DNA Barcoding reveals targeted fisheries for endangered sharks in Indonesia.
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DNA Barcoding reveals targeted fisheries for
endangered sharks in Indonesia
ARTICLE in FISHERIES RESEARCH · APRIL 2015
Impact Factor: 1.9 · DOI: 10.1016/j.fishres.2014.11.003
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Indonesian Biodiversity Research Center
San Diego State University
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Retrieved on: 20 October 2015
Fisheries Research 164 (2015) 130–134
Contents lists available at ScienceDirect
Fisheries Research
journal homepage: www.elsevier.com/locate/fishres
Short Communication
DNA barcoding reveals targeted fisheries for endangered sharks in
Indonesia
Andrianus Sembiring a,g , Ni Putu Dian Pertiwi a , Angka Mahardini a , Rizki Wulandari a ,
Eka Maya Kurniasih b , Andri Wahyu Kuncoro c , N.K. Dita Cahyani a , Aji Wahyu Anggoro a ,
Maria Ulfa d , Hawis Madduppa b , Kent E. Carpenter e , Paul H. Barber f ,
Gusti Ngurah Mahardika a,∗
a
The Indonesian Biodiversity Research Centre, The Animal Biomedical and Molecular Biology Laboratory of Udayana University, Jl Sesetan-Markisa 6,
Denpasar, Bali, Indonesia
b
Faculty of Fisheries and Marine Science, Bogor Agricultural University, Jl Rasamala, Bogor, West Java, Indonesia
c
Marine Science Department, Faculty of Husbandry, Fisheries, and Marine Science, University State of Papua, Jalan Gunung Salju Amban, Manokwari,
Papua, Indonesia
d
Flora and Fauna International, Jl Cumi-Cumi 15, Banda Aceh, Sumatra, Indonesia
e
Department of Biological Sciences, Old Dominion University, Norfolk, VA 23529, USA
f
Department of Ecology and Evolutionary Biology, University of California Los Angeles, Los Angeles, CA 90095-7239, USA
g
Master program in Environmental Sciences, Udayana University, Jl P.B. Sudirman, Denpasar, Bali, Indonesia
a r t i c l e
i n f o
Article history:
Received 9 October 2014
Received in revised form 4 November 2014
Accepted 9 November 2014
Handling Editor Prof. George A. Rose
Available online 11 December 2014
Keywords:
Shark
DNA barcoding
Indonesia
a b s t r a c t
Sharks are apex predators and keystone species that have a profound influence on the ecology and
food-web dynamics of coral reefs and epipelagic marine ecosystems. However, sharks are being heavily
overfished compromising the health of the world’s reefs and pelagic environments. Although Indonesia
is the world’s largest and most diverse coral reef ecosystem, information on the exploitation of sharks
in this region is scarce. Results of DNA barcoding of shark fin revealed two alarming findings: (1) a rarity of reef sharks that should dominate Indonesia’s coastal ecosystems, and (2) a fishery that targets
endangered sharks. The diversity and number of threatened species recovered in this study highlights
the urgent need for improved regulation and control of Indonesia’s shark fishery.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
As apex predators, many sharks are keystone species that have a
significant influence on the ecology and food-web dynamics of coral
reef and epipelagic ocean ecosystems (Ferretti et al., 2010; Myers
et al., 2007). However, shark populations have declined globally
by up to 90% (Myers et al., 2007), largely as a result of a multibillion dollar industry that harvests hundreds of millions of sharks
annually (Chapman et al., 2013) and life history traits such as low
fecundity, late maturity, and a long gestation period that make
shark populations particularly sensitive to overfishing and habitat
degradation (Baum et al., 2003). Global shark fisheries are largely
∗ Corresponding author at: The Indonesian Biodiversity Research Centre, The
Animal Biomedical and Molecular Biology Laboratory of Udayana University, Jl
Sesetan-Markisa 6, Denpasar, Bali 80226, Indonesia. Tel.: +62 361 8423061;
fax: +62 361 223791.
E-mail address: gnmahardika@indosat.net.id (G.N. Mahardika).
http://dx.doi.org/10.1016/j.fishres.2014.11.003
0165-7836/© 2014 Elsevier B.V. All rights reserved.
driven by the demand for shark fins, a key ingredient in the Asian
delicacy, shark fin soup.
