Secular change in seaweed species composition and coverage of Sargassaceae on the artificial reef in Wakasa Bay, Japan

doi:10.21203/rs.3.rs-4708540/v1

Download PDF

Research Article

Secular change in seaweed species composition and coverage of Sargassaceae on the artificial reef in Wakasa Bay, Japan

https://doi.org/10.21203/rs.3.rs-4708540/v1

This work is licensed under a CC BY 4.0 License

You are reading this latest preprint version

The threat of declining seaweed beds has been a concern around the world. Seagrass and seaweed (brown algae) beds are essential habitats supporting fisheries. However, approximately 22% of these habitats have been lost in Japan due to increased coastal landfill sites and ports. This study aims to rehabilitate the depletion of these habitats by constructing an artificial reef in Wakasa Bay, Japan, and monitoring Sargassaceae succession in the second and fourth years after the construction was completed. In this study, we set up four sites on the artificial reef. Then we identified the seaweed species composition and coverage of the Sargassaceae using underwater visual observation by scuba divers. The seaweed coverage was already over approximately 80% in the second year after construction. However, the dominant species changed to Sargassum horneri in the second year after construction and Myagropsis myagroides in the fourth year after construction. Thus, the recovery of species composition takes longer than that of coverage. Therefore, when the artificial reef is constructed, it is important to observe the recovery of species composition.

Artificial reef

Monitoring

Myagropsis myagroides

Sargassum horneri

Wakasa Bay - Japan

Seaweed beds of brown algal communities of Sargassaceae are formed in the coastal Japan Sea. The brown algal communities of Sargassaceae play an important role in useful marine functions, i.e., habitats, feeding grounds, and spawning grounds (Steneck et al., 2002; Harley et al., 2012). The construction, maintenance, and management of seaweed beds are thus important issues in fisheries (Yoshikawa, 1987).

Unfortunately, 6,400 ha of seagrass and seaweed beds have been lost along Japan's coast, of which Sargassaceae beds accounted for 22% from 1978 to 1991 due to the increase in coastal landfill sites at ports (Terawaki et al., 2003). The 4th Basic Survey of Nature Conservation conducted by Japan's Ministry of the Environment from 1989 to 1991 identified 201,212 ha of seaweed beds. Seaweed bed surveys were also conducted by Japan's Fisheries Agency from 2006 to 2008, and information was obtained on 41.6% of the seaweed beds described in the 4th Basic Survey of Nature Conservation. These surveys demonstrated that the area of seaweed beds on Japan's coasts decreased from 83,798 ha to 65,260 ha over 17 years (Baba, 2021). More recently, according to the results of seaweed bed surveys conducted in 2018–2020, the total area of seaweed beds nationwide, excluding some closed sea areas, was 164,340 ha (Ministry of the Environment, 2021). As mentioned above, the threat of declining seaweed beds has been a concern not only in Japan but also around the world (e.g., Frederick & Wyllie-Echeverria, 1996; Krumhansl et al., 2016; Wernberg et al., 2019; Smale, 2020).

To rehabilitate or mitigate against these losses, attempts have mainly been made to construct seaweed beds worldwide, such as in Japan since the 1980s (e.g., Tomiyama, 1981; Yamauchi, 1984; Ohno et al., 1990; Watanuki & Yamamoto, 1990; Ohno, 1993; Choi et al., 2000; Choi et al., 2002; Terawaki et al., 2003; Choi et al., 2006); in USA (e.g., Reed & Foster, 1984; Arkema et al., 2009; Benes & Carpenter, 2015; Schroeter et al., 2015); and in Korea (e.g., Jung et al., 2020). It is important to know which types of seaweed will colonize at an installed artificial substrate, undergo growth transition, and eventually dominate to create effective seaweed beds. Regarding such vegetation succession, pioneer species cannot grow in the presence of successor species (conversely, pioneer species can grow without successor species). The influences of pioneer species on successor species can be divided into three pattern models: (i). The facilitation model indicates the presence of earlier species facilitates the colonization and growth of later species; (ii). The inhibition model indicates later species can colonize and grow only when earlier species disappear; (iii). In the tolerance model, later species can colonize and grow in the presence of earlier species (Connell & Slatyer, 1977; Connell et al., 1987).

