Biotic resistance of native fouling communities to bioinvasions could not be demonstrated by transplant experiments in Northern Italy.

Biotic resistance is considered an important driver in the establishment of non-indigenous species (NIS), but experiments in the marine environment have led to contradictory results. In this context, a transplant experiment of fouling communities was carried out over five months. Settlement panels were moved from low impact (species-rich native communities) to high impact sites by NIS in two Italian areas to test the biotic resistance hypothesis. Fouling communities displayed significant differences among treatments before and after the transplant, thus indicating the maintenance of a peculiar fouling community in transplanted panels. On the other hand, newly recruited species were similar between treatments and neither a facilitation nor a mitigation role from native fouling communities on NIS was observed. Our results highlight the importance to better investigate the factors affecting the high variability obtained in experiments testing this hypothesis, with the aim to identify potential solutions for NIS management in ports.

Biopollution by Invasive Marine Non-Indigenous Species: A Review of Potential Adverse Ecological Effects in a Changing Climate.

Biopollution by alien species is considered one of the main threats to environmental health. The marine environment, traditionally less studied than inland domains, has been the object of recent work that is reviewed here. Increasing scientific evidence has been accumulated worldwide on ecosystem deterioration induced by the development of massive non-indigenous population outbreaks in many coastal sites. Biopollution assessment procedures have been proposed, adopting criteria already used for xenochemical compounds, adjusting them to deal with alien species invasions. On the other hand, prevention and mitigation measures to reduce biopollution impact cannot always mimic the emission countermeasures that have been successfully applied for chemical pollutants. Nevertheless, in order to design comprehensive water-quality criteria, risk assessment and management strategies, based on scientific knowledge, have been developed in a similar way as for chemical pollution. The Mediterranean Sea is a well-known case of alien species invasion, mainly linked to the opening of the Suez Canal. Non-indigenous species have caused well-documented changes in many coastal ecosystems, favoured by concomitant changes induced by global warming and by the heavy load of nutrients and pollutants by various anthropogenic activities. Naval commercial traffic and leisure boats are among the most active vectors of spread for alien species inside the Mediterranean, and also towards other ocean regions. The scientific evidence gathered and summarized in this review suggests that effective management actions, under a precautionary approach, should be put in place in order to control introductions of species in new areas. These management measures are already established in international treaties and national legislations, but should be enforced to prevent the disruption of the dynamic ecological equilibria in the receiving environment and to control the direct adverse effects of alien species.

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.

Management priorities for marine invasive species.

Managing invasive alien species is particularly challenging in the ocean mainly because marine ecosystems are highly connected across broad spatial scales. Eradication of marine invasive species has only been achieved when species were detected early, and management responded rapidly. Generalized approaches, transferable across marine regions, for prioritizing actions to control invasive populations are currently lacking. Here, expert knowledge was elicited to prioritize 11 management actions for controlling 12 model species, distinguished by differences in dispersion capacity, distribution in the area to be managed, and taxonomic identity. Each action was assessed using five criteria (effectiveness, feasibility, acceptability, impacts on native communities, and cost), which were combined in an 'applicability' metric. Raising public awareness and encouraging the commercial use of invasive species were highly prioritized, whereas biological control actions were considered the least applicable. Our findings can guide rapid decision-making on prioritizing management options for the control of invasive species especially at early stages of invasion, when reducing managers' response time is critical.

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.

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.

Trophic interactions between indigenous and non-indigenous species in Lampedusa Island, Mediterranean Sea.

Using stable isotope analysis, we investigated trophic interactions between indigenous benthic taxa and the non-indigenous species (NIS): the green alga Caulerpa cylindracea, the red alga Asparagopsis taxiformis, the crab Percnon gibbesi and the sea hare Aplysia dactylomela. The study was conducted on Lampedusa Island, Mediterranean Sea. We evaluated the trophic positions and isotopic niches of consumers. Using Bayesian mixing models, we quantified the food source contribution to diets of indigenous and non-indigenous herbivores. Isotopic niche of NIS showed no overlap with the ones of indigenous macroinvertebrates and fish. Caulerpa cylindracea provided the largest contribution to the diet of P. gibbesi (0.431-1), while the dietary contribution estimates overlapped considerably for all sources of A. dactylomela and indigenous herbivores. From these results, we conclude that the invasion of C. cylindracea is increasing the diversity of available prey and might facilitate the expansion of other NIS.

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.

Consumer depletion alters seagrass resistance to an invasive macroalga.

Few field studies have investigated how changes at one trophic level can affect the invasibility of other trophic levels. We examined the hypothesis that the spread of an introduced alga in disturbed seagrass beds with degraded canopies depends on the depletion of large consumers. We mimicked the degradation of seagrass canopies by clipping shoot density and reducing leaf length, simulating natural and anthropogenic stressors such as fish overgrazing and water quality. Caulerpa racemosa was transplanted into each plot and large consumers were excluded from half of them using cages. Potential cage artifacts were assessed by measuring irradiance, scouring by leaf movement, water flow, and sedimentation. Algal invasion of the seagrass bed differed based on the size of consumers. The alga had higher cover and size under the cages, where the seagrass was characterized by reduced shoot density and canopy height. Furthermore, canopy height had a significant effect depending on canopy density. The alteration of seagrass canopies increased the spread of C. racemosa only when large consumers were absent. Our results suggest that protecting declining habitats and/or restoring fish populations will limit the expansion of C. racemosa. Because MPAs also enhance the abundance and size of fish consuming seagrass they can indirectly promote algal invasion. The effects of MPAs on invasive species are context dependent and require balancing opposing forces, such as the conservation of seagrass canopy structure and the protection of fish grazing the seagrass.

