Habitat associations of grouper (Teleostei: Epinephelidae) assemblages across reefs in the Bidong Archipelago, Malaysia
Article Sidebar
Abstract Views: 0
File Views: 0
Main Article Content
Abstract
Abstract. Afiq-Firdaus AM, Safuan CDM, Abdullah MM, Awalludin EA, Syafruddin RS, Qamarina MFN, Mohamad Y, Bachok Z. 2026. Habitat associations of grouper (Teleostei: Epinephelidae) assemblages across reefs in the Bidong Archipelago, Malaysia. Biodiversitas 27 (4): d270426. https://doi.org/10.13057/biodiv/d270426. Groupers (Teleostei: Epinephelidae) are important predatory fishes in coral reef ecosystems, yet their relationships with coral habitat remain insufficiently understood. This study aimed to evaluate grouper assemblages are structured by coral genus composition and benthic habitat, including live coral cover, across reefs in the Bidong Archipelago, Malaysia. Surveys were conducted at 18 stations between March and May 2022 using 100 m belt transects (5×100 m). Grouper assemblages were recorded using Underwater Visual Census (UVC) with video support, while benthic composition and coral genera were assessed using Coral Video Transects (CVT). Data were analyzed using canonical correspondence analysis (CCA), non-metric multidimensional scaling (NMDS), PERMANOVA, and Spearman correlation. A total of 388 individuals representing 11 species were recorded. Assemblages were dominated by Cephalopholis formosa (27%), Cephalopholis boenak (26%), and Cephalopholis cyanostigma (24%). NMDS indicated substantial overlap among sites, suggesting weak spatial structuring of assemblages. Coral genus composition explained 48.9% of constrained variation in CCA but was not statistically significant (p>0.05), consistent with PERMANOVA results (R²: 0.492, p: 0.811). Benthic cover explained 36.0% of variation in CCA and showed a marginal effect in PERMANOVA (R²: 0.434, p: 0.078), with only the “other invertebrates” category showing a significant relationship (p<0.05). Spearman correlation analyses revealed no significant relationships between grouper abundance and habitat variables. Grouper assemblages in the Bidong Archipelago showed weak and largely non-significant associations with coral genus composition and benthic habitat variables, indicating that factors other than measured habitat characteristics may play a greater role in structuring these communities.
Article Details
Issue
Section
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
References
Afiq-Firdaus AM, Lim CS, Safuan CDM, Kadir STSA, Ramasamy AMA, Manaf NAB, Ali MS, Lachs L, Wright HE, Bachok Z. 2021. Coral reef fish community at Bidong Island, Terengganu, South China Sea. J Sustain Sci Manag 16 (5): 48. https://doi.org/10.46754/jssm.2021.07.004.
Afiq-Firdaus AM, Safuan CDM, Shafie S, Izhar LI, Awalludin EA, Ahmad MF, Johari NAM, Bachok Z. 2023. Current status of coral reef fish abundances at Bidong Island and nearby islands, South China Sea using stereo-diver operated video system. Ocean Sci J 58: 16. https://doi.org/10.1007/s12601-023-00110-5.
Allen GR, Steene R, Humann P, DeLoach N. 2003. Reef Fish Identification: Tropical Pacific. New World Publications, Florida.
Allen GR, Erdmann MV. 2012. Reef ishes of the East Indies. University of Hawai'i Press, Perth.
Ambak MA, Isa MM, Zakaria MZ, Ghaffar MA. 2010. Fishes of Malaysia. Universiti Malaysia Terengganu, Kuala Terengganu.
Ambak MA, Mansor MI, Zakaria MZ, Mazlan AG. 2012. Fishes of Malaysia 2nd Eds. Universiti Malaysia Terengganu, Kuala Terengganu.
Anderson MJ, Millar RB. 2004. Spatial variation and effects of habitat on temperate reef fish assemblages in northeastern New Zealand. J Exp Mar Biol Ecol 305: 191-221. https://doi.org/10.1016/j.jembe.2003.12.011.
Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol 26 (1): 32-46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x.
Arai T, Amalina R, Bachok Z. 2015. Variation in fatty acid composition of the bigeye snapper Lutjanus lutjanus collected in coral reef habitats of the Malaysian South China Sea. J Biol Res-Thessalon 22: 1-8. https://doi.org/10.1186/s40709-015-0027-2.
Astuti R, Yonvitner, Kamal MM. 2016. Community structure of grouper fish (Serranidae) landed in Peukan Bada subdistrict, Aceh Province. Jurnal Ilmu dan Teknologi Kelautan Tropis 8 (1): 73-84.
Aziz N, Muhammad Z, Ghazali F, Talaat WIAW, Saputra J. 2019. Marine spatial planning: The way forward for sustainable development of central Terengganu, Malaysia. J Southwest Jiaotong Univ 54 (4): 9. https://doi.org/10.35741/issn.0258-2724.54.4.9.
Barik TK, Swain SN, Sahu B, Tripathy B, Acharya UR. 2018. The first record of Cephalopholis formosa (Perciformes: Serranidae) from the marine waters of Odisha coast, Bay of Bengal, India. J Ichthyol 58 (5): 751-753. https://doi.org/10.1134/S0032945218050028.
Bart J, Fligner MA, Notz WI. 1998. Pseudoreplication. Cambridge University Press, United Kingdom.
Chou LM, Wilkinson CR, Suraphol S. 1994. Status of coral reefs in the ASEAN region. In: Proceedings of the 3rd ASEAN-Australia Symposium on Living Coastal Resources. Australian Institute of Marine Science, Townsville, Australia, 16-20 Mei 1994.
Craig MT, Sadovy de Mitcheson Y, Heemstra PC. 2011. Groupers of the world. A field and market guide. NISC (Pty) Ltd. Grahamstown, South Africa.
Crochelet E. 2015. Le Centre pour la Communication Scientifique Directe [Dissertation]. Université de la Réunion, Réunion, France. [French]
Donaldson TJ. 2002. Habitat association and depth distribution of two sympatric groupers of the genus Cephalopholis. Ichthyol Res 49 (2): 191. https://doi.org/10.1007/s102280200025.
Eggleston DB, Lipcius RN, Grover J. 1997. Predator and shelter-size effects on coral reef fish and spiny lobster prey. Mar Ecol Prog Ser 149: 43. https://doi.org/10.3354/meps149043.
English S, Wilkinson C, Baker V. 1997. Survey Manual for Tropical Marine Resources. Australian Institute of Marine Science, Townsville.
Ersts PJ. 2020. DotDotGoose (version 1.5.1). American Museum of Natural History, Center for Biodiversity and Conservation, New York.
Field J, Clarke KR, Warwick RM. 1982. A practical strategy for analysing multispecies distribution patterns. Mar Ecol Prog Ser 8: 37-52. https://doi.org/10.3354/meps008037.
Fricke R, Mahafina J, Behivoke F, Jaonalison H, Léopold M, Ponton D. 2018. Annotated checklist of the fishes of Madagascar, southwestern Indian Ocean, with 158 new records. FishTaxa 3 (1): 1-432.
Froese R, Pauly D. 2018. FishBase. World Wide Web Electronic Publication.
Graham NA, Nash KL. 2013. The importance of structural complexity in coral reef ecosystems. Coral Reefs 32 (2): 315-326. https://doi.org/10.1007/s00338-012-0984-y
Grismer LL, Wood Jr PL, Ahmad AB. 2014. A new species of insular Rock Gecko (genus Cnemaspis Strauch, 1887) from the Bidong Archipelago, Terengganu. Zootaxa 3755 (5): 447-456.
