sustainability Article Settlement and Recruitment Potential of Four Invasive and One Indigenous Barnacles in South Korea and Their Future Michael Dadole Ubagan 1,2,†, Yun-Sik Lee 1,3,† , Taekjun Lee 1 , Jinsol Hong 4 , Il Hoi Kim 1 and Sook Shin 1,3,*,† 1 Marine Biological Resources Institute, Sahmyook University, Seoul 01795, Korea; [email protected] (M.D.U.); [email protected] (Y.-S.L.); [email protected] (T.L.); [email protected] (I.H.K.) 2 Department of Animal Biotechnology and Resource, College of Science and Technology, Sahmyook University, Seoul 01795, Korea 3 O-Jeong Resilience Institute, Korea University, Seoul 02841, Korea 4 Division of Environmental Science and Ecological Engineering, Korea University, Seoul 02841, Korea; [email protected] * Correspondence: [email protected]; Tel.: +85-02-3399-1717; Fax: +85-02-3399-1762 † These authors contributed equally to this work. Abstract: Invasion by nonindigenous species is a major threat to marine ecosystems. In this study, the distribution and occupied area (as a percentage) of four invasive barnacles (Amphibalanus am- phitrite, Amphibalanus eburneus, Amphibalanus improvisus, Perforatus perforatus), and one indigenous (Balanus trigonus) barnacle in 13 ports in three Korean seas (East sea, Korea Strait, and Yellow Sea) were investigated. The average ratio for all five species was 11.17% in summer and 7.59% in winter, indicating a higher occupancy in summer. B. trigonus, which is an indigenous species, was found on all ports, except for one (IC). Of the invasive species, A. amphitrite was found mainly in the Yellow Sea, A. improvisus in the Korea Strait, and A. eburneus along with P. perforatus were found in the East Sea. From nonmetric multidimensional scaling (NMDS) analysis, six parameters related to water temperature and salinity were found to be significantly correlated with the distribution and Citation: Ubagan, M.D.; Lee, Y.-S.; occupancy status of these five barnacles. Using the six parameters as independent variables, random Lee, T.; Hong, J.; Kim, I.H.; Shin, S. forest (RF) models were developed. Based on these models, the predicted future dominant invasive Settlement and Recruitment Potential of Four Invasive and One Indigenous species were A. improvisus and A. amphitrite in the Yellow Sea and P. perforatus in the East Sea and Barnacles in South Korea and Their Korea Strait. This study suggests that long-term monitoring of invasive species is crucial, and that Future. Sustainability 2021, 13, 634. determining the relationship between the results of monitoring and environmental variables can be https://doi.org/10.3390/su13020634 helpful in predicting the damage caused by invasive species resulting from environmental changes. Received: 17 November 2020 Keywords: Barnacles; distribution; environmental factors; invasive species; seasons Accepted: 7 January 2021 Published: 11 January 2021 Publisher’s Note: MDPI stays neu- 1. Introduction tral with regard to jurisdictional clai- Barnacles are sessile, filter-feeding crustaceans that attach to a variety of marine ms in published maps and institutio- nal affiliations. substrata [1], making space for attachment and facilitating feeding and reproduction [2]. Hence, barnacles are found attached to rocks, wharf pilings, mollusk shells, crustacean exoskeletons, and other hard surfaces [3]. They are well-known ship-fouling organisms, and thus many species have been translocated to new regions of the world through human Copyright: © 2021 by the authors. Li- activities, such as the international shipping trade [4]. If invasive species succeed in the censee MDPI, Basel, Switzerland. colonization of the new region, they affect the ecology of indigenous species. In many This article is an open access article studies, invasive species have been found to coexist with indigenous species [5,6]; however, distributed under the terms and con- these invasive species can reduce the biodiversity or abundance of indigenous species when ditions of the Creative Commons At- the environment is modified to provide favorable conditions for invasive species [7,8]. One tribution (CC BY) license (https:// such environmental change is water temperature and salinity shifts due to climate change. creativecommons.org/licenses/by/ For example, the invasive barnacles in Europe, Austrominius modestus, has been present at 4.0/). Sustainability 2021, 13, 634. https://doi.org/10.3390/su13020634 https://www.mdpi.com/journal/sustainability Sustainability 2021, 13, 634 2 of 14 low density since the 1940s, but now, the number of A. modestus has been recorded as more than that of the indigenous barnacle at some locations, including the Irish marine nature reserve [9]. For this reason, the biology of invasive barnacles and their establishment in new