The Convention on International Trade in Endangered Species
of Wild Fauna and Flora (CITES) currently lists many sharks
as Appendix I (species threatened with extinction) or Appendix
II (species where trade must be regulated to prevent overutilization). A further 60 sharks and rays are listed as “vulnerable”
or “near threatened” (Camhi et al., 2009). While CITES designation
should promote regulation of international trade in shark products, the primary commodity resulting from shark fisheries are fins.
Whole sharks are rarely landed at commercial ports (Clarke et al.,
2006; Liu et al., 2013) throughout much of the world; instead sharks
are “finned” at sea, a process by which fins are removed and bodies discarded, and then fins dried for sale to wholesalers (Fig. 1).
This process is common whether sharks are the targeted fisheries
species or the result of by-catch (Afonso et al., 2012). Dried fins typically lack key diagnostic features, making identification of fins to
species, and therefore regulation of trade in fins, extremely challenging. While DNA barcoding based on a short fragment of the
mitochondrial cytochrome oxidase I (COI) gene has been used to
A. Sembiring et al. / Fisheries Research 164 (2015) 130–134
131
Fig. 1. Photographs of shark and shark-fin sample collection. Sun-dried fins (left) in Bali, November 1, 2011; whole shark and elasmobranch auction at the harbour in Lombok
(right), July 12, 2012.
Source: Indonesian Biodiversity Research Centre.
identify fins to species (Holmes et al., 2009; Moftah et al., 2011;
Pinhal et al., 2012; Wong et al., 2009), this technique is not widely
used to promote regulation of shark fisheries.
Comprised of more than 17,000 islands, Indonesia is the largest
geographic area and heart of the “Coral Triangle”, a six-nation
region of South East Asia that is home to the world’s most diverse
seas (Carpenter et al., 2011; Dubinsky and Stambler, 2011; Roberts
et al., 2002). Approximately 30% of the world’s shark and ray
species are present in this region (Last and Stevens, 1994) including
regional endemics unique to the Coral Triangle and other broadly
distributed Indian and Pacific Ocean species (Barnett et al., 2012;
Bond et al., 2012; Campana et al., 2011; Nadon et al., 2012; Oliver
et al., 2011). The high value of shark fins on global markets has
sparked rapid growth in shark-fishing in Indonesia focused on
supplying fins to growing markets in Asia. Comprised of a mixture of commercial and opportunistic artisanal fisheries, the total
elasmobranch catch in Indonesia was estimated at more than
110,000 tonnes in 2007 (Camhi et al., 2009), representing the
largest recorded harvest in the world (Tull, 2009). Despite the size
and value of Indonesian shark fisheries, the expansive nature of
Indonesia combined with the diffuse nature of the shark fin fishery
means that basic fisheries data needed for effective management
and regulation in Indonesia (e.g. species composition, harvest levels, etc.) is severely lacking.
2. Materials and methods
We collected 582 shark fins from traditional fish markets and
shark-fin exporters across Indonesia from mid-2012 to mid-2014,
including Aceh, Jakarta, West Java, Central Java, East Java, Bali, West
Kalimantan, South Sulawesi, North Sulawesi, Maluku, and West
Papua. Additional samples were collected from shark fin export
warehouses in Cilacap (Central Java) and Tanjung Luar (West Nusa
Tenggara) (Fig. 2). We sampled a thin slice of tissue from dried
fins in fish markets. In export warehouses, we randomly sampled a
minimum of five caudal fins from boxes of fresh fins. The total numbers of dried and fresh fins were 164 and 418, respectively. Samples
were preserved in 96% alcohol for subsequent DNA analysis.
Whole DNA was extracted using a simple Chelex protocol
(Walsh et al., 1991). A fragment of the mitochondrial cytochrome
oxidase C subunit-1 (COI) was amplified using AmplyTaq RedTM
(Applied Biosystems) and the standard fish DNA-barcoding primers
Fish-BCL and Fish-BCH (Baldwin et al., 2009). The amplification
parameters were an initial denaturation of 94 ◦ C for 15 min, 38
cycles of 94 ◦ C for 30 s, 50 ◦ C for 30 s, and 72 ◦ C for 45 s, with a
final extension of 72 ◦ C for 5 min. PCR products were visualized via
electrophoresis on agarose gels and ethidium bromide staining.
