their impacts: considerations for application in marine management.

Assessment of the ecological and economic/societal impacts of the introduction of non-indigenous species (NIS) is one of the primary focus areas of bioinvasion science in terrestrial and aquatic environments, and is considered essential to management. A classification system of NIS, based on the magnitude of their environmental impacts, was recently proposed to assist management. Here, we consider the potential application of this classification scheme to the marine environment, and offer a complementary framework focussing on value sets in order to explicitly address marine management concerns. Since existing data on marine NIS impacts are scarce and successful marine removals are rare, we propose that management of marine NIS adopt a precautionary approach, which not only would emphasise preventing new incursions through pre-border and at-border controls but also should influence the categorisation of impacts. The study of marine invasion impacts requires urgent attention and significant investment, since we lack the luxury of waiting for the knowledge base to be acquired before the window of opportunity closes for feasible management.

Horizon scanning for invasive alien species with the potential to threaten biodiversity in Great Britain.

Invasive alien species (IAS) are considered one of the greatest threats to biodiversity, particularly through their interactions with other drivers of change. Horizon scanning, the systematic examination of future potential threats and opportunities, leading to prioritization of IAS threats is seen as an essential component of IAS management. Our aim was to consider IAS that were likely to impact on native biodiversity but were not yet established in the wild in Great Britain. To achieve this, we developed an approach which coupled consensus methods (which have previously been used for collaboratively identifying priorities in other contexts) with rapid risk assessment. The process involved two distinct phases: Preliminary consultation with experts within five groups (plants, terrestrial invertebrates, freshwater invertebrates, vertebrates and marine species) to derive ranked lists of potential IAS. Consensus-building across expert groups to compile and rank the entire list of potential IAS. Five hundred and ninety-one species not native to Great Britain were considered. Ninety-three of these species were agreed to constitute at least a medium risk (based on score and consensus) with respect to them arriving, establishing and posing a threat to native biodiversity. The quagga mussel, Dreissena rostriformis bugensis, received maximum scores for risk of arrival, establishment and impact; following discussions the unanimous consensus was to rank it in the top position. A further 29 species were considered to constitute a high risk and were grouped according to their ranked risk. The remaining 63 species were considered as medium risk, and included in an unranked long list. The information collated through this novel extension of the consensus method for horizon scanning provides evidence for underpinning and prioritizing management both for the species and, perhaps more importantly, their pathways of arrival. Although our study focused on Great Britain, we suggest that the methods adopted are applicable globally.

Rapid assessment of the bryozoan, Zoobotryon verticillatum (Delle Chiaje, 1822) in marinas, Canary Islands.

A rapid assessment, using the abundance and distribution range method, was used to evaluate the status of a large branching bryozoan, Zoobotryon verticillatum attached to the immersed part of marina pontoons in the Canary Islands. Colonies were also found attached to the hulls of leisure craft berthed alongside pontoons at three marinas in Lanzarote during 2012. Low levels of abundance and distribution of the bryozoan occurred in marinas with a freshwater influence whereas in a sheltered marina lacking direct freshwater inputs colonies occurred at ∼2 per metre of combined pontoon length. While the occurrence of this bryozoan is recent it may be expected to occur elsewhere in Macaronesia most probably spread by leisure craft.

Recommendations on methods for the detection and control of biological pollution in marine coastal waters.

Adverse effects of invasive alien species (IAS), or biological pollution, is an increasing problem in marine coastal waters, which remains high on the environmental management agenda. All maritime countries need to assess the size of this problem and consider effective mechanisms to prevent introductions, and if necessary and where possible to monitor, contain, control or eradicate the introduced impacting organisms. Despite this, and in contrast to more enclosed water bodies, the openness of marine systems indicates that once species are in an area then eradication is usually impossible. Most institutions in countries are aware of the problem and have sufficient governance in place for management. However, there is still a general lack of commitment and concerted action plans are needed to address this problem. This paper provides recommendations resulting from an international workshop based upon a large amount of experience relating to the assessment and control of biopollution.

Use of caged Nucella lapillus and Crassostrea gigas to monitor tributyltin-induced bioeffects in Irish coastal waters.

