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Article

Evaluating the Trophic Structure of an Artificial Macroalgal Bed of Eisenia bicyclis Using C and N Stable Isotopes

by
Dong-Young Lee
1,†,
Dongyoung Kim
1,†,
Chan-Kil Chun
2,
Youngkweon Lee
3,
Kyu-Sam Han
2,
Hyun Kyum Kim
4,
Tae Hee Park
5 and
Hyun Je Park
1,*
1
Department of Marine Ecology and Environment, Gangneung-Wonju National University, Gangneung 25457, Republic of Korea
2
21 Century Ocean Development Co., Ltd., Gangneung 25459, Republic of Korea
3
West Sea Branch, Korea Fisheries Resources Agency, Kunsan 54021, Republic of Korea
4
East Sea Branch, Korea Fisheries Resources Agency, Pohang 37601, Republic of Korea
5
Marine Environment Research Division, National Institute of Fisheries Science, Busan 46083, Republic of Korea
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
J. Mar. Sci. Eng. 2025, 13(8), 1514; https://doi.org/10.3390/jmse13081514
Submission received: 2 June 2025 / Revised: 24 July 2025 / Accepted: 5 August 2025 / Published: 6 August 2025
(This article belongs to the Section Ocean Engineering)
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Abstract

In this study, we applied a new technique for vegetatively transplanting kelp Eisenia bicyclis to restore macroalgal habitats. We aimed to assess the restoration success of the E. bicyclis bed by comparing the carbon and nitrogen stable isotope ratios of macrobenthic consumers and their isotopic niches in artificial and control (barren ground) habitats. Except for the deposit feeding group, no significant differences were observed in isotopic values of the other feeding groups (suspension feeders, herbivores, omnivores, and carnivores) between the two sites. In contrast, our results showed wider isotopic niche indices for all feeding groups at the transplantation site compared to those at the control site, suggesting increased trophic diversity in the artificial habitat. Overall, these results indicate that the macroalgal bed created using the new method can play an ecological role in restoring functional properties of food web structures via trophic support of degraded coastal ecosystems.

1. Introduction

Globally, macroalgal beds play diverse ecological roles in supporting biodiversity and complex food webs, and providing habitats for marine organisms [1,2,3]. However, various anthropogenic activities seriously affect ecosystem services, including nutrient cycling, primary production, species biodiversity and abundance, and habitats [4]. In coastal areas, macroalgal beds experience large-scale losses due to environmental pollution [5]. Such habitat destruction may threaten ecological functions of marine ecosystems. Therefore, many practical ecological approaches have been attempted to restore diminished and destroyed macroalgal forests and support species richness and biodiversity in coastal ecosystems [6,7]. Several ecological engineering activities based on structuring artificial macroalgal habitats have received considerable attention to mitigate macroalgal deforestation via enhancing biodiversity through restoration and reconciliation efforts [8,9].
Restoration efforts involve creating artificial macroalgal forests, which are constructed via deploying artificial reefs with attached macroalgae [7,10]. Various techniques using seaweed ropes, spore bags, encapsulating macroalgal zygotes, and transplanted cultures with the artificial reefs have been applied to restore macroalgal forests [11,12,13,14,15]. These methods have various purposes: accelerating macroalgal growth, aiding their successful colonization in deforested macroalgal beds, enhancing the abundance and biodiversity of invertebrates and nekton, and providing valuable ecological functions in coastal ecosystems [8,14]. Actually, natural kelp forests play significant ecological roles as supporting organic matter for fishery resources, high biodiversity, and complex food webs [16,17]. Therefore, assessing ecological functions of macroalgal beds created using new techniques after restoration activities is necessary. Evaluating effective strategies to ensure the success and sustainability of restoration efforts should involve comprehensively understanding artificially created macroalgal beds and their trophic function in organic matter flow through food webs [18,19,20].
Carbon and nitrogen stable isotope ratios have been employed extensively for identifying consumer species that are fed on and organic matter movement through food webs [21,22]. Isotope ratios in consumer tissues usually mirror ratios in their food, with slight differences because of different processing of these elements in their bodies. Heavier isotopes (carbon and nitrogen) are slightly more concentrated (by less than 1‰ for carbon and 2–4‰ for nitrogen) in consumer tissues than in their food [23,24,25]. Consequently, this technique facilitates understanding consumer long-term diets and tracking nutrient paths from the food chain base to higher levels [26]. Several studies have shown consumer species returning to their diets after coastal ecosystem rehabilitation via comparing stable isotope ratios between artificial and natural systems [18,19,27].
In South Korea, various artificial macroalgal bed types have been constructed to mitigate the declining kelp biomass under the Korean Fish Stock Enhancement Program [10]. Many attempts have been made to develop artificial reefs attached to kelp species Eisenia bicyclis, Ecklonia cava, Ecklonia stolonifera, and Sargassum via seedling transplantation [7,10,18]. In this study, an engineering technique for vegetatively transplanting Eisenia bicyclis was applied to restore the macroalgal habitat, in which sub-adult species growing on an acrylic plate were directly installed on a natural rock substratum via scuba diving (Figure 1a). Our study assessed the rehabilitation success of the newly settled E. bicyclis bed constructed using the method in comparison to a natural bed, based on the trophic role of the artificial macroalgal habitat on organic matter flow through food webs. However, E. bicyclis had no natural habitat in nearby areas, hindering the comparison of benthic community trophic structures between transplanted and natural sites. In Korean coastal areas, with the exception of two offshore islands (Ulleungdo and Dokdo), Changpo on the mainland is the only native habitat located approximately 170 km south of the transplanting site. Therefore, results of a previous study in the Changpo site were used as a reference for a natural E. bicyclis habitat [20]. Thus, we compared carbon and nitrogen stable isotope ratios of macrobenthic consumers, classified by feeding strategy and organic matter sources, in the constructed kelp site with those in a nearby barren rocky site as a control. Our hypothesis is that carbon and nitrogen stable isotope ratios of macrobenthic consumers in the artificial kelp bed would be different to those in the barren habitat when the kelp species E. bicyclis was successfully rehabilitated with the colonization of the macrobenthic community. Specifically, we anticipate that the restoration might lead a broader isotopic niche, as reflected by an expanded of δ13C and δ15N values, indicating enhanced trophic complexity within the restored habitat.