The COI fragment could be amplified and sequenced from
all samples. The sequencing was conducted using both forward
and reverse directions at the University of California Berkeley
Sequencing Facility. The result was aligned using MEGA5 (Tamura
et al., 2007). We then determined species identity by comparing sequences to GenBank and Barcode of Life Data Systems
(http://www.boldsystems.org) databases enforcing a sequence
homology threshold of >99% as previously applied (Liu et al., 2013).
3. Results
DNA barcoding of a 600–654 bp of mitochondrial COI gene successfully determined the species identity of 582 fins collected from
markets across the Indonesian archipelago based on a 99% sequence
similarity criterion in GenBank and Barcode of Life Data Systems
(BOLD) databases. In total, analyses determined 40 different shark
species (Table 1). Five species (silky, scalloped hammerhead, blue,
big eye thresher, and thresher sharks) represented more than 50%
of the total fins sampled. Silky (19.10%), scalloped hammerhead
(10.50%) and blue sharks (8.20%) were the most common species
recovered, followed by bigeye thresher (7.60%) and thresher sharks
(7.20%). In contrast, 29 species were observed at less than 2% of the
total samples, including 7 species that were represented by only
one or two samples.
The vast majority of the samples (92%) were listed as “endangered” (1) “vulnerable” (12) or “near threatened” (19) while only
4 species were listed as species of least concern. The remaining
3 species are classified as data deficient. Similarly, 83% of species
identified were pelagic species of shark while only 17% were reef
sharks.
4. Discussion
Identification of unknown shark fins from Indonesian fish markets revealed a fishery that is heavily exploiting threatened and
near threatened species. In total, 80% of the species identified are
either considered “endangered” (1 sample) “vulnerable” (12 samples) or “near threatened” (19 samples). In total, 38.5% of all fins
came from sharks classified as endangered or vulnerable and 54.1%
of fins came from sharks listed as near threatened. In contrast,
only 7.2% of fins harvested came from three species categorized
132
A. Sembiring et al. / Fisheries Research 164 (2015) 130–134
Fig. 2. Sampling sites of shark-fin collection in Indonesia during 2012–2014. The sites were Lampulo, Banda Aceh (1), Lhokseumawe, Banda Aceh (2), Meulaboh, West
Aceh (3), Langsa, Banda Aceh (4), Simeulue Island, Aceh (5), Muara Baru, Jakarta (6), Pelabuhan Ratu, West Java (7), Pelabuhan Perikanan Samudra Cilacap, Central Java (8),
Pelabuhan Perikanan Muncar, East Java (9), Bali (10), Tanjung Luar, Lombok (11), Paotere, Makassar, South Sulawesi (12), Pelabuhan Perikanan Bitung, North Sulawesi (13),
Pasar Remu Sorong, West Papua (14), Pasar Jimbatan Puri Sorong, West Papua (15), Pasar Sanggeng Manokwari, West Papua (16), Pelabuhan Samudra Ambon, Maluku (17),
Singkawang West Kalimantan (18).
as species of “least concern”. Given that sharks are characterized
by low fecundity, late maturity, and a long gestation period (Baum
et al., 2003), the finding that nearly 93% of all fins sampled came
from species viewed by IUCN as threatened with extinction or
vulnerable to over-exploitation strongly suggests that Indonesian
shark fisheries are unsustainable.
Fishing effort for sharks was strong biased with more than
50% of the total samples coming from five species: silky, scalloped hammerhead, blue, big eye thresher, and thresher sharks.
The endangered scalloped hammerhead (CITES Appendix 1)
represented more than 10% of the total fins sampled. Most disturbing, this high frequency of scalloped hammerheads was seen
across sampling locations, including Aceh, Java, Lombok, Sulawesi,
Kalimantan and Papua, indicating that fisherman are likely specifically targeting these endangered sharks across the Indonesian
archipelago. Similarly, the vulnerable thresher and big eye thresher
sharks comprised nearly 15% of the total catch, while the nearly
threatened silky and blue sharks represented 19.10% and 8.20%
respectively. The high frequency of these species across Indonesia
strongly suggests that they are not the result of by-catch or smallscale artisanal fisheries, but instead result from large-scale targeted
shark fisheries.
