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ISSN : 1229-3431(Print)
ISSN : 2287-3341(Online)
Journal of the Korean Society of Marine Environment and Safety Vol.31 No.2 pp.201-213
DOI : https://doi.org/10.7837/kosomes.2025.31.2.201

Application of Fulvic Acid Supplementation to Improve Macroalgae Communities through Field Experiments

Ilwon Jeong*, Chang Geun Choi**,***, Hyun-Kyum Kim****, Jong Ryol Kim****, Kyunghoi Kim*****†
*Assistant professor Graduate School of Advanced Science and Engineering, Hiroshima University, Hiroshima, 739-0046, Japan
**Professor, Department of Ecological Engineering Pukyong, National University, Busan, 48513, Korea
***Director, Underwater Panorama Institute, Busan 48428, Korea
****Resercher, Korea Fisheries Research Agency, Busan, 46041, Korea
*****Professor, Department of Ocean Engineering, Pukyong National University, Busan, 48513, Korea

* First Author : jeongiw@hiroshima-u.ac.jp, +81-82-424-7818


† Corresponding Author : hoikim@pknu.ac.kr, 051-629-6583

March 11, 2025 March 31, 2025 April 25, 2025

Abstract


Fulvic acid (FA) chelates Fe(III) to bioavailable Fe(II), promoting macroalgae growth and thus restoring impacted coastal seaweed bed (CSB). This study aimed to elucidate the effects of FA supplementation on the restoration of a CSB through enhanced macroalgal growth. In a coastal area characterized by iron limitation, FA supplementation was implemented on an artificial reef, and additional monitoring points were established nearby. Seasonal surveys of macroalgae and the surrounding marine environment were conducted over four seasons using scuba diving. The results revealed that the increased Fe availability due to FA supplementation stimulated photosynthesis and nutrient uptake, thus fostering macroalgal growth. Furthermore, the total biomass of the dominant species was strongly correlated with the total biomass of the entire macroalgal community. This indicates that Fe supplements contribute to a quantitative increase in the dominant species, thereby driving both quantitative and structural shifts in the macroalgal community. The results provide basic conditions for the precise application of FA supplementation in CSB restoration.


Coastal seaweed bed , Iron , Fulvic acid , Macroalgal community , Restoration

풀빅산 공급으로 개선된 해조류 군집에 관한 현장 실험 연구

정일원*, 최창근**,***, 김현겸****, 김종렬****, 김경회*****†
*일본 히로시마대학 공학연구과 조교수
**국립부경대학교 생태공학과 교수
***수중경관연구소 이사
****한국수산자원공단 연구원
*****국립부경대학교 해양공학과 교수

초록


풀빅산(FA)은 Fe(III)을 킬레이트화하여 생물학적으로 이용 가능한 Fe(II)로 전환함으로써 대형 해조류의 성장을 촉진하고 손상된 해중림의 복원을 돕는다. 이에 본 연구에서는 풀빅산의 공급에 따른해중림 개선에 미치는 효과를 조사, 분석하였다. FA 보충제는 철(Fe) 부족 해역 내 인공 어초에 설치되었으며, 해조류 군집 및 해양 환경조사는 사계절을 대표하는 학술 잠수를 통해 수행되었다. 연구 결과, 풀빅산 공급으로 인해 가용 철(Fe) 농도가 증가하면서 해조류의 광합성과 영양소 흡수가 촉진되어 성장률이 향상되는 것으로 나타났다. 우점종의 총 생물량은 전체 해조류 총 생물량과 비우점종에 비해 더욱 강한 상관관계를 나타내었다. 이는 철 보충제가 특정 우점종의 양적 증가에 기여하며, FA 보충제가 설치된 어초에서 해조류 군집의 양적 및 구조적 변화를 유발했음을 시사한다. 본 연구 결과는 풀빅산을 해중림 복원에 적용하기 위한 기초적인 정보를 제공하며, 향후 해조류 생태계 관리 및 보존 전략 수립에 기여할 수 있을 것으로 기대된다.


