Taming the terminological tempest in invasion science.

Standardised terminology in science is important for clarity of interpretation and communication. In invasion science - a dynamic and rapidly evolving discipline - the proliferation of technical terminology has lacked a standardised framework for its development. The result is a convoluted and inconsistent usage of terminology, with various discrepancies in descriptions of damage and interventions. A standardised framework is therefore needed for a clear, universally applicable, and consistent terminology to promote more effective communication across researchers, stakeholders, and policymakers. Inconsistencies in terminology stem from the exponential increase in scientific publications on the patterns and processes of biological invasions authored by experts from various disciplines and countries since the 1990s, as well as publications by legislators and policymakers focusing on practical applications, regulations, and management of resources. Aligning and standardising terminology across stakeholders remains a challenge in invasion science. Here, we review and evaluate the multiple terms used in invasion science (e.g. 'non-native', 'alien', 'invasive' or 'invader', 'exotic', 'non-indigenous', 'naturalised', 'pest') to propose a more simplified and standardised terminology. The streamlined framework we propose and translate into 28 other languages is based on the terms (i) 'non-native', denoting species transported beyond their natural biogeographic range, (ii) 'established non-native', i.e. those non-native species that have established self-sustaining populations in their new location(s) in the wild, and (iii) 'invasive non-native' - populations of established non-native species that have recently spread or are spreading rapidly in their invaded range actively or passively with or without human mediation. We also highlight the importance of conceptualising 'spread' for classifying invasiveness and 'impact' for management. Finally, we propose a protocol for classifying populations based on (i) dispersal mechanism, (ii) species origin, (iii) population status, and (iv) impact. Collectively and without introducing new terminology, the framework that we present aims to facilitate effective communication and collaboration in invasion science and management of non-native species.

Assessment of the effectiveness of antifouling solutions for recreational boats in the context of marine bioinvasions.

The recreational boating sector is a major vector for the introduction of non-indigenous species (NIS) via biofouling. Despite applying control measures to prevent the growth of fouling communities, most vessels are NIS carriers. This study assessed the effectiveness of different antifouling strategies in a manipulative experiment by testing two common coating typologies (biocide-based and foul-release coatings), accompanied with simulated maintenance practices. The experiment was carried out in the Gulf of La Spezia (Italy) and samples were collected at two different periods. Results showed significant differences among antifouling treatments regarding community structure, diversity, coverage and biovolume of the sessile component, alongside a significant decrease in the performance of biocide-based coating with time. Interestingly, peracarid NIS/native species ratio was higher for biocide-based treatments, suggesting potential biocide resistance. This study highlights the urgent need to develop common and feasible biofouling management plans and provides insights towards identification of best practices for recreational vessels.

Assessing the effect of Amphistegina lobifera invasion on infralittoral benthic foraminiferal assemblages in the Sicily Channel (Central Mediterranean).

This article documents, through a quantitative approach, the negative effect of the highly invasive species Amphistegina lobifera Larsen, 1976 on native benthic foraminiferal assemblages of coastal areas in the Sicily Channel (Central Mediterranean). A nested sampling design was applied through the comparison of benthic foraminiferal community structure across three areas that are known to be at different stages of invasion (i.e. Maltese Islands - advanced, southern Sicily - medium, and eastern Sicily - early). Results suggested that both diversity and richness of benthic foraminiferal community from the Maltese Islands were strongly modified by increased abundances of A. lobifera. In contrast, this phenomenon is less evident in southern and eastern Sicily, where the invader displayed lower abundances and the community structure was more diversified. Collected data also allowed for predicting what could happen in the near future in the whole Sicily Channel, as well as in the rest of the Mediterranean Sea.

First attempt to quantify microplastics in Mediterranean Sabellaria spinulosa (Annelida, Polychaeta) bioconstructions.

This work focuses on the arenaceous reefs by the polychaete Sabellaria spinulosa and addresses microplastics pollution. The main aim is to assess microplastics amount in a bioconstruction located in the Adriatic coast of Italy (Mediterranean Sea) through a comparative approach: sea-floor sediment and bioconstruction samples were analysed to quantify microplastics absolute abundance in both substrates. A total of 431 MPs were found in the investigated substrates: respectively 85 % fibers and 15 % fragments. Multivariate analysis indicates that MPs within bioconstruction occur in higher abundances and with different morphologies than in sediment samples. The analysis of bioconstruction polished sections allowed for observation of MPs agglutinated in their original position: higher concentration is reported in inter-tube areas. Results suggest that physical characteristics of MPs could play a key-role in bioconstruction inclusion processes and raise questions on effective role of sabellariid bioconstructions as a trap for this pollutant in the littoral environment.