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.

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.

Assessing coastal benthic macrofauna community condition using best professional judgement--developing consensus across North America and Europe.

Benthic indices are typically developed independently by habitat, making their incorporation into large geographic scale assessments potentially problematic because of scaling inequities. A potential solution is to establish common scaling using expert best professional judgment (BPJ). To test if experts from different geographies agree on condition assessment, sixteen experts from four regions in USA and Europe were provided species-abundance data for twelve sites per region. They ranked samples from best to worst condition and classified samples into four condition (quality) categories. Site rankings were highly correlated among experts, regardless of whether they were assessing samples from their home region. There was also good agreement on condition category, though agreement was better for samples at extremes of the disturbance gradient. The absence of regional bias suggests that expert judgment is a viable means for establishing a uniform scale to calibrate indices consistently across geographic regions.

Global change and marine communities: alien species and climate change.

Anthropogenic influences on the biosphere since the advent of the industrial age are increasingly causing global changes. Climatic change and the rising concentration of greenhouse gases in the atmosphere are ranking high in scientific and public agendas, and other components of global change are also frequently addressed, among which are the introductions of non indigenous species (NIS) in biogeographic regions well separated from the donor region, often followed by spectacular invasions. In the marine environment, both climatic change and spread of alien species have been studied extensively; this review is aimed at examining the main responses of ecosystems to climatic change, taking into account the increasing importance of biological invasions. Some general principles on NIS introductions in the marine environment are recalled, such as the importance of propagule pressure and of development stages during the time course of an invasion. Climatic change is known to affect many ecological properties; it interacts also with NIS in many possible ways. Direct (proximate) effects on individuals and populations of altered physical-chemical conditions are distinguished from indirect effects on emergent properties (species distribution, diversity, and production). Climatically driven changes may affect both local dispersal mechanisms, due to the alteration of current patterns, and competitive interactions between NIS and native species, due to the onset of new thermal optima and/or different carbonate chemistry. As well as latitudinal range expansions of species correlated with changing temperature conditions, and effects on species richness and the correlated extinction of native species, some invasions may provoke multiple effects which involve overall ecosystem functioning (material flow between trophic groups, primary production, relative extent of organic material decomposition, extent of benthic-pelagic coupling). Some examples are given, including a special mention of the situation of the Mediterranean Sea, where so many species have been introduced recently, and where some have spread in very large quantities. An increasing effort by marine scientists is required, not only to monitor the state of the environment, but also to help predicting future changes and finding ways to mitigate or manage them.

Macrobenthos community structural changes off Cesenatico coast (Emilia Romagna, Northern Adriatic), a six-year monitoring programme.

Soft bottom macrobenthos at a station located off Cesenatico (Emilia Romagna, Northern Adriatic Sea) was investigated seasonally for six years from July 1996 to July 2002. Species composition and abundance of the community have been studied in relation to fluctuation in the water environment parameters, sediment texture patterns and mucilage, that occurred mainly in the water column at the study site. Three major Po river flow peaks occurred in November 1996, October 2000 and May 2002; after these events the community was reduced to minimum abundance values (total density<2000 individuals m(-2)). In the period between the first two episodes the river discharge remained rather low and conditions of increased salinity, lower nutrients and chl a and good oxygen saturation were experienced. The fossorial Crustacean Ampelisca diadema became dominant in the community between the first two river flow events, reaching maximum density of 10,200 individuals m(-2) and substituting the bivalve Corbula gibba, indicator of sediment instability. Species richness increased in the same period. The role of Ampelisca as a facilitator in structuring the community is discussed. Corbula gibba never recovered to initial densities, apart from an abundance peak that occurred in the summer of 2000. Faunal composition seemed to evolve slowly towards a higher degree of structural complexity (positive trend in diversity and evenness index). In the study site near-bottom mucilage events occurred in the summers of 1997, 1998, 2002; they appeared uncorrelated with the observed changes in the community structure. Multivariate analysis of community structure (MDS, ANOSIM) illustrates that community changes in this station are driven mainly by hydrographical conditions influencing sediment texture patterns and trophic resources for the benthos.

A uniform terminology on bioinvasions: a chimera or an operative tool?

A consensual set of definitions regarding bioinvasions is essential in order to facilitate discourse among the science, policy and management communities dealing with the issue. Considering both the mode of entry and the extent of the impact of an alien species into a new environment, a set of key terms is proposed as an operative tool for marine scientists.

Spatial and temporal variability of hard-bottom macrofauna in a disturbed coastal lagoon (Sacca di Goro, Po River Delta, Northwestern Adriatic Sea).

The sessile and mobile macrobenthos on artificial hard bottoms was studied in 12 stations of the Sacca di Goro lagoon, a brackish, highly stressed water basin in the delta of the river Po, open to the Northwestern Adriatic Sea. Three sampling surveys were carried out in June and September 2000 and June 2001 in order to make three types of temporal comparisons: (i) on a seasonal scale, before and after a summer dystrophic event; (ii) on an annual basis, before and after the works of excavation of a canal through the outer sand bank; (iii) on a multiannual scale, comparing the data with those of a survey carried out in 1988. The biocoenoses did not show large fluctuations after a moderately severe summer dystrophic crisis, while the digging of the canal caused clear changes in the macrobenthos community structure after one year. The long-term comparison showed a shift in the community patterns after a decade.