2. Materials and Methods

2.1. Experimental Sites and Transplantation Design

The E. bicyclis transplantation site was located in the shallow coastal zone of Sacheon, Gangneung-si, Gangwon-do Province, on the Korean eastern coast (Figure 1b). Transplantation was conducted on rocky bottoms in the subtidal area (depth range, 5–7 m), consisting of sand and multiple rock beds, from 2013 to 2016. The barren rocky site was located 200 m from the transplant site, which was sparsely inhabited by macroalgal species.
The plate (or slab) for macroalgae transplantation included a concrete main body (50 cm × 30 cm × 10 cm: length × width × height) with a central vertical perforation, two 5 cm deep attachment holes on the upper surface to secure seedling ropes, and two fixing loops on both sides of the upper part (Figure 2a). Seedling ropes were attached to wooden plates which were combined with attachment holes in the main body to establish a macroalgae habitat. Multiple plates were transported via ship and deployed to the transplantation site via threading rope through the fixing loop. Plates were fixed on the transplantation site rocky bed using 19 mm × 25 cm (diameter × height) anchor bolts inserted into the vertically perforated hole and secured with a nut (Figure 2b).

2.2. Sample Collection and Treatment

Sample collection was conducted in the artificial kelp bed and barren rocky habitat to ensure consistent comparisons. Within each habitat, samples were randomly collected considering spatial heterogeneity. The sampling effort was standardized across both habitats, with an equal number of random sampling points selected in each treatment. Multiple independent samples were collected at random points, with each representing a distinct individual, thus avoiding pseudo-replication. Macroinvertebrate consumers were collected using rectangular can cores at the transplantation and barren rocky sites and sampled via sieving sediments through a 1 mm mesh net on board. Multiple independent samples were collected at random points, with each representing a distinct individual, thus avoiding pseudo-replication. In total, 112 samples were obtained including 50 samples from an artificial kelp bed and 62 samples from the barren habitat. Macroalgae were collected by scuba divers, who scrapped substrata attached on the transplantation plate or rocky shore with a steel knife. After laboratory transportation, all specimens were kept alive overnight in filtered seawater to evacuate their gut contents. Only muscle tissues of most consumers and whole-body specimens of polychaetes and small crustaceans were collected for stable isotope analysis. All pre-treated samples were lyophilized and finely ground into a powder using a ball mill (Retsch MM200 Mixer Mill, Hyland Scientific, Stanwood, WA, USA) and kept in a deep freezer (−50 °C) until isotope analysis.
Seawater was sampled at transplanted and barren rocky sites using a Van Dorn water sampler to obtain suspended particulate organic matter (SPOM). Seawater samples were gently filtered to collect particulates onto pre-combusted (450 °C for 4 h) Whatman GF/F glass fiber filters after removing zooplankton and large particles via screening a 200 μm mesh net. Concentrated SPOM samples were fumed with 1 N HCl steam to remove inorganic carbonates and wrapped in aluminum foil for isotopic analysis. Sediment organic matter samples were collected using a 2.9 cm2 core made from cutoff syringes during low tide and top 0.5 cm samples were sliced with a knife. In the laboratory, the sediment organic matter sample for isotope analyses was obtained via dropping 1 N HCl to remove carbonates until bubbling stopped and then drying in an oven at 60 °C for 72 h.

