Phenology of Codium cylindricum (Ulvophyceae, Bryopsidales) on the central Pacific coast of Japan

Minoru Miyadai; Shingo Akita; Daisuke Fujita

doi:10.1515/bot-2022-0013

Article

Phenology of Codium cylindricum (Ulvophyceae, Bryopsidales) on the central Pacific coast of Japan

Minoru Miyadai

Minoru Miyadai is a researcher at Kaneryo Kaiso Co. Ltd. He studied the lifecycle of Codium spp. in his Master’s research. Currently, he works to develop land-based aquaculture of edible seaweeds.
, Shingo Akita

Shingo Akita is an assistant professor at Hokkaido University in Hokkaido, Japan. He is a phycologist and marine ecologist. His dominant study is restoration of kelp forests. He is also interested in phylogeny, population genetics and physiology of kelp species and the other members of the Phaeophyceae.
and Daisuke Fujita

Daisuke Fujita is an associate professor at Tokyo University of Marine Science and Technology in Tokyo, Japan. He is a marine ecologist and phycologist and has worked on the ecology of deforestation and restoration of macroalgal beds for more than 40 years.

Published/Copyright: July 21, 2022

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From the journal Botanica Marina Volume 65 Issue 5

Abstract

Codium cylindricum is a large green alga distributed along the temperate Northeast Pacific coasts. Although the species is edible and contains pharmaceutical substances, little is known about its ecology. In this study, we characterized the phenology of C. cylindricum by monthly observations in Tateyama on the central Pacific coast of Japan from March 2018 to February 2019. The average length of attached thalli in three quadrats (2 × 2 m) was 5 cm from April to July. After disappearing in August, recruits appeared in November and the maximum density (1.08 ± 3.5 inds·m⁻²) was reached in February. On the sea bottom, detached thalli were present from April to October; the biomass monitored in a single quadrat (2 × 20 m) was high from June to August. Based on monthly observations of 50–100 utricles in each of 18–25 thalli, gametangium formation started in June and reached a peak (i.e., gametangia detected in 75% of thalli and 63.4% of utricles) in September, before the disappearance of the detached thalli. These results strongly suggest that C. cylindricum is annual and reproduces mainly while they are drifting. Therefore, growth during detached stage is critically important to increase biomass and dispersal.

Keywords: annual; Codiaceae; macroalgal bed; phenology

Corresponding author: Shingo Akita, Laboratory of Applied Phycology, Graduate School of Tokyo University of Marine Science and Technology, Tokyo 108-8477, Japan; and Faculty of Fisheries Sciences, Hokkaido University, 3-1-1 Minato, Hakodate, Hokkaido 041-8611, Japan, E-mail: sakitam@fish.hokudai.ac.jp

Funding source: Sasakawa Sicentific Grand from the Japan Science Society

Award Identifier / Grant number: 2018-7038

About the authors

Minoru Miyadai

Minoru Miyadai is a researcher at Kaneryo Kaiso Co. Ltd. He studied the lifecycle of Codium spp. in his Master’s research. Currently, he works to develop land-based aquaculture of edible seaweeds.

Shingo Akita

Shingo Akita is an assistant professor at Hokkaido University in Hokkaido, Japan. He is a phycologist and marine ecologist. His dominant study is restoration of kelp forests. He is also interested in phylogeny, population genetics and physiology of kelp species and the other members of the Phaeophyceae.

Daisuke Fujita

Daisuke Fujita is an associate professor at Tokyo University of Marine Science and Technology in Tokyo, Japan. He is a marine ecologist and phycologist and has worked on the ecology of deforestation and restoration of macroalgal beds for more than 40 years.

Acknowledgments

We thank the staff of Tateyama Field Station of Tokyo University of Marine Science and Technology. We also thank Bioedit for their professional English editing.

Author contributions: Original concept: MM and SA; field survey and methodology: MM and SA; data curation: MM; formal analyses and visualization: SA; funding acquisition: SA; draft writing: MM and SA; editing and review of manuscript: MM, SA, and DF. All authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: This study was financially supported, in part, by the Sasakawa Scientific Grant from the Japan Science Society to SA (grant no. 2018-7038).
Conflict of interest statement: The authors declare that they have no conflicts of interest regarding this article.