Another disturbing finding of our study was that the vast majority (83%) of the species recovered were pelagic sharks, while
common Carcharhiniformes such as Galapagos (0.52%), grey reef
(01.20%), black-tip reef (3.61%), and white-tip reef shark (0.86%)
that typically dominate coral reef ecosystems were extremely rare
as were common reef Orectolobiformes, such as tawny nurse (1.37%)
and brown-banded bamboo (0.86%) sharks. On pristine coral reefs,
reef sharks make up a nearly 63% of total fish biomass (Sandin
et al., 2008). Because the greatest fishing pressure in Indonesian
waters is in shallow coastal areas where reef sharks typically thrive,
the alarmingly low number of reef sharks recovered in our sampling strongly indicates that reef-shark populations in Indonesia
have collapsed, most like due to overfishing (Allen and Erdmann,
2012) as happened in the Great Barrier Reef (Robbins et al., 2006),
and/or reef degradation (Burke et al., 2011). Low incidence of reef
sharks is consistent with the rarity of shark sightings during scuba
activities across most of Indonesia, with the exception of regions
of Eastern Indonesia such as Raja Ampat (M. Erdmann, pers. commun.). Indeed results show that 18 reef shark fins were identified
from samples in Western Indonesia and 19 in Java, whereas 32 and
36 were identified from Eastern Indonesia and Central Indonesia.
Even the most common reef shark in our sampling, the blacktip,
was not observed in 75% of sampling locations and 59% of blacktip fins came from one locality in Papua. These data suggest that
many reef sharks may be ecologically extinct in parts of Indonesian
waters.
While sampling revealed that a diversity of sharks entering
the Indonesian shark fin trade, three species represented new
records for Indonesia, including the western spotted gummy,
galapagos, and whitecreek sharks. It is not clear whether these
sharks were caught while migrating through Indonesian waters or
whether there are resident populations. If the former is true, fishing
pressures within Indonesian waters could have a negative impact
on resident populations outside Indonesia. If the latter is true, the
rarity of these species in our sample may indicate that their populations are heavily depressed, requiring special conservation status
within Indonesia.
Although this study only provides a snapshot of the Indonesian shark fishery, our study does provide some critical insight
into changes in fishing effort. Previous research published in 2009
indicated that the most common commercially harvested sharks
in this region were, in order, dusky, spot-tail, blue, and scalloped
hammerhead sharks (Ovenden et al., 2009). However, while blue
and scalloped hammerhead sharks were common in our sample,
spot-tail sharks were less common and no dusky sharks were
recovered despite extensive sampling across the entire Indonesian archipelago. This sharp discrepancy between studies four years
apart may signal that even some pelagic shark species may be
heavily overfished, resulting in a precipitous drop in species abundance across the archipelago.
A. Sembiring et al. / Fisheries Research 164 (2015) 130–134
Table 1
Distribution, catch frequency, IUCN/CITES status of various shark species harvested
in different geographical areas in Indonesia.
No
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
Species
Total
Frequency
IUCN status
Carcharhinus
falciformis
Silky shark
Sphyrna lewini
Scalloped
hammerhead
Prionace glauca
Blue shark
Alopias
superciliosus
Thresher shark
Alopias pelagicus
Bigeye thresher
shark
Carcharhinus sorrah
Spottail shark
Carcharhinus
limbatus
Blacktip shark
Isurus oxyrinchus
Shortfin mako
Rhizoprionodon
acutus
White-eyed shark
Squalus hemipinnis
Indonesian
shortsnout spurdog
Galeocerdo cuvier
Tiger shark
Isurus paucus
Long fin mako
Carcharhinus
longimanus
Whitetip oceanic
shark
Centrophorus
niaukang
Taiwan gulper
shark
Carcharhinus
melanopterus
Blacktip reef shark
Carcharhinus sealei
Blackspot shark
Carcharhinus
brevipinna
Spinner shark
Hemipristis