Then, we have been interested in a research question: how long will it take for the seaweed species composition and coverage on the artificial reef to reach the climax? To address the above research questions, the objective of this study is to monitor and compare the brown seaweed, especially the Sargassaceae distribution and coverage multi-temporally at four points, as well as to investigate their succession over the observation times (second and fourth years) on the artificial reef constructed in Wakasa Bay, Japan.

Survey sites

The structure on the artificial reef consists of paving stones on the seabed and X-blocks on the top (Fig. 2). The type of paving stone is granite from Tsuruga City, Fukui Prefecture. The paving stone weight is approximately 50–200 kg, while the X-block weight is approximately 2,000 kg. The paving stones were placed at 5.3-m intervals.

Survey period and method

The first and second monitoring studies were conducted in May and October 2019 in the second year after artificial reef construction. The third and fourth monitoring studies were performed in June and October 2021 in the fourth year after artificial reef construction. As part of each monitoring study, we investigated the seaweed species composition and coverage to determine whether those on the artificial reef approached the climax. The seaweed species composition and coverage were observed visually and recorded by scuba divers. The scuba divers who use underwater lights are expert persons and can identify seaweed at the species level by direct visualization. If the species name was unknown, the scuba divers brought back the seaweed to the laboratory and identified based on the reference books of Tanaka & Nakamura (2004) and Yoshida et al. (2015).

The species identification and coverage counting of seaweeds on the artificial reef were recorded by the divers using two-3.2 m scale bares, which cover observation areas of 3.2 m × 3.2 m (10.24 m²). The seaweed coverage was then estimated using the percentage coverage; the seaweed coverage is 100% when seaweeds cover the entire square (Braun-Blanquet, 1964). When seaweeds are scarce, they are indicated as +, and the coverage is assumed to be 1% (see Table S1 in the online Supplementary Material).

Analysis method

As for the seaweed species composition of the Sargassaceae that dominated in this study, we performed a nonmetric multidimensional scaling (NMDS) using a Chao index, a cluster analysis using Ward's method, and an indicator value (IndVal) method for the seaweed species composition and coverage.

As to the seaweed coverage, we performed a Kruskal-Wallis test for the difference in average coverage of all seaweed species, Sargassum horneri, S. confusum, Myagropsis myagroides, and S. patens between the first (May 2019), second (October 2019), third (June 2021), and fourth (October 2021) monitoring studies.

These analyses were conducted at 16 monitoring study sites in total, four in the first, four in the second, four in the third, and four in the fourth. We used the statistical software R (ver. 4.20) to perform these analyses.

Seaweed species composition

Thirty-eight species were successfully identified in the four monitoring studies conducted in May 2019 (the first monitoring study), October 2019 (the second monitoring study), June 2021 (the third monitoring study), and October 2021 (the fourth monitoring study) (Table S1 in the online Supplementary Material). Regarding species diversity, nine species of large brown seaweed of Sargassaceae were confirmed as M. myagroides, S. confusum, S. hemiphyllum, S. horneri, S. macrocarpum, S. patens, S. piluliferum, S. ringgoldianum ssp. coreanum, and S. siliquastrum (Table S1).

Based on Table S1, ranges of the Sargassaceae observed at the four artificial reef sites (Stns. 1–4) were 5 to 7 species, 4 to 9 species, 5 to 6 species, and 5 to 7 species with an average of 6, 7, 6, and 6 species for the first, second, third, and fourth monitoring studies, respectively. Regarding seaweed coverage of the Sargassaceae, S. horneri was confirmed in the first monitoring study, however S. horneri decreased and S. confusum increased in the second monitoring study. After that, S. confusum decreased and M. myagroides or S. patens increased in the third and fourth monitoring studies (Fig. 3).

Seaweed coverage

The seaweed coverage of all seaweed species at the four artificial reef sites (Stns. 1–4) was 55–95%, 60–95%, 90–95%, and 70–95% with an average of 79%, 83%, 94%, and 88% for the first, second, third, and fourth monitoring studies, respectively (Fig. 4). Statistical analysis (Kruskal-Wallis test) showed that there were no significant differences in average coverage of all seaweed species (p = 0.3362).