Hackradt CW, García-Charton JA, Harmelin-Vivien M, Pérez-Ruzafa Á, Le Diréach L, Bayle-Sempere JT, Charbonnel É, Ody D, Reñones O, Sánchez-Jerez P, Valle C. 2014. Response of rocky reef top predators (Serranidae: Epinephelinae) in and around marine protected areas in the western Mediterranean Sea. PLoS One 9 (6): e98206. https://doi.org/10.1371/journal.pone.0098206.
Hemingson CR, Mihalitsis M, Bellwood DR. 2022. Are fish communities on coral reefs becoming less colourful? Glob Change Biol 28 (10): 3321-3332. https://doi.org/10.1111/gcb.16095.
Hempson TN, Graham NAJ, MacNeil MA, Hoey AS, Almany GR. 2017. Mesopredator trophodynamics on thermally stressed coral reefs. Coral Reefs 37 (1): 135. https://doi.org/10.1007/s00338-017-1639-9.
Jankowski MW. 2022. Relationships among Depth Distributions, Habitat Specialisation and Demography in Coral Reef Fish Communities. James Cook University, Australia.
Kingsford M, Battershill C. 1998. Studying temparate marine environments: A handbook for ecologists. Canterbury University Press, New Zealand.
Kohler KE, Gill SM. 2006. Coral point count with Excel extensions (CPCe): A visual basic program for the determination of coral and substrate coverage using random point count methodology. Comput Geosci 32: 1259-1269. https://doi.org/10.1016/j.cageo.2005.11.009.
Komyakova V, Munday PL, Jones GP. 2013. Relative importance of coral cover, habitat complexity and diversity in determining the structure of reef fish communities. PLoS One 8 (12): e0083178. https://doi.org/10.1371/journal.pone.0083178.
Lim APK, Ali A, Zakaria NA, Noor MS. 2018. Field guide to fishes and crustaceans of the Southeast Asian region. Jabatan Perikanan Malaysia, Putrajaya.
Liu M, Sadovy Y. 2005. Habitat association and social structure of the chocolate hind Cephalopholis boenak (Pisces: Serranidae: Epinephelinae) at Ping Chau Island, northeastern Hong Kong waters. Environ Biol Fish 74 (1): 9. https://doi.org/10.1007/s10641-005-2258-9.
Manojkumar PP, Ranjith L, Karuppasamy K, Kanthan KP. 2019. Fishery and population dynamics of Epinephelus malabaricus off Tuticorin, southeast coast of India. J Mar Biol Assoc India 61 (1): 26. https://doi.org/10.6024/jmbai.2019.61.1.2072-03.
Matsunuma M, Motomura H, Matsuura K, Shazili NAM, Ambak MA, eds. 2011. Fishes of Terengganu: East coast of Malay Peninsula, Malaysia. National Museum of Nature and Science, Tokyo.
Mehanna SF, Al-Marzouqi A, El-Siabi B. 2013. Stock characteristics and population dynamics of the spiny cheek grouper Epinephelus diacanthus from Arabian Sea, Oman. Turk J Fish Aquat Sci 13: 127-132.
Meyer AL, Dierking J. 2011. Elevated size and body condition and altered feeding ecology of the grouper Cephalopholis argus in non-native habitats. Mar Ecol Prog Ser 439: 203-213. https://doi.org/10.3354/meps09338.
Mitcheson YS, Craig MT, Bertoncini AA, Carpenter KE, Cheung WW, Choat JH, Sanciangco J. 2013. Fishing groupers towards extinction: A global assessment of threats and extinction risks in a billion-dollar fishery. Fish Fish 14 (2): 119-136. https://doi.org/10.1111/j.1467-2979.2011.00455.x.
Mitcheson YS, Craig M, Bertoncini A, Carpenter K, Cheung W, Choat J, Cornish A, Fennessy S, Ferreira B, Heemstra P, Liu M, Myers R, Pollard D, Rhodes K, Rocha L, Russell B, Samoilys M, Sanciangco J. 2013. Fishing groupers towards extinction: A global assessment of threats and extinction risks in a billion-dollar fishery. Fish Fish 14 (2): 119-136. https://doi.org/10.1111/j.1467-2979.2011.00455.x.
