23南太平洋海域調査研究報告
OCCASIONAL PAPERS

No.58（2017 年 3 月）
No.58（March 2017）

The Diversity of Grouper (Epinephelinae)
in Ambon Island, Maluku, Indonesia
LIMMON Gino V.1, 2, RIJOLY Frederik1, 2, KHOUW Abraham S.1, 2, MANUPUTTY Gratia D.1, 2 andPATTIKAWA Jesaya A.1, 2
1: Maritime and Marine Science Center of Excellence, Pattimura University
2: Faculty of Fisheries and Marine Science, Pattimura University

Abstract
Located in the heart of world’s coral triangle, Maluku seas were estimated to harbor around 1,500
species of fish, which make Maluku seas one of the highest in fish diversity. However, the data to support
this claim is not yet available. In this report, we focused our research on the diversity of grouper (familySerranidae, subfamily Epinephelinae) that have the highest economic value and usually exported to various
countries around the world. Our preliminary research on diversity of groupers landed at fish market around
Ambon Island showed astonishing result. We identified 36 species of groupers that belong to 9 genera.
Importantly, two of the species Epinephelus ergastularius Whitley 1930 and Saloptia powelli Smith 1964
were never reported to be found in Indonesia and can be potentially be declared as a new record.
Furthermore, there is one species Cephalopholis igarashiensis Katayama 1957 that has been found in North
Sulawesi but never reported to be found in Maluku waters. The mitochondrial DNA of the above mentioned
species are being sequenced and will be reported in a separated report. Our results will have a great
contribution in building a new database on the diversity of fish in Maluku and will provide new information
to revise the geographical distribution of groupers.
Keywords: coral fish, fisheries, geographical distribution, management, Serranidae

Introduction
Epinephelinae is Subfamily of Serranidae, a large family of fishes from Order
Perciformes that comprises about 450 species in 65 genera. They are recognized as groupers.
Fishes belong to this group have considerable high economic value. Groupers are among themost marketable group of tropical marine fish. They have high prices at markets andconsequently become the main target in fisheries industry (BEETS and HIXON 1994, MORRIS etal. 2000, RANDALL 1987, SLUKA and REICHENBACH 1996). The taste and high market value
are some of the reasons that cause this group becoming the most important mariculturecommodity in Asia and around the world (CHIU et al. 2008, JEFRI et al. 2015).

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LIMMON Gino V., RIJOLY Frederik, KHOUW Abraham S., MANUPUTTY Gratia D. and PATTIKAWA Jesaya A.

The subfamily Epinephelinae has approximately 159 species in 15 genera (HEEMSTRAand RANDALL 1993, MORRIS et al. 2000). The group populates a wide range of habitats andexhibits a wide variety of reproductive and growth strategies (JOHANNES 1978, MORRIS et al.
2000, SHAPIRO 1987). Some species have a home range larger than 1.8 ha and can migrate ina distance up to 2 km (SAMOILYS 1987, SAMOILYS et al. 1997, UNSWORTH et al. 2007).
Groupers play key function in structuring coral reef communities due to its role as top
predatory fish feeding on fish. A thriving and productive reef community is indicated by alarge grouper population. However, the population is intensely exploited (BOHNSACK 1994,
CHIAPPONE et al. 2000, COSTA et al. 2003, UNSWORTH et al. 2007). Currently, some species ofgroupers such as Giant Grouper (Epinephelus lanceolatus), Mouse Grouper (Cromileptesaltivelis) and Brown Marbled Grouper (Epinephelus fuscoguttatus) are listed as vulnerable,threatened and near-threatened, respectively, based on the Red Data listed by IUCN(RODRIGUES et al. 2010). Some researches have been conducted to explore the biodiversity ofgroupers around the world. HEEMSTRA et al. (2002), for example, describes groupers inAtlantic Sea. The result is quite comprehensive, comprises diagnostic character, size, habitat,biology, fisheries, distribution, remarks and key identification to species level. On the otherhand, other researches concerning phylogenetic relationship that are still poorly understood
due to the high variety of taxa that must be considered. Information about the relationships
among the Serranidae has been equally limited (CRAIG and HASTINGS 2007, JEFRI et al.
2015).
Evaluation of genetic diversity and phylogeny using modern molecular biology
techniques has enabled comparisons between nucleotide and amino acid sequences ofdifferent populations. Studies in fish taxonomy using DNA markers have been developed byfor example RODRIGUES et al. (2010) that utilized microsatellite markers for the identificationof some groupers including E. lanceolatus, C. altivelis and E. fuscoguttatus. Recently, the useof molecular phylogenetic approach has been widely accomplished by the newly developed
DNA barcoding method. However, identification of fish species based on morphological trait
still play important role and irreplaceable especially when the access to sophisticatedmolecular biology equipment is limited.