References

Akagawa, I. and Okiyama, M. (1997). Reproductive and feeding ecology of Rudarius ercodes in different environments. Ichthyol. Res. 44: 82–88. (in Japanese), https://doi.org/10.1007/bf02672762.Search in Google Scholar

Akita, S., Yamada, H., Ito, M., Kobayashi, M., and Fujita, D. (2014). Phenology of annual kelp Eckloniopsis (Phaeophyceae, Laminariales) forest on a Diadema barren in Uchiura Bay, central Pacific coast of Honshu, Japan. J. Appl. Phycol. 26: 1141–1148, https://doi.org/10.1007/s10811-013-0213-2.Search in Google Scholar

Alvarez-Hernández, S., Lara-Isassi, G.D., Arreguín-Espinoza, R., Arreguín, B., Hernández-Santoyo, A., and Rodríguez-Romero, A. (1999). Isolation and partial characterization of giraffine, a lectin from the Mexican endemic alga Codium giraffa Silva. Bot. Mar. 42: 573–580.10.1515/BOT.1999.064Search in Google Scholar

Arasaki, S., Tokuda, H., and Fujiyama, K. (1956). The reproduction and morphology in Codium fragile. Bot. Mag. Tokyo 69: 39–45. (in Japanese with English abstract), https://doi.org/10.15281/jplantres1887.69.39.Search in Google Scholar

Armitage, C.S. and Sjøtun, K. (2017). Can an old alien benefit from rising ocean temperatures? An experimental and field study on the growth and local distribution of Codium fragile subsp. fragile (Chlorophyta). Mar. Biol. 164: 1–20, https://doi.org/10.1007/s00227-017-3170-5.Search in Google Scholar

Borden, C.A. and Stein, J.R. (1969). Reproduction and early development in Codium fragile (Surngar) Hariot: Chlorophyceae. Phycologia 8: 91–99, https://doi.org/10.2216/i0031-8884-8-2-91.1.Search in Google Scholar

Bulleri, F. and Airoldi, L. (2005). Artificial marine structures facilitate the spread of a nonindigenous green alga, Codium fragile ssp. Tomentosoides, in the North Adriatic Sea. J. Appl. Ecol. 42: 1063–1072, https://doi.org/10.1111/j.1365-2664.2005.01096.x.Search in Google Scholar

Campbell, S.J. (1999). Occurrence of Codium fragile subsp. Tomentosoides (Chlorophyta, Bryopsidales) in marine embayments of Southeastern Australia. J. Phycol. 35: 938–940, https://doi.org/10.1046/j.1529-8817.1999.3550938.x.Search in Google Scholar

Chang, J.S., Dai, C.F., and Chang, J. (2003). Gametangium-like structures as propagation buds in Codium edule silva (Bryopsidales, Chlorophyta). Bot. Mar. 46: 431–437, https://doi.org/10.1515/bot.2003.043.Search in Google Scholar

Chapman, A.S. (1999). From introduced species to invader: what determines variation in the success of Codium fragile ssp. Tomentosoides (Chlorophyta) in the North Atlantic Ocean? Helgol. Meeresunters. 52: 277–289.10.1007/BF02908902Search in Google Scholar

Chapman, V.J. and Chapman, D.J. (1973). The algae, 2nd ed. Hong Kong: The Macmillan Press.10.1007/978-1-349-27910-4Search in Google Scholar

Chavanich, S., Harris, L.G., Je, J.G., and Kang, R.S. (2006). Distribution pattern of the green alga Codium fragile (Suringar) Hariot, 1889 in its native range, Korea. Aquat. Invasions 1: 99–108, https://doi.org/10.3391/ai.2006.1.3.1.Search in Google Scholar

Churchill, A.C. and Moelloer, H.A. (1972). Seasonal patterns of reproduction in New York populations of Codium fragile (Sur.) Hariot subsp. Tomentosoides (Van goor) Silva. J. Phycol. 8: 147–152, https://doi.org/10.1111/j.0022-3646.1972.00147.x.Search in Google Scholar

Dromgoole, F.I. (1975). Occurrence of Codium fragile subspecies tomentosoides in New Zealand waters. N. Z. J. Mar. Freshw. Res. 9: 257–264, https://doi.org/10.1080/00288330.1975.9515564.Search in Google Scholar