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.

Selection or random picking? Foraminiferal tests in Sabellaria alveolata (Linnaeus, 1767) bioconstructions.

This work investigates whether the honeycomb worm Sabellaria alveolata (Polychaeta) actively selects foraminiferal tests to build its arenaceous bioconstructions and if the tests are chosen based on a defined criterion. To this purpose, both foraminiferal content and structure of communities were compared across samples of bioconstructions and samples of neighbouring sediment collected from two sites of southern Sicily (Central Mediterranean). Results document a higher concentration of foraminiferal tests within the tubes than in sediment, with a clear preference for biconvex and spherical morphologies. We hypothesize that the high proportion of biconvex and spherical tests in the bioconstruction is probably due to the active selection operated by the polychaete combined with the different buoyancy of foraminiferal tests kept in suspension by the wave motion. Among the grains agglutinated in the tubes, we also observed sporadic specimens of Amphistegina lobifera Larsen, a non-indigenous foraminifer native to the Red Sea.

An intertidal life: Combined effects of acidification and winter heatwaves on a coralline alga (Ellisolandia elongata) and its associated invertebrate community.

In coastal marine ecosystems coralline algae often create biogenic reefs. These calcareous algal reefs affect their associated invertebrate communities via diurnal oscillations in photosynthesis, respiration and calcification processes. Little is known about how these biogenic reefs function and how they will be affected by climate change. We investigated the winter response of a Mediterranean intertidal biogenic reef, Ellissolandia elongata exposed in the laboratory to reduced pH conditions (i.e. ambient pH - 0.3, RCP 8.5) together with an extreme heatwave event (+1.4 °C for 15 days). Response variables considered both the algal physiology (calcification and photosynthetic rates) and community structure of the associated invertebrates (at taxonomic and functional level). The combination of a reduced pH with a heatwave event caused Ellisolandia elongata to significantly increase photosynthetic activity. The high variability of calcification that occurred during simulated night time conditions, indicates that there is not a simple, linear relationship between these two and may indicate that it will be resilient to future conditions of climate change. In contrast, the associated fauna were particularly negatively affected by the heatwave event, which impoverished the communities as opportunistic taxa became dominant. Local increases in oxygen and pH driven by the algae can buffer the microhabitat in the algal fronds, thus favouring the survival of small invertebrates.

Trends in the detection of aquatic non-indigenous species across global marine, estuarine and freshwater ecosystems: A 50-year perspective.

Aim: The introduction of aquatic non-indigenous species (ANS) has become a major driver for global changes in species biogeography. We examined spatial patterns and temporal trends of ANS detections since 1965 to inform conservation policy and management. Location: Global. Methods: We assembled an extensive dataset of first records of detection of ANS (1965-2015) across 49 aquatic ecosystems, including the (a) year of first collection, (b) population status and (c) potential pathway(s) of introduction. Data were analysed at global and regional levels to assess patterns of detection rate, richness and transport pathways. Results: An annual mean of 43 (±16 SD) primary detections of ANS occurred-one new detection every 8.4 days for 50 years. The global rate of detections was relatively stable during 1965-1995, but increased rapidly after this time, peaking at roughly 66 primary detections per year during 2005-2010 and then declining marginally. Detection rates were variable within and across regions through time. Arthropods, molluscs and fishes were the most frequently reported ANS. Most ANS were likely introduced as stowaways in ships' ballast water or biofouling, although direct evidence is typically absent. Main conclusions: This synthesis highlights the magnitude of recent ANS detections, yet almost certainly represents an underestimate as many ANS go unreported due to limited search effort and diminishing taxonomic expertise. Temporal rates of detection are also confounded by reporting lags, likely contributing to the lower detection rate observed in recent years. There is a critical need to implement standardized, repeated methods across regions and taxa to improve the quality of global-scale comparisons and sustain core measures over longer time-scales. It will be fundamental to fill in knowledge gaps given that invasion data representing broad regions of the world's oceans are not yet readily available and to maintain knowledge pipelines for adaptive management.

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.

Historical baselines in marine bioinvasions: Implications for policy and management.