elongata
Snaggletooth shark
Nebrius ferrugineus
Tawny nurse shark
Carcharhinus
amblyrhynchos
Grey reef shark
Hemitriakis falcata
Sicklefin hound
shark
Mustelus
lenticulatus
Spotted
smoothhound
Hemigaleus
microstoma
Sickle fin weasel
shark
Loxodon
macrorhinus
Jordan’s blue
dogshark
Sphyrna zygaena
Smooth
hammerhead
111
19.07%
Near threatened
61
10.48%
Near threatened
Table 1 (Continued)
No
Species
26
Chiloscyllium
punctatum
Brownbanded
bamboo shark
Triaenodon obesus
Whitetip reef shark
Hemitriakis
indroyonoi
Indonesian
houndshark
Carcharhinus
albimarginatus
Silvertip shark
Carcharhinus
galapagensis
Galapagos shark
Carcharhinus
plumbeus
Sandbar shark
Squalus montalbani
Philippines
spurdog
Squatina legnota
Indonesian
angleshark
Carcharhinus leucas
Bull shark
Carcharhinus
amboinensis
Pigeye shark
Carcharhinus
coatesi
Whitecreek shark
Heptranchias perlo
Sharpnose
sevengill shark
Pseudocarcharias
kamoharai
Crocodile shark
Atelomycterus
marmoratus
Coral catshark
Carcharhinus
obscurus
Dusky shark
27
28
48
8.25%
Endangered
44
7.56%
Vulnerable
29
42
7.22%
Vulnerable
30
39
6.70%
Near threatened
31
21
3.61%
Near threatened
32
21
3.61%
Vulnerable
18
3.09%
Least concern
17
2.92%
Near threatened
33
34
35
12
2.06%
Near threatened
11
1.89%
Vulnerable
10
1.72%
Vulnerable
10
1.72%
Near threatened
36
37
38
39
9
1.55
Near threatened
40
9
1.55%
Near threatened
9
1.55%
Near threatened
8
1.37%
Least concern
8
1.37%
Vulnerable
7
1.20%
Near threatened
7
1.20%
Least concern
7
1.20%
Least concern
6
1.03%
Vulnerable
6
1.03%
Least concern
133
Total
Frequency
IUCN status
5
0.86%
Near threatened
5
0.86%
Near threatened
4
0.69%
Data deficient
4
0.69%
Near threatened
3
0.52%
Vulnerable
3
0.52%
Vulnerable
2
0.34%
Vulnerable
2
0.34%
Data deficient
1
0.17%
Near threatened
1
0.17%
Data deficient
1
0.17%
Data deficient
1
0.17%
Near threatened
1
0.17%
Near threatened
1
0.17%
Near threatened
1
0.17%
Vulnerable
Indonesia’s marine ecosystems are an extremely valuable natural resource that contributes significantly to its GDP and food
needs of its people (Barber et al., 2014). Because of the importance
of sharks in maintaining healthy marine ecosystems, achieving
the biodiversity preservation and food security goals of the Coral
Triangle Initiative (www.coraltriangleinitiative.org) will require
enforcement of existing fisheries regulations and expanding the
management of shark fisheries to protect ecologically important, but highly threatened shark species. Recently, the West
Papua Province enacted regulations prohibiting the capture of
sharks, rays and certain other fish species in Raja Ampat waters
(www.rajaampatkab.go.id/index.php). This initiative serves as a
model that could be adopted and enforced by other districts in
Indonesia to prevent a further decline in Indonesia’s vulnerable shark population, further jeopardizing its already imperilled
marine ecosystems (Burke et al., 2011).
5. Conclusion
6
1.03%
Vulnerable
The high frequency of “endangered”, “vulnerable”, and “near
threatened” taxa, the predominance of pelagic sharks entering the
Indonesian shark markets, and absence of a once abundant shark
species should be a wakeup call to the Indonesian Government.
134
A. Sembiring et al. / Fisheries Research 164 (2015) 130–134
Acknowledgements
This study was funded by the Partnerships for Enhanced
Engagement in Research (PEER) Science Programme (AID-OAA-A11-00012) funded by the United States Agency for International
Development (USAID) and the National Science Foundation (NSF)
in partnership with NSF PIRE Programme (OISE-0730256). Facilities and training for this study were provided by UCLA and the
Smithsonian Institution under USAID (grant number 497-A-0010-00008-00). We thank B. Subhan, A.A. Wibowo, I.A. Putra, S.
Bahri, Rahmad, N. Akbar, P. Akna, WWF Indonesia, D. Suprapti,
Agri, Masriana, Reef Check Indonesia, P. Borsa, N. Putra, A. Yusmalinda, Ambariyanto, S. Indriawan, A.A. Tarekat, Stevanus, A. Arimbi,
C.A.K. Hardani, Ma’rufah, A. Kusuma for their assistance with sample and/or data collection.