Brown seaweeds in the second and fourth years after artificial reef construction

The seaweed coverage of Sargassaceae species on the artificial reef was already over approximately 80% in the second year after construction. However, the seaweed species composition of Sargassaceae differs between the second and fourth years after construction. That is, S. horneri and S. confusum were dominant in the second year after construction. After that, M. myagroides dominated in the fourth year after construction. It is thus the recovery of species composition takes longer than that of coverage.

In the Tango Peninsula, Kyoto Prefecture showed that the large annual seaweed S. horneri flourished well on the substrate in the first year. In the second year, the substrate was dominated by the perennial large size of S. patens and S. piluliferum (Yatsuya et al., 2008), while in the third year, it was dominated permanently by S. fulvellum, which also had a large size (Douke et al., 2004). Endo et al. (2019) clarified that S. horneri and S. patens/S. piluliferum harm each other's growth in the first year of colonization, whereas the presence of S. horneri in the first year seems to have a minimal effect on the dominance of S. patens/S. piluliferum in the second year. Together, these findings indicate that on an artificial reef, annual seaweeds settle in the first year, and then are followed by perennial seaweeds. As for S. horneri was dominant in the second year after construction in this study, this result supported previous knowledge.

Sargassum confusum is often the first species of brown algae of Sargassaceae to be colonized when an artificial reef is constructed, and S. confusum may have characteristics that other Sargassaceae seaweeds do not have, i.e., (i) it attaches easily to new substrates, and (ii) it is difficult for phytophagous animals to eat the juvenile form of this seaweed (Kyoto Prefectural Agriculture, Forestry and Fisheries Technology Center, Fisheries Technology Department). A common feature of S. confusum is that it can adapt to unstable environments where other Sargassaceae seaweeds cannot grow. As time passes, species other than S. confusum will dominate (Douke et al., 2004).

In the present study, it changed from S. horneri to S. confusum in the second year after construction and from S. confusum to M. myagroides in the fourth year after construction. Regarding the reason for the decrease in S. confusum and the increase in M. myagroides on the artificial reef, it is considered that the fact that M. myagroides covers the upper part of S. confusum is advantageous in terms of competition for light (Yatsuya et al., 2005). Therefore, these changes are considered to be a process of vegetation succession.

Vegetation succession: Further research challenges

Myagropsis myagroides was dominated on the artificial reef in the fourth year after construction. On the other hand, because S. patens also has increased, which is the climax species in this survey area? The maturity season of M. myagroides is February-March in Kyoto near Wakasa Bay, and that of S. patens is May-July (Kyoto Prefectural Agriculture, Forestry and Fisheries Technology Center, Fisheries Technology Department, 2009). On the other hand, the optimal temperature and maximum critical temperature for the growth of M. myagroides are 10–25°C and 30°C, and those of S. patens are 20–25°C and 31°C (Haraguchi et al., 2005). From the above, it is considered that M. myagroides prefers lower temperature to S. patens.

Water temperature has been increasing according to global warming (Kuwahara et al., 2006; Tanaka et al., 2012; Khana et al., 2018). Therefore, it is considered that the dominant species in this area change from M. myagroides to S. patens in the future.

An artificial reef was constructed in Wakasa Bay, Japan, and we monitored the reef in the second and fourth years after the construction was completed. We set up four sites on the artificial reef and then identified the seaweed species composition and coverage of the Sargassaceae. The seaweed coverage on the artificial reef was already over approximately 80% in the second year after construction. However, the dominant species changed to S. horneri in the second year after construction and M. myagroides in the fourth year after construction. Thus, the recovery of species composition takes longer than that of coverage. Therefore, when the artificial reef is constructed, it is important to observe the recovery of species composition.

Ethical Responsibilities of Authors: The authors made substantial contributions to the conception and design of the work; the acquisition, analysis, and interpretation of data; drafted the work and revised it critically for important intellectual content; and agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Ethics approval and consent to participate: Not applicable.

Funding: The authors did not receive support from any organization for the submitted work.