2.3. Stable Isotope Analysis

Carbon and nitrogen stable isotope ratios were analyzed using continuous-flow isotope ratio mass spectrometry (IsoPrime100; IsoPrime Ltd., Cheadle Hulme, UK) coupled with an elemental analyzer (Vario MICRO Cube elemental analyzer; Elementar Analysensysteme, Hessen, Germany). All powdered samples were packed into tin capsules; filter samples were wrapped with tin foil, and introduced into the elemental analyzer to combust at a high temperature (1030 °C). Resultant carbon dioxide and nitrogen gases were subjected to continuous-flow isotope ratio mass spectrometry using helium as the carrier gas. Data were calculated as relative differences between isotopic ratios of sample and reference gases, utilizing Vienna Pee Dee Belemnite for carbon and atmospheric nitrogen gas for nitrogen. The Delta (δ) notation was used to express relative differences, according to the following equation—δX (‰) = [(Rsample/Rstandard) − 1] × 1000—where X is 13C or 15N, and R values are the 13C/12C or 15N/14N ratios. International standards were used as reference materials (sucrose for δ13C; ANU C12H22O11; NIST, MD, USA) and (ammonium sulfate for δ15N; [NH4]2SO4; NIST) for calibration. The analytical precision for the 20 urea replicates was approximately 0.11‰ and 0.20‰ for δ13C and δ15N, respectively.

2.4. Data Analysis

Data analyses were performed using PRIMER version 6 with PERMANOVA + PRIMER add-on [28] and R version 3.5.3 (R Core Team, 2019). Significant differences in δ13C and δ15N values of organic matter sources (SPOM and E. bicyclis, respectively) between transplantation and barren rocky sites were tested using a permutational multivariate analysis of variance (PERMANOVA). PERMANOVA was used to test the significant differences in δ13C and δ15N values of each feeding guild (suspension feeder, deposit feeder, herbivore, omnivore, and carnivore) between the two sites.
Similarities in resource utilization among consumers were evaluated via comparing the overall variability in isotopic niche areas (‰2) of each feeding guild the two sites using the package Stable Isotope Bayesian Ellipses in R (SIBER) [29]. Isotopic niche area comparisons for each feeding guild between the two sites were conducted using the total area (TA) and small sample size-corrected standard ellipse area (SEAc), a quantitative indicator of trophic diversity among consumer species determined by the spread and extent of isotopic data points [29,30]. These indices were determined based on a conservative estimate of the maximum potential overlap among consumer species, considering uncertainties and biases that occurred because of small or differing sample sizes [29]. Based on SEAc evaluation that expressed the core isotopic niche at each site, the percentile overlap of isotopic niches between consumers at both sites was calculated by the ratio between overlap areas using the ‘MaxLikOverlap’ function [31].

3. Results

3.1. Isotopic Ratios of Organic Matter Sources

Macroalgae showed wide ranges of δ13C and δ15N values at both the transplanted (−21.2 ± 0.3 to −15.4 ± 0.4‰ and 4.0 ± 0.3 to 5.8 ± 0.5‰, respectively) and control (−21.8 ± 0.7 to −15.0 ± 0.5‰ and 4.6 ± 0.9 to 7.2 ± 0.3‰, respectively) sites (Table 1). PERMANOVA revealed that macroalgal isotopic values differed significantly between the two sites (pseudo-F1, 25 = 4.47, p = 0.026). No significant differences were observed in δ13C and δ15N values of POM between the transplanted and control sites (pseudo-F1, 7 = 0.05, p = 0.911), with overall mean values of −21.2 ± 0.4 and 4.5 ± 0.4‰, respectively.