Drouin, A., McKindsey, C.W., and Johnson, L.E. (2016). Dynamics of recruitment and establishment of the invasive seaweed Codium fragile within an eelgrass habitat. Mar. Biol. 163: 1–12, https://doi.org/10.1007/s00227-016-2832-z.Search in Google Scholar PubMed PubMed Central

Fralick, R.A. and Mathieson, A.C. (1972). Winter fragmentation of Codium fragile (Suringar) Hariot ssp. Tomentosoides (van Goor) Silva (Chlorophyceae, Siphonales) in New England. Phycologia 11: 67–70, https://doi.org/10.2216/i0031-8884-11-1-67.1.Search in Google Scholar

Fujita, D. (2010). Current status and problems of Isoyake in Japan. Bull. Fish. Res. Agency 32: 33–42.Search in Google Scholar

Gagnon, K., McKindsey, C.W., and Johnson, L.E. (2015). Roles of dispersal mode, recipient environment and disturbance in the secondary spread of the invasive seaweed Codium fragile. Biol. Invasions 17: 1123–1136, https://doi.org/10.1007/s10530-014-0782-2.Search in Google Scholar

Ganesan, P., Noda, K., Yuki, M., Ohkubo, T., Tanaka, Y., Maoka, T., and Hirata, T. (2011). Siphonaxanthin, a marine carotenoid from green algae, effectively induces apoptosis in human leukemia (HL-60) cells. Biochim. Biophys. Acta 1810: 497–503, https://doi.org/10.1016/j.bbagen.2011.02.008.Search in Google Scholar PubMed

Gonzalez, A.V., Beltran, J., and Santelices, B. (2014). Colonization and growth strategies in two Codium species (Bryopsidales, Chlorophyta) with different thallus forms. Phycologia 53: 353–358, https://doi.org/10.2216/13-251.1.Search in Google Scholar

Guiry, M.D. and Guiry, G.M. (2021). AlgaeBase. World-wide electronic publication. National University of Ireland, Galway, Available at: http://www.algaebase.org (Searched on 26 August 2021).Search in Google Scholar

Hamatani, I. (1967). Notes on veligers of Japanese Opisthobranchs (7). Publ. Seto Mar. Biol. Lab. 15: 121–131, https://doi.org/10.5134/175461.Search in Google Scholar

Harada, K., Ookei, N., Senbokuya, K., and Okuno, J. (2021). Present condition and issues of environment and fishery in inner bay – a case of Nanao Bay. Syst. Control Inf. 65: 3–6. (in Japanese).Search in Google Scholar

Hwang, E.K., Baek, J.M., and Park, C.S. (2008). Cultivation of the green alga, Codium fragile (Suringar) Hariot, by artificial seed production in Korea. J. Appl. Phycol. 20: 469–475, https://doi.org/10.1007/s10811-007-9265-5.Search in Google Scholar

Lee, I.K. and Kang, J.W. (1986). A check list of marine algae in Korea. Kor. J. Phycol. 1: 311–325.Search in Google Scholar

Lee, R.E. (2008). Phycology, 4th ed. New York: Cambridge University Press, pp. 448–464.10.1017/CBO9780511812897Search in Google Scholar

Lee, S. and Park, S. (2013). Proceedings of the IEEE sensors applications symposium proceedings, Galveston, TX, USA, 19–21 February 2013: energy savings of home growing vegetables by using daylight and LED. IEEE, New York, pp. 202–204.Search in Google Scholar

Lewis, J.E. and Norris, J.N. (1987). A history and annotated account of the benthic marine algae of Taiwan. Smithsonian Contrib. Mar. Sci. 29: 1–38, https://doi.org/10.5479/si.01960768.29.iv.Search in Google Scholar

Li, Z.S., Zheng, J.W., Manabe, Y., Hirata, T., and Sugawara, T. (2018). Anti-obesity properties of the dietary green alga, Codium cylindricum, in high-fat diet-induced obese Mice. J. Nutr. Sci. Vitaminol. 64: 347–356, https://doi.org/10.3177/jnsv.64.347.Search in Google Scholar