Competing interests: The authors have no relevant financial or nonfinancial interests to disclose.

Availability of data and material: All data and materials generated or analyzed during this study are included in this published article.

Author's contributions: The authors made substantial contributions to the conception and design of the work; the acquisition, analysis, and interpretation of data; drafted the work and revised it critically for important intellectual content; and agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Arkema, K.K., Reed, D.C., & Schroeter, S.C. (2009) Direct and indirect effects of giant kelp determine benthic community structure and dynamics. Ecology, 90(11), 3126–3137. https://doi.org/10.1890/08-1213.1
Baba, M. (2021) Growth responses and distributional changes of large brown seaweeds due to global warming (in Japanese with English abstract). Report of Marine Ecology Research Institute, 26, 1–28.
Benes, K.M., & Carpenter, R.C. (2015) Kelp canopy facilitates understory algal assemblage via competitive release during early stages of secondary succession. Ecology, 96(1), 241–251. https://doi.org/10.1890/14-0076.1
Braun-Blanquet, J. (1964) Pflanzensoziologie: Grundzüge der Vegetationskunde. Springer. https://doi.org/10.1007/978-3-7091-8110-2
Choi, C.G., Ohno, M., & Sohn, C.H. (2006) Algal succession on different substrata covering the artificial iron reef at Ikata in Shikoku, Japan. Algae, 21(3), 305–310.
Choi, C.G., Serisawa, Y., Ohno, M., & Sohn, C.H. (2000) Construction of artificial seaweed beds; Using the spore bag method. Algae, 15(3), 179–182.
Choi, C.G., Takeuchi, Y., Terawaki, T., Serisawa, Y., Ohno, M., & Sohn, C.H. (2002) Ecology of seaweed beds on two types of artificial reef. Journal of Applied Phycology, 14(5), 343–349. https://doi.org/10.1023/A:1022126007684
Connell, J.H., Noble, I.R., & Slatyer, R.O. (1987) On the mechanisms producing successional change. OIKOS, 50(1), 136–137.
Connell, J.H., & Slatyer, R.O. (1977) Mechanisms of succession in natural communities and their role in community stability and organization. The American Naturalist, 111(982), 1119–1144.
Douke, A., Nishigaki, T., Yatsuya, K., & Wada, Y. (2004) Succession of a Sargassaceae seaweed community planted on an artificial stone bed on the coast of Amino, central Japan (in Japanese with English abstract). Bulletin of the Kyoto Institute of Oceanic and Fisheries Science 26, 9–14.
Endo, H., Nishigaki, T., Yamamoto, K., & Takeno, K. (2019) Subtidal macroalgal succession and competition between the annual, Sargassum horneri, and the perennials, Sargassum patens and Sargassum piluliferum, on an artificial reef in Wakasa Bay, Japan. Fisheries Science, 85(1), 61–69. https://doi.org/10.1007/s12562-018-1263-9
Frederick, T.S., & Wyllie-Echeverria, S. (1996) Natural and human-induced disturbance of seagrasses. Environmental Conservation, 23(1), 17–27. https://doi.org/10.1017/S0376892900038212
Fukui Prefecture. Public water area water quality constant monitoring survey results (in Japanese). http://www.erc.pref.fukui.jp/sogo/h122/
Haraguchi, H., Murase, N., Mizukami, Y., Noda, M., Yoshida, G., & Terawaki, T. (2005) The optimal and maximum critical temperatures of nine species of the Sargassaceae in the coastal waters of Yamaguchi Prefecture (in Japanese with English abstract). The Japanese Journal of Phycology, 53(1), 7–13.
Harley, C.D.G., Anderson, K.M., Demes, K.W., Jorve, J.P., Kordas, R.L., Coyle, T.A., & Graham, M.H. (2012) Effects of climate change on global seaweed communities. Journal of Phycology, 48(5), 1064–1078. https://doi.org/10.1111/j.1529-8817.2012.01224.x