regions has become the focal point of research regarding the protection of indigenous barnacles under climate change. Successful colonization of invasive barnacles depends primarily on water temperature and salinity [10,11]. Since colonization is the most important step in their life cycle, the effects of water temperature and salinity on settlement and establishment rates have been investigated in laboratory experiments [11,12]. However, few studies have investigated the relationship between the distribution and occupancy status of barnacles and environmental variables in the field. As the inflow of invasive barnacles is concentrated mainly in ports, such as international shipping traffic ports [13], it is necessary to investigate their settlement and establishment potential by analyzing the composition of barnacle communities in major ports, along with water temperature and salinity. Distribution and dissemination of invasive barnacles in Korean coastal waters are usually influenced by ships, and several invasive barnacles have already spread to all Korean coasts (East sea, Korea Strait, and Yellow Sea) [14]. The first reported points of entry for invasive barnacles in the Korean seas were in parts of the Korea Strait and the East Sea [15–17]. Consequently, continuous monitoring of species has been performed in major ports in Korea [18]. Based on this monitoring, four invasive barnacles (Amphibalanus amphitrite, Amphibalanus eburneus, Amphibalanus improvisus, and Perforatus perforatus) were selected as candidates for analysis of ecological disturbance because they were dominant in several ports [18]. In addition, Balanus trigonus, a known indigenous barnacle found nationwide, was also chosen for comparative study [19]. The objectives of this study were: (1) to investigate the distribution and occupancy sta- tus of four invasive and one indigenous barnacle; (2) to evaluate the relationship between the status of the five barnacles and environmental variables related to water temperature and salinity; and (3) to predict future dominant species. The relationship between predicted water temperature and salinity and the composition of the present community of barna- cles are briefly discussed. Based on this relationship, the possibility of invasive species dominance under climate change was predicted and discussed. This is the first study to investigate and predict the relationship between invasive and indigenous barnacles on a regional scale in Korea. 2. Materials and Methods 2.1. Study Area and Sampling Sites Korea, the area of interest in the present study, is located in a temperate zone with four distinct seasons. The Korean peninsula is surrounded on three sides by seas, and there are three sea areas (Yellow Sea, Korea Strait, and East Sea) based on the coastal area (Figure1). In total, 13 harbors or ports that had a high potential influx of barnacles were selected as sampling sites. Five sampling sites (SC, DH, JB, YP, and US) in the East Sea were selected; four (BS, TY, KY, YS) in the Korea Strait; and four (MP, BE, DJ, IC) in the Yellow Sea (Figure1, Table S1). The locations of the sampling sites are shown in Figure1 and their GPS coordinates are listed in Table S1. Sustainability 2021, 13, 634 3 of 14 Figure 1. A map showing the 13 sampling sites surveyed in East Sea, Korea Strait, and Yellow Sea. Information on each sampling site is presented in Table S1. 2.2. Test Barnacles Four invasive and one indigenous species were selected for this study (Table1). A. amphitrite (Darwin, 1854) (AMP), A. eburneus (Gould, 1841) (EBU), A. improvisus (Darwin, 1854) (IMP), and P. perforatus (Bruguière, 1789) (PER) have been known as invasive barnacles because they may cause disturbances in the marine ecosystems of Korea [18]. Balanus trigonus Darwin, 1854 (TRI), was selected because it is the most prevalent barnacle in Korea [19] and is a type of indigenous species that may be disturbed by invasive species. Sustainability 2021, 13, 634 4 of 14 Table 1. Scientific name, abbreviation, origin, year of invasion, and reference for the examined species in the present study. Species Abbr. Origin Year of Invasion Reference Amphibalanus amphitrite AMP Unknown 1979 [15] Amphibalanus eburneus EBU North Atlantic Ocean - [16] Amphibalanus improvisus IMP Easern North America 1990s [16] Western Europe, Northwest coast of Africa, Perforatus perforatus PER 2000 [17] Mediterranean Sea Balanus trigonus TRI Native species 2.3. Sampling Design and Calculation of Barnacle Occupied Area At each sampling site, 10 acrylic attachment plates (30 cm × 30 cm) to which barnacles could attach and inhabit were installed at a depth of between 1 and 3 m from the sea level at low tide. The attachment plates were submerged and exposed for 6 months each in