1 Introduction

The rapid growth of maritime transportation since the industrial revolution has increased the movement of marine organisms via ships, both in the ballast and when attached to the hull (Suk 2018). Several studies have suggested that biofouling introduces and spreads more organisms than those introduced through ballast water (Eldredge and Carlton 2002; Farrapeira et al. 2011).

In 2004, the International Maritime Organization (IMO) adopted the International Convention for the Control and Management of Ships’ Ballast Water and Sediments in response to the challenges posed by the movement of organisms via ships. For organisms adhering to hulls, in 2011, the IMO introduced a guideline for the control and management of ship biofouling aimed at minimizing the transfer of invasive aquatic species. However, unlike the preventive measures targeting ballast water, in which the recommendation took the form of a resolution, the guideline is not legally enforceable (Suk 2018). In several countries, national laws regulating the management of hull-attached organisms have been enacted (Hyun et al. 2018; Park et al. 2022; Shin and Park 2020), but there are no clear guidelines in South Korea.

Biofouling on ships has increased, despite advances in antifouling paints (Lewis 2001). Biofouling of the hull causes a variety of economic and environmental problems, including increasing the cost of ship repair and maintenance (Schultz et al. 2011), and exerting drag, which reduces energy efficiency and, in turn, increases greenhouse gas emissions (Liu et al. 2023). In particular, biofouling of the hull is an important vector for the introduction of non-indigenous species (NIS). International ships are a major route for the introduction, spread, and settlement of NIS (Davidson et al. 2009), with negative effects on native species and human health (Georgiades et al. 2021; Shine et al. 2000). Information on biofouling species is needed to determine the impacts of NIS on marine ecosystems, but studies are very limited.

Ships have large underwater surface areas; this favors the growth of marine organisms (Liu et al. 2023), whose composition and density may differ depending on the attachment area. For example, niche areas are less affected by external factors than exposed areas and, due to their complex structure, are less likely to be coated with antifouling paint, thus providing a safe sheltering place for organisms (Davidson et al. 2009; Moser et al. 2017; Otani 2006; Ulman et al. 2019). Bulbous bows also increase biofouling due to hydrodynamic forces (Alamsyah et al. 2018). For such reasons, macroinvertebrates that attach to the hull may have regional specificity.

Several recent studies have reported that international ships are the main vector for introducing NIS (Çinar et al. 2014; Pinochet et al. 2023). However, while barnacles have been surveyed as an evaluation method for managing biofouling in South Korea (Park et al. 2022; Shin and Park 2020), only biofouling of international ships has been investigated (Park et al. 2022). No accurate species information has been obtained, and the number of studies is limited (Lee et al. 2010; Park et al. 2022). This study aimed to investigate and compare the species distribution patterns of attached macroinvertebrates on six ships with different navigation types (domestic–international and international) and attachment areas in 2021 and 2022.

2 Materials and Methods

Six ships (A–F) were assessed to investigate the management of attached macroinvertebrates. Ship type, size, construction date, main routes, average speed, type of antifouling paint used, and cleaning status were determined. Information on ship management was obtained directly from ship owners and inspectors. Additional operational information was obtained from TradLinx (www.tradlinx.com), the Integrated Port Management Information System (new.portmis.go.kr), a public database of ship operations (www.data.go.kr), and My Ship Tracking (www.myshiptracking.com).

Scuba divers collected quadrat samples (15 × 15 cm) from eight attachment areas (bottom, bow, hull, rudder, screw, shaft, stern, and thruster)on six ships (three each in 2021 and 2022) (Fig. 1a), and qualitative samples were collected from eight attachment areas (bottom, bow, hull, rudder, screw, shaft, stern, and thruster) where high concentrations of macroinvertebrates were randomly sampled (Fig. 1b). For qualitative analyses, sections within the eight areas with high concentrations of macroinvertebrates were randomly sampled. The samples were transported to the laboratory, where species identification was performed by sieving the organisms through a 1-mm mesh sieve, after which the densities and wet weights of the organisms were recorded. Once analyzed, the samples were fixed in 70% ethanol.

Fig. 1
figure 1

Sample methods for attached macroinvertebrates: a Quantitative sampling; b Qualitative sampling

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The number and wet weight (g) of individuals were measured, and the organisms were identified at the species level. Macroinvertebrate number and wet weight (g) were calculated per m2, and the species number, density (individuals/m2), and biomass (g/m2) were analyzed. The Shannon–Weiner diversity index H (loge) (Colwell 2005) was calculated for the density data. Analysis of variance (ANOVA) was used to determine differences in density based on navigation type and attachment area (SigmaPlot 11; Systat Software Inc., San Jose, CA, USA). The results of cluster analysis of biofouling community structure were analyzed using the Bray–Curtis similarity index (Chapman 1998) on fourth-root-transformed species density data. A similarity profile permutation (SIMPROF) test was used to identify differences among species groups, and a similarity percentage (SIMPER) analysis was used to determine which species were the main drivers of the similarity and dissimilarity values of the groups. Permutational analysis of variance (PERMANOVA) was used to analyze differences in macroinvertebrate species similarity among attachment areas and navigation types. Community analyses were performed using PRIMER 7 (Systat Software Inc.).