Jung, S.M., Lee, J.H., Han, S.H., Jeon, W.B., Kim, G.Y., Kim, S., Kim, S., Lee, H.R., Hwang, D.S., Jung, S., Lee, J., & Shin, H.W. (2020) A new approach to the restoration of seaweed beds using Sargassum fulvellum. Journal of Applied Phycology, 32(4), 2575–2581. https://doi.org/10.1007/s10811-020-02054-y
Khana, A.H., Levacb, E., Guelphenc, L.V., Pohlec, G., & Chmuraa, G.L. (2018) The effect of global climate change on the future distribution of economically important macroalgae (seaweeds) in the northwest Atlantic. FACET, 3, 275–286. https://doi:10.1139/facets-2017-0091
Krumhansl, K.A., Okamoto, D.K., Rassweiler, A., Novak, M., Bolton, J.J., Cavanaugh, K.C., Connell, S.D., Johnson, C.R., Konar, B., Ling, S.D., Micheli, F., Norderhaug, K.M., Pérez-Matus, A., Sousa-Pinto, I., Reed, D.C., Salomon, A.K., Shears, N.T., Wernberg, T., Anderson, R.J., Barrett, N.S., Buschmann, A.H., Carr, M.H., Caselle, J.E., Derrien-Courtel, S., Edgar, G.J., Edwards, M., Estes, J.A., Goodwin, C., Kenner, M.C., Kushner, D.J., Moy, F.E., Nunn, J., Steneck, R.S., Vásquez, J., Watson, J., Witman, J.D., Byrnes, J.E.K. (2016) Global patterns of kelp forest change over the past half-century. Proceeding of the National Academy of Sciences of the United States of America, 113(48), 13785–13790. https://www.pnas.org/doi/abs/10.1073/pnas.1606102113
Kuwahara, H., Akeda, S., Kobayashi, S., Takeshita, A., Yamashita, Y., & Kido, K. (2006) Predicted changes on the distribution areas of marine organisms around Japan caused by the global warming. Global Environmental Research, 10(2), 189–199.
Kyoto Prefectural Agriculture, Forestry and Fisheries Technology Center, Fisheries Technology Department (2009) Propagation of Sargassum (in Japanese). Quarterly report, 96, 1–13.
Kyoto Prefectural Agriculture, Forestry and Fisheries Technology Center, Fisheries Technology Department. S. confusum (in Japanese). https://www.pref.kyoto.jp/kaiyo2/fushisuji.html
Ministry of the Environment (2021) About the results of seaweed bed survey (2018–2020) (in Japanese). https://www.biodic.go.jp/moba/1_4.html#1_4_1
Nakae, S., Komatsubara, T., & Naito, K. (2002) Geology of the Nishizu District, Quadrangle Series, 1:50,000 (in Japanese with English abstract). Geological Survey of Japan, National Institute of Advanced Industrial Science and Technology (AIST).
Ohno, M. (1993) Succession of seaweed communities on artificial reefs in Ashizuri, Tosa Bay, Japan. Algae, 8(2), 191–198.
Ohno, M., Arai, S., & Watanabe, M. (1990) Seaweed succession on artificial reefs on different bottom substrata. Journal of Applied Phycology, 2(4), 327–332. https://doi.org/10.1007/BF02180922
Reed, D.C., & Foster, M.S. (1984) The effects of canopy shadings on algal recruitment and growth in a giant kelp forest. Ecology, 65(3), 937–948. https://doi.org/10.2307/1938066
Schroeter, S.C., Reed, D.C., & Raimondi, P.T. (2015) Effects of reef physical structure on development of benthic reef community: a large-scale artificial reef experiment. Marine Ecology Progress Series, 540, 43–55. https://doi.org/10.3354/meps11483
Smale, D.A. (2020) Impacts of ocean warming on kelp forest ecosystems. New Phytologist, 225(4), 1447–1454. https://doi.org/10.1111/nph.16107
Steneck, R.S., Graham, M.H., Bourque, B.J., Corbett, D., Erlandson, J.M., Estes, J.A., & Tegner, M.J. (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental Conservation, 29(4), 436–459. https://doi.org/10.1017/S0376892902000322
Tanaka, J., & Nakamura, T. (2004) A photographic Guide; Japanese Seaweeds (in Japanese). Heibonsha Limited, Publishers.
