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Article

Structure of Non-Indigenous Fouling Assemblages and Biocontamination Levels in Portuguese Recreational Marinas Under Different Salinity Conditions

by
Jesús Fernández-Gutiérrez
1,2,3,*,
Marcos Rubal
3,
Leandro Sampaio
1,
Juan Moreira
4,
Fran Ramil
5,
Isabel Sousa-Pinto
1,2 and
Puri Veiga
1,2
1
Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, Novo Edifício do Terminal de Cruzeiros do Porto de Leixões, Avenida General Norton de Matos, 4450-208 Matosinhos, Portugal
2
Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre s/n, 4169-007 Porto, Portugal
3
Centre of Molecular and Environmental Biology (CBMA/ARNET), Department of Biology, University of Minho, 4710-057 Braga, Portugal
4
Departamento de Biología (Unidad de Zoología) & Centro de Investigación en Biodiversidad y Cambio Global (CIBC-UAM), Universidad Autónoma de Madrid, E-28049 Madrid, Spain
5
CIM-UVigo—Centro de Investigación Mariña, Facultade de Ciencias do Mar, Universidade de Vigo, E-36310 Vigo, Spain
*
Author to whom correspondence should be addressed.
Diversity 2025, 17(4), 245; https://doi.org/10.3390/d17040245
Submission received: 29 January 2025 / Revised: 16 March 2025 / Accepted: 27 March 2025 / Published: 29 March 2025
(This article belongs to the Special Issue Impacts of Invasive Species on Local Biodiversity and Ecology in the Context of Climate Change)
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Abstract

:
The number of recreational marinas has increased in recent years due to the growing demand for leisure boating. Recreational marinas are key points for the introduction of non-indigenous species (NIS), which are considered a source of biocontamination. However, there is scarce knowledge on the influence of environmental features on NIS fouling assemblages, especially regarding different salinity conditions. The aim of this study is to explore the effect of salinity on the structure of NIS fouling assemblages and biocontamination levels. Therefore, fouling assemblages associated with floating pontoons were studied in recreational marinas located in fully marine and brackish habitats on the Northern Portuguese coast. Twenty-four NIS were found, of which arthropods and bryozoans represented the most abundant taxa. Except for NIS abundance, univariate and multivariate analyses showed that NIS assemblage structure was shaped by salinity conditions. Thus, NIS richness and the ratio between NIS richness and total richness were significantly higher in marine than in brackish habitats. Similarly, consistently higher biocontamination levels were found in marine habitats, compromising their ecological status. Quantitative data provided here will be useful in the development of NIS management strategies. Thus, in Northern Portugal, efforts should be focused on marinas under fully marine salinity conditions because they harbor a greater number of NIS and, consequently, a worse ecological status.

