Population structure of commercially important groupers in the coral triangle Gorontalo, Indonesia to support conservation

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DEWI SHINTA ACHMAD
MUH. SALEH NURDIN
IVAN TASLIM
ABIGAIL M. MOORE

Abstract

Abstract. Achmad DS, Nurdin MS, Taslim I, Moore AM. 2023. Population structure of commercially important groupers in the coral triangle Gorontalo, Indonesia to support conservation. Biodiversitas 24: 6592-6601. Appropriate management units are fundamental to the conservation of species and ecosystems. In the case of exploited fishes, sustainable approaches to fisheries management are generally based on population units (stocks). This study aimed to address the lack of data to define the population structure of the stocks of two commercially important grouper species (Variola albimarginata (Baissac, 1953) and Variola louti (Forsskål, 1775)) in the Sulawesi Sea and Tomini Bay waters of Gorontalo Province, Sulawesi, Indonesia, in the Wallacea biodiversity hotspot. We used a combined morphometric and molecular (DNA barcoding, COI marker). We used truss network analysis with 14 characters to evaluate inter and intraspecies morphometric differences. DNA was extracted (Qiagen protocols) from tissue samples from individuals of both species in both sea areas, followed by polymerase chain reaction (PCR) and Sanger sequencing. Sequence processing and phylogenetic analyses conducted in MEGA X. Both approaches show clear separation between V. albimarginata and V. louti but indicate close kinship between the north coast (Sulawesi Sea) and south coast (Tomini Bay) populations of these groupers. Under the authority of the Gorontalo Province Marine and Fisheries Service, these two populations could be managed as one stock without compromising fisheries sustainability or the conservation of these ecologically and economically valuable species.

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References
Abdullah A, Rehbein H. 2016. DNA barcoding for the species identification of commercially important fishery products in Indonesian markets. Intl J Food Sci Technol 52: 266-274. DOI: 10.1111/ijfs.13278.
Abesamis RA, Saenz-Agudelo P, Berumen ML, Bode M, Jadloc CRL, Solera LA, Villanoy CL, Bernardo LPC, Alcala AC, Russ GR. 2017. Reef-fish larval dispersal patterns validate no-take marine reserve network connectivity that links human communities. Coral Reefs 36: 791-801. DOI: 10.1007/s00338-017-1570-0.
Abinawanto, Sriyani ED, Bowolaksono A. 2018. Characterization of Sentani gudgeon, Oxyeleotris heterodon (Weber, 1907) at Sentani Lake, Papua, Indonesia based on truss morphometric. Biodiversitas 19: 1013-1020. DOI: 10.13057/biodiv/d190333.
Achmad DS, Sudirman, Jompa J, Nurdin MS. 2020. Estimating the catchable size of orange-spotted grouper (Epinephelus coioides) in Kwandang Bay, Gorontalo Utara District, Indonesia. IOP Conf Ser: Earth Environ Sci 473: 012133. DOI: 10.1088/1755-1315/473/1/012133.
Achmad DS, Gani S, Ardiansyah W, Mokoginta MM, Nurdin MS, Jompa J, Indrianti MA, Achmad N. 2022. Population dynamics of reef fish in the Kwandang Bay, Sulawesi Sea, Indonesia. Biodiversitas 23: 5217-5226. DOI: 10.13057/biodiv/d231030.
Achmad DS, Nurdin MS, Azmi F, Indrianti MA, Hulukati E, Jompa J, Haser TF, Achmad N. 2023. Species composition and growth pattern of a multi-species grouper in Kwandang Bay, Sulawesi Sea, Indonesia. Jurnal Ilmiah Perikanan dan Kelautan 15: 31-43. DOI: 10.20473/jipk.v15i1.36673. [Indonesian]
Afifah N, Zairion Z, Maduppa HH, Hakim AA, Wardiatno Y. 2020. Identifying blue swimming crab (Portunus pelagicus) stocks with truss network analysis approach in Indonesian Fisheries Management Area 712. J Nat Res Environ Manag 10: 390-401. DOI: 10.29244/jpsl.10.3.390-401.
Akbar N, Wibowo ES, Irfan M, Achmad MJ, Wahab I, Ramili Y, Paembonan RE, Baksir A, Tahir I, Ismail F, Najamuddin, Marus I, Siolimbona AA, Toha AHA, Subhan B. 2022. DNA barcoding and morphometric of Rastrelliger spp. in North Maluku Sea, Indonesia. Aceh J Anim Sci 7: 73-81. DOI: 10.13170/ajas.7.3.25872.