Mitcheson YS, Liu M. 2022. The importance of grouper and threats to their future. In: Félix-Hackradt FC, Hackradt CW, García-Charton JA (eds). Biology and Ecology of Groupers. CRC Press, Boca Raton.
Mitcheson YS, Colin PL. 1995. Sexual development and sexuality in the Nassau grouper. J Fish Biol 46: 961-976. https://doi.org/10.1111/j.1095-8649.1995.tb01401.x.
Montgomery AD, Fenner D, Donahue MJ, Toonen RJ. 2021. Community similarity and species overlap between habitats provide insight into the deep reef refuge hypothesis. Sci Rep 11 (1): 23787. https://doi.org/10.1038/s41598-021-03128-8.
Mwijage AP, Shilla DA, Machiwa JF. 2018. Differences in trophic resources and niches of two juvenile predatory species in three Pangani estuarine zones, Tanzania. J Biol Res-Thessalon 25: 13. https://doi.org/10.1186/s40709-018-0084-4.
Nanami A, Sato T, Takebe T, Teruya K, Soyano K. 2013. Microhabitat association in white-streaked grouper Epinephelus ongus: Importance of Acropora spp. Mar Biol 160 (6): 1511. https://doi.org/10.1007/s00227-013-2205-9.
Nanami A. 2021. Spatial distribution of parrotfishes and groupers in an Okinawan coral reef: size-related associations in relation to habitat characteristics. PeerJ 9: 12134. https://doi.org/10.7717/peerj.12134.
Pears R. 2005. Comparative Demography and Assemblage Structure of Serranid Fishes: Implications for Conservation and Fisheries Management. James Cook University, Australia.
Pothin K, Letourneur Y, Lecomte-Finiger R. 2004. Age, growth and mortality of the tropical grouper Epinephelus merra (Pisces, Serranidae) on Réunion Island, SW Indian Ocean. Vie et Milieu 54 (4): 193-202. [French]
Pranata B, Kusuma AB, Azhar MI. 2022. Reef fish species diversity using environmental DNA metabarcoding in Mansinam and Lemon Island waters, Manokwari Regency. J Fish Sci 24 (2): 129-138. https://doi.org/10.22146/jfs.73037.
Prihatiningsih P, Edrus IN, Hartati ST. 2019. Parameter populasi ikan kerapu karang bintik biru (Cephalopholis cyanostigma) di perairan Karimunjawa, Jawa Tengah. Bawal 11 (1): 59-68. https://doi.org/10.15578/bawal.11.1.2019.59-68. [Indonesian]
Prodon R, Lebreton J. 1994. Analyses multivariées des relations espèces-milieu: Structure et interprétation écologique. Vie et Milieu 44: 69-91. [French]
R Development Core Team. 2014. R: A language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Reef Check Malaysia. 2015. Status of Coral Reefs in Malaysia, 2014. Reef Check Malaysia Bhd, Kuala Lumpur.
Rhodes KL, Amorim P, Choat J, Law C, Yan K, Myers RA, Nair RJ, Russell BD, Samoilys M, Suharti S, To A. 2018. Epinephelus corallicola, Coral Grouper. CMFRI, Kochi, Kerala, India.
Richardson LE, Graham NAJ, Hoey AS. 2017. Cross-scale habitat structure driven by coral species composition on tropical reefs. Sci Rep 7 (1): 7557. https://doi.org/10.1038/s41598-017-08109-4.
Richardson LE, Graham NAJ, Pratchett MS, Hoey AS. 2017. Structural complexity mediates functional structure of reef fish assemblages among coral habitats. Environ Biol Fish 100 (3): 193. https://doi.org/10.1007/s10641-016-0571-0.
Rumeaida MP, Daud SMM, Badri FMI. 2014. Fish diversity and abundance in Bidong Island, South China Sea, Malaysia. AACL Bioflux 7 (3): 176-183.