1. Introduction

Marine biodiversity is facing an unprecedented global decline due to several factors such as climate change, habitat loss and fragmentation, pollution, overexploitation and biological invasions [1]. Biological invasions are a well-known driver of ecological change on coasts and in estuaries [2]. Non-indigenous species (NIS)—those introduced outside of their natural range (past or present) and outside of their natural dispersal potential by intentional or unintentional human activities [3]—are still increasing elsewhere [4]. After their establishment, NIS may exhibit an invasive behavior, displacing natives through competition, habitat destruction or even predation [5]. Consequently, NIS can potentially lead to irreversible changes in native assemblages, resulting in a variety of ecological and economic impacts [6,7]. Therefore, thorough knowledge of the main factors controlling the introduction, establishment and secondary spread of NIS is crucial to minimize their associated impacts [8]. Once detected, NIS are nearly impossible to eradicate in coastal areas due to the difficulty of delimiting physical boundaries in the marine environment [9]. Therefore, pre-border management strategies, such as identifying or controlling invasion pathways, are strongly recommended to prevent NIS introductions [10]. In this context, commercial shipping and aquaculture have traditionally been identified as the main pathways for NIS introduction in estuaries and coastal areas [11]. Although some regulations and prevention measures have been implemented to minimize the spread of NIS associated with these activities [12,13], some other important pathways (e.g., recreational boating) remain underregulated [14].
The spread of recreational boating in recent years has resulted in an increase in subsidiary infrastructures such as ports and marinas [14]. These structures modify the original environmental conditions by affecting hydrodynamics, sedimentation rate, organic matter, turbidity and pollutant concentration [15,16]. Consequently, marinas are an important source of physical and chemical pollution, which results in a loss of ecosystem services [17]. In addition, the presence of breakwaters, piles and floating pontoons increases surface availability, providing new habitats for fouling assemblages, which may enhance biodiversity in these impacted areas [18,19]. However, these assemblages are often dominated by NIS in marinas worldwide [20,21]. In addition, the variety of submerged substrates derived from boating activity like boat hulls [22], buoys [23], litter [24] or even ropes [25] may act as ‘stepping stones’ for the spread of NIS in these areas. In this way, recreational vessels may eventually facilitate NIS spread among marinas, increase NIS propagule pressure or even allow their propagation to natural surrounding habitats [26,27].
The successful establishment of NIS in fouling assemblages results from the interplay between different biotic and abiotic factors [28]. On the one hand, biotic factors, such as the interaction of NIS with recipient assemblages, are an important filter for NIS establishment [5,29]. For instance, it has been demonstrated that the establishment of NIS in marinas increases alongside a decrease in total species richness [30]. Moreover, native and NIS habitat-forming species may facilitate NIS occurrence by creating new and heterogenous habitats in artificial structures (e.g., [31,32]). On the other hand, several abiotic factors have been pointed out as important drivers of the structure of NIS fouling assemblages in marinas: the type and orientation of substrates [33,34], the increasing concentration of pollutants [35,36], the intensity of boating activity [37,38] and marina design [39,40]. However, little attention has been paid to the environment where a marina is located [41] and, specifically, to the effect of salinity on NIS fouling assemblages [42,43].
Salinity is considered one of the most important drivers of the structure of benthic assemblages in coastal areas [44,45]. In general, native benthic assemblages in transitional systems experience an increase in abundance and diversity from freshwater to marine habitats [46,47]. Regarding biological invasions, the fall in native species richness in brackish habitats has been considered an advantage for NIS establishment [48,49]. In addition, the introduction and propagule pressure of NIS in these areas may be higher due to the great number of ports and aquaculture facilities present in worldwide estuaries [48,50]. Consequently, biocontamination levels in brackish habitats are expected to be greater than in marine ones [51]. For instance, Boets et al. [52] reported that the number of NIS in ports decreased along a gradient of increasing salinity values. However, there is mounting evidence that this pattern is not consistent. Thus, Jimenez et al. [42] and Afonso et al. [43] showed that NIS richness in marinas was positively correlated with salinity. Similarly, some marinas under the influence of high freshwater inputs show lower numbers of NIS [37,53], or none at all [54].
Understanding the role of salinity as a driver of NIS fouling assemblages is crucial in terms of optimizing efforts for NIS management [43]. This management should be based on quantitative and replicable monitoring programs allowing for spatial and temporal comparisons [55]. In recent years, the capacity of NIS monitoring in marinas has been improved by the standardization of several sampling methodologies ([56] and references therein). Furthermore, some legislative tools to prevent and manage the introduction and spread of NIS have been developed by the European Union (EU) [57,58,59]. To facilitate complying with legislative requirements, different indexes have been proposed to describe the impact of NIS on the ecological status of aquatic ecosystems regarded as a source of biocontamination/biopollution: the Site-specific BioContamination Index (SBCI, [60]), Integrated BioPollution Risk Index (IBPR, [61]) and ALien Biotic IndEX (ALEX, [62]). To calculate IBPR and ALEX, previous knowledge with respect to NIS effects and invasion status (casual, established or invasive) in the studied area is required, which are difficult to assess when dealing with small fouling invertebrates in marinas [40]. However, SBCI is exclusively based on native and NIS abundance and richness. Although SBCI has been widely applied in freshwater ecosystems (e.g., [60,63]), Guerra-García et al. [40] demonstrated its usefulness in assessing the ecological status of recreational marinas.
The present study aims to explore the abundance, richness and multivariate structure of NIS fouling assemblages and biocontamination levels in floating pontoons of marinas located in brackish and marine habitats. Specifically, we hypothesized that NIS fouling assemblages and biocontamination levels will differ between marinas under brackish conditions and marine conditions.

2. Materials and Methods

2.1. Study Area

This study was carried out in June 2023 at six marinas on the Northern Portuguese coast: three subjected to fully marine conditions (>32 psu) and three under brackish conditions (<20 psu). The studied marinas were selected because recreational boating was the only known activity to occur there (see https://www.dgrm.pt/en/marinas-e-portos-de-recreio accessed on 20 February 2025), thus avoiding the potential effects that other different activities (e.g., fishing, commercial, recreational) could have on the studied assemblages. From north to south, marinas located in marine habitats were in Viana do Castelo (VCM), Póvoa do Varzim (PV) and Leça da Palmeira (LE), while brackish marinas were located in Viana do Castelo (VCB), Esposende (ES) and Afurada (AF) (Table 1, Figure 1).

