Size Variation and Survival after Transplantation of the Tropical Box Marine Mussel Septifer bilocularis on the Three Coastal Sites of North Sulawesi, Indonesia

Main Article Content

Medy Ompi
Farnis Binea Boneka
Sandra Tilaar
Stella T. Kaunang

Abstract

Box mussels exhibit patchy distribution patterns across intertidal and subtidal zones, where environmental contrasts strongly influence their physiology and ecology. Intertidal box mussels experience frequent air exposures, variable salinity, acidity, and turbidity during low tide, whereas subtidal mussels generally experience more stable conditions. However, with rising sea temperatures related to global climate change, these stressors may intensify, disrupting the mussel’s activities. Consequently, their roles in marine ecosystems may change, yet knowledge of box mussel responses to environmental change remains limited. This study investigated the effects of site, time (monthly intervals), and position (intertidal vs. subtidal) on mussel growth and survival. Box mussels were transplanted to intertidal and subtidal seabeds at three sites in North Sulawesi: Tiwoho, Tongkaina, and Blongko, from August to November 2023. Shell length and survival rates were analyzed using a three-way ANOVA, with site, time, and position as main factors. The results showed that mean shell length was significantly influenced by all three factors. The box mussels grew rapidly from August to September, followed by slower growth from October to November. The final mean size was higher at Tongkaina compared to Blongko, while Tiwoho did not differ significantly from Tongkaina. Survival declined steadily, averaging 22–40% by November, and was influenced by time and position but not by site. Ascidians were observed attaching to the cages in November. Seawater temperature, ascidian presence, and food availability may influence mussel size and survival. Finally, although the tropical mussel, S. bilocularis, exhibits higher thermal tolerance, it remains vulnerable to ocean warming.

Article Details

How to Cite
Ompi, M., Boneka, F. B. ., Tilaar, S., & Kaunang, S. T. . (2026). Size Variation and Survival after Transplantation of the Tropical Box Marine Mussel Septifer bilocularis on the Three Coastal Sites of North Sulawesi, Indonesia. Journal of Fisheries and Environment, 50(1), 43–56. retrieved from https://li01.tci-thaijo.org/index.php/JFE/article/view/269099
Section
Research Article

References

Ambarak, M.Z., M. Ompi, D.S.J. Paransa, J.R.T.S.L. Rimper, A.P. Rumengan and N.E. Bataragoa. 2021. The diversity of macrobenthos attached to the coral aggregation, on the coast of Tiwoho, North of Minahasa, North Sulawesi. The Coastal and Tropical Marine Journal 9(3): 133–140. DOI: 10.35800/jplt.9.3.2021.38043.

Arrieche, D., A.N. Maeda-Martínez, V. Acosta-Balbás, L. Freites, H. Acosta-Salmón and C. Lodeiros-Seijo. 2020. Optimum temperature for growth of an invasive green mussel Perna viridis population from Venezuela, determined in an open-flow system. Aquaculture Reports 16: 100284. DOI: 10.1016/j.aqrep.2020.100284.

Barbosa, R.V., Bacher, C., Jean, F., Thomas and Y. 2021. Linking individual and population patterns of rocky-shore mussels. PeerJ 9: e12550. DOI: 10.7717/peerj.12550.

Benjamin, E.D., T.A. Toone, J.R. Hillman, S.E. Handley and A. Jeffs. 2024. Aerial exposure and critical temperatures limit the survival of restored intertidal mussels. Restoration Ecology 32(4): e14105. DOI: 10.1111/rec.14105.

Bridger, D., M.J. Attrill, B.F.R. Davies, L.A. Holmes, A. Cartwright, S.E. Rees, L.M. Cabre and E.V. Sheeha. 2022. The restoration potential of offshore mussel farming on degraded seabed habitat. Aquaculture Fish and Fisheries 2: 437–449. DOI: 10.1002/aff2.77.

Bayne, B. L., A.J.S. Hawkins, E. Navarro, I.P. Iglesias. 1989. Effects of seston concentration on feeding, digestion and growth in the mussel Mytilus edulis. Marine Ecology Progress Series 55: 47–54. DOI: 10.3354/MEPS055047.

Clements, J.C., K. Ramesh, J. Nysveen, S. Dupontand F. Jutfelt. 2020. Animal size and sea water temperature, but not pH, influence a repeatable startle response behaviour in a wide-ranging marine mollusc. Animal Behaviour 173: 191–205. DOI: 10.1016/j.anbehav.2020.12.008.

Chelyadina, N.S. and M. Popov. 2020. Individual variability of growth of the cultivated Mytilus galloprovincialis Lam. in various habitat conditions of the Black sea coastal zone. Aquaculture Research 51: 4846–4851. DOI: 10.1111/are.14838.