Tanaka, K., Taino, S., Haraguchi, H., Prendergast, G., & Hiraoka, M. (2012) Warming off southwestern Japan linked to distributional shifts of subtidal canopy-forming seaweeds. Ecology and Evolution, 2(11), 2854–2865. https://doi.org/10.1002/ece3.391
Terawaki, T., Yoshikawa, K., Yoshida, G., Uchimura, M., & Iseki, K. (2003) Ecology and restoration techniques for Sargassum beds in the Seto Inland Sea, Japan. Marine Pollution Bulletin, 47(1–6), 198–201. https://doi.org/10.1016/S0025-326X(03)00054-7
Tomiyama, A. (1981) Aquatic afforestation with Sargassum (in Japanese). In: The Japanese Society of Fisheries Science (ed), Seaweed beds (pp. 142–157). KOUSEISHA KOUSEIKAKU Co., Ltd.
Watanuki, A., & Yamamoto, A. (1990) Settlement of seaweeds on coastal structures. Hydrobiologia, 204(1), 275–280. https://doi.org/10.1007/BF00040245
Wernberg, T., Krumhansl, K., Filbee-Dexter, K., & Pedersen, M.F. (2019) Status and trends for the world’s kelp forests. In: Sheppard C (ed), World Seas: An Environmental Evaluation: Ecological Issues and Environmental Impacts (2nd ed., pp. 57–78). Academic Press.
Yamauchi, K. (1984) The formation of Sargassum beds on artificial substrata by transplanting seedlings of S. horneri (TURNER) C. AGARDH and S. muticum (YENDO) FENSHOLT. Bulletin of the Japanese Society of Scientific Fisheries, 50(7), 1115–1123. https://doi.org/10.2331/suisan.50.1115
Yatsuya, K., Nishigaki, T., Douke, A., Itani, M., & Wada, Y. (2005) Succession of a Sargassaceae community on an artificially installed stone bed off Amino, Japan Sea Ⅱ Productive structure of Sargassaceae community and age composition of Sargassum confusum. (in Japanese with English abstract). Bulletin of the Kyoto Institute of Oceanic and Fisheries Science, 27, 19–24.
Yatsuya, K., Nishigaki, T., Shirafuji, N., & Takeno, K. (2008) Effect of drifting seaweeds captured by a floating rope on the supply of embryos to new substrata of an artificial reef area off Yoro-Oshima, and algal succession in this area (in Japanese with English abstract). Bulletin of the Kyoto Institute of Oceanic and Fisheries Science, 30, 31–37.
Yoshida, T., Suzuki, M., & Yoshinaga, K. (2015) Checklist of marine algae of Japan (Revised in 2015) (in Japanese). The Japanese Journal of Phycology, 63(3), 129–189.
Yoshikawa, K. (1987) Studies on the formation of Sargassum beds-Ⅲ The formation of Sargassum beds by setting campus sheets for embryo to settle down effectively (in Japanese with English abstract). Bulletin of the Nansei Regional Fisheries Research Laboratory, 21, 25–35.

Tables are available in the Supplementary Files section.

No competing interests reported.

Download PDF

Editorial decision: Revision requested
29 Aug, 2024
Reviews received at journal
24 Aug, 2024
Reviews received at journal
11 Aug, 2024
Reviewers agreed at journal
06 Aug, 2024
Reviewers agreed at journal
05 Aug, 2024
Reviewers agreed at journal
03 Aug, 2024
Reviewers invited by journal
01 Aug, 2024
Editor assigned by journal
26 Jul, 2024
Submission checks completed at journal
26 Jul, 2024
First submitted to journal
08 Jul, 2024

You are reading this latest preprint version

Secular change in seaweed species composition and coverage of Sargassaceae on the artificial reef in Wakasa Bay, Japan

Status:

Version 1

Abstract

Figures

Introduction

Materials and Methods

Survey sites

Survey period and method

Analysis method

Results

Seaweed species composition

Seaweed coverage

Discussion

Brown seaweeds in the second and fourth years after artificial reef construction

Vegetation succession: Further research challenges

Conclusions

Declarations

References

Tables

Additional Declarations

Supplementary Files

Status:

Version 1