2.2. Sampling and Sample Procedure

At each marina, three sites (tens of meters apart) were selected on different floating pontoons. All pontoons were made of fiberglass, and, according to marina staff, none were recently deployed (>5 years) or cleaned, avoiding the sampling of incipient or very disturbed assemblages. At each site, measurements of salinity (psu) were made in situ using a salinity probe. To study the fouling assemblage, 4 haphazard 10 × 10 cm quadrats per site were located on the vertical submerged surface of the pontoons, just below water level. The fouling community attached to the pontoon surface in each selected quadrat was scraped into a 0.5 mm mesh bag. In the same bag, samples were immediately washed and the retained fraction was fixed using a 4% formaldehyde solution stained with Rose Bengal.
In the laboratory, animals were sorted and identified to the lowest taxonomical level possible. The abundances of mobile and solitary sessile epibionts were quantified as number of individuals per 100 cm2. Additionally, stolonal, encrusting and/or modular sessile taxa were quantified as number of colonies per 100 cm2. Although animals can break during the scraping and sieving procedures, colonial species were still individually recognized during sorting under dissection microscope since they were attached to different substrates (mussel shells and byssus, barnacles, algae, ascidians, sponges or even litter). Thus, colonies were only counted when attached to the substrate.

2.3. Data Analysis

The biogeographic status (native, cryptogenic or NIS) of each identified taxon was assigned according to the most recent and/or specialized literature (Table S1). Following the approach of previous studies [20,25,64], cryptogenic and NIS were analyzed together (hereafter referred as NIS) to assess the worst-case scenario.
The biocontamination level was assessed for each replicate based on the SBCI [60], which is derived from two subindices: (i) Abundance Contamination Index (ACI), defined as the ratio between NIS abundance (NNIS) and total abundance (N) per replicate (ACI = NNIS/N), and (ii) the Richness Contamination Index (RCI), which is the ratio between NIS richness (SNIS) and total species richness (S) per replicate (RCI = SNIS/S). With ACI and RCI values, the SBCI is obtained from a matrix with five biocontamination levels ranging from 0 (no biocontamination, high ecological status) to 4 (severe contamination, bad ecological status) [60].
Analyses of variance (ANOVAs) were performed to test significant differences between marine and brackish marinas with respect to the abundance and richness of NIS (NNIS and SNIS, respectively) and ACI, RCI and SBCI values. The following three-way design was considered: Habitat as a fixed orthogonal factor with two levels (marine and brackish); Marina as a random factor nested in Habitat with three levels; and Site as a random factor nested in Marina and Habitat with three levels and 4 replicates. Prior to ANOVA, normality of data was checked by Shapiro–Wilk test [65] and Cochran’s tests were carried out to check for homogeneity of variances [66]. When necessary, data were transformed to achieve homogeneity of variance. When after transformation homogeneity of variance was not achieved, untransformed data were analyzed and the most stringent criterion of p < 0.01 was used to reject null hypotheses [67].
In order to explore differences in NIS assemblage structure between marine and brackish habitats, a permutational multivariate analysis of variance (PERMANOVA) was performed following the aforementioned three-way design. To reduce the relative abundance of numerically dominant species and increase the contribution of less abundant taxa, abundance values of each NIS were square root transformed for the calculation of the Bray–Curtis similarity matrix by permutation of residuals under a reduced model [68]. Due to the lack of NIS individuals in some replicas, a “dummy species” was added to the matrix [69]. When the number of unique permutations was lower than 30, the Monte Carlo P-values were considered [70]. To test if differences in the multivariate assemblage structure between habitats were due to varying multivariate dispersion, the PERMDISP procedure was used [71]. PERMANOVA and PERMDISP used 999 random permutations. Multivariate patterns were illustrated by non-metric multidimensional scaling (nMDS) ordination based on centroids per marina [70]. The reliability of representations was checked, comparing the stress index with threshold values provided by Sturrock and Rocha [72].
The SIMPER procedure [73] was used to determine the percentage contribution (δi%) of each taxon to the Bray–Curtis dissimilarity between assemblages from marine and brackish marinas (δi). A taxon was considered important if its contribution to total percentage dissimilarity was ≥4% [70]. The ratio δi/SD(δi) was used to quantify the consistency of the contribution of a particular taxon to the average dissimilarity in all pair-wise comparisons of samples between habitats. Values ≥1 indicated a high degree of consistency [70].