Collins, C.L., N. Burnett, M.J. Ramsey, K. Wagner and M. Zippay. 2020. Physiological responses to heat stress in an invasive mussel Mytilus galloprovincialis depend on tidal habitat. Marine Environment Research 154: 104849. DOI: 10.1016/j.marenvres.2019.104849.

Conley, K.R., A. Ben-Tal, Y. Jacobi, G. Yahel and K.R. Sutherland. 2018. Not-so-simple sieving by ascidians: re-examining particle capture at the mesh and organismal scale. Marine Biology 165: 45. DOI: 10.1007/s0022 7-018-3300-8.

Commito, J.A., B.J. Jones, M.A. Jones, S.E. Winders and S. Como. 2019. After the Fall: Legacy effects of biogenic structure on wind-generated ecosystem processes following mussel bed collapse. Diversity 11(1): 11. DOI: 10.3390/d11010011.

Fernandes-Reiriz, M.J., J. Irisarri and U. Labarta. 2016. Flexibility of physiological traits underlying inter-individual growth differences in intertidal and subtidal mussel Mytilus galloprovincialis. PLoS One 11(2): e0148245. DOI: 10.1371/journal.pone.0148245.

Fowler, J., L. Cohen and P. Jarvis. 1998. Practical Statistics for Field Biology, 2nd ed. John Wiley and Sons, New York - Toronto, USA. 259 pp.

Gosling, E. 1992. The Mussel Mytilus: Ecology, Physiology, Genetics and Culture (Developments in Aquaculture and Fisheries Science). Elsevier Science, Amsterdam, Netherlands. 589 pp.

Helmuth, B., C.D.G. Harley, P.M. Halpin, D.E. O’Donnell, C.A. Hofmann and Blanchette. 2002. Climate change and latitudinal patterns of intertidal thermal stress. Science 298: 1015–1017. DOI: 10.1126/science.1076814.

Iskandar, M.R., H.Y. Jia, R. Sasaki, S. Furue, T. Kida, Suga and K.J. Richards. 2023. Effects of high-frequency flow variability on the pathways of the Indonesian Throughflow. Journal of Geophysical Research: Oceans 128: e2022JC019610. DOI: 10.1029/2022JC019610.

Ibarrola, I., K. Arranz, P. Markaide and E. Navarro. 2022. Metabolic size scaling reflects growth performance effects on age-size relationships in mussels (Mytilus galloprovincialis). PLoS ONE 17(9): e0268053. DOI: 10.1371/journal. pone.0268053.

Jaatinen, K., M. Westerbom, A. Norkko, O. Mustonen and D.N. Koons. 2020. Detrimental impacts of climate change may be exacerbated by density-dependent population regulation in blue mussels. Journal of Animal Ecology 90(3): 562–573. DOI: 10.1111/1365-2656.13377.

Jørgensen, C.B., P.S. Larsen and H.U. Riisgard. 1990. Effects of temperature on the mussel pump. Marine Ecology Progress Series 64: 89–97. DOI: 10.3354/meps064089.

Kamermans, P. and C. Saurel. 2022. Interacting climate change effects on mussels (Mytilus edulis and M. galloprovincialis) and oysters (Crassostrea gigas and Ostrea edulis): experiments for bivalve individual growth models. Aquatic Living Resources 2022(35): 1. DOI: 10.1051/alr/2022001.

Kusuma, D.W., A. Murdimanto, L.Y.B Aden, B. Sukresno, D. Jatisworo and R. Hanintyo. 2017. Sea surface temperature dynamics in Indonesia. IOP Conference Series: Earth and Environmental Science 98(2017): 012038. DOI: 10.1088/1755-1315/98/1/012038.

Kittner, C. and H.U. Riisgård. 2005. Effect of temperature on filtration rate in the mussel Mytilus edulis: no evidence for temperature compensatio. Marine Ecology Progress Series 305: 147–152. DOI: 10.3354/meps305147.

Marshall, A.E. M.A. Kathryn, N.E.M. Brown, J.K. Dytnerski, K.L. Flynn, J.R. Bernhardt, C.A. Konecny, H.G. Smith and C.D.G. Harley. 2021. Whole-organism responses to constant temperatures do not predict responses to variable temperatures in the ecosystem engineer Mytilus trossulus. Proceedings of The Royal Society B 288(1947): 20202968. DOI: 10.1098/rspb.2020.2968.

Matoo, O.B., G. Lannig, C. Bock and I. M. Sokolova. 2021. Temperature but not ocean acidificationaffects energy metabolism and enzyme activities in the blue mussels, Mytilus edulis. Ecology and Evolution 2021(11): 3366–3379. DOI: 10.1101/2020.11.29.402933.