The human-mediated introduction of marine non-indigenous species is a centuries- if not millennia-old phenomenon, but was only recently acknowledged as a potent driver of change in the sea. We provide a synopsis of key historical milestones for marine bioinvasions, including timelines of (a) discovery and understanding of the invasion process, focusing on transfer mechanisms and outcomes, (b) methodologies used for detection and monitoring, (c) approaches to ecological impacts research, and (d) management and policy responses. Early (until the mid-1900s) marine bioinvasions were given little attention, and in a number of cases actively and routinely facilitated. Beginning in the second half of the 20th century, several conspicuous non-indigenous species outbreaks with strong environmental, economic, and public health impacts raised widespread concerns and initiated shifts in public and scientific perceptions. These high-profile invasions led to policy documents and strategies to reduce the introduction and spread of non-indigenous species, although with significant time lags and limited success and focused on only a subset of transfer mechanisms. Integrated, multi-vector management within an ecosystem-based marine management context is urgently needed to address the complex interactions of natural and human pressures that drive invasions in marine ecosystems.

Correction: A massive update of non-indigenous species records in Mediterranean marinas.

[This corrects the article DOI: 10.7717/peerj.3954.].

A massive update of non-indigenous species records in Mediterranean marinas.

The Mediterranean Sea is home to over 2/3 of the world's charter boat traffic and hosts an estimated 1.5 million recreational boats. Studies elsewhere have demonstrated marinas as important hubs for the stepping-stone transfer of non-indigenous species (NIS), but these unique anthropogenic, and typically artificial habitats have largely gone overlooked in the Mediterranean as sources of NIS hot-spots. From April 2015 to November 2016, 34 marinas were sampled across the following Mediterranean countries: Spain, France, Italy, Malta, Greece, Turkey and Cyprus to investigate the NIS presence and richness in the specialized hard substrate material of these marina habitats. All macroinvertebrate taxa were collected and identified. Additionally, fouling samples were collected from approximately 600 boat-hulls from 25 of these marinas to determine if boats host diverse NIS not present in the marina. Here, we present data revealing that Mediterranean marinas indeed act as major hubs for the transfer of marine NIS, and we also provide evidence that recreational boats act as effective vectors of spread. From this wide-ranging geographical study, we report here numerous new NIS records at the basin, subregional, country and locality level. At the basin level, we report three NIS new to the Mediterranean Sea (Achelia sawayai sensu lato, Aorides longimerus, Cymodoce aff. fuscina), and the re-appearance of two NIS previously known but currently considered extinct in the Mediterranean (Bemlos leptocheirus, Saccostrea glomerata). We also compellingly update the distributions of many NIS in the Mediterranean Sea showing some recent spreading; we provide details for 11 new subregional records for NIS (Watersipora arcuata, Hydroides brachyacantha sensu lato and Saccostrea glomerata now present in the Western Mediterranean; Symplegma brakenhielmi, Stenothoe georgiana, Spirobranchus tertaceros sensu lato, Dendostrea folium sensu lato and Parasmittina egyptiaca now present in the Central Mediterranean, and W. arcuata, Bemlos leptocheirus and Dyspanopeus sayi in the Eastern Mediterranean). We also report 51 new NIS country records from recreational marinas: 12 for Malta, 10 for Cyprus, nine for Greece, six for Spain and France, five for Turkey and three for Italy, representing 32 species. Finally, we report 20 new NIS records (representing 17 species) found on recreational boat-hulls (mobile habitats), not yet found in the same marina, or in most cases, even the country. For each new NIS record, their native origin and global and Mediterranean distributions are provided, along with details of the new record. Additionally, taxonomic characters used for identification and photos of the specimens are also provided. These new NIS records should now be added to the relevant NIS databases compiled by several entities. Records of uncertain identity are also discussed, to assess the probability of valid non-indigenous status.

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 fuzzy 'boater' model to detect fouling and spreading risk of non-indigenous species by recreational boats.