3. Results

A total of 24 NIS were found: 14 cryptogenic and 10 NIS (Table S1). A total of 13 NIS were found only in marine habitats: 5 in brackish marinas and 6 in both. NIS included 10 arthropods, 7 bryozoans (both phyla found in marine and brackish marinas), 3 ascidians (only in the marine habitat), 3 cnidarians and 1 annelid (both found only in brackish waters) (Table S1). Among NIS, Arthropoda was also the dominant phylum in terms of both abundance (13,800 individuals, 76.11% of NNIS) and species richness (10 species, 41.67% of SNIS) followed by Bryozoa (3,319 colonies, 18.31% of NNIS; 7 species, 29.17% SNIS). Only four NIS represented more than 80% of NNIS: two crustaceans, Zeuxo holdichi Bamber, 1990 (54.94%) and Apocorophium acutum (Chevreux, 1908) (14.81%); and two bryozoans, Watersipora subatra (Ortmann, 1890) (7.53%) and Amathia gracillima (Hincks, 1877) (5.76%).

3.1. NIS Abundance, Richness and Biocontamination Levels

Results of univariate analyses did not detect significant differences in terms of NNIS and ACI values between habitats (Table 2 and Table 3; Figure 2A,C). However, SNIS, RCI and SBCI values were significantly lower in brackish habitats than in marine ones (Table 2 and Table 3; Figure 2B,D and Figure 3A). In marine habitats, the biocontamination level (SBCI = 2.56 ± 0.08) ranged from moderate to high, revealing a moderate/poor ecological status (Figure 3A,B). In contrast, the biocontamination level of brackish habitats (SBCI = 1.36 ± 0.13) was between low and moderate levels, ranking, therefore, within a high/moderate ecological status (Figure 3A,B).

3.2. NIS Assemblage Structure

PERMANOVA analysis also detected significant differences in the multivariate structure of NIS assemblages between marine and brackish habitats (Table 4). PERMDISP results suggested that the dispersion of samples could contribute to these differences (F = 23.335, p = 0.001). Specifically, samples from brackish marinas showed greater dispersion than samples from marine ones. However, the nMDS ordination shows a clear separation between both studied habitats in Figure 4.
SIMPER analysis showed an average dissimilarity of assemblages between marine and brackish marinas of 94.03%. In total, 12 taxa were identified as the most responsible for these differences (Table 5). Collectively, these taxa contributed more than 90% to the total dissimilarity, but in only nine of them the contribution was ≥4%. The contribution to the percentage of dissimilarity of Z. holdichi, A. gracillima, A. acutum and W. subatra was consistent among pair-wise comparisons of samples between the two habitats. Ten species were more abundant or exclusively found in marine habitats, except for Cordylophora caspia (Pallas, 1771) and Sinelobus stanfordi (Richardson, 1901), which were exclusively found in brackish marinas.

4. Discussion

Previous work has pointed out the importance of substrate type for NIS assemblages in marinas [30,74,75,76]. However, few studies have explored the effect on the habitat where the marina is located [41,42]. Regarding salinity, significant differences were reported for NIS assemblages in marinas located along a brackish salinity gradient [77]. Nevertheless, formal comparisons of NIS assemblages between marine and brackish marinas are scarce [42,43]. In our study, NIS assemblage structure and biocontamination levels were studied in marinas located in brackish and marine conditions. The results partially supported our hypothesis because biocontamination levels and NIS assemblage structure differed significantly between marine and brackish marinas except for NIS abundance (NNIS) and ACI values.