Caging studies have been previously reported to be useful for providing valuable information on biological effects of mollusks over short periods of time where resident species are absent. The degree of imposex in caged dog whelk (Nucella lapillus), was measured using the vas deferens sequence index (VSDI) and the Relative Penis Size Index (RPSI) and the extent of shell thickening in caged Pacific oyster (Crassostrea gigas) was investigated at t = 0 and t = 18 weeks. Nucella lapillus, when provided with mussels as a food source at the control site at Omey Island on the west Irish coast, did not demonstrate imposex features, whereas those transplanted to port areas did. Dunmore East exhibited the highest level of imposex (3.25 VDSI and 2.37 RPSI). Shell thickening was evident in C. gigas transplanted to Dunmore East, with low effects evident at the control location, Omey Island, and Dublin Bay at t = 18 weeks. Dry weight whole-body concentrations of organotins were most elevated in all species held at Dunmore East compared with other locations. Greatest delta15N and delta13C enrichment was observed within the tissues of the predatory N. lapillus in all three test sites. Increased assimilation in the Dublin Bay oysters might have been influenced by the presence of more nutrients at this location. Surficial sediment organotin levels were most elevated in the Dunmore East <2-mm fraction (22,707 microg tributyltin/kg dry weight), whereas low organotin levels were determined from Dublin and Omey Island sediments. The valuable application of cost-effective caging techniques to deliver integrated biological effects and chemical measurements in the absence of resident gastropod populations in potential organotin/tributyltin hotspot locations is discussed.

Alien species in a warmer world: risks and opportunities.

Climate change and biological invasions are key processes affecting global biodiversity, yet their effects have usually been considered separately. Here, we emphasise that global warming has enabled alien species to expand into regions in which they previously could not survive and reproduce. Based on a review of climate-mediated biological invasions of plants, invertebrates, fishes and birds, we discuss the ways in which climate change influences biological invasions. We emphasise the role of alien species in a more dynamic context of shifting species' ranges and changing communities. Under these circumstances, management practices regarding the occurrence of 'new' species could range from complete eradication to tolerance and even consideration of the 'new' species as an enrichment of local biodiversity and key elements to maintain ecosystem services.

Biomonitoring of surface and coastal water for Cryptosporidium, Giardia, and human-virulent microsporidia using molluscan shellfish.

Surface inland and coastal waters in Ireland were surveyed for the human waterborne enteropathogens; Cryptosporidium parvum, Giardia lamblia, Encephalitozoon intestinalis, Encephalitozoon hellem, and Enterocytozoon bieneusi by utilizing bivalve mussel species, i.e., Mytilus edulis (blue mussel), Anodonta anatina (duck 'mussel', actually a unionid clam), and the invasive Dreissena polymorpha (zebra mussel) as biomonitors at twelve sites located in three Irish river-basin districts with various water-quality pressures. Biomolecular techniques were utilized to assess the presence and concentration of these pathogens. At least one pathogen species was detected in shellfish at each site. Cryptosporidium, implicated in several recent Irish gastrointestinal epidemics, was recorded at all sites subjected to agricultural runoff and at one sewage discharge site, linking source-track directly to human and animal fecal wastes. G. lamblia was present at eleven of the twelve sites in a range of concentrations. A coastal bay with raw urban sewage discharge was 100% positive for all analyzed enteropathogens. Overall, the results demonstrate long-term human enteropathogen contamination of Irish waters with consequent public-health risk factors for drinking-water abstraction and water-based activities.

Assessment of biopollution in aquatic ecosystems.

The introduction of alien species (AS) in marine environments is a factor of disturbance that can be viewed as a pollution agent. Using basic information on abundance and distribution of alien species, we developed an index that classifies AS impacts on native species, communities, habitats and ecosystem functioning. This method can be used to evaluate impact at five different levels of biopollution, fitting within the existing schemes for water quality assessment. Both spatial and temporal comparisons are possible. The assessments may also be used to evaluate management performance where avoidance measures were necessary and assist in preventing further unwanted introductions. Such assessments made for the same areas over time provide opportunities for measuring change in biopollution. We have tested the method using four different well-studied areas within the Baltic Sea (brackish to freshwater environments) for two different times, 20 years apart. Further developments of the scheme may be needed to cover some specific cases and taxonomic groups according to their life history.

Aquaculture and transport in a changing environment: overlap and links in the spread of alien biota.

Aquaculture has been practiced for some millennia. The speed and access of different transport modes in the spread of cultured species, their pests, parasites, diseases and associates, has changed over this time. There now exists an overlap and interlinking of different transport networks with further routes planned. Coupled with environmental changes and habitat alterations alien biota are presented with further opportunities to become more widely distributed. The certainty of the responsible pathway for the arrival of an alien species is not always easily deduced unless imported directly. A scheme for classifying different levels of certainty is proposed. Aquaculture itself consists of different cultivation intensities ranging from part to all of a species life-history and are classified accordingly in this account. It is inevitable that further species intended for cultivation will be utilized in different world regions and that other biota, some considered to be harmful, will also be transmitted. Nevertheless there are codes of practice such as those used by the IMO and ICES that can reduce some risks.