Materials and Methods
This research was conducted from April to November 2016 in Ambon Island, Maluku,Indonesia. Coral reef fish were collected at fish markets around Ambon Island (Fig. 1). Three
to five specimens from each species were bought and kept in the cool box filled with ice tomaintain the integrity of DNA. To avoid redundancy in sampling, list of species collected
were developed following each sampling activity. The sellers were interviewed to collect data

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The Diversity of Grouper (Epinephelinae) in Ambon Island, Maluku, Indonesia

for biogeography distribution. Samples from other islands were separated. Samples were thenbrought to marine ecology laboratory, at Maritime and Marine Science Center of Excellence,
Pattimura University. Each specimen was measured, tagged, then laid on styrofoam. The finswere spread with nail and arranged for photograph. The tissue samples were then collectedand stored in 95% ethanol for DNA extraction. The reef fish found were identified to thespecies level based on ALLEN (2000), KUITER and TONOZUKA (2001), ALLEN et al. (2003),
KUITER and DEBELIUS (2006) and ALLEN and ERDMANN (2012). Samples were then stored in
4% formalin for long term storage.

Results and Discussion
It is widely known that landings of marine fishes in the markets are not similar but
depended on natural abundance, consumer preference, geography, history and ease of catch.
Consequently, in areas surrounded by coral reef ecosystems, high diversity of species isharvested with various fishing techniques. Usually fish landed in the fish markets of theseareas including snappers (Lutjanidae), surgeonfishes and unicornfishes (Acanthuridae),parrotfishes (Labridae), emperor breams (Lethrinidae) and groupers (Epinephelinae) (GARCIAand ROSENBERG 2010, SALAS et al. 2007). Among them, groupers are known to be heavily
exploited, because they have the highest market price (CHIAPPONE et al. 2000, SADOVY 1994).
The consequence of dropping grouper fisheries sometimes devastated for many coastal
communities and ecosystems especially for those that depend solely on fisheries.

Fig. 1. Map of fish markets in Ambon Island.

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LIMMON Gino V., RIJOLY Frederik, KHOUW Abraham S., MANUPUTTY Gratia D. and PATTIKAWA Jesaya A.

Strikingly, despite the reports of decreasing groupers population in Indonesia, we found
36 species of groupers (Epinephelinae) that belong to 9 genera during the study in fishmarkets of Ambon Island (Table 1). The diversity of groupers found in our study is higher thatfound in similar studies conducted by RHODES and TUPPER (2007) that found 24 species ofgroupers in fish markets of Pohnpei, Micronesia and ALCANTARA and YAMBOT (2016) that
identified 27 species of groupers from major fish landing sites and markets in the Philippines.
Interestingly, two of the species found in Ambon fish markets Epinephelus ergastularius
Whitley 1930 and Saloptia powelli Smith 1964 were never reported to be found in Indonesia
and can be potentially declared as a new record. Epinephelus ergastularius Whitley 1930 isalso known as sevenbar grouper that usually inhabits deep rocky reefs. The original name ofthis species was recently changed to Hyporthodus ergastularius (CRAIG and HASTINGS 2007,
SMITH and CRAIG 2007). This species was previously reported to be found only in Southwest
Pacific and the Eastern coast of Australia. Saloptia powelli Smith 1964 with common namegolden grouper was reported to be found in Pacific Ocean, Western Pacific and French
Polynesia. This species has been found in Taiwan, Okinawa (Japan), the Mariana Islands, theSociety Islands, American Samoa, Samoa, the Cook Islands, Federated States of Micronesia,French Polynesia, Fiji, Kiribati, New Caledonia, Niue, Palau, Papua New Guinea, the Solomon
Islands, South China Sea, Tokelau, Tonga, Tuvalu, the Tuamotu Islands and Vanuatu(HEEMSTRA and RANDALL 1993). This species is widely known to inhabit deep rocky reefs.