4.1. NIS Assemblage Structure

Values of SNIS in natural habitats are usually higher in brackish waters associated with a reduction in native species richness (S) in these habitats [48,49,50,51]. This was also found in Belgian ports [52]. However, our results pointed out greater SNIS values in marine than in brackish habitats. Similarly, most studies carried out in recreational marinas found that fouling NIS richness is positively correlated with salinity [37,42,43,53]. Marked reductions in the number of NIS fouling invertebrates associated with floating pontoons also occurred under high freshwater inputs [53] and NIS were not found in marinas under the direct influence of rivers [43,54]. The brackish marinas selected for this study were located within rivers in an area subjected to tidal exchange (4.18–20.12 psu, oligohaline/mesohaline zone). Nevertheless, huge drops in salinity may occur on the Portuguese coast during autumn and winter heavy rainfalls, affecting benthic assemblages [78,79]. This could limit species dispersal in oligohaline/mesohaline areas [51,80] and explain why marinas located in brackish areas harbor a lower SNIS in comparison to marine habitats.
Most studies in marinas have focused on the effect of salinity on SNIS [37,42,43,53], and therefore it can be expected to be a relevant influence on the abundance of NIS [32,81]. In fact, some studies reported a greater abundance of NIS in oligohaline habitats [52,77]. However, our results did not show significant differences in NNIS between habitats. This pattern could be explained due to differences in the variability of NNIS values between habitats (marine: 9–2158 individuals vs. brackish: 0–242 individuals). Similar trends were also found in natural soft-bottom communities along a salinity gradient in which abundance did not differ significantly according to salinity values [80]. Given the importance of NNIS to an understanding of invasion dynamics [60], further studies seem necessary to elucidate the role of salinity with respect to NNIS in recreational marinas.
Concerning the effect of salinity on NIS assemblage structure, significant differences were found between brackish and marine habitats. Therefore, our results suggest that salinity shapes NIS assemblage structure by affecting NIS composition according to their different salinity tolerance. Similarly, salinity was one of the most important drivers of NIS fouling assemblages in marinas on the Atlantic and Mediterranean coasts of the Iberian Peninsula and Northern Africa [32,81]. The great influence of salinity is also reflected in the observed average dissimilarity between brackish and marine NIS assemblages (94.03%). Similar values (~85%) were previously reported in the San Francisco Bay under analogous salinity conditions [42]. However, PERMDISP results showed that dispersion of samples could contribute to the observed differences between habitats. Warwick and Clarke [82] reported a higher dispersion in communities under an increased anthropogenic perturbation. In the present study, greater dispersion was observed in assemblages of brackish marinas, suggesting that salinity changes may act as an environmental stressor for NIS fouling assemblages [47]. In fact, brackish marinas showed more fluctuating salinity values than marine ones. On the contrary, NIS assemblages of marine habitats showed lower dispersion and thus seem subjected to lower stress. Despite differences in dispersion, a clear separation between brackish and marine habitats can be detected in the nMDS ordination, suggesting that NIS assemblage structure is related to salinity conditions.
Regarding SIMPER results, the hydroid C. caspia and the tanaid S. stanfordi were exclusively found in brackish habitats, while 10 other species were more abundant or exclusively found in marine ones. C. caspia is a well-known fouling NIS in brackish habitats, where it can reach high densities on artificial structures [83,84]. On the other hand, S. stanfordi is a worldwide distributed cryptogenic species, with a few European records in the Netherlands and Belgium in areas near ports [85]. This tanaid can tolerate a wide range of salinity and high densities of the species can be found in marine, brackish and freshwater habitats [85].
Differences in assemblages between brackish and marine habitats were consistently due to the peracarid crustaceans Z. holdichi and A. acutum and the bryozoans A. gracillima and W. subatra. In general, Arthropoda (mainly represented by crustaceans) and Bryozoa often constitute the most abundant phyla in NIS fouling assemblages of marinas [64,76,86]. The tanaid Z. holdichi is a cryptogenic species widely distributed in Europe [87,88] that can reach high abundances in brackish and marine habitats [89,90,91]. In our study, it was the most abundant species in both investigated types of marinas. Z. holdichi was previously reported in areas close to recreational marinas, pointing out the potential importance of marinas with respect to the dispersal of this species [91]. Recreational boating was also pointed out as a dispersal vector for A. acutum [22], which has been previously found in recreational marinas [92] and Portuguese estuaries [89]. Regarding bryozoans, W. subatra was the most abundant species in marine habitats, but one colony was also found in brackish marinas. Although Reverter-Gil and Souto [93] indicated that this species had a gap in its distribution in North Portugal, our results revealed that W. subatra is present there and reached high abundances in marinas, as it has also happened in central Portugal [29]. Finally, the ctenostomatid bryozoan A. gracillima, previously known in Northern Portugal [94], was abundant in marine habitats (1,044 colonies). This cryptogenic species was previously found in ports and marinas [94,95], but its few records, small size and possible misidentifications hinder the proper assessment of its distribution and invasiveness [96].