Alcantara SG, Yambot AV. 2016. DNA barcoding of commercially important grouper species (Perciformes, Serranidae) in the Philippines. Mitochondrial DNA Part A 27: 3837-3845. DOI: 10.3109/19401736.2014.958672.
Almany GR, Connolly SR, Heath DD, Hogan JD, Jones GP, McCock LJ, Mills M, Pressey RL, Williamson DH. 2009. Connectivity, biodiversity conservation and the design of marine reserve networks for coral reefs. Coral Reefs 28: 339-351. DOI: 10.1007/s00338-009-0484-x.
Almany GR, Hamilton RJ, Bode M, Matawai M, Potuku T, Saenz-Agudelo P, Planes S, Berumen ML, Rhodes KL, Thorrold SR, Russ GR, Jones GP. 2013. Dispersal of grouper larvae drives local resource sharing in a coral reef fishery. Curr Biol 23: 626-630. DOI: 10.1016/j.cub.2013.03.006.
Ambo-Rappe R, Moore AM. 2019. Sulawesi Seas, Indonesia. World Seas: An Environmental Evaluation. DOI: 10.1016/B978-0-08-100853-9.00032-4.
Ariyanto D, Listiyowati N, Imron I. 2011. Analisis truss morfometrik beberapa varietas ikan nila (Oreochromis niloticus). Jurnal Riset Akuakultur 6: 187-196. DOI: 10.15578/jra.6.2.2011.187-196. [Indonesian]
Baldwin CC, Mounts JH, Smith DG, Weigt LA. 2009. Genetic identification and color descriptions of early life-history stages of Belizean Phaeoptyx and Astrapogon (Teleostei: Apogonidae) with comments on identification of adult Phaeoptyx. Zootaxa 22: 1-22. DOI: 10.11646/zootaxa.2008.1.1.
Basheer VS, Vineesh N, Bineesh KK, Kumar RG, Mohitha C, Venu S, Kathirvelpandian A, Gopalakrishnan A, Jena JK. 2017. Mitochondrial signatures for identification of grouper species from Indian waters. Mitochondrial DNA Part A: DNA Mapp Seq Anal 28: 451-457. DOI: 10.3109/19401736.2015.1137899.
Basith A, Abinawanto, Kusrini E, Yasman. 2021. Genetic diversity analysis and phylogenetic reconstruction of groupers Epinephelus spp. from Madura Island, Indonesia based on partial sequence of CO1 gene. Biodiversitas 22: 4282-4290. DOI: 10.13057/biodiv/d221020.
Begg GA, Friedland KD, Pearce JB. 1999. Stock identification and its role in stock assessment and fisheries management: An overview. Fish Res 43: 1-8. DOI: 10.1016/S0165-7836(99)00062-4.
Bemis KE, Girard MG, Santos MD, Carpenter KE, Deeds JR, Pitassy DE, Flores NAL, Hunter ES, Driskell AC, Macdonald III KS, Weigt LA. 2023. Biodiversity of Philippine marine fishes: A DNA barcode reference library based on voucher specimens. Sci Data 10: 411. DOI: 10.1038/s41597-023-02306-9.
Cadrin SX, Karr LA, Mariani S. 2014. Stock Identification Methods: An Overview. Academic Press, Cambridge, Massachusetts. DOI: 10.1016/C2011-0-07625-1.
Condini MV, García-Charton JA, Garcia AM. 2018. A review of the biology, ecology, behavior and conservation status of the dusky grouper, Epinephelus marginatus (Lowe 1834). Rev Fish Biol Fisheries 28: 301-330. DOI: 10.1007/s11160-017-9502-1.
Damora A, Fadli N, Muchlisin ZA, Dewiyanti I, Batubara AS, Nur FM, Zhelfi Z, Roka NF, Fitriani F, Siti-Azizah MN. 2021. White-edged lyretail (Variola albimarginata): A preliminary study on some biological aspects. IOP Conf Ser: Earth Environ Sci 674: 012091. DOI: 10.1088/1755-1315/674/1/012091.
Dimarchopoulou D, Mous PJ, Firmana E, Wibisono E, Coro G, Humphries AT. 2021. Exploring the status of the Indonesian deep demersal fishery using length-based stock assessments. Fish Res 243: 106089. DOI: 10.1016/j.fishres.2021.106089.
Durand J-D, Pham MH, Tran TTV, Hoang DH, Van Vo Q. 2020. Sorting the wheat from the chaff: a review of BINs associated with groupers of Vietnam and the implications for species identification from DNA Barcoding. Mar Biodivers 50:38. DOI: 10.1007/s12526-020-01051-1.