3.2. Isotopic Ratios of Macrobenthic Consumers

A total of 25 and 18 macrobenthic consumers were analyzed at the transplanted and control sites, respectively (Table 2 and Figure 3). Isotopic values for all consumers differed significantly between the two sites (pseudo-F1, 108 = 4.11, p = 0.025). However, at both sites, consumer δ13C and δ15N values were significantly different among the five feeding groups (PERMANOVA, p = 0.001 for both cases). Mean δ13C and δ15N values of feeding groups ranged from −20.5 ± 1.0 (deposit feeder at the control site) to −15.8 ± 3.4‰ (herbivore at the transplanted site) and 6.6 ± 0.8 (suspension feeder at the transplanted site) to 9.7 ± 0.6‰ (omnivore at the control site). Except for the deposit feeder group (pseudo-F1, 15 = 4.52, p = 0.020), no significant differences were observed in isotopic values for the remaining feeding groups (suspension feeder, pseudo-F1, 26 = 2.13, p = 0.140; herbivore, pseudo-F1, 27 = 1.83, p = 0.160; omnivore, pseudo-F1, 19 = 0.53, p = 0.584; and carnivore, pseudo-F1, 17 = 0.64, p = 0.511) between the transplanted and control sites.

3.3. Isotopic Niche Indices of Macrobenthic Consumers

TA and SEAc isotopic niche indices (‰2) for all macrobenthic consumers were relatively high at the transplantation site (46.44 ‰2 and 12.05 ‰2, respectively) compared to those at the control site (21.61 ‰2 and 6.31 ‰2, respectively) (Table 3). Isotopic niches for all feeding groups were relatively wide at the transplantation site compared to those at the control site. The control site carnivore group had the lowest TA and SEAc (1.40 ‰2 and 0.94 ‰2, respectively), whereas the herbivore group at the transplanted site had the highest TA and SEAc (20.61 ‰2 and 10.58 ‰2, respectively). Overlapping proportions of isotopic niche areas between the two sites ranged from 1.0% for deposit feeders to 34.5% for omnivores (Figure 4).