Table 1. Groupers found at fish markets in Ambon Island.

No. FamilySpecies
1 Serranidae Aethaloperca rogaa
2 Serranidae Anyperodon leucogrammicus

No. Family
19 Serranidae
20 Serranidae

Species
Epinephelus coralicola
Epinephelus cyanopodus

345Serranidae Cephalopholis argus
Serranidae Cephalopholis aurantia
Serranidae Cephalopholis boenak

21 Serranidae
22 Serranidae
23 Serranidae

Epinephelus epistictus
Epinephelus ergastularius
Epinephelus fasciatus

6789Serranidae
Serranidae
Serranidae
Serranidae

Cephalopholis cyanostigma
Cephalopholis igarashiensis
Cephalopholis miniata
Cephalopholis nigripinis

2425
2627

Serranidae
Serranidae
Serranidae
Serranidae

Epinephelus faveatus
Epinephelus maculatus
Epinephelus melanostigma
Epinephelus merra

10111213

Serranidae
Serranidae
Serranidae
Serranidae

Cephalopholis polleni
Cephalopholis sexmaculata
Cephalopholis spiloparaea
Cephalopholis urodeta

28293031Serranidae
Serranidae
Serranidae
Serranidae

Epinephelus ongus
Epinephelus quoyanus
Epinephelus spilotoceps
Gracila albomarginata

14 Serranidae Epinephelus amblycephalus
15 Serranidae Epinephelus areolatus
16 Serranidae Epinephelus bilobatus

32 Serranidae
33 Serranidae
34 Serranidae

Liopropoma lemniscatum
Pogonoperca punctata
Saloptia powelli

17 Serranidae Epinephelus caeruleopunctatus
18 Serranidae Epinephelus coioides

35 Serranidae
36 Serranidae

Variola albimarginata
Variola louti

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The Diversity of Grouper (Epinephelinae) in Ambon Island, Maluku, Indonesia

Furthermore, there is one species Cephalopholis igarashiensis Katayama 1957 that has beenfound in North Sulawesi waters but never reported to be found in Maluku waters. Previously,
this species has been reported to be found in Tropical Western Pacific, Southern Japan, Taiwan,
Guam, Philippines, South China Sea, Samoa and Tahiti (PERISTIWADY et. al. 2009). Our results
will have a great contribution in building a new database on the diversity of fish in Maluku
and will provide new information to revise the geographical distribution of groupers.
Given that fishing pressure is the major driver of population declines in most threatenedgrouper species, it must be addressed to move towards their recovery. Grouper management
has been attempted in various ways, ranging from minimum size limits to protect juvenile fish,
recreational bag limits and commercial fishing quotas, gear and seasonal controls, marine
protected areas, to limited entry fisheries and slot sizes. Moreover, the establishment ofno-take-area (NTA) has been shown to be effective management strategy to increase thepopulation and help maintain and increase the grouper stocks.

Acknowledgement
We would like to thank Ministry of Research Technology and Higher Education andPattimura University for funding this research through UPT Research Grant from DIPARISTEKDIKTI (2016).