Efendi DS, Adrianto L, Yonvitner, Wardiatno Y, Agustina S. 2020. The performance of stock indicators of grouper (Serranidae) and snapper (Lutjanidae) fisheries in Saleh Bay, Indonesia. AACL Bioflux 13: 2431-2444.
Ernawati T, Agustina S, Kembaren DD, Yulianto I, Satria F. 2021. Life history parameters and spawning potential ratio of some reef fish species in fisheries management area 715 of Indonesia. AACL Bioflux 14: 3092-3103.
Excoffier L, Laval G, Schneider S. 2005. Arlequin (Version 3.0): An integrated software package for population genetics data analysis. Evol Bioinform 1: 117693430500100. DOI: 10.1177/117693430500100003.
Fadli N, Muchlisin ZA, Siti-Azizah MN. 2021. DNA barcoding of commercially important groupers (Epinephelidae) in Aceh, Indonesia. Fish Res 234: 105796. DOI: 10.1016/j.fishres.2020.105796.
Food and Agriculture Organization [FAO]. 2022. Fishery and Aquaculture Statistics. Global capture production 1950-2022. FAO Fisheries and Aquaculture Department [online or CD-ROM]. FAO Fisheries and Aquaculture.
Félix-Hackradt FC, Hackradt CW, García-Charton JA. 2022. Biology and Ecology of Groupers. CRC Press, Boca Raton, Florida. DOI: 10.1201/b20814.
Frisch AJ, Cameron DS, Pratchett MS, Williamson DH, Williams AJ, Reynolds AD, Hoey AS, Rizzari JR, Evans L, Kerrigan B, Muldoon G. 2016. Key aspects of the biology, fisheries and management of coral grouper. Rev Fish Biol Fish 26: 303-325. DOI: 10.1007/s11160-016-9427-0.
Froese R, Pauly D. 2023. FishBase, The Global Database of Fishes. https://www.fishbase.se/search.php
Halim A, Wiryawan B, Loneragan NR, Hordyk A, Sondita MFA, White AT, Koeshendrajana S, Ruchimat T, Pomeroy RS, Yuni C. 2019. Developing a functional definition of small-scale fisheries in support of marine capture fisheries management in Indonesia. Mar Pol 100: 238-248. DOI: 10.1016/j.marpol.2018.11.044.
Halim A, Loneragan NR, Wiryawan B, Hordyk AR, Sondita MFA, Yulianto I. 2020. Evaluating data-limited fisheries for grouper (Serranidae) and snapper (Lutjanidae) in the Coral Triangle, eastern Indonesia. Reg Stud Mar Sci 38: 101388. DOI: 10.1016/j.rsma.2020.101388.
Han YS, Lin YF, Wu CR, Iizuka Y, Castillo TR, Yambot IU, Mamalangkap MD, Yambot AV. 2016. Biogeographic distribution of the eel Anguilla luzonensis: dependence upon larval duration and oceanic currents. Mar Ecol Prog Ser 551: 227-238. DOI: 10.3354/meps11728.
Hargiyatno IT, Faizah R. 2021. Population parameters of the yellow-edged lyretail (Variola louti, Forsskål, 1775) in Sibolga Waters. E3S Web Conf 322: 01015. DOI: 10.1051/e3sconf/202132201015.
Hawkins SJ, Bohn K, Sims DW, Ribeiro P, Faria J, Presa P, Pita A, Martins GM, Neto AI, Burrows MT, Genner MJ. 2016. Fisheries stocks from an ecological perspective: Disentangling ecological connectivity from genetic interchange. Fish Res 179: 333-341. DOI: 10.1016/j.fishres.2016.01.015.
Heemstra PC, Randall JE. 1993. Groupers of the world. An annotated and illustrated catalogue of the grouper, rockcod, hind, coral, grouper, and Lyretail species known to date. Food and Agriculture Organization of the United Nations, Rome.
Hidayani AA, Tassakka ACMAR, Umar W, Alam MJ, Neogi AK, Andriyono S. 2022. Low genetic diversity study on leopard coral grouper Plectropomus leopardus (Perciformes: Serranidae) from Sulawesi, Indonesia. Jurnal Ilmiah Perikanan dan Kelautan 14: 349-359. DOI: 10.20473/jipk.v14i2.32815. [Indonesian]
Jefri E, Zamani NP, Subhan B, Madduppa HH. 2015. Molecular phylogeny inferred from mitochondrial DNA of the grouper Epinephelus spp. in Indonesia collected from local fish market. Biodiversitas 16: 254-263. DOI: 10.13057/biodiv/d160221.