4. Discussion

The trophic assessment for the transplanting experiment, which was devised using a new ecological design, emphasized the differences in isotopic values of macrobenthic consumers and isotopic niches of feeding groups between transplantation and control sites. Restoration success of artificially created systems can generally be estimated via providing suitable habitats for plant and animal communities, thereby supporting high biodiversity and complex food webs. In the study area, transplanted E. bicylis showed remarkable differences in biomass compared to the other macroalgal species. Accordingly, we can characterize the trophic niches of consumer organisms to assess whether the transplanted species served as a distinct source contributing to energy flow within the system. Therefore, our results showed wider isotopic niche indices for all feeding groups at the transplantation site compared to those at the control site, suggesting increased trophic diversity in the artificial habitat compared to the barren ground. Therefore, this study indicates the complex trophic diversity in artificial kelp habitats in ecosystem energy flows, an effective tool for assessing restoration success of newly created systems.
Several studies on restoration success have performed assessments via comparing community characteristics (e.g., abundance, biomass, and diversity) in man-made and natural habitats [32,33,34], enabling the ecological function-related restoration to involve organizing natural trophic structures and pathways in artificial ecosystems [35]. Our study showed that isotopic values of SPOM and two common macroalgae (Grateloupia comea and G. elliptica) at the transplantation and control sites were similar, suggesting no differences in basal resources supporting food webs. δ13C and δ15N ranges of all organic matter sources at both sites were consistent with isotopic values of phytoplankton and macroalgae previously reported in eastern and southern coastal waters of the Korean Peninsula and temperate coastal waters [23,36,37]. The E. bicyclis δ13C and δ15N values were within the ranges reported from native habitats (mean δ13C and δ15N of −16.2‰ and 5.6‰, respectively) in the eastern coastal waters of Korean [20]. Transplanting primary producers can have many effects on organic matter pools as basal resources supporting the food web [18,38]. Overall, considering general isotopic distributions of organic matter sources at the transplanted and barren sites, it suggests the isotopic similarity of basal resources supporting the food web that can be an indicator for restoration assessment after E. bicyclis transplantation [35].
Feeding strategies of most consumers have a definite influence on prey item types that can determine the isotopic signatures in their tissues [39]. Our study also showed that isotopic ranges of macrobenthic consumers were well-divided based on their functional feeding groups, regardless of sampling sites. Specifically, the suspension feeder group had relatively low δ13C and δ15N values overlapping the SPOM isotopic range, suggesting the utilization of typical phytoplankton-derived organic matter [36]. The herbivore group had a relatively wide range of δ13C values, similar to those of macroalgae, suggesting that consumers were likely to use organic matter derived from diverse macroalgal sources [20]. Macroalgae generally have broad δ13C ranges depending on their taxonomic and ecological characteristics [40]. Omnivore and carnivore groups with higher trophic levels had relatively high δ13C and δ15N values, suggesting that animal consumption was linked to macroalgal-derived rather than phytoplankton-derived organic matter [18]. δ13C values for the omnivorous group had a relatively wide range, probably because of the diversity effect of prey items owing to their feeding plasticity [41,42]. Most feeding groups showed isotopic similarities between the transplanted and barren sites; however, only the deposit feeder group differed significantly. Deposit feeders at the transplantation site had relatively high δ13C values compared to those at the barren site, suggesting a high contribution of macroalgal-derived organic matter at the transplantation site. These results are reflected by C isotopic separation between macroalgae and SPOM, where benthic primary producers are generally 13C-enriched compared to planktonic microalgae [43]. Therefore, although suspension feeders primarily feed on phytoplankton-derived organic matter, our results may be attributed to the high availability of macroalgal-derived organic matter in other feeding group diets.
Isotopic niche indices of consumer species provide ecological information on trophic diversity and redundancy of individuals and communities via evaluating dietary niche overlap [44]. Our study showed a relatively wide TA (multiples of 1.5 to 5.4) and SEAc (multiples of 1.6 to 5.8) for all feeding groups at the transplantation site compared to those at the barren site. These results suggest that consumers at the transplantation site feed on a broad range of dietary items through diverse trophic pathways [45,46]. Although kelp forest has influence on the physical condition [47], considering the transplanted individuals reached an average length of approximately 40 cm, they were unlikely to provide sufficient physical structure to alter local hydrodynamics or habitat complexity. Therefore, the observed expansion of isotopic niches is presumably attributed to increased basal resource availability such as kelp-derived detritus and primary production, rather than physical habitat modification. In contrast, the relatively narrow isotopic niches in the barren ground likely indicate a simplified trophic pathway resulting from the low macroalgal biomass [20]. Thus, wider isotopic niches at the transplantation site suggest that increased macroalgal biomass obtained using the acrylic plate method has an ecological role in creating more complicated trophic structures compared to barren ground [19,48]. Despite no statistical isotopic differences in suspension feeders, herbivores, omnivores, and carnivores between the transplantation and barren sites, feeding groups showed low niche overlaps (10.5 for carnivores to 34.5% for omnivores). Deposit feeders rarely overlapped (1%) between sites with isotopic differences. The overlapping proportion of isotopic niches between experimental and control habitats can be effectively used as an indicator of trophic assessment for consumer dietary similarity after establishing a new artificial system [24,38]. Overall, isotopic niches of feeding groups and their overlap estimation between transplanted and barren sites may provide scientific evidence for increased trophic diversity in artificial macroalgal habitats, with the trophic importance of macroalgal-derived organic matter for macrobenthic consumer nutrition [18,41].
Various methods (e.g., transplanting, seeding, grazer control, and artificial reefs) have been developed for restoring kelp forests worldwide [7]. In particular, transplanting kelp involves adhering the holdfast to artificial or natural substrata, dispersing it to the nearby seafloor, and then restoring kelp forests [49,50,51]. In this study, E. bicyclis leaves were transplanted onto the bedrock flat surface, on which the algal leaves gradually spread to nearby natural rock ground. The E. bicyclis habitat zone in the study area consistently increased from 0.060 ha in 2018 to 0.096 ha in 2022 after establishing the transplant [52]. The barren ground or rock substratum had been restored to a normal kelp bed using this method, wherein the extension likely contributed to the nutritional source of macrobenthic consumers. The recovery of ecological structures and functions after transplantation should be considered during restoration success evaluation of the kelp bed. For ecological function, our study may provide a basis for assessing restoration success via monitoring stable isotope signatures over time in consumer feeding groups [53].
In conclusion, our isotopic data demonstrated ecological functions following E. bicyclis transplantation using a new method to support the macrobenthic food web, confirmed by the higher trophic diversity of consumer species in the artificial habitat compared to nearby barren ground. Classified feeding groups at the artificial macroalgal site utilized different dietary resources and showed relatively wide isotopic niches compared to those at the control site, suggesting the contribution of macroalgal-derived organic matter to consumer nutrition. These results indicate that creating a macroalgal bed can play ecological roles in restoring functional properties of the food web structure via trophic recovery of degraded coastal ecosystems [18,20]. Overall, stable isotope data can provide a better understanding of restored ecosystem ecological functioning and managing successful restoration through post-restoration assessment after establishing artificial macroalgal beds.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/jmse13081514/s1, Table S1. Complete δ13C and δ15N values of organic matter sources (Dictyopteris divaricata; Eisenia bicyclis; Grateloupia asiatica; Gelidium comea; Gelidium elegans; Grateloupia elliptica; Undaria pinnatifida; SPOM, suspended particulate organic matter) and benthic consumers at the artificial kelp (E. bicyclis) bed and barren ground (control) site.