4.2. Biocontamination Levels

Regarding biocontamination levels, the same patterns were found for RCI and SNIS and for ACI and NNIS. ACI values did not differ significantly between the two investigated types of marinas, suggesting that salinity did not influence the relative abundance of NIS. Conversely, previous studies found higher ACI values (>0.5) alongside a decrease in salinity from marine to nearly freshwater locations [52,60]. Great ACI values (>0.5) indicate the dominance of NIS in terms of abundance, reflecting the displacement of native species due to the presence of highly competitive NIS [60,63]. Conversely, low to moderate ACI values (<0.2) were found in the studied marinas, suggesting a great dominance of fouling native species regardless of salinity values. Similar ACI values were also reported for sessile and vagile fouling assemblages in marine habitats [64].
For the SNIS/S ratio, significantly higher RCI values were found in marine habitats, suggesting that NIS dominance of fouling assemblages in terms of species richness is shaped by salinity. Similar RCI values (~0.2) were found in Mediterranean marinas under marine conditions [38,64,97]. In contrast, higher RCI values were reported in brackish areas of Belgian ports, alongside a decrease in salinity [52]. Values of RCI are more sensitive than ACI when describing changes in recipient communities, since a change in species composition due to the presence of NIS could not be reflected in NIS and native abundance at the early stages of biological invasions [60]. However, this is crucial in NIS management. Thus, considering RCI values in the studied area, NIS management efforts, in our studied area, should be focused on marine habitats.
In the present study, biocontamination levels were assessed through the SBCI [60], which showed significantly higher values in marine habitats. On the contrary, SBCI values in brackish marinas were lower than those observed by Boets et al. [52] in the inner oligohaline/mesohaline areas of Belgian ports (SBCI = 3–4). In marine habitats, SBCI values were also lower than those reported in marinas of the Southern Iberian Peninsula (SBCI = 3–4) [73,98]. Considering the fove categories proposed by the EU Water Framework Directive [57], ecological status was good/moderate in the studied brackish marinas and moderate/poor in the marine ones [60]. Again, SBCI values obtained in the studied area prioritize NIS management efforts in marinas located in fully marine conditions.

5. Conclusions

Our results partly supported the hypothesis that NIS assemblage structure and biocontamination levels will differ between recreational marinas according to salinity conditions, with higher biocontamination levels in marine than in brackish marinas. In this way, the present study emphasizes the importance of the habitat where a marina is located in terms of overall salinity conditions (brackish vs. marine), but we cannot attribute the observed pattern unambiguously to salinity without manipulative studies. Thus, the influence of other factors on NIS assemblages, such as pollution, intensity of boating, competition and predation, cannot be discarded [5,28,29,35,36,37,38]. However, to our knowledge, previous studies have not tested the effects of these factors on NIS in marine and brackish marinas, making it difficult to discuss them in detail in an explanation of our results.
Due to the importance of marinas in NIS monitoring programs, the results of this study provide empirical data that can aid in the development of NIS management strategies. Thus, according to SNIS, RCI and SBCI values, management efforts should be focused on marinas under fully marine conditions; this is paramount with respect to the prevention of NIS infiltration and overall spread in natural surrounding habitats. Our study also provides relevant baseline data for marinas under different salinity conditions that could be useful in the future in terms of testing the effects of NIS on native assemblages.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/d17040245/s1: Table S1: List of the found cryptogenic and NIS with reference to their biogeographical status and the habitat where they were collected. References [22,29,83,84,85,86,87,88,92,93,96,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,114,115,116,117] are cited in the supplementary materials.

Author Contributions

Conceptualization, M.R. and P.V.; methodology, J.F.-G., M.R., L.S., J.M., F.R. and P.V.; validation, M.R., L.S., J.M., F.R. and P.V.; formal analysis, P.V.; investigation, J.F.-G., M.R., L.S., J.M., F.R. and P.V.; resources, P.V. and I.S.-P.; data curation, J.F.-G., M.R., L.S., J.M., F.R. and P.V.; writing—original draft preparation, J.F.-G.; writing—review and editing, J.F.-G., M.R., L.S., J.M., F.R., I.S.-P. and P.V.; visualization, J.F.-G., M.R., L.S., J.M., F.R., I.S.-P. and P.V.; supervision, M.R. and P.V.; project administration, P.V.; funding acquisition, P.V. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the project Marina-Forests (https://doi.org/10.54499/2022.06806.PTDC) funded by the Foundation for Science and Technology (FCT) and partially through national funds within the scope of UIDB/04423/2020 and UIDP/04423/2020 granted to CIIMAR and LA/P/ 0069/2020 and to the Associate Laboratory ARNET and (10.54499/UIDB/04050/2020) to CBMA. P. Veiga (https://doi.org/10.54499/2023.08939.CEECIND/CP2848/CT0002) and M. Rubal (https://doi.org/10.54499/CEECINST/00018/2021/CP2806/CT0021) were hired through the ‘Regulamento do Emprego Científico e Tecnológico—RJEC’ and J. Fernández-Gutiérrez (2023.04100.BD) was supported by a PhD scholarship from the Portuguese Foundation for Science and Technology (FCT) program.