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DNA Barcoding reveals targeted fisheries for
endangered sharks in Indonesia
ARTICLE in FISHERIES RESEARCH · APRIL 2015
Impact Factor: 1.9 · DOI: 10.1016/j.fishres.2014.11.003
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13 AUTHORS, INCLUDING:
Dian Pertiwi
Rizki Wulandari
Indonesian Biodiversity Research Center
San Diego State University
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2 PUBLICATIONS 2 CITATIONS
SEE PROFILE
SEE PROFILE
Dita Cahyani
Gusti Ngurah Mahardika
Indonesian Biodiversity Research Center
Udayana University
6 PUBLICATIONS 7 CITATIONS
42 PUBLICATIONS 110 CITATIONS
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Available from: Gusti Ngurah Mahardika
Retrieved on: 20 October 2015
Fisheries Research 164 (2015) 130–134
Contents lists available at ScienceDirect
Fisheries Research
journal homepage: www.elsevier.com/locate/fishres
Short Communication
DNA barcoding reveals targeted fisheries for endangered sharks in
Indonesia
Andrianus Sembiring a,g , Ni Putu Dian Pertiwi a , Angka Mahardini a , Rizki Wulandari a ,
Eka Maya Kurniasih b , Andri Wahyu Kuncoro c , N.K. Dita Cahyani a , Aji Wahyu Anggoro a ,
Maria Ulfa d , Hawis Madduppa b , Kent E. Carpenter e , Paul H. Barber f ,
Gusti Ngurah Mahardika a,∗
a
The Indonesian Biodiversity Research Centre, The Animal Biomedical and Molecular Biology Laboratory of Udayana University, Jl Sesetan-Markisa 6,
Denpasar, Bali, Indonesia
b
Faculty of Fisheries and Marine Science, Bogor Agricultural University, Jl Rasamala, Bogor, West Java, Indonesia
c
Marine Science Department, Faculty of Husbandry, Fisheries, and Marine Science, University State of Papua, Jalan Gunung Salju Amban, Manokwari,
Papua, Indonesia
d
Flora and Fauna International, Jl Cumi-Cumi 15, Banda Aceh, Sumatra, Indonesia
e
Department of Biological Sciences, Old Dominion University, Norfolk, VA 23529, USA
f
Department of Ecology and Evolutionary Biology, University of California Los Angeles, Los Angeles, CA 90095-7239, USA
g
Master program in Environmental Sciences, Udayana University, Jl P.B. Sudirman, Denpasar, Bali, Indonesia
a r t i c l e
i n f o
Article history:
Received 9 October 2014
Received in revised form 4 November 2014
Accepted 9 November 2014
Handling Editor Prof. George A. Rose
Available online 11 December 2014
Keywords:
Shark
DNA barcoding
Indonesia
a b s t r a c t
Sharks are apex predators and keystone species that have a profound influence on the ecology and
food-web dynamics of coral reefs and epipelagic marine ecosystems. However, sharks are being heavily
overfished compromising the health of the world’s reefs and pelagic environments. Although Indonesia
is the world’s largest and most diverse coral reef ecosystem, information on the exploitation of sharks
in this region is scarce. Results of DNA barcoding of shark fin revealed two alarming findings: (1) a rarity of reef sharks that should dominate Indonesia’s coastal ecosystems, and (2) a fishery that targets
endangered sharks. The diversity and number of threatened species recovered in this study highlights
the urgent need for improved regulation and control of Indonesia’s shark fishery.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
As apex predators, many sharks are keystone species that have a
significant influence on the ecology and food-web dynamics of coral
reef and epipelagic ocean ecosystems (Ferretti et al., 2010; Myers
et al., 2007). However, shark populations have declined globally
by up to 90% (Myers et al., 2007), largely as a result of a multibillion dollar industry that harvests hundreds of millions of sharks
annually (Chapman et al., 2013) and life history traits such as low
fecundity, late maturity, and a long gestation period that make
shark populations particularly sensitive to overfishing and habitat
degradation (Baum et al., 2003). Global shark fisheries are largely
∗ Corresponding author at: The Indonesian Biodiversity Research Centre, The
Animal Biomedical and Molecular Biology Laboratory of Udayana University, Jl
Sesetan-Markisa 6, Denpasar, Bali 80226, Indonesia. Tel.: +62 361 8423061;
fax: +62 361 223791.