Lyons, D.A. and Scheibling, R.E. (2008). Context-dependant survival of the invasive seaweed Codium fragile ssp. tomentosoides in kelp bed and urchin barren habitats off Nova Scotia. Aquat. Biol. 2: 17–27, https://doi.org/10.3354/ab00035.Search in Google Scholar

Lyons, D.A., Van Alstyne, K.L., and Scheibling, R.E. (2007). Anti-grazing activity and seasonal variation of dimethylsulfoniopropionate-associated compounds in the invasive alga Codium fragile ssp. tomentosoides. Mar. Biol. 153: 179–188, https://doi.org/10.1007/s00227-007-0795-9.Search in Google Scholar

Malinowski, K.C. and Ramus, J. (1973). Growth of the green alga Codium fragile in a Connecticut estuary. J. Phycol. 9: 102–110, https://doi.org/10.1111/j.0022-3646.1973.00102.x.Search in Google Scholar

Matsubara, K., Matsuura, Y., Bacic, A., Liao, M.L., Hori, K., and Miyazawa, K. (2001). Anticoagulant properties of a sulfated galactan preparation from a marine green alga, Codium cylindricum. Int. J. Biol. Macromol. 28: 395–399, https://doi.org/10.1016/s0141-8130(01)00137-4.Search in Google Scholar

Matsubara, K., Mori, M., Matsumoto, H., and Hori, K. (2003). Antiangiogenic properties of a sulfated galactan isolated from a marine green alga, Codium cylindricum. J. Appl. Phycol. 15: 87–90, https://doi.org/10.1023/a:1022958222915.10.1023/A:1022958222915Search in Google Scholar

Narita, M., Agatsuma, Y., and Taniguchi, K. (2008). Marine algae in Matsushima Bay, Northeastern Honshu, Japan. Aquacult. Sci. 56: 387–399.Search in Google Scholar

Neill, P.E., Alcalde, O., Faugeron, S., Navarrete, S.A., and Correa, J.A. (2006). Invasion of Codium fragile ssp. tomentosoides in Northern Chile: a new threat for Gracilaria farming. Aquaculture 259: 202–210, https://doi.org/10.1016/j.aquaculture.2006.05.009.Search in Google Scholar

Nguyen, T.V., Le, N.H., Lin, S.M., Steen, F., and De Clerck, O. (2013). Checklist of the marine macroalgae of Vietnam. Bot. Mar. 56: 207–227, https://doi.org/10.1515/bot-2013-0010.Search in Google Scholar

Ohta, Y., Lee, J.B., Hayashi, K., and Hayashi, T. (2009). Isolation of sulfated galactan from Codium fragile and its antiviral effect. Biol. Pharm. Bull. 32: 892–898, https://doi.org/10.1248/bpb.32.892.Search in Google Scholar PubMed

Okamura, K. (1915). Icones of Japanese algae, Vol. III PL.CI-CL. Self-Publish, Tokyo.Search in Google Scholar

Pedroche, F.F., Silva, P.C., and Chacana, M. (2002). El género Codium (Codiaceae, Chlorophyta) en el Pacífico de México. In: Sentíes, A. and Dreckmann, K.M. (Eds.). Monografías ficológicas. Universidad Autónoma Metropolitana-Iztapalapa, México, DF, pp. 11–74.Search in Google Scholar

Prince, J.S. and Trowbridge, C.D. (2004). Reproduction in the green macroalga Codium (Chlorophyta): characterization of gametes. Bot. Mar. 47: 461–470, https://doi.org/10.1515/bot.2004.062.Search in Google Scholar

Riosmena-Rodríguez, R. and Holguín-Acosta, E. (2008). Population structure of Codium amplivesiculatum (Chlorophyta) associated with rhodolith beds from the Southwestern Gulf of California. Algae 23: 141–150.10.4490/ALGAE.2008.23.2.141Search in Google Scholar

Scheibling, R.E. and Anthony, S.X. (2001). Feeding, growth and reproduction of sea urchins (Strongylocentrotus droebachiensis) on single and mixed diets of kelp (Laminaria spp.) and the invasive alga Codium fragile ssp. tomentosoides. Mar. Biol. 139: 139–146.10.1007/s002270100567Search in Google Scholar

Scheibling, R.E. and Melady, R.A. (2008). Effect of water movement and substratum type on vegetative recruitment of the invasive green alga Codium fragile ssp. tomentosoides. Bot. Mar. 51: 341–349, https://doi.org/10.1515/bot.2008.046.Search in Google Scholar