References
ALCANTARA, S. G. and YAMBOT, A. V. 2016. DNA Barcoding of Commercially ImportantGrouper Species (Perciformes, Serranidae) in the Philippines. Mitochondrial DNA Part A
DNA Mapping, Sequencing, and Analysis, 27(6): 3837–3845.
ALLEN, G. R. 2000. Marine Fishes of South-East Asia: A Field Guide for Anglers and Divers,
292 pp., Periplus Editions (HK) Ltd., Hong Kong, China.
ALLEN, G. R., STEENE, R., HUMANN, P. and DELOACH, N. 2003. Reef Fish Identification,
Tropical Pacific, 457 pp., New World Publications Inc., Jacksonville, Florida, USA.
ALLEN, G. R. and ERDMANN, M. V. 2012. Reef Fishes of the East Indies, Vol. I–III, 1260 pp.,
Tropical Reef Research, Perth, Australia in cooperation with Conservation International,Indonesia Marine Program, Denpasar, Indonesia.
BEETS, J. and HIXON, M. A. 1994. Distribution, Persistence, and Growth of Groupers (Pisces:Serranidae) on Artificial and Natural Patch Reefs in the Virgin Islands. Bulletin ofMarine Science, 55(2–3): 470–483.

28
LIMMON Gino V., RIJOLY Frederik, KHOUW Abraham S., MANUPUTTY Gratia D. and PATTIKAWA Jesaya A.

BOHNSACK, J. A. 1994. The Impacts of Fishing on Coral Reefs. In: Proceedings of theColloquium on Global Aspects of Coral Reefs: Health Hazards and History (Ed.
Ginsburg, R. F.), 169–199, RSMAS, University of Miami, Coral Gables, Florida, USA.
CHIAPPONE, M., SLUKA, R. and SEALEY, K. S. 2000. Groupers (Pisces: Serranidae) in Fishedand Protected Areas of the Florida Keys Bahamas and Northern Caribbean. MarineEcology Progress Series, 198: 261–272.
CHIU, S. T., TSAI, R. T., HSU, J. P., LIU, C. H. and CHENG, W. 2008. Dietary Sodium Alginate
Administration to Enhance the Non-Specific Immune Responses, and Disease Resistanceof the Juvenile Grouper Epinephelus fuscoguttatus. Aquaculture, 277: 66–72.
COSTA, P. A. S., BRAGA, A. D. and DA ROCHA, L. O. F. 2003. Reef Fisheries in Porto Seguro,Eastern Brazilian Coast. Fisheries Research, 60: 577–583.
CRAIG, M. T. and HASTINGS, P. A. 2007. A Molecular Phylogeny of the Groupers of theSubfamily Epinephelinae (Serranidae) with a Revised Classification of the Epinephelini.
Ichthyological Research, 54: 1–17.
GARCIA, S. M. and ROSENBERG, A. A. 2010. Food Security and Marine Capture Fisheries:
Characteristics, Trends, Drivers and Future Perspectives. Philosophical Transactions ofthe Royal Society B, 365(1554): 2869–2880.
HEEMSTRA, P. C., ANDERSON, W. D. and LOBEL, P. S. 2002. Serranidae: Groupers (Seabasses,Creolefish, Coney, Hinds, Hamlets, Anthiines, and Soapfishes). In: The Living Marine
Resources of the Western Central Atlantic, Volume 2: Bony Fishes Part 1 (Acipenseridaeto Grammatidae) (Ed. CARPENTER, K. E.), 1308–1369, FAO Species Identification Guidefor Fishery Purposes and American Society of Ichthyologists and Herpetologists SpecialPublication No. 5, FAO, Rome, Italy.
HEEMSTRA, P. C. and RANDALL, J. E. 1993. FAO Species Catalogue Vol. 16, Groupers of theWorld (Family Serranidae, Subfamily Epinephelinae), an Annotated and Illustrated
Catalogue of the Grouper, Rockcod, Hind, Coral Grouper and Lyretail Species Known toDate, FAO Fisheries Synopsis No. 125, 522 pp., FAO, Rome, Italy.
JEFRI, E., ZAMANI, N. P., SUBHAN, B. and MADDUPA, H. H. 2015. Molecular PhylogenyInferred from Mitochondrial DNA of the Grouper Epinephelus spp. in Indonesia
Collected from Local Fish Market. Biodiversitas, 16(2): 254–263.
JOHANNES, R. E. 1978. Reproductive Strategies of Coastal Marine Fishes in the Tropics.
Environmental Biology of Fishes, 3(1): 65–84.
KUITER, R. H. and TONOZUKA, T. 2001. Pictorial Guide to: Indonesian Reef Fishes, Vol. I–III,
893 pp., Zoonetics, Seaford, Australia.
KUITER, R. H. and DEBELIUS, H. 2006. World Atlas of Marine Fishes, 720 pp.,
IKAN-Unterwasserarchiv, Frankfurt, Germany.
MORRIS, A. V., ROBERTS, C. M. and HAWKINS, J. P. 2000. The Threatened Status of Groupers(Epinephelinae). Biodiversity and Conservation Journal, 9: 919–942.