Morton, B., P.T.Y. Leung, J. Wei and G.Y. Lee. 2020. A morphological and genetic comparison of Septifer bilocularis, Mytilisepta virgata and Brachidontes variabilis (Bivalvia: Mytiloidea) from Hong Kong and erection of the Mytiliseptiferinae sub-fam. Regional Study in Marine Science 34: 100981. DOI: 10.1016/j.rsma.2019.100981.

McLeod, I.M., P.S.E. zu Ermgassen, C.L. Gillies, B. Hancock and A. Humphries. 2019. Can bivalve habitat restoration improve degraded estuaries?. In: Coasts and Estuaries: The Future (eds. E. Wolanski, J.W. Day, M. Elliott and R. Ramachandran), pp. 427–442. Elsevier, Amsterdam, Netherlands. DOI: 10.1016/B978-0-12-814003-1.00025-3.

Menge, B.A., F. Chan, and J. Lubchenco. 2008. Response of a rocky intertidal ecosystem engineer and community dominant to climate change. Ecology Letters 11: 151–162. DOI: 10.1111/j.1461-0248.2007. 01135.x.

Nauta, J., M.J.A. Christianen, R.J.M. Temmink, et al. 2022. Biodegradable artificial reefs enhance food web complexity and biodiversity in an intertidal soft-sediment ecosystem. Journal of Applied Ecology 2023(60): 541–552. DOI: 10.1111/1365-2664.14348.

Ompi, M. 1997. Ecology of the intertidal box mussel, Septifer bilocularis L., North Sulawesi, Indonesia. Phuket Marine Biological Center Special Publication 16 (1996): 249–256.

Ompi, M. and I. Svane. 2018. Comparing spawning, larval development, and recruitments of four mussel species (Bivalvia: Mytilidae) from South Australia. AACL Bioflux 11(3): 576–588.

Ompi, M. and L.J.L. Lumingas. 2019. The effect of patch size on morphology and growth on the intertidal box mussel Septifer bilocularis L., in North Sulawesi, Indonesia. Indonesia Journal of Mollusk 3(1): 1–4. DOI: 10.54115/jmi.v3i1.33.

Ompi, M., F.B. Boneka, E.Y. Kaligis and S.T. Kaunang. 2023a. Settlement of the tropical box mussel, Septifer bilocularis: Effects of site, position, and substratum. Aquaculture Research 2023: 4498844. DOI: 10.1155/2023/4498844.

Ompi, M., F.B. Boneka, E.Y. Kaligis and S.T. Kaunang. 2023b. The Role of particle-feeding box mussels on the diversity of macrobenthos on mussel aggregation in the coastal area of Tiwoho and Blongko, North Sulawesi. Bawal 15(1): 1–13. DOI: 10.15578/bawal.15.1.2023.1-13.

Ompi, M., A.R. Simbolon, J.R.T.S.L. Rimper, S.T. Kaunang and K.R. Jensen. 2024. The first records of pelagic gastropods species from the Celebes Sea, North Sulawesi, Indonesia. Journal of Fisheries and Environment 48(30): 1–16. DOI: 10.34044/j.jfe.2024.48.3.01.

Palit, D.A., F.B. Boneka, E.Y. Kaligis, J.T.S.L. Rimper, C. Lumenta and M. Ompi. 2021. Rekruitment tropical box mussel, Septifer Bilocularis in Tiwoho Coastal Area. The Journal of Coastal and Marine Journal 19(2): 321–327. DOI: 10.35800/jip.v9i2.35726.

Petraitis, P.S. and S.R. Dudgeon. 2020. Declines over the last two decades of five intertidalinvertebrate species in the western North Atlantic. Communication Biology 3(591): 1–7. DOI: 10.1038/s42003-020-01326-0.

Prioto, D., D. Tamayo, I. Urrutxurtu, E. Navarro, I. Ibarrola and M.B. Urrutia. 2020. Nature more than nurture affects the growth rate of mussels. Scientific Reports (2020)10: 3539. DOI: 10.1038/s41598-020-60312-y.

People, J. 2006. Mussel beds on different types of structures support different macroinvertebrate assemblages. Austral Ecology 31(2): 271–281. DOI: 10.1111/j.1442- 9993.2006.01585.

Petersen, J.J. and I. Svane. 2002. Filtration rate in seven Scandinavian ascidians: Implications of the morphology of the gill sac. Marine Biology 140(2): 397–402. DOI: 10.1007/s002270100706.

Rahim, A.R., D.R. Utami and Ubaidillah. 2025. Density of green mussels (Perna viridis) and its impact on growth and lead accumulation in polyculture systems in tropical waters. Asian Journal of Fisheries and Aqutic Research 27(1): 79–89. DOI: 10.9734/ajfar/2025/v27i1865.