Kadir NN, Ala Husain AA, Priosambodo D, Jamal M, Moore AM. 2023. Diverse and predominantly sub-adult Epinephelus sp. groupers from small-scale fisheries in South Sulawesi, Indonesia. Fish Aquat Sci 26: 380-392. DOI: 10.47853/FAS.2023.e32.
Khasanah M, Kadir NN, Jompa J. 2019. Reproductive biology of three important threatened/near-threatened groupers (Plectropomus leopardus, Epinephelus polyphekadion and Plectropomus areolatus) in Eastern Indonesia and implications for management. Animals 9: 643. DOI: 10.3390/ani9090643.
Khasanah M, Nurdin N, Sadovy de Mitcheson Y, Jompa J. 2020. Management of the grouper export trade in Indonesia. Rev Fish Sci Aquacult 28: 1-15. DOI: 10.1080/23308249.2018.1542420.
Kocovsky PM, Sullivan TJ, Knight CT, Stepien CA. 2013. Genetic and morphometric differences demonstrate fine?scale population substructure of the yellow perch Perca flavescens: need for redefined management units. J Fish Biol 82: 2015-2030. DOI: 10.1111/jfb.12129.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35: 1547-1549. DOI: 10.1093/molbev/msy096.
Madduppa HH, Martaulina R, Zairion Z, Renjani RM, Kawaroe M, Anggraini NP, Subhan B, Verawati I, Sani LMI. 2021. Genetic population subdivision of the blue swimming crab (Portunus pelagicus) across Indonesia inferred from mitochondrial DNA Implication to sustainable fishery. PLoS ONE 16: e0240951. DOI: 10.1371/journal.pone.0240951.
Masumoto Y, Kagimoto T, Yoshida M, Fukuda M, Hirose N, Yamagata T. 2001. Intraseasonal eddies in the Sulawesi Sea simulated in an ocean general circulation model. Geophys Res Lett 28: 1631-1634. DOI: 10.1029/2000GL011835.
Mehanna SF, Osman YAA, Khalil MT, Hassan A. 2019. Age and growth, mortality and exploitation ratio of Epinephelus summana (Forsskål, 1775) and Cephalopholis argus (Schneider, 1801) from the Egyptian Red Sea Coast, Hurghada fishing area. Egypt J Aquat Biol Fish 23: 65-75. DOI: 10.21608/ejabf.2019.52050.
Michailidis N, Manitaras I, Bernardi G, Kleitou P. 2020. Variola louti (Perciformes?: Epinephelidae) in the Mediterranean Sea: Incidental introduction or aquarium release? J Appl Ichthyol 36: 231-234. DOI: 10.1111/jai.14001.
Ministry of Maritime Affairs and Fisheries [MMAF]. 2022. Export Statistics of Fishery Products for 2017-2021. Ministry of Maritime Affairs and Fisheries, Jakarta. [Indonesian]
Moore AM, Jompa J, Tassakka ACMAR, Yasir I, Ndobe S, Umar W, Gold Z, Barber PH. 2021. Sharks and rays (Chondrichthyes) around Banggai Island, Banggai MPA, Indonesia: Biodiversity data from an environmental DNA pilot study. AACL Bioflux 14: 725-745.
Muawanah U, Kurniasari N, Pramodha R, Zulham A, Rosyidah L. 2021. Assessment on the governance of fisheries management at fishery management area in Indonesia. IOP Conf Ser: Earth Environ Sci 716: 012022. DOI: 10.1088/1755-1315/716/1/012022.
Muchlisin ZA. 2013. Morphometric variations of rasbora group (Pisces: Cyprinidae) in Lake Laut Tawar, Aceh Province, Indonesia, based on truss character analysis. HAYATI J Biosci 20: 138-143. DOI: 10.4308/hjb.20.3.138.
Nadiarti N, Moore A, Abu N, Rahim SW, Chasanah M. 2021. Ecosystems Approach to Fisheries Management (EAFM) assessment for grouper and snapper fisheries in Bontang, East Kalimantan, Indonesia. IOP Conf Ser: Earth Environ Sci 763: 012031. DOI: 10.1088/1755-1315/763/1/012031.
Nair R, Samoilys M, Cabanban AS. 2018. Variola louti (yellow-edged lyretail). The IUCN Red List of Threatened Species 2018: e.T132738A100572909. DOI: 10.2305/IUCN.UK.2018- 2.RLTS.T132738A100572909.en
National Center for Biotechnology Information [NCBI]. 2016. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 44: D7-D19. DOI: 10.1093/nar/gkv1290.
Ndobe S, Moore A. 2013. Banggai cardinalfish (Pterapogon kauderni) populations (stocks) around Banggai Island, a geometric and classical morphometric approach. PeerJ PrePrints 1: e182v1. DOI: 10.7287/peerj.preprints.182v1.