Schmidt, A.L. and Scheibling, R.E. (2006). A comparison of epifauna and epiphytes on native kelps (Laminaria species) and an invasive alga (Codium fragile ssp. tomentosoides) in Nova Scotia, Canada. Bot. Mar. 49: 315–330, https://doi.org/10.1515/bot.2006.039.Search in Google Scholar

Serisawa, Y., Makita, A., Kimbara, K., and Matsuyama-Serisawa, K. (2020). Seasonal changes in frond and utricle size of Codium fragile at Omaezaki, Shizuoka Prefecture, Central Japan. Algal Resour. 13: 1–12. (in Japanese with English abstract).Search in Google Scholar

Silva, P.C. (1957). Codium in Scandinavian waters. Sven. Bot. Tidskr. 51: 117–134.Search in Google Scholar

Silva, P.C. (1960). Codium (Chlorophyta) of the tropical Western Atlantic. Nova Hedwigia 1: 497–536.Search in Google Scholar

Silva, P.C., Meñez, E.G., and Moe, R.L. (1987). Catalog of the benthic marine algae of the Philippines. Smithsonian Contrib. Mar. Sci. 27: 1–179, https://doi.org/10.5479/si.1943667x.27.1.Search in Google Scholar

Skriptsova, A.V. and Levenets, I.R. (2012). Seasonal dynamics of subtidal macrophyte assemblages in Sobol Bay (Peter the Great Bay, Sea of Japan) in relation to depth. J. Mar. Biol. Assoc. U. K. 92: 429–437, https://doi.org/10.1017/s0025315411000968.Search in Google Scholar

Steller, D.L., Riosmena-Rodríguez, R., Foster, M.S., and Roberts, C.A. (2003). Rhodolith bed diversity in the Gulf of California: the importance of rhodolith structure and consequences of disturbance. Aquat. Conserv. Mar. Freshw. Ecosyst. 13: S5–S20, https://doi.org/10.1002/aqc.564.Search in Google Scholar

Trowbridge, C.D. (1996). Demography and phenology of the intertidal green alga Codium setchellii: the enigma of local scarcity on sand-influenced rocky shores. Mar. Biol. 127: 341–351, https://doi.org/10.1007/bf00942119.Search in Google Scholar

Trowbridge, C.D., Hirano, Y.J., and Hirano, Y.M. (2008). Sacoglossan opisthobranchs associated with the green macroalgae Codium spp. on Pacific rocky shores of Japan. Venus J. Malacol. Soc. Jpn. 66: 175–190.Search in Google Scholar

Tseng, C.K. (1984). Common seaweeds of China. Science Press, Beijing.Search in Google Scholar

Verbruggen, H., Leliaert, F., Maggs, C.A., Shimada, S., Schils, T., Provan, J., Booth, D., Murphy, S., De Clerck, O., Littler, D.S., et al.. (2007). Species boundaries and phylogenetic relationships within the green algal genus Codium (Bryopsidales) based on plastid DNA sequences. Mol. Phylogenet. Evol. 44: 240–254, https://doi.org/10.1016/j.ympev.2007.01.009.Search in Google Scholar PubMed

Watanabe, S., Metaxas, A., and Scheibling, R.E. (2009). Dispersal potential of the invasive green alga Codium fragile ssp. fragile. J. Exp. Mar. Biol. Ecol. 381: 114–125, https://doi.org/10.1016/j.jembe.2009.09.012.Search in Google Scholar

Yoshida, T. (1998). Marine algae of Japan. Uchida Rokakuho Publishing, Tokyo.Search in Google Scholar

Yotsui, T. and Migita, S. (1989). Cultivation of a green alga Codium fragile by regeneration of medullary threads. Nippon Suisan Gakkaishi 55: 41–44. (in Japanese with English abstract), https://doi.org/10.2331/suisan.55.41.Search in Google Scholar

Received: 2022-02-20

Accepted: 2022-06-07

Published Online: 2022-07-21

Published in Print: 2022-10-26

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https://doi.org/10.1515/bot-2022-0013

Keywords for this article

annual; Codiaceae; macroalgal bed; phenology