Data Availability Statement

The original contributions presented in this study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding author.

Acknowledgments

We would like to thank the staff of recreational marinas for their kindness and facilities for sampling.

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Figure 1. Location of the studied marinas along the North Portuguese coast. Black triangles indicate brackish marinas and white squares represent marine ones. Viana do Castelo (marine, VCM), Póvoa do Varzim (PV), Leça da Palmeira (LE), Viana do Castelo (brackish, VCB), Esposende (ES) and Afurada (AF).
Figure 1. Location of the studied marinas along the North Portuguese coast. Black triangles indicate brackish marinas and white squares represent marine ones. Viana do Castelo (marine, VCM), Póvoa do Varzim (PV), Leça da Palmeira (LE), Viana do Castelo (brackish, VCB), Esposende (ES) and Afurada (AF).
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Figure 2. Mean values (+SE) in marine and brackish habitats for (A) non-indigenous species (NIS) abundance (NNIS); (B) NIS richness (SNIS); (C) Abundance Contamination Index (ACI); and (D) Richness Contamination Index (RCI). Asterisk indicates significant differences among localities (p < 0.05).
Figure 2. Mean values (+SE) in marine and brackish habitats for (A) non-indigenous species (NIS) abundance (NNIS); (B) NIS richness (SNIS); (C) Abundance Contamination Index (ACI); and (D) Richness Contamination Index (RCI). Asterisk indicates significant differences among localities (p < 0.05).
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Figure 3. (A) Mean values (+SE) for the Site-Specific Biocontamination Index (SBCI) in marine and brackish habitats. Asterisk indicates significant differences among habitats (p < 0.05). (B) Mean values for the Richness Contamination Index (RCI, black bars), Abundance Contamination Index (ACI, gray bars) and Site-Specific Biocontamination Index (SBCI, dots) per marina.
Figure 3. (A) Mean values (+SE) for the Site-Specific Biocontamination Index (SBCI) in marine and brackish habitats. Asterisk indicates significant differences among habitats (p < 0.05). (B) Mean values for the Richness Contamination Index (RCI, black bars), Abundance Contamination Index (ACI, gray bars) and Site-Specific Biocontamination Index (SBCI, dots) per marina.
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Figure 4. nMDS plots of centroids from marine (gray squares) and brackish (black triangles) marinas. Based on centroids per site and marina. Viana do Castelo (marine, VCM), Póvoa do Varzim (PV), Leça da Palmeira (LE), Viana do Castelo (brackish, VCB), Esposende (ES) and Afurada (AF).
Figure 4. nMDS plots of centroids from marine (gray squares) and brackish (black triangles) marinas. Based on centroids per site and marina. Viana do Castelo (marine, VCM), Póvoa do Varzim (PV), Leça da Palmeira (LE), Viana do Castelo (brackish, VCB), Esposende (ES) and Afurada (AF).
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Table 1. Location of sampled marinas in brackish and marine habitats and measured values of salinity in June 2023.
Table 1. Location of sampled marinas in brackish and marine habitats and measured values of salinity in June 2023.
HabitatMarinaCoordinatesSalinity (psu)
BrackishAfurada41°08′32.7″ N 8°39′03.7″ W7.37–7.94
Esposende41°31′37.2″ N 8°46′49.1″ W4.18–4.71
Viana do Castelo41°41′38.8″ N 8°49′17.9″ W19.05–20.12
MarineLeça da Palmeira41°11′11.5″ N 8°42′18.0″ W31.9–32.7
Póvoa do Varzim41°22′16.7″ N 8°45′54.0″ W34.4–34.6
Viana do Castelo41°41′06.4″ N 8°50′18.0″ W33.8–34.1
Table 2. Summary of ANOVAs testing significant differences in terms of abundance (NNIS) and richness (SNIS) of non-indigenous species (NIS) between marine and brackish habitats. Significant differences are indicated in bold. *: p < 0.05; ***: p < 0.001. ns: non-significant.
Table 2. Summary of ANOVAs testing significant differences in terms of abundance (NNIS) and richness (SNIS) of non-indigenous species (NIS) between marine and brackish habitats. Significant differences are indicated in bold. *: p < 0.05; ***: p < 0.001. ns: non-significant.
Source of VariationdfNNISSNIS
MSFMSF
Habitat (Ha)13,211,000.342.771073.3914.06 *
Marina (Ma)(Ha)41,160,390.3027.98 ***76.3630.38 ***
Site (Si) (Ha × Ma)1241,466.570.582.511.86
Residual5471,242.75 1.35
Total71
Transformation none
Cochran’s test C = 0.67p < 0.01C = 0.23ns
Table 3. Summary of ANOVAs testing significant differences for biocontamination indexes (ACI, RCI and SBCI) between marine and brackish habitats. Significant differences are indicated in bold. *: p < 0.05; **: p < 0.01; ***: p < 0.001. ns: non-significant.
Table 3. Summary of ANOVAs testing significant differences for biocontamination indexes (ACI, RCI and SBCI) between marine and brackish habitats. Significant differences are indicated in bold. *: p < 0.05; **: p < 0.01; ***: p < 0.001. ns: non-significant.
Source of VariationdfACIRCISBCI
MSFMSFMSF
Habitat (Ha)10.253.140.1510.18 *25.6820.78 *
Marina (Ma)(Ha)40.08130.80 ***0.0211.75 ***1.247.42 **
Site (Si) (Ha × Ma)12<0.010.23<0.010.660.170.40
Residual54<0.01 <0.01 0.41
Total71
Transformation none none none
Cochran’s test C = 0.31p < 0.05C = 0.28nsC = 0.27ns
Table 4. Results of PERMANOVA testing of significant differences in terms of the structure of non-indigenous species (NIS) assemblages between marine and brackish habitats. Significant differences indicated in bold. *: p < 0.05; **: p < 0.01.
Table 4. Results of PERMANOVA testing of significant differences in terms of the structure of non-indigenous species (NIS) assemblages between marine and brackish habitats. Significant differences indicated in bold. *: p < 0.05; **: p < 0.01.
Source of VariationdfMSPseudo-FUnique Permutations
Habitat (Ha)176,2133.6041 *10
Marina (Ma)(Ha)421,14614.416 **998
Site (Si) (Ha × Ma)121466.82.3584 **998
Residual54621.95
Total71
Table 5. Contribution (δi) of individual taxa to the average Bray–Curtis dissimilarity of non-indigenous species (NIS) assemblages between marine and brackish habitats. SD = standard deviation.
Table 5. Contribution (δi) of individual taxa to the average Bray–Curtis dissimilarity of non-indigenous species (NIS) assemblages between marine and brackish habitats. SD = standard deviation.
SpeciesAverage Abundanceδiδi%δi/SD(δi)
MarineBrackish
Zeuxo holdichi12.042.3619.3820.611.41
Amathia gracillima4.99011.412.132.37
Apocorophium acutum5.7109.29.791.18
Watersipora subatra5.170.039.069.642.21
Austrominius modestus2.290.236.737.150.94
Monocorophium sextonae1.9606.246.640.95
Cordylophora caspia02.245.796.160.74
Monocorophium acherusicum1.640.064.855.150.84
Tricellaria inopinata2.6604.54.790.91
Diplosoma listerianum1.8302.762.941.14
Sinelobus stanfordi01.052.722.90.55
Botryllus schlosseri1.6202.622.790.7
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MDPI and ACS Style