E-mail address: gnmahardika@indosat.net.id (G.N. Mahardika).
http://dx.doi.org/10.1016/j.fishres.2014.11.003
0165-7836/© 2014 Elsevier B.V. All rights reserved.
driven by the demand for shark fins, a key ingredient in the Asian
delicacy, shark fin soup.
The Convention on International Trade in Endangered Species
of Wild Fauna and Flora (CITES) currently lists many sharks
as Appendix I (species threatened with extinction) or Appendix
II (species where trade must be regulated to prevent overutilization). A further 60 sharks and rays are listed as “vulnerable”
or “near threatened” (Camhi et al., 2009). While CITES designation
should promote regulation of international trade in shark products, the primary commodity resulting from shark fisheries are fins.
Whole sharks are rarely landed at commercial ports (Clarke et al.,
2006; Liu et al., 2013) throughout much of the world; instead sharks
are “finned” at sea, a process by which fins are removed and bodies discarded, and then fins dried for sale to wholesalers (Fig. 1).
This process is common whether sharks are the targeted fisheries
species or the result of by-catch (Afonso et al., 2012). Dried fins typically lack key diagnostic features, making identification of fins to
species, and therefore regulation of trade in fins, extremely challenging. While DNA barcoding based on a short fragment of the
mitochondrial cytochrome oxidase I (COI) gene has been used to
A. Sembiring et al. / Fisheries Research 164 (2015) 130–134
131
Fig. 1. Photographs of shark and shark-fin sample collection. Sun-dried fins (left) in Bali, November 1, 2011; whole shark and elasmobranch auction at the harbour in Lombok
(right), July 12, 2012.
Source: Indonesian Biodiversity Research Centre.
identify fins to species (Holmes et al., 2009; Moftah et al., 2011;
Pinhal et al., 2012; Wong et al., 2009), this technique is not widely
used to promote regulation of shark fisheries.
Comprised of more than 17,000 islands, Indonesia is the largest
geographic area and heart of the “Coral Triangle”, a six-nation
region of South East Asia that is home to the world’s most diverse
seas (Carpenter et al., 2011; Dubinsky and Stambler, 2011; Roberts
et al., 2002). Approximately 30% of the world’s shark and ray
species are present in this region (Last and Stevens, 1994) including
regional endemics unique to the Coral Triangle and other broadly
distributed Indian and Pacific Ocean species (Barnett et al., 2012;
Bond et al., 2012; Campana et al., 2011; Nadon et al., 2012; Oliver
et al., 2011). The high value of shark fins on global markets has
sparked rapid growth in shark-fishing in Indonesia focused on
supplying fins to growing markets in Asia. Comprised of a mixture of commercial and opportunistic artisanal fisheries, the total
elasmobranch catch in Indonesia was estimated at more than
110,000 tonnes in 2007 (Camhi et al., 2009), representing the
largest recorded harvest in the world (Tull, 2009). Despite the size
and value of Indonesian shark fisheries, the expansive nature of
Indonesia combined with the diffuse nature of the shark fin fishery
means that basic fisheries data needed for effective management
and regulation in Indonesia (e.g. species composition, harvest levels, etc.) is severely lacking.
2. Materials and methods
We collected 582 shark fins from traditional fish markets and
shark-fin exporters across Indonesia from mid-2012 to mid-2014,
including Aceh, Jakarta, West Java, Central Java, East Java, Bali, West
Kalimantan, South Sulawesi, North Sulawesi, Maluku, and West
Papua. Additional samples were collected from shark fin export
warehouses in Cilacap (Central Java) and Tanjung Luar (West Nusa
Tenggara) (Fig. 2). We sampled a thin slice of tissue from dried
fins in fish markets. In export warehouses, we randomly sampled a
minimum of five caudal fins from boxes of fresh fins. The total numbers of dried and fresh fins were 164 and 418, respectively. Samples
were preserved in 96% alcohol for subsequent DNA analysis.