Recreational boating is an unregulated and underestimated vector of spread of non-indigenous species (NIS) in marine environments. The risk of a single boat to spread NIS depends not only on the local environmental context, but also on the type of boat and on the boat owner's behaviour (hull cleaning and painting frequency, travel history). In this paper we present a model to assess the risk of fouling and spreading of NIS and its application to data derived from a questionnaire given to Italian boat owners. The model uses a two-levels fuzzy logic approach: (1) the first level assesses the risk of hull fouling and risk of spreading separately; (2) the second level combines the two separate risks in an overall index ranging from 0 (null risk) to 100 (highest risk) and measures the global risk of NIS introduction and spread through recreational boating. The questionnaire and the fuzzy model allow for a simple and rapid assessment of boats most likely to be infested. The proposed fuzzy model can be easily edited and adapted to context-specific ecological and social conditions. The results of this Italian study showed that 53.9% of the respondents were in the very-low and low risk categories, and 46.1% in the medium, high and very-high risk categories. Possible associations between some boaters habits and the fouling and spreading risk were explored using logistic regression analyses. The results indicate a high-risk profile of boat owner as an experienced sailor who visits many marinas during the summer season. Biosecurity guidelines, containment measures and awareness raising programmes should be implemented to prevent and avoid further spread of NIS in marine environments, and such management actions would benefit from the early detection of high-risk boats, and from the identification of profiles of boaters upon which these initiatives should be prioritized.

Recommendations on standardizing lists of marine alien species: Lessons from the Mediterranean Sea.

Analyses of marine alien species based on national/regional datasets are of paramount importance for the success of regulation on the prevention and management of invasive alien species. Yet in the extant data systems the criteria for the inclusion of records are seldom explicit, and frequently inconsistent in their definitions, spatial and temporal frames and comprehensiveness. Agreed-upon uniform guiding principles, based on solid and transparent scientific criteria, are therefore required in order to provide policy makers with validated and comparable data. Following a meta-analysis on the records of marine alien species in the Mediterranean Sea, we recommend a judicious approach to compiling the data. Here, three categories of uncertainty were identified: species' taxonomic identification, species' actual occurrence in the area, and its status as an alien. In proposing guiding principles to standardize such datasets, we aim to encourage discourse on logical, standardized and transparent criteria to substantiate records of alien species.

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.

Opportunities for web-based indicators in environmental sciences.

This paper proposes a set of web-based indicators for quantifying and ranking the relevance of terms related to key-issues in Ecology and Sustainability Science. Search engines that operate in different contexts (e.g. global, social, scientific) are considered as web information carriers (WICs) and are able to analyse; (i) relevance on different levels: global web, individual/personal sphere, on-line news, and culture/science; (ii) time trends of relevance; (iii) relevance of keywords for environmental governance. For the purposes of this study, several indicators and specific indices (relational indices and dynamic indices) were applied to a test-set of 24 keywords. Outputs consistently show that traditional study topics in environmental sciences such as water and air have remained the most quantitatively relevant keywords, while interest in systemic issues (i.e. ecosystem and landscape) has grown over the last 20 years. Nowadays, the relevance of new concepts such as resilience and ecosystem services is increasing, but the actual ability of these concepts to influence environmental governance needs to be further studied and understood. The proposed approach, which is based on intuitive and easily replicable procedures, can support the decision-making processes related to environmental governance.

Critical appraisal on the identification of Reference Conditions for the evaluation of ecological quality status along the Emilia-Romagna coast (Italy) using M-AMBI.

According to the European Water Framework Directive, the ecological status (ES) of a water body is determined by comparing observation data with undisturbed Reference Conditions (RCs). Defining RCs is crucial when evaluating the ES of a water body as it strongly affects the final outcome of any index application. Identifying RCs by observing real sites is not feasible in many marine environments, such as the Emilia-Romagna coast (Italy, N-Adriatic Sea). We used a statistical approach on a large dataset to derive RCs for the application of the benthic index M-AMBI in this area. We then applied M-AMBI to samples collected along a gradient of presumed environmental disturbance. The results put 14.8% of the Emilia-Romagna samples in "High" ES, 60.2% in "Good", 23.0% in "Moderate" and 2.0% in "Poor", showing a spatial gradient of improving quality. These results are in agreement with the extensive ecological knowledge available for this area.

Functions and ecological status of eight Italian lagoons examined using biological traits analysis (BTA).

The soft-bottom communities of eight Italian lagoons were analyzed for eight biological traits (feeding, mobility, adult life habitat, body size, life span, reproductive technique, type of larva and reproductive frequency) in order to identify the dominant traits in different transitional environments. We considered the ecological quality status (EcoQS) of the stations, assessed by two biotic indices, AMBI and Bentix. Stations were categorized into EcoQS classes to investigate the relationship between biological functions and ecological quality. The results indicate that the variability of the data was governed by traits linked to resource utilization rather than to life cycle. Lagoons affected by chronic disturbance displayed a poor functional composition, which usually corresponded to poor EcoQS in some cases, correlations between ecological groups and traits modalities were ecologically relevant; however, classes of EcoQS were found to be relatively independent from the functional structure of the considered stations.