Soria, S.A., J.L.Gutierrez, J.A. Gonzalez, S.L. Calla and M.G. Palomo. 2022. Habitat properties and invertebrate composition in mussel-dominated rocky shores: A test of edge effects. Estuarine Coastal and Shelf Science 277(2022): 108035. DOI: 10.1016/j.ecss.2022.108035.

Schotanus, J., J.J. Capelle, E. Paree, G.S. Fivash, J. Van De Koppel and T.J. Bouma. 2020. Restoring mussel beds in highly dynamic environments by lowering environmental stressors. Restoration Ecology 28(5): 1124–1134. DOI: 10.1111/rec.13168.

Seitz, R.D., H. Wennhage, U. Bergström, R.N. Lipcius and T. Ysebaert. 2014. Ecological value of coastal habitats for commercially and ecologically important species. ICES Journal of Marine Science 71: 648–665. DOI: 10.1111/1365-2656.13377.

Soon, T.K. and J. Ransangan. 2016. Feasibilty of green mussels Perna viridis farming in Marudu Bay, Malaysia. Aquaculture reports 4: 130–135. DOI: 10.1016/j.aqrep.2016.06.006.

Steffani, C.N. and G.M. Branch. 2003. Growth rate, condition, and shell shape of Mytilus galloprovincialis: responses to wave exposure. Marine Ecology Progress Series 246: 197–209. DOI: 10.3354/meps246197.

Seed, R. and T. Suchanek. 1992. Population and community ecology of Mytilus. In: Developments in Aquaculture and Fisheries Science, Chapter 4: The Mussel Mytilus: Ecology, Physiology, Genetics and Culture (ed. E. Gosling), pp. 86–169. Elsevier Science, Amsterdam, Netherlands.

Telesca, L., K. Michalek, T. Sanders, L.S. Peck, J. Thyrring and E.M. Harper. 2018. Blue mussel shell shape plasticity and natural environments: A quantitative approach. Scientific Reports 8: 2865. DOI: 10.1038/s41598-018-20122-9.

van den Bogaart, L.A., J. Schotanus, J.J. Capelle and T.J. Bouma. 2023. Comparing traditional vs. biodegradable seed mussel collectors (SMCs) for seed settlement, seed density, and seed growth: Effect of deployment depth and locations. Aquacultural Engineering 102: 102344. DOI: 10.1016/j.aquaeng.2023.102344.

Wang, H.Y., L.M. Tsang, F.P. Lima, R. Seabra, M. Ganmanee, G.A. Williams and B.K.K Chang. 2022. Spatial variation in thermal stress experienced by barnacles on rocky shores: The interplay between geographic variation, tidal cycles and microhabitat temperatures. Frontiers in Marine Science 7(553): 1–14. DOI: 10.3389/fmars.2020.00553.

Wagiu, F.J.G., M. Ompi, E.Y. Kaligis, J.R.T.S.L. Rimper, K.A. Roeroe and F.B. Manginsela. 2021. Attachment of Septifer bilocularis to Substrate in mussel bed on the intertidal area of the coastal of Tiwoho. Tropical Coastal and Marine Journal 10(3): 223–230. DOI: 10.35800/jplt.10.3.2022.55017.

Williams, G.A., B.K.K. Chan and Y.W. Dong. 2019. Rocky shores of mainland China, Taiwan and Hong Kong: past, present and future. In: Interactions in the Marine Benthos: Global Patterns and Processes (eds. S.J. Hawkins, K. Bohn, L.B. Firth and G.A. Williams), pp. 360–390. Cambridge University Press, Cambridge, UK.

Yuan, W.S., L.J. Walters, S.A. Brodsky, K.R. Schneider, E.A. Hoffman and B. Rinkevich. 2016. Synergistic effects of salinity and temperature on the survival of Perna viridis and Mytella charruana. Journal of Marine Biology 2016: 9261309. DOI: 10.1155/2016/9261309.

Zelin, N.I. and Y.Y. Latypov. 2006. Distribution pattern, population structure, and growth of Septifer bilocularis (Bivalvia: Mytilidae) on reefs of Southern Vietnam. RusianJournal of Marine Biology 32: 88–95. DOI: 10.1134/S1063074006020039.

Zu Ermgassen, P.S.E, M.D. Spalding, R.E. Grizzle and R.D. Brumbaugh. 2013. Quantifying the loss of a marine ecosystem service: filtration by the eastern oyster in US Estuaries. Estuaries and Coasts 36: 36–43. DOI: 10.1007/s12237-012-9559-y.