Whole DNA was extracted using a simple Chelex protocol
(Walsh et al., 1991). A fragment of the mitochondrial cytochrome
oxidase C subunit-1 (COI) was amplified using AmplyTaq RedTM
(Applied Biosystems) and the standard fish DNA-barcoding primers
Fish-BCL and Fish-BCH (Baldwin et al., 2009). The amplification
parameters were an initial denaturation of 94 ◦ C for 15 min, 38
cycles of 94 ◦ C for 30 s, 50 ◦ C for 30 s, and 72 ◦ C for 45 s, with a
final extension of 72 ◦ C for 5 min. PCR products were visualized via
electrophoresis on agarose gels and ethidium bromide staining.
The COI fragment could be amplified and sequenced from
all samples. The sequencing was conducted using both forward
and reverse directions at the University of California Berkeley
Sequencing Facility. The result was aligned using MEGA5 (Tamura
et al., 2007). We then determined species identity by comparing sequences to GenBank and Barcode of Life Data Systems
(http://www.boldsystems.org) databases enforcing a sequence
homology threshold of >99% as previously applied (Liu et al., 2013).
3. Results
DNA barcoding of a 600–654 bp of mitochondrial COI gene successfully determined the species identity of 582 fins collected from
markets across the Indonesian archipelago based on a 99% sequence
similarity criterion in GenBank and Barcode of Life Data Systems
(BOLD) databases. In total, analyses determined 40 different shark
species (Table 1). Five species (silky, scalloped hammerhead, blue,
big eye thresher, and thresher sharks) represented more than 50%
of the total fins sampled. Silky (19.10%), scalloped hammerhead
(10.50%) and blue sharks (8.20%) were the most common species
recovered, followed by bigeye thresher (7.60%) and thresher sharks
(7.20%). In contrast, 29 species were observed at less than 2% of the
total samples, including 7 species that were represented by only
one or two samples.
The vast majority of the samples (92%) were listed as “endangered” (1) “vulnerable” (12) or “near threatened” (19) while only
4 species were listed as species of least concern. The remaining
3 species are classified as data deficient. Similarly, 83% of species
identified were pelagic species of shark while only 17% were reef
sharks.
4. Discussion
Identification of unknown shark fins from Indonesian fish markets revealed a fishery that is heavily exploiting threatened and
near threatened species. In total, 80% of the species identified are
either considered “endangered” (1 sample) “vulnerable” (12 samples) or “near threatened” (19 samples). In total, 38.5% of all fins
came from sharks classified as endangered or vulnerable and 54.1%
of fins came from sharks listed as near threatened. In contrast,
only 7.2% of fins harvested came from three species categorized
132
A. Sembiring et al. / Fisheries Research 164 (2015) 130–134
Fig. 2. Sampling sites of shark-fin collection in Indonesia during 2012–2014. The sites were Lampulo, Banda Aceh (1), Lhokseumawe, Banda Aceh (2), Meulaboh, West
Aceh (3), Langsa, Banda Aceh (4), Simeulue Island, Aceh (5), Muara Baru, Jakarta (6), Pelabuhan Ratu, West Java (7), Pelabuhan Perikanan Samudra Cilacap, Central Java (8),
Pelabuhan Perikanan Muncar, East Java (9), Bali (10), Tanjung Luar, Lombok (11), Paotere, Makassar, South Sulawesi (12), Pelabuhan Perikanan Bitung, North Sulawesi (13),
Pasar Remu Sorong, West Papua (14), Pasar Jimbatan Puri Sorong, West Papua (15), Pasar Sanggeng Manokwari, West Papua (16), Pelabuhan Samudra Ambon, Maluku (17),
Singkawang West Kalimantan (18).
as species of “least concern”. Given that sharks are characterized
by low fecundity, late maturity, and a long gestation period (Baum
et al., 2003), the finding that nearly 93% of all fins sampled came
from species viewed by IUCN as threatened with extinction or
vulnerable to over-exploitation strongly suggests that Indonesian
shark fisheries are unsustainable.
Fishing effort for sharks was strong biased with more than
50% of the total samples coming from five species: silky, scalloped hammerhead, blue, big eye thresher, and thresher sharks.
The endangered scalloped hammerhead (CITES Appendix 1)
represented more than 10% of the total fins sampled. Most disturbing, this high frequency of scalloped hammerheads was seen
across sampling locations, including Aceh, Java, Lombok, Sulawesi