Fernández-Gutiérrez, J.; Rubal, M.; Sampaio, L.; Moreira, J.; Ramil, F.; Sousa-Pinto, I.; Veiga, P. Structure of Non-Indigenous Fouling Assemblages and Biocontamination Levels in Portuguese Recreational Marinas Under Different Salinity Conditions. Diversity 2025, 17, 245. https://doi.org/10.3390/d17040245

AMA Style

Fernández-Gutiérrez J, Rubal M, Sampaio L, Moreira J, Ramil F, Sousa-Pinto I, Veiga P. Structure of Non-Indigenous Fouling Assemblages and Biocontamination Levels in Portuguese Recreational Marinas Under Different Salinity Conditions. Diversity. 2025; 17(4):245. https://doi.org/10.3390/d17040245

Chicago/Turabian Style

Fernández-Gutiérrez, Jesús, Marcos Rubal, Leandro Sampaio, Juan Moreira, Fran Ramil, Isabel Sousa-Pinto, and Puri Veiga. 2025. "Structure of Non-Indigenous Fouling Assemblages and Biocontamination Levels in Portuguese Recreational Marinas Under Different Salinity Conditions" Diversity 17, no. 4: 245. https://doi.org/10.3390/d17040245

APA Style

Fernández-Gutiérrez, J., Rubal, M., Sampaio, L., Moreira, J., Ramil, F., Sousa-Pinto, I., & Veiga, P. (2025). Structure of Non-Indigenous Fouling Assemblages and Biocontamination Levels in Portuguese Recreational Marinas Under Different Salinity Conditions. Diversity, 17(4), 245. https://doi.org/10.3390/d17040245

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