해중림 , 철 , 풀빅산 , 해조류 , 복원

    1. Introduction

    Coastal seaweed beds (CSB) balance the coastal environment through high primary production and are highly advantageous to the ecosystem (including spawning grounds and marine habitats). Thereby, these contribute to the preservation and expansion of marine biodiversity (Mann, 1982;Smale et al., 2020). CSB consists mainly of seaweeds that alleviate environmental problems such as global warming and eutrophication by absorbing CO2 during photosynthesis and removing the excess inorganic matter (Hamilton et al., 2022;Hayashi et al., 2010). For example, seaweed aquaculture sequesters approximately 1,500 tons of CO2/km2/year (Duarte et al., 2017).

    Although CSB is essential for a healthy coastal ecosystem, it has been devastated significantly by coastal reclamation and development (Okuda, 2008), seawater pollution (Duarte Moreno et al., 2021), and acidification by global climate changes (Pajusalu et al., 2020). The Korea Fisheries Resources Agency (FIRA) reported that 17,000 ha of barren ground formation caused a loss of CSB, and reduced fisheries catch amount by 40%. This corresponded to a loss of approximately 50 million USD for the Korean fishery industry (KOREA FISHERIES RESOURCES AGENCY, 2022b). Therefore, CSB restoration is necessary to promote the stability and sustainability of coastal ecosystems.

    Iron (Fe) is one of the most important metallic elements in living organisms in terms of photosynthesis and respiration (Hartnett et al., 2012). It promotes seaweed growth through enzymatic reactions such as chlorophyll synthesis, oxygen metabolism, and electron transfer processes (Naito et al., 2005;Polat et al., 2020). It has also been reported that Fe addition improves seagrass growth even in carbonate sediments (Marbà et al., 2008). Although Fe plays a vital role in sustaining coastal ecosystems, its bioavailable fraction of seawater is significantly low (Johnson et al., 1997;Naito et al., 2005). The general form of Fe in seawater is Fe(III) owing to oxidization (Yamamoto et al., 2012). It is less bioavailable than Fe(II) (Yang et al., 2022).

    Meanwhile, terrestrial fulvic acid (FA) is considered an important substance. It is formed naturally during the decomposition of floral-faunal residues (Tuhkanen and Ignatev, 2019), and can accelerate nutrient assimilation by plants (Piccolo et al., 1992). FA chelates Fe(III) to bioavailable Fe(II) in coastal areas, thereby contributing to seaweed growth (Matsunaga et al., 1998b;Nigi et al., 2000). Additionally, increased seagrass growth and aquaculture production by FA supports the application of FA in marine environments to enhance CSB (Jusadi et al., 2020;Matsunaga et al., 1998a).

    Fe and FA are generally originated from the terrestrial environment into coastal areas through rivers, rainwater runoff, and groundwater. However, the supply of both the substances to coastal areas has been limited because of the development of coastal areas, such as harbors, estuary dykes, land reclamation, and coastal cities (Oura et al., 2023;Yamamoto et al., 2012). Therefore, deficient bioavailable Fe inhibits the growth of seaweed, thereby causing a reduction in CSB.

    Recently, the application of the biological chelating agent, FA, has been studied for CSB restoration to develop a healthy coastal ecosystem (Lee et al., 2021;Matsunaga et al., 1998b;Yamamoto et al., 2012). The installation of FA supplement on ARs is likely to improve CSB by providing additional bioavailable Fe(II). through eluted FA. In addition, the application of FA supplements is considered to add chemical functions to the existing AR which may improve its structural functions for CSB improvement.

    Before the demonstration of the definitive effects of FA supplementation, a preliminary investigation is required as part of establishing baseline conditions to clarify its effective range and ecological responses. This study assessed the potential of FA supplementation for CSB restoration in an artificial reef (AR). Macroalgae are used as bioindicators of CSB variations (D'Archino and Piazzi, 2021). Therefore, FA supplement were installed in the AR, and the variations in the macroalgal communities were monitored and analyzed throughout the year.