Author Contributions

Conceptualization, H.J.P.; methodology, D.-Y.L., D.K., C.-K.C., D.K., H.K.K., and T.H.P.; formal analysis, H.J.P.; investigation, D.-Y.L., D.K., C.-K.C., Y.L., K.-S.H., and H.K.K.; writing—original draft preparation, H.J.P.; writing—review and editing, D.K., D.K., T.H.P., and H.J.P.; visualization, H.J.P. and D.K.; supervision, H.J.P.; funding acquisition, H.J.P. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by the Korea Institute of Marine Science & Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (KIMST-20220553). This research was also supported by the National Institute of Fisheries Science, Korea (R2025015).

Data Availability Statement

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

Conflicts of Interest

Author Chan-Kil Chun and Kyu-Sam Han are employed by the company “21 Century Ocean Development Co., Ltd.”. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Figure 1. Location of sampling sites on the eastern coast of Korean peninsula. Detailed locations of macroalgal (Eisenia bicyclis) transplanting (A) and barren ground ((B), control) sites.
Figure 1. Location of sampling sites on the eastern coast of Korean peninsula. Detailed locations of macroalgal (Eisenia bicyclis) transplanting (A) and barren ground ((B), control) sites.
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Figure 2. Schematic diagrams of the transplantation plate in (a) cross section and (b) fixed state on the rocky bed. Photographs of (c) a single transplantation of Eisenia bicyclis and (d) monitoring of transplanted community in the shallow coastal zone of Sacheon on the Korean eastern coast.
Figure 2. Schematic diagrams of the transplantation plate in (a) cross section and (b) fixed state on the rocky bed. Photographs of (c) a single transplantation of Eisenia bicyclis and (d) monitoring of transplanted community in the shallow coastal zone of Sacheon on the Korean eastern coast.
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Figure 3. Dual isotope plots of δ13C and δ15N values of consumers (green circles, herbivores; red circles, suspension feeders; yellow circles, deposit feeders; blue circles, omnivores; pink circles, carnivores) and organic matter sources (grey squares) at the artificial kelp (Eisenia bicyclis) bed (a) and barren ground (control) site (b). Values of the organic matter sources are illustrated by black squares (Dictyopteris divaricata; Eisenia bicyclis; Grateloupia asiatica; Gelidium comea; Gelidium elegans; Grateloupia elliptica; Undaria pinnatifida; SPOM, suspended particulate organic matter). Values are expressed as means (‰) ± 1 SD.
Figure 3. Dual isotope plots of δ13C and δ15N values of consumers (green circles, herbivores; red circles, suspension feeders; yellow circles, deposit feeders; blue circles, omnivores; pink circles, carnivores) and organic matter sources (grey squares) at the artificial kelp (Eisenia bicyclis) bed (a) and barren ground (control) site (b). Values of the organic matter sources are illustrated by black squares (Dictyopteris divaricata; Eisenia bicyclis; Grateloupia asiatica; Gelidium comea; Gelidium elegans; Grateloupia elliptica; Undaria pinnatifida; SPOM, suspended particulate organic matter). Values are expressed as means (‰) ± 1 SD.
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Figure 4. Isotopic niche areas of each feeding group ((a), herbivores; (b), suspension feeders; (c), deposit feeders; (d), omnivores; (e), carnivores) estimated as the total area (TA, dotted lines) and standard ellipse area (SEAc, colored ellipse) at the artificial kelp (Eisenia bicyclis) bed (red) and barren ground site (black) using the Stable Isotope Bayesian Ellipse in R (SIBER) procedure.
Figure 4. Isotopic niche areas of each feeding group ((a), herbivores; (b), suspension feeders; (c), deposit feeders; (d), omnivores; (e), carnivores) estimated as the total area (TA, dotted lines) and standard ellipse area (SEAc, colored ellipse) at the artificial kelp (Eisenia bicyclis) bed (red) and barren ground site (black) using the Stable Isotope Bayesian Ellipse in R (SIBER) procedure.
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Table 1. δ13C and δ15N values of organic matter sources (Dictyopteris divaricata; Eisenia bicyclis; Grateloupia asiatica; Gelidium comea; Gelidium elegans; Grateloupia elliptica; Undaria pinnatifida; SPOM, suspended particulate organic matter) at the artificial kelp (E. bicyclis) bed and barren ground (control) site. PERMANOVA test of δ13C and δ15N values for macroalgae and SPOM between the two sites (significance at p < 0.05, bold). Data represent means ± 1 SD. ‘n’ indicates the number of analyzed samples.
Table 1. δ13C and δ15N values of organic matter sources (Dictyopteris divaricata; Eisenia bicyclis; Grateloupia asiatica; Gelidium comea; Gelidium elegans; Grateloupia elliptica; Undaria pinnatifida; SPOM, suspended particulate organic matter) at the artificial kelp (E. bicyclis) bed and barren ground (control) site. PERMANOVA test of δ13C and δ15N values for macroalgae and SPOM between the two sites (significance at p < 0.05, bold). Data represent means ± 1 SD. ‘n’ indicates the number of analyzed samples.