Safuan M, Boo WH, Siang HY, Chark LH, Bachok Z. 2015. Optimization of coral video transect technique for coral reef survey: Comparison with intercept transect technique. Open J Mar Sci 5 (4): 379-397. https://doi.org/10.4236/ojms.2015.54031.
Scales H, Balmford A, Manica A. 2007. Impacts of the live reef fish trade on populations of coral reef fish off northern Borneo. Proc R Soc B 274 (1612): 989-994. https://doi.org/10.1098/rspb.2006.0280.
Seraphim MJ, Sloman KA, Alexander ME, Janetski N, Jompa J, Ambo-Rappe R, Harborne AR. 2020. Interactions between coral restoration and fish assemblages: Implications for reef management. J Fish Biol 97 (3): 633-655. https://doi.org/10.1111/jfb.14440.
Shapiro SS, Wilk MB. 1965. An analysis of variance test for normality (complete samples). Biometrika 52: 591-611. https://doi.org/10.1093/biomet/52.3-4.591.
Shpigel M, Fishelson L. 1989. Habitat partitioning between species of the genus Cephalopholis (Pisces, Serranidae) across the fringing reef of the Gulf of Aqaba (Red Sea). Mar Ecol Prog Ser 58: 17-22. https://doi.org/10.3354/meps058017.
Shpigel M, Fishelson L. 1991. Territoriality and associated behaviour in three species of the genus Cephalopholis (Pisces: Serranidae) in the Gulf of Aqaba, Red Sea. J Fish Biol 38 (6): 887-901. https://doi.org/10.1111/j.1095-8649.1991.tb03628.x.
Siqueira AC, Morais RA, Bellwood DR, Cowman PF. 2020. Trophic innovations fuel reef fish diversification. Nat Commun 11 (1): 2669. https://doi.org/10.1038/s41467-020-16498-w.
Sluka R. 2001. Influence of habitat on grouper abundance in the Florida Keys, USA. J Fish Biol 58 (3): 682. https://doi.org/10.1006/jfbi.2000.1478.
Smallhorn-West P, Bridge TCL, Munday PL, Jones GP. 2017. Habitat morphology constrains the depth distribution and growth rate of a coral-associated reef fish. Mar Ecol Prog Ser 576: 43. https://doi.org/10.3354/meps12226.
Somerfield PJ. 2008. Identification of the Bray-Curtis similarity index: Comment on Yoshioka (2008). Mar Ecol Prog Ser 372: 303-306. https://doi.org/10.3354/meps07841.
Stewart BD, Jones GP. 2001. Associations between the abundance of piscivorous fishes and their prey on coral reefs: Implications for prey-fish mortality. Mar Biol 138 (2): 383. https://doi.org/10.1007/s002270000468.
Stewart BD. 1998. Interactions between Piscivorous Coral Reef Fish and Their Prey. James Cook University, Australia.
Sugama K, Tridjoko T, Haryanti H, M SB, Cholik F. 2017. Genetic variation and population structure in the humpback grouper Cromileptes altivelis throughout its range in Indonesian waters. Indones Fish Res J 5 (1): 32-38. https://doi.org/10.15578/ifrj.5.1.1999.32-38.
Tuohy E, Schärer-Umpierre M, Penrod L, Appeldoorn RS. 2023. Home range, space use, and vertical distribution of Nassau grouper (Epinephelus striatus) during non-spawning times in western Puerto Rico. Front Mar Sci 10 (6): 70. https://doi.org/10.3389/fmars.2023.1206070.
Yulianto I, Wiryawan B, Taurusman AA. 2013. Responsible grouper fisheries in Weh Island, Aceh Province, Indonesia. Galaxea J Coral Reef Stud 15: 269-276. https://doi.org/10.3755/galaxea.15.269.
Zeller D. 1997. Home range and activity patterns of the coral trout Plectropomus leopardus (Serranidae). Mar Ecol Prog Ser 154: 65. https://doi.org/10.3354/meps154065.