    2. Materials and methods

    2.1 Production and property of fulvic acid supplement

    The FA used in this study was a commercial product (NEOMAX, Korea). It had an Fe concentration of 754.2 mg/L. FA (6.6 L) was mixed with a mixture of coal bottom ash and oyster shell mixture (13.5 L; mixing ratio by weight 1:1). The resulting mixture was molded into a square block (0.25 × 0.25 × 0.1 m) and demolded after a curing period of one month. A total of 18 FA supplements were prepared for field experiment. Meanwhile, Jeong and Kim (2023) reported that this coal bottom ash and oyster shell mixture showed a compressive strength of 0.93 MPa. This indicated a sufficient durability for use as an FA supplement.

    The primary and auxiliary functions of the FA supplement were to elute FA and Fe, respectively. Elution experiments were conducted to investigate the elution of Fe from the FA supplement. The FA supplement (100 g) and 1 L of ultrapure water (Ultima Duo 200, Balmann Tech) were placed in a 1 L high-density polyethylene (HDPE) bottle. The ultrapure water was replaced daily, and the Fe-eluted solution was sampled at 1, 2, 3, 5, 10, 20, 30, 40, 50, 60, 70, and 80 days. The Fe concentration in the Fe-eluted solution was analyzed using inductively coupled plasma mass spectrometry (ICP-MS; NexION 300D, Perkin Elmer).

    2.2 Study site property and FA supplements installation

    The study was conducted along the coast of Changpo-ri, Yeongdeok-gun, Gyeongbuk, Republic of Korea. Based on preliminary field observations and a literature review, the macroalgal community at the study site was uniform without significant differences. The sea bottom at the study site consisted of boulders and rocks (Fig. 1a). These provided a suitable substratum for macroalgal growth (Akrong et al., 2021). The phosphorus (P) and Fe ratio in the seawater of the study site was 1 P: 0.00320 – 0.00447 Fe based on the preliminary field observations. This ratio was lower than the Redfield ratio, 1 P:0.0075 Fe (Bristow et al., 2017). This indicated that Fe is a limiting factor for primary production. Therefore, this site was selected as an appropriate study site to evaluate the effects of FA supplementation.

    In this study site, the AR was installed a water depth of 6 m in 2007 and approximately 200 m offshore from the coast line to provide a seaweed habitat and spread seaweed (Korea Fisheries Resources Agency, 2022c). The AR was made of reinforced concrete with a cross-shape (3.0 × 3.0 × 0.5 m, 4.4 ton) of 5 m2 projected area (Fig. 1b) (Korea Fisheries Resources Agency, 2022a).

    A total of five monitoring points were designated at the study site considering the primary current flowing south to north (Fig. 1d and Table 1). First, the point where the AR was located was selected (E-0) to install the FA supplements. Additional monitoring points 10 m (E-10), 20 m (E-20), and 30 m (E-30) north of E-0 were selected to monitor the effects of the FA supplements. A monitoring point for the control (C-0) was located 100 m south of E-0. No ARs existed in C-0, E-10, E-20, and E-30.

    2.3 Marine environment observation

    The periodic scuba diving on the study site was conducted in Jul, Oct, and Nov 2020, and Apr, Jun, Oct, and Nov 2021. The investigation in Jul 2020 was conducted to determine the study site. Six FA supplements were installed in Oct 2020 and replaced with six new FA supplements in Apr and Oct 2021 (Fig. 1c). The FA supplements were not lost or destroyed during the observation period.

    Light intensity and water temperature loggers (DEFI2-L and DEFI2-T, JFE Advantech, Japan) were installed on the AR at E-0. These were operated periodically for 60 min from Jul 2020 to Nov 2020, and from Apr 2021 to Nov 2021. No light intensity and water temperature data were obtained owing to the loss of loggers from Dec 2020 to Mar 2021.

    Seawater from C-0 to E-30 was sampled 1 m above the sea bottom and transported to the laboratory for analysis. Seawater was not collected from E-10, E-20, and E-30 in Jul 2020. The seawater was filtered using a syringe filter (0.45 μm). Subsequently, the pH, PO4-P, and dissolved inorganic nitrogen(dissolved inorganic nitrogen (DIN): NH3-N+NO2-N+ NO3-N) were measured using a pH meter (LAQUAF-53, Horiba) and spectrometer (DR3900, Hach). The pH, PO4-P, and DIN analyses were not conducted in Jul 2020. The Fe concentration was measured using ICP-MS. Fe analysis was not performed at any of the monitoring points in Jul 2020. All the analyses were repeated three times.