Artificial Kelp BedBarren Ground SitePERMANOVA
Organic Matter Source δ13C δ15N δ13C δ15N
nMeanSDMeanSDnMeanSDMeanSDPseudo-Fp-Value
Dictyopteris divaricata3−16.30.34.60.3 4.470.026
Eisenia bicyclis5−15.70.44.00.3
Grateloupia asiatica 3−20.20.57.20.3
Gelidium comea3−15.40.45.70.23−15.00.55.90.4
Gelidium elegans
Grateloupia elliptica3−21.20.35.80.53−21.80.74.60.9
Undaria pinnatifida 3−17.70.35.80.3
SPOM4−21.10.54.50.34−20.20.57.20.30.050.911
Table 2. δ13C and δ15N values of macrobenthic consumers (herbivore, suspension feeder, deposit feeder, omnivore, and carnivore) collected at the artificial kelp (Eisenia bicyclis) bed and barren ground (control) site. The taxon abbreviations are as follows: Gas, Gastropoda; Biv, Bivalvia; Cho, Chordata; Cni, Cnidaria; Cru, Crustacea; Ech, Echinodermata; Pol, Polychaeta; Ppl, Polyplacophora. Data represent means ± 1 SD.
Table 2. δ13C and δ15N values of macrobenthic consumers (herbivore, suspension feeder, deposit feeder, omnivore, and carnivore) collected at the artificial kelp (Eisenia bicyclis) bed and barren ground (control) site. The taxon abbreviations are as follows: Gas, Gastropoda; Biv, Bivalvia; Cho, Chordata; Cni, Cnidaria; Cru, Crustacea; Ech, Echinodermata; Pol, Polychaeta; Ppl, Polyplacophora. Data represent means ± 1 SD.
No.Species NameTaxonArtificial Kelp BedBarren Ground Site
nδ13C δ15N nδ13C δ15N
Herbivore
1Acmaea pallidaGas3−15.70.68.40.43−17.40.28.10.3
2Aplysia japonicaGas2−20.50.75.80.62−19.90.26.60.2
3Cantharidus jessoensisGas 2−14.30.28.80.1
4Chlorostoma turbinataGas3−17.20.37.80.43−17.40.38.30.2
5Haliotis discus hannaiGas 2−19.80.45.90.5
6Kelletia lischkeiGas3−17.30.28.30.3
7Lottia tenuisculptataGas 3−11.10.98.20.3
8Strongylocentrotus nudusEch 2−11.60.66.70.2
Suspension feeder
9Arca boucardiBiv3−19.30.27.40.32−18.50.46.60.2
10Crassostrea nipponicaBiv 2−18.20.28.10.5
11Crepidula onyxGas3−19.70.26.30.33−19.20.66.30.2
12Halocynthia roretziCho3−21.00.36.90.43−20.70.36.70.2
13Modiolus agripetus lredaleBiv2−20.10.36.40.2
14Mytilisepta keenaeBiv 3−19.70.35.60.3
15Mytilus unguiculatusBiv 3−18.70.26.80.2
Deposit feeder
16Acanthochitona achatesPpl2−20.00.28.20.52−19.70.37.90.4
17Ampithoe lacertosaCru 3−15.10.35.80.6
18Apostichopus japonicusEch3−21.70.36.30.1
19Pachycheles stevensiiCru 3−18.00.59.20.5
20Pugettia quadridensCru3−19.60.48.70.4
Omnivore
21Asterina pectiniferaEch 2−13.70.28.50.5
22Eunice sp.Pol2−20.00.99.50.42−19.50.39.80.1
23Halosydna brevisetosaPol2−18.00.49.10.32−17.50.39.30.2
24Henricia leviusculaEch 2−14.90.27.80.4
25Paguristes ortmanniCru2−16.10.39.80.72−16.60.210.91.0
26Pagurus samuelisCru 2−17.30.59.90.5
27Pagurus proximusCru2−15.60.210.20.5
Carnivore
28Doris odhneriGas3−17.10.27.40.5
29Mitrella bicinctaGas3−17.10.39.60.33−17.50.410.00.3
30Reishia bronniGas3−17.10.210.00.23−17.60.39.50.4
31Triopha modestaGas 3−14.10.47.80.4
Table 3. δ13C and δ15N values of functional feeding groups (herbivore, suspension feeder, deposit feeder, omnivore, and carnivore) at the artificial kelp (Eisenia bicyclis) bed and barren ground (control) site. PERMANOVA test of δ13C and δ15N values for each feeding guild between the two sites (significance at p < 0.05, bold). Data represent means ± 1 SD. Isotopic niche areas of each feeding group estimated as the total area (TA) and standard ellipse area (SEAc) and isotopic niche overlaps (percentage, %) between the two sites using the Stable Isotope Bayesian Ellipse in R (SIBER) procedure.
Table 3. δ13C and δ15N values of functional feeding groups (herbivore, suspension feeder, deposit feeder, omnivore, and carnivore) at the artificial kelp (Eisenia bicyclis) bed and barren ground (control) site. PERMANOVA test of δ13C and δ15N values for each feeding guild between the two sites (significance at p < 0.05, bold). Data represent means ± 1 SD. Isotopic niche areas of each feeding group estimated as the total area (TA) and standard ellipse area (SEAc) and isotopic niche overlaps (percentage, %) between the two sites using the Stable Isotope Bayesian Ellipse in R (SIBER) procedure.
Artificial Kelp BedBarren Ground SitePERMANOVA
Feeding Groups δ13C δ15N δ13C δ15N
nMeanSDMeanSDnMeanSDMeanSDPseudo-Fp-Value
Herbivore17−15.83.47.61.011−17.41.77.71.11.830.160
Suspension feeder16−19.30.96.60.811−20.00.76.80.52.130.140
Deposit feeder8−17.32.07.61.68−20.51.07.71.24.520.020
Omnivore12−16.62.09.41.18−17.41.99.70.60.530.584
Carnivore9−16.41.79.11.09−17.10.29.01.30.640.511
Isotopic niche areasArtificial kelp bedBarren ground sitePercentage overlap (%)
TA SEAc TA SEAc
Herbivore 20.61 10.58 3.83 2.55 19.8
Suspension feeder 4.19 2.11 2.27 1.30 20.5
Deposit feeder 8.91 8.17 1.88 1.41 1.0
Omnivore 11.88 6.25 4.43 3.36 34.5
Carnivore 3.81 2.75 1.40 0.94 10.5
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Lee, D.-Y.; Kim, D.; Chun, C.-K.; Lee, Y.; Han, K.-S.; Kim, H.K.; Park, T.H.; Park, H.J. Evaluating the Trophic Structure of an Artificial Macroalgal Bed of Eisenia bicyclis Using C and N Stable Isotopes. J. Mar. Sci. Eng. 2025, 13, 1514. https://doi.org/10.3390/jmse13081514