Nei M. 1972. Genetic distance between populations. Am Nat 106: 283-292. DOI: 10.7312/nei-92038-010.
Nurkhozin AA, Achmad DS, Bakti NS, Yasin IA, Natsir SRA. 2022. Prevalence of Viral Nervous Necrosis (VNN) in lunar-tailed grouper (Variola sp.) in Gorontalo Waters. Jurnal Ilmu Perikanan dan Kelautan 4: 99-108. DOI: 10.36526/lemuru.v4i3.2295. [Indonesian]
Palma J, Andrade JP. 2002. Morphological study of Diplodus sargus, Diplodus puntazzo, and Lithognathus mormyrus (Sparidae) in the Eastern Atlantic and Mediterranean Sea. Fish Res 57: 1-8. DOI: 10.1016/S0165-7836(01)00335-6.
Pane ARP, Widyastuti H, Suman A. 2021. The exploitation status of the slender grouper (Anyperodon leucogrammicus) in Arafura Sea, Indonesia. IOP Conf Ser: Earth Environ Sci 695: 012002. DOI: 10.1088/1755-1315/695/1/012002.
Pertiwi NPD, Hidayat NI, Henderson C, Putra I, Sembiring A. 2019. Redefining dispersal boundaries of Siganus fuscescens in the coral triangle area. J Mar Sci/Ilmu Kelautan 24: 31-40. DOI: 10.14710/ik.ijms.24.1.31-40. [Indonesian]
Razi NM, Muchlisin ZA, Maulida S, Ramadhaniaty M, Nur FM, Damora A, Manalu SLB, Fadli N. 2021. Grouper DNA barcoding studies in Indonesia: A short review. Depik 10: 186-193. DOI: 10.13170/depik.10.2.21255.
Rodriguez-Dominguez A, Connell SD, Coni EOC, Sasaki M, Booth DJ, Nagelkerken I. 2022. Phenotypic responses in fish behaviour narrow as climate ramps up. Clim Change 171: 1-18. DOI: 10.1007/s10584-022-03341-y.
Sadovy de Mitcheson YJ, Cornish A, Domeier M, Colin PL, Russell M, Lindeman KC. 2008. A global baseline for spawning aggregations of reef fishes. Conserv Biol 22: 1233-1244. DOI: 10.1111/j.1523-1739.2008.01020.x.
Sadovy de Mitcheson YJ, Cabanban AS, Fennessy S, Myers R, Pollard DA, Rhodes K. 2018. Variola albimarginata, white-edged lyre tail. the IUCN Red List of threatened species 2018.
Safira A, Zairion Z, Mashar A. 2019. Analysis morphometric diversity of blue swimming crab (Portunus pelagicus Linnaeus, 1758) in FMA 712 as a base management. J Trop Fish Manag 3: 9-19. DOI: 10.29244/jppt.v3i2.30175.
Santoso SY, Atmadipoera AS, Nurjaya IW, Nugroho D, Koch-Larrouy A. 2022. Simulated ocean circulation from INDESO data in the region of the Gulf of Tomini. Ilmu Kelautan 27: 223-232. DOI: 10.14710/ik.ijms.27.3.223-232. [Indonesian]
Selkoe KA, Aloia CC, Crandall ED, Iacchei M, Liggins L, Puritz JB, von der Heyden S, Toonen RJ. 2016. A decade of seascape genetics: contributions to basic and applied marine connectivity. Mar Ecol Prog Ser 554: 1-19. DOI: 10.3354/meps11792.
Timm J, Kochzius M. 2008. Geological history and oceanography of the Indo?Malay Archipelago shape the genetic population structure in the false clown anemonefish (Amphiprion ocellaris). Mol Ecol 17: 3999-4014. DOI: 10.1111/j.1365-294X.2008.03881.x.
Valenzuela-Quiñonez F. 2016. How fisheries management can benefit from genomics?. Briefings Funct Genomics 15: 352-357. DOI: 10.1093/bfgp/elw006.
von der Heyden S, Beger M, Toonen RJ, van Herwerden L, Juinio-Meñez MA, Ravago-Gotanco R, Fauvelot C, Bernardi G. 2014. The application of genetics to marine management and conservation: examples from the Indo-Pacific. Bull Mar Sci 90: 123-158. DOI: 10.5343/bms.2012.1079.
von der Heyden S. 2017. Making evolutionary history count: biodiversity planning for coral reef fishes and the conservation of evolutionary processes. Coral Reefs 36: 183-194. DOI: 10.1007/s00338-016-1512-2.

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