    2.4 Collection and analysis of macroalgae and macro invertebrates

    Macroalgae were collected from all the monitoring points by scuba diving. Macroalgae was collected only at C-0 and E-0 in Jul 2020. Before collecting the macroalgae, a 0.5 × 0.5 m quadrat (subdivided into 0.1 × 0.1 m) was applied randomly to capture photographs, and the number of individuals was counted. Subsequently, all macroalgae inside the quadrats were collected. This procedure was repeated three times at each monitoring point. The collected macroalgae were stored in an icebox and transported to the laboratory.

    Macroalgae identification was conducted with the naked eye and using a microscope (Olympus SZX9, Olympus BX50, Japan). The wet weight (up to 0.01 g) of macroalgae was measured using an electronic balance (CAS, CBL2300H, Korea) and converted to biomass (g wet weight/m2).The macroalgae species were listed using a list provided (Kim et al., 2013;Okamura, 1909-1937;1910-1937;1916-1923).

    The ecological indices of richness (Margalef, 1958), evenness (Pielou, 1977), diversity (Shannon et al., 1963), and dominance (Simpson, 1949) in macroalgae were calculated to evaluate the macroalgae community transformations.

    2.5 Statistical methods

    The collected data were organized using Microsoft EXCEL. Principal component analysis (PCA) was conducted using the normalized environmental data and plotted using PRIMER 7. The variations in the marine environmental data, number of species, and total biomass of macroalgae were plotted using Origin 2021b. The correlations between the number of species, biomass, and ecological indices were calculated based on Pearson’s correlation coefficient with p-values. The correlations were plotted using Origin 2021b.

    3. Results and discussion

    3.1 Variations of Fe concentration in elution experiment

    Fig. 2 shows the variation in Fe concentration from the FA supplement in elution experiment. Although the Fe concentration fluctuated significantly from 50.8 μg/L to 470.2 μg/L during 40 days, it became a steady range of 81.1–95.7 μg/L. This indicates that the FA supplementation frame installed at the AR site can stably release Fe at a rate of approximately 88.4 μg per liter per day. A previous study reported that the average Fe concentration around the coastal area of Korea was 33μg/L (KINS, 2014). This indicated that FA supplements can provide sufficient Fe elution potential.

    3.2 Variations in the marine environment

    The water temperature in the study site was 9.7–25.5°C in Jul –Nov 2020 and 4.4–27.7°C in Apr–Nov 2021 (Fig. 3a). The highest monthly average water temperature was 20.7°C in Sep 2020 and 24.5°C in Aug 2021. The lowest average monthly water temperature was 16.5°C in Nov 2020 and 12.5°C in Apr 2021. The light intensity was 0.1–846.7 μmol∙m-2∙s-1 in 2020 and 0.2– 890.5 μmol∙m-2∙s-1 in 2021 (Fig. 3b). The highest and lowest monthly average light intensity was 104.2 μmol∙m-2∙s-1 in Aug 2020 and 0.8 μmol∙m-2∙s-1 in Sep 2021, respectively. Both the water temperature and light intensity were lower in autumn and winter and higher in spring and summer. A similar pattern of seasonal water temperature variations was observed in a previous study (Kim et al., 2014). Therefore, it is considered that the water temperature and light intensity exhibited typical seasonality.

    The pH at the study site ranged from 8.1 to 9.0 throughout the observation period (Fig. 4a). However, it was 8.5–8.7 in Oct 2020 and 8.7–8.9 in Jun 2021. This was higher than that in another season with a pH range of 8.1–8.5. Seasonal plankton blooms are considered to increase the pH in autumn (Oct 2020) and spring (Jun 2021) (Yoo and Kim, 2004). In addition, the water temperature and light intensity were higher during these periods, thereby enhancing phytoplankton blooms. Therefore, it can be concluded that the pH increased temporarily because of the period when phytoplankton growth became active (Pedersen et al., 2013).

    The concentrations of PO4-P, NH3-N, NO2-N, and NO3-N (DIN) at all the monitoring points were 0.01–0.05 mg/L, 0 mg/L, 0.002 –0.006 mg/L, and 0.01–0.03 mg/L, respectively, during the observation period (Fig. 4b and 4c). The PO4-P and DIN concentrations were relatively higher in Nov 2020, and Apr, and Nov 2021, but relatively lower in Oct 2020 and Oct 2021. This revealed a similar pattern owing to phytoplankton blooms. The accumulation and consumption of nutrients typically occurs before and after phytoplankton blooms. This indicates that the seasonality of temperate zones significantly influences the study site (Yamamoto et al., 2022).

    The Fe concentration at all the monitoring points was 0.03– 0.99 μg/L during the observation period (Fig. 4d). The average Fe concentrations at all the monitoring points showed no statistically significant differences. However, the Fe concentration at E-0 was 0.53 μg/L, which was numerically higher than the range at the other monitoring points (0.43–0.46 μg/L). Fe would have been consumed by the macroalgae growth in the summer of 2020 (Nwankwegu et al., 2020), thereby causing the lowest Fe concentrations at all the monitoring points in Oct and Nov 2020. The seasonal precipitation in Apr and Jun 2021 would also have released Fe from the land to the coastal area and increased the Fe concentration. Subsequently, these high Fe concentrations decreased gradually in Oct and Nov 2021 owing to the uptake by the macroalgae.

    The concentrations and rates of variation in PO4-P, DIN, and Fe were similar at all the monitoring points. Therefore, it was difficult to separate E-0 (which was directly affected by FA supplements) from the other monitoring points, as revealed by the PCA analysis. The PCA showed 65.5% of the total variability in the first two axes (PC1 (42.9%) and PC2 (24.2%)) in the measured environmental variables (Fig. 5). It separated all the monitoring points from the pH at negative scores to PO4-P and NO3-N at positive scores on the PC1 axis, and from Fe at negative scores to NO2-N at positive scores on the PC2 axis. A cluster from Apr 2021 was placed at the end of PC1 compared with another cluster. This is considered to be a temporary phenomenon owing to the higher PO4-P and NO3-N concentrations. E-0 of Nov 2020 also separated from a cluster in Nov 2020 due to the temporary high Fe concentration. Most importantly, it is conjectured that there were no significant differences between monitoring points in the marine environment because all these points formed clusters at a Euclidean distance of 1.85 for each sampling date.

    3.3 Variations in species and biomass of macroalgae

    A total of 130 macroalgal species were identified at the study site during the observation period (Fig. 6). Of these, 18 (13.8%) belonged to Chlorophyta, 17 (13.1%) to Phaeophyta, and 95 (73.1%) to Rhodophyta. Rhodophyta typically appear where strong water flow is observed (Shepherd and Womersley, 1981), supporting that many Rhodophyta species were observed at the study site with an active seawater flow.

    The maximum and minimum numbers of macroalgal species appearing at the study site were 79 in Jun 2021 and 52 in Oct 2020. The numbers of macroalgae species that appeared at C-0, E-0, E-10, E-20, and E-30, during the observation period were 91 (Chlorophyta: 7, Phaeophyta: 17, Rhodophyta: 67), 94 (Chlorophyta: 10, Phaeophyta: 10, Rhodophyta: 74), 90 (Chlorophyta: 10, Phaeophyta: 13, Rhodophyta: 67), 84 (Chlorophyta: 10, Phaeophyta: 13, Rhodophyta: 61), 83 (Chlorophyta: 6, Phaeophyta: 11, Rhodophyta: 66), respectively.

    From Oct 2020 to Nov 2021, the numbers of macroalgal species that appeared during each sampling period were 27–49, 25–54, 30–43, 31–46, and 32–44 at C-0, E-0, E-10, E-20, and E-30, respectively. The total biomass of the macroalgae species were 482.74–5,210.82 g/m2, 94.08–4,581.42 g/m2, 353.94–4,676.72 g/m2, 246.72–4,866.62 g/m2, and 249.44–2,940.92 g/m2 at C-0, E-0, E-10, E-20, and E-30, respectively. The number of species and total biomass of the macroalgae were highest for Rhodophytaduring the observation period.

    The most common and dominant macroalgae were Eisenia bicyclis, Gelidium elegans, and Pachymeniopsis elliptica in all the monitoring points during the observation period. The ratio of total biomass for these three dominant macroalgae for the total appeared species was 57.2–99.5%, 47.6–98.1%, 55.0–97.9%, 20.9– 98.5%, and 38.8–98.0% at C-0, E-0, E-10, E-20, and E-30, respectively, from Oct 2020 to Nov 2021. The ratio of total biomass for these three dominant macroalgae at all the monitoring points was 90.5–98.5%, 20.9–84.2%, and 96.4–99.5% in Oct 2020, Apr 2021, and Nov 2021, respectively. The three dominant macroalgae are perennial species (Choi, 2008;Park and Choi, 2009;Park et al., 2014). These maintain high biomass ratios throughout the year. The abrupt decrease in the ratio of the three dominant macroalgae in Apr 2021 is considered to coincide with the increased growth rate of other macroalgae owing to the seasonality.

    The number of species and total biomass of the macroalgae appeared to be highest in Jun 2021. This phenomenon was associated with the lower PO4-P and DIN concentrations and higher pH in Jun 2021 compared with those in Apr 2021. However, the highest values for the number of species and total biomass in macroalgae are typically influenced by the seasonality (i.e., increased water temperature and nutrient accumulation) and are generally observed in spring and summer (Jankowska et al., 2014). This hindered the evaluation of the improvement in the macroalgal community owing to FA supplementation during spring and summer. Therefore, the effect of FA supplementation on the macroalgae was evaluated by comparing Nov 2020 and Nov 2021, when the macroalgal growth was suppressed by the low water temperatures and light intensity.

    The number of macroalgal species decreased by 5.1% at C-0 and increased by 64.3% at E-0 in Nov 2021 compared with Nov 2020. The total biomass of macroalgae increased by 111.9% at C-0 and 1455.6% at E-0 in Nov 2021 compared with Nov 2020. However, the three dominant macroalgae, Eisenia bicyclis, Gelidium elegans, and Pachymeniopsis elliptica, contributed significantly to the variation in total biomass. This is supported by the high correlation coefficients between the total biomass of all the macroalgae and that of three dominant macroalgae: the correlation coefficients were 0.99, 0.98, 1.00, 0.87, and 0.75 at C-0, E-0, E-10, E-20, and E-30, respectively (Fig. 7).

    Because of the high correlation between the total biomass of the three dominant macroalgae and of the entire macroalgae, we focused on the total biomass variations in E-0 where the FA supplements were installed. The total biomass of macroalgae increased by 2.1 times at C-0 and 15.6 times at E-0 in Nov 2021 compared with Nov 2020. The total biomass of the three dominant macroalgae increased by 2.4 times at C-0 and 21.4 times at E-0 in Nov 2021 compared with Nov 2020.

    The three dominant macroalgae, Eisenia bicyclis, Gelidium elegans, and Pachymeniopsis elliptica, are classifiedby size into canopy- (> 50 cm), sub-canopy- (10–50 cm), and turf- (around 10 cm) forming species, respectively (Jung, 2021). These sizes were relatively larger than those of other macroalgae at the study site. Based on the positive relationship between the size and nutrient uptake rate (Hein et al., 1995), provided Fe would have promoted the efficiency of photosynthesis, and nutrient uptake rates in the three dominant macroalgae (Chen et al., 2017;Rana and Prajapati, 2021). Although the Fe concentration showed no significant differences between all the monitoring points, Chen et al. (2017) already reported that enhanced photosynthesis by Fe increases the macroalgal growth without insignificant variations in Fe levels.

    The total macroalgal biomass at E-10, E-20, and E-30 increased by 4.5, 2.9, and 0.9 times, respectively, in Nov 2021 compared with Nov 2020. These were marginal variations compared with those at C-0 and E-0. Although the monthly biomass ratio of C-0 to E-0 ranged from 0.89 to 8.39 between Oct 2020 and Nov 2021, suggesting a limited effect of FA supplementation at E-0, this interpretation may be misleading due to the influence of species composition, individual abundance, or the emergence of large-bodied macroalgae. Therefore, to more accurately assess the ecological impact of FA supplementation, ecological indices should also be considered, as further discussed in Section 3.5.

    3.4 Ecological indices at monitoring points

    Table 2 presents the ecological indices of all the monitoring points during the observation period. The richness, evenness, diversity, and dominance at all the monitoring points were 3.97– 7.37, 0.19–0.51, 0.68–2.01, and 0.18–0.66, respectively. The maximum richness, evenness, and diversity of macroalgae were 7.37, 0.51, and 2.01 at E-0 in April 2021, whereas the maximum dominance was 0.66 at E-30 in Oct 2021. The minimum richness was 3.97 at C-0 in Oct 2020; minimum evenness and diversity were 0.19 and 0.68, respectively, at E-30 in Oct 2021; and minimum dominance was 0.18 at E-0 in Apr 2021.

    Although the richness at E-0 was 1.5 times higher than that at C-0 in Apr 2021, that at all the monitoring points showed a similar pattern throughout the observation period. The richness at C-0 and E-30 decreased by 18% and 10%, respectively, in Nov 2021 compared with that in Nov 2020. However, that at E-0, E-10, and E-20 increased by 1–11% owing to the increased number of macroalgal species. It is considered that the number of macroalgal species that appeared after FA supplementation suppressed the decrease in richness in Nov 2021.

    The highest values of evenness and diversity were 0.49 and 1.77 at C-0, 0.51 and 2.01 at E-0, 0.43 and 1.60 at E-10, and 0.45 and 0.22 at E-30 in Apr 2021. Meanwhile, those at E-20 were 0.39 and 1.45 in Jun 2021. The evenness and diversity at most of the monitoring points showed similar patterns with high correlation coefficients of 0.99–1.00 during the observation period. Although the evenness and diversity at C-0 increased by 30% and 42%, respectively, in Nov 2021 compared with Nov 2020, this occurred owing to the lowest values of evenness and diversity in Nov 2020.

    The evenness and diversity increased by 30% and 42% at C-0, decreased by 28% and 25% at E-0, and decreased by 30% and 23% at E-10 in Nov 2021 compared with Nov 2021. This corresponds to a variation in dominance. The dominance decreased by 36% at C-0, increased by 26% at E-0, and increased by 29% at E-10. In addition, the correlation coefficient between evenness and dominance and that between diversity and dominance were −0.88 and −0.85 at C-0, −0.86 and −0.84 at E-0, and −0.91 and − 0.93 at E-10, revealing a significant negative relationship during the observation period. Therefore, an increased dominant macroalgal community would have increased the dominance and decreased the evenness and dominance at E-0 and E-10.

    In contrast, the evenness and diversity at E-20 and E-30 showed strong negative correlations with dominance during the observation period. However, the variation rates of evenness, diversity, and dominance at E-20 were 7%, 9%, and −16% in Nov 2021 compared with Nov 2020. This trend at E-20 was similar to that observed at C-0. In addition, the evenness and diversity at E-30 were 0.27 and 0.95, respectively. These were lower than those at C-0. The dominance at E-30 was 0.51, which was the highest among all the monitoring points in Nov 2021. The ecological indices at E-20 and E-30 showed a low consistency because the dilution effect of seawater limited the effective range of FA supplements. This phenomenon indicated that the effect of FA supplement extended up to 10 m (E-10).

    3.5 Estimated diffusion range of FA Supplementation

    In this study, FA supplements were attached to AR, thereby, macroalgal communities located below the AR were considered to be less directly influenced by the eluted FA. In addition, based on the observed number of species, biomass, and ecological indices, the effective influence of the FA supplement was interpreted to extend up to approximately 10 meters (E-10). However, considering the seasonal ocean current patterns in the East Sea— the northward flow of the East Korea Warm Current in summer and the southward flow of the North Korea Cold Current in winter —the direction and extent of horizontal diffusion are expected to vary seasonally.

    Although numerical modeling of dilution effects, diffusion ranges, and optimal spacing of FA supplements was not conducted in this study, such analysis should be performed in future research to support the practical application of FA supplementation.

    4. Conclusions

    The limitations of FA introduction have recently resulted in low Fe(II) concentrations in coastal areas. FA can chelate Fe(III) to bioavailable Fe(II), thereby promoting CSB restoration by improving the macroalgal community. In this study, the improvement in the macroalgal community by FA supplements was evaluated in an Fe-limited coastal area. The marine environment at all the monitoring points was clustered by the pH and concentrations of PO4-P, DIN, and Fe. This revealed that all the monitoring points were clustered according to the seasonality. The Fe eluted from the FA supplements was diluted strongly by seawater and displayed a significantly low contribution in distinguishing the environmental differences at E-0 from the other monitoring points.

    Although the number of species and total biomass in macroalgae showed severe variability owing to the seasonality, the effect of FA supplements on the macroalgal community was practical after one year. The rate of increase in the number of species and total biomass of macroalgae was higher at E-0 and E-10 than at C-0. However, the high rate of increase in the macroalgal community at E-0 was closely related to the quantitative increase in the three dominant macroalgae: Eisenia bicyclis, Gelidium elegans, and Pachymeniopsis elliptica. The total biomass of these dominant macroalgae and that of all the macroalgae were highly correlated. Therefore, the effect of FA supplementation was not uniformly distributed across all species but was predominantly driven by a few dominant species.

    This indicated that the three dominant macroalgae resulted in a quantitative improvement in the macroalgal community at E-0 and E-10. The enhancement of the macroalgal community was associated with the dominant species. This resulted in a decrease in the evenness and diversity and an increase in the dominance at E-0 and E-10. The application of FA supplements to improve CSB increased the dominant species community and decreased the ecological indices.

    Therefore, long-term monitoring considering seasonal influences is required to analyze the changes in the macroalgal community in future research. In addition, although the effect of FA supplements extended up to 10 m, the practical arrangement of FA supplements should be studied through modeling considering the dilution effect and elution range. The results of the this study indicate that FA supplements can quantitatively improve CSB, thereby providing fundamental knowledge that can serve as baseline information for future CSB restoration.

    Acknowledgment

    This work was supported by the Pukyong National University Research Fund in 2021.

    Figure

    KOSOMES-31-2-201_F1.gif

    The panoramic view of the study site (a), cross-shaped AR (b), installed FA supplements on AR (c), and monitoring points (d).

    KOSOMES-31-2-201_F2.gif

    Variations in Fe concentration obtained from FA supplement in the elution experiment.

    KOSOMES-31-2-201_F3.gif

    Variations in water temperature (a) and light intensity (b) in 2020–2021 at the study site.

    KOSOMES-31-2-201_F4.gif

    Variations in pH (a), PO4-P (b), DIN (c), and Fe (d) in the seawater at the study site. The red dot in the Fe concentration variations (d) indicates the average Fe concentration in Oct and Nov 2020, and Apr, Jun, Oct, and Nov 2021.

    KOSOMES-31-2-201_F5.gif

    Principal component analysis of environmental variables at the study site. The green ellipses represent groups from a slice by cluster analysis at a Euclidean distance of 1.85.

    KOSOMES-31-2-201_F6.gif

    Variations in the number of species that appeared (a) and total biomass (b) of the macroalgae at the study site.

    KOSOMES-31-2-201_F7.gif

    Matrix of Pearson’s correlation coefficients between total appeared species, total biomass, and ecological indices of macroalgae at the study site. The values in the lower triangular indicate the correlation coefficients. Those in the ellipse in the upper triangular present the p-values. T-Sp: Total number of macroalgae species, T-Bio: Total biomass of macroalgae, Bio-D: Total biomass of Eisenia bicyclis, Gelidium elegans, and Pachymeniopsis elliptica, Bio-N.D: Total biomass of macroalgae without that of Eisenia bicyclis, Gelidium elegans, and Pachymeniopsis elliptica.

    Table

    Coordinates of monitoring points.

    The ecological indices at all the monitoring points

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