29
The Diversity of Grouper (Epinephelinae) in Ambon Island, Maluku, Indonesia

PERISTIWADY, T., RAHARDJO, M. F. and SIMANJUNTAK, C. P. H. 2009. A New Record ofCephalopholis igarashiensis Katayama, 1957 (Perciformes, Serranidae) from Indonesia.
Jurnal Iktiologi Indonesia, 9 (1): 25–33.
RANDALL, J. E. 1987. A Preliminary Synopsis of the Groupers (Perciformes: Serranidae:Epinephelinae) of the Indo-Pacific Region. In: Tropical Snappers and Groupers: Biology
and Fisheries Management (Eds. POLOVINA, J. J. and RALSTON, S.), 89–189, Westview
Press, Boulder, Colorado, USA.
RHODES, K. L. and TUPPER, M. H. 2007. A Preliminary Market-Based Analysis of the Pohnpei,
Micronesia, Grouper (Serranidae; Epinephelinae) Fishery Reveals Unsustainable Fishing
Practices. Coral Reefs, 26: 335–344.
RODRIGUES, K. F., SHIGEHARU, S. and CH’NG, C. L. 2010. Microsatellite Markers for theIdentificationof

Commercially

ImportantGroupers

Epinephelus

lanceolatus,

Cromileptes altivelis and Epinephelus fuscoguttatus. Pertanika Journal of TropicalAgricultural Science, 34(2): 311–315.
SADOVY, Y. 1994. Grouper Stocks of the Western Central Atlantic: The Need for Managementand Management Needs. Proceedings of the Gulf and Caribbean Fisheries Institute, 43:
43–64.
SALAS, S., CHUENPAGDEE, R., SEIJO, J. C. and CHARLES, A. 2007. Challenges in theAssessment and Management of Small-Scale Fisheries in Latin America and theCaribbean. Fisheries Research, 87: 5–16.
SAMOILYS, M. A. 1987. Aspects of the Behaviour, Movements and Population Density of theCoral Trout, Plectropomus leopardus (Lacepede) (Pisces: Serranidae), at Heron Island,Southern Great Barrier Reef, 185 pp., MSc Thesis, Queensland University, Brisbane,Australia.
SAMOILYS, M. A. 1997. Movement in a Large Predatory Fish: Coral Trout, Plectropomus
leopardus (Pisces: Serranidae), on Heron Reef, Australia. Coral Reefs, 16: 151–158.
SHAPIRO, D. Y. 1987. Reproduction in Groupers. In: Tropical Snappers and Groupers: Biology
and Fisheries Management (Eds. POLOVINA, J. J. and RALSTON, S.), 295–327, Westview
Press, Boulder, Colorado, USA.
SLUKA, R. D. and REICHENBACH, N. 1996. Grouper Density and Diversity at Two Sites in theRepublic of Maldives. Atoll Research Bulletin, 438: 1–16.
SMITH, W. L. and CRAIG, M. T. 2007. Casting the Percomorph Net Widely: The Importance ofBroad Taxonomic Sampling in the Search for the Placement of Serranid and Percid
Fishes. Copeia, 2007: 35–55.
UNSWORTH, R. K. F., POWELL, A. HUKOM, F. and SMITH, D. J. 2007. The Ecology ofIndo-Pacific Grouper (Serranidae) Species and the Effects of a Small Scale No Take
Area on Grouper Assemblage, Abundance and Size Frequency Distribution. Marine
Biology, 152(2): 243–254.