AMA Style

Lee D-Y, Kim D, Chun C-K, Lee Y, Han K-S, Kim HK, Park TH, Park HJ. Evaluating the Trophic Structure of an Artificial Macroalgal Bed of Eisenia bicyclis Using C and N Stable Isotopes. Journal of Marine Science and Engineering. 2025; 13(8):1514. https://doi.org/10.3390/jmse13081514

Chicago/Turabian Style

Lee, Dong-Young, Dongyoung Kim, Chan-Kil Chun, Youngkweon Lee, Kyu-Sam Han, Hyun Kyum Kim, Tae Hee Park, and Hyun Je Park. 2025. "Evaluating the Trophic Structure of an Artificial Macroalgal Bed of Eisenia bicyclis Using C and N Stable Isotopes" Journal of Marine Science and Engineering 13, no. 8: 1514. https://doi.org/10.3390/jmse13081514

APA Style

Lee, D.-Y., Kim, D., Chun, C.-K., Lee, Y., Han, K.-S., Kim, H. K., Park, T. H., & Park, H. J. (2025). Evaluating the Trophic Structure of an Artificial Macroalgal Bed of Eisenia bicyclis Using C and N Stable Isotopes. Journal of Marine Science and Engineering, 13(8), 1514. https://doi.org/10.3390/jmse13081514

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