3 Results

3.1 Ship Information

The six investigated ships were designated as A–F based on the date of the survey. Specific information on the ships is presented in Table 1. Three of the ships (A–C) were research ships that were operated both domestically and internationally. The other three ships (D–F) were full container ships that were operated only internationally. The container ships were larger than the research ships and were operated at higher speeds. The antifouling paint was oldest on ship B (February 2003), while the hulls of ships D and F had not been cleaned. Information on hull cleaning was not available for ship C (Table 1).

Table 1 Ship information
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3.2 Species Composition

Forty species belonging to seven phyla were identified in the qualitative and quantitative surveys (Table 2). Based on navigation type, 21 species belonging to seven phyla appeared on domestic–international ships, and 22 species belonging to three phyla appeared on international ships. Among all species, 17 were attached, 10 of which were NIS; 7 attached NIS were on domestic–international ships, while 5 were on international ships (Table 2).

Table 2 List of species detected on the seven studied ships: species name, non-indigenous species (NIS) classification, NIS origin (first recorded area), and appearance of macroinvertebrate by navigation type
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Ten dominant species were high ranking based on average density (> 2% average density); Balanus trigonus (Thecostraca) predominated (45.39%) (Table 3), followed by Amphibalanus amphitrite (Thecostraca) (9.22%), Bugula neritina (Gymnolaemata) (7.56%), Magallana gigas (Bivalvia) (6.18%), Amphibalanus reticulatus (Thecostraca) (4.66%), Fistulobalanus kondakovi (Thecostraca) (3.91%), Pseudopotamilla occelata (Polychaeta), Actinia equina (Anthozoa), Megabalanus rosa (Thecostraca), and Monocorophium acherusicum (Amphipoda) (Table 3). A. amphitrite had the highest frequency of appearance, at 81.82%, followed by B. trigonus (36.36%) and M. acherusicum (36.36%) (Table 3).

Table 3 Dominant species ranking based on the density of macroinvertebrates as a result of quantitative survey
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3.3 Distribution Patterns According to Navigation Type and Attachment Area

Cluster and non-metric multidimensional scaling analyses (nMDS) of species density revealed four groups (PERMANOVA, df = 3, F = 5.919, p = 0.001; Fig. 2). Groups A and B were domestic–international and differed significantly from groups C and D, which were international (PERMANOVA, df = 1, F = 4.036, p = 0.005). Group A was attached at the stern of domestic–international ships; based on SIMPER analysis, the average similarity was 50.63%, and the species that contributed to the community was B. trigonus. Group B was attached at the bow and midships of domestic–international ships; the average similarity was 54.95%, and the species that contributed to the community were B. neritina, P. occelata, A. equina, and A. amphitrite. Group C was attached to the midships and stern of international ships; the average similarity was 47.27%, and the species that contributed to the community was A. amphitrite. Group D was attached at the bow of international ships; the average similarity was 34.97%, and the species that contributed to the community were M. rosa, A. amphitrite, and Ericthonius pugnax (Table 4).

Fig. 2
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Cluster analysis and non-metric multidimensional scaling (nMDS) using Bray–Curtis similarities, based on the fourth-root transformed abundance data

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Table 4 SIMPER analysis of main characterizing species at each group (A–D) (Av. Abund, average abundance; Av. Diss, average dissimilarity; Contrib%, contribution%; Cum%, cumulative)
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There were significant differences among groups in number of species (one-way ANOVA, df = 3, p = 0.009), species density (one-way ANOVA, df = 3, p = 0.005), species richness (one-way ANOVA, df = 3, p = 0.01), and diversity index (H') (One-way ANOVA, df = 3, p = 0.05) (Fig. 3), all four of which were highest in group D. Based on the SIMPER analysis, the average dissimilarity between groups ranged from 76.65% (D and C) to 100% (A and C) (Table 5). In addition to the previously mentioned species, Hydroides elegans and Koinostylochus sp. also contributed to the dissimilarity between communities (Table 5).

Fig. 3
figure 3

The macroinvertebrate communities according to navigation type and groups: a Number of species (S); b Density (N); c Richness (d); d Diversity (H´)

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Table 5 SIMPER analysis of main characterizing species at each group (A–D; Av. Abund, average abundance; Av. Diss, average dissimilarity; Contrib%, contribution%; Cum%, cumulative%; 5 < Contrib%)
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The effect of navigation type was significantly dependent on the attachment area (two-way ANOVA, df = 2, F = 10.18, p = 0.02; Table 6). On domestic–international vessels, there was a significant difference between midships and stern (p = 0.004) and bow and stern (p = 0.03); on international vessels, there was a significant difference between bow and midships (p = 0.002; Table 6).

Table 6 Results of statistical analysis of navigation and attachment area effects Shannon–Wiener diversity index (H′) of Two-Way ANOVA (p-values: *, < 0.05)
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4 Discussion

Forty species were identified in qualitative and quantitative surveys of eight attachment areas on six ships (Table 2). B. trigonus was the most predominant species (Table 3), while A. amphitrite had the highest frequency of appearance (Table 3). A. amphitrite, Amphibalanus eburneus, A. reticulatus, B. neritina, H. elegans, Ciona intestinalis, Conchoderma auritum, M. rosa, Mytilus galloprovincialis, and Perna viridis were NIS identified in this study (Carlton et al. 2011; Çinar 2012; Foster and Willan 2010; Lee et al. 2010; Park et al. 2018; Siddall 1980). In previous studies, only juvenile P. viridis were reported domestically (Lee et al. 2010) However, in this study, adults were also discovered. Thus, we anticipated that P. viridis would establish itself in Korea in the future. Additionally, C. intestinalis is a known biofouling organism and a designated NIS, and it is managed as a disturbance organism by the Ministry of Oceans and Fisheries (Park et al. 2018). C. intestinalis may decrease ecosystem diversity.

The species composition and distribution patterns differed between the navigation types (Table 2). Reported that international ships are the main factor of NIS, and the domestic–international navigation type acts as a secondary factor in spreading NIS in the country (Otani 2006). In this study, A. reticulatus and M. rosa appeared only on the international navigation type of ship (Table 1). This species was NIS with a low habitat density on domestic–international (Kim et al. 2019). Among the NIS, A. amphitrite, A. eburneus, C. intestinalis, and M. galloprovincialis are completely settled in country (Kim et al. 2019; Lee et al. 2010; Lee and Shin 2014), and Hydroides eleganss is a representative invasive species (Bagaveeva and Zvyagintsev 2000). In this study, A. amphitrite and A. eburneus were dense on international hulls, but H. eleganss was dense on the domestic and international sterns, and C. intestinalis, H. eleganss and M. galloprovincialis were dense on the mid and bow (Fig. 4). Previous studies concluded that ship speed is one of the most important determinants of the survival of biofouling organisms (Coutts et al. 2010; Davidson et al. 2009). The average speed of the domestic–international ships examined in this study was 12 kn, which is less than half that of international ships (29.7 kn) (Table 1). Species density was higher on the slower domestic–international ships (Fig. 2). International ships were the main contributor to NIS, and domestic–international vessels will spread such species into domestic waters, where they have not yet been introduced.

Fig. 4
figure 4

The density of domestically settled non-indigenous species (NIS) by group

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In this study, no clear trend emerged when comparing density, cleaning information, and operating period on each ship (Figure 5). However, the number and density of species on the examined attachment areas differed based on the navigation type (Figure 3). While previous studies showed differences in exposed and niche areas due to external environmental factors (Moser et al. 2017), this study found no such difference. However, a unique finding of this study was the difference in biofouling between bows, midships, and sterns depending on the navigation type (Figure 4). This difference can be attributed to several factors, such as the condition of the antifouling paint, the shape of the ship, and ship speed. Cargo ships, in particular, have a unique bow shape and may have a high rate of antifouling paint removal (Coutts and Taylor 2004), which can increased biofouling due to external factors, such as shear and pressure forces (Alamsyah et al. 2018). The international ships investigated in this study were also cargo ships (Table 1), and the occurrence of high biofouling in Group D (bow) was influenced by these factors. Group B, which showed high biofouling in midships and bows, appeared to have high biofouling even on the flat and wide midships due to low-speed operation (Coutts et al. 2010; Davidson et al. 2009). These results suggest that different management approaches are needed for each attached area depending on the navigation type.

Fig. 5
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The density, operating date, and cleaning information (C/Y = Cleaning/Yes, C/N = Cleaning/No and C/Un = Cleaning/Unknown) of each ship

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Maritime transportation has brought significant benefits to humanity, but it has also caused many problems. Korea is surrounded by the sea on three sides, and its many ports, together with its oceanographic characteristics, provide a perfect environment for the settlement of NIS (Kim et al. 2020; Ubagan et al. 2021). However, only a few NIS have been surveyed to date, and their current status is unknown (Lee et al. 2010). The results of this study indicate that different management strategies are required depending on the type of ship and the location of the operation, as there were differences in species number and density between the navigation types and attachment areas. Future research should investigate the differences between attachment areas with by increasing sampling frequency. Close communication with ship owners and shipping companies is required to obtain more ship information.

5 Conclusion

This study investigated the diversity and distribution patterns of biofouling macroinvertebrates on different types of ships. We identified 40 species, among which B. trigonus was the most dominant in terms of density. Several NIS were identified, including A. amphitrite, A. eburneus, and M. rosa, and P. viridis could potentially settle in Korean waters in the future. Significant differences in species composition and density were found between navigation types, indicating that international ships play a major role in introducing NIS, while domestic–international ships contribute to their spread; ship speed was determined to be a crucial factor, with slower speeds associated with higher species densities. The variation in species diversity between navigation types and attachment areas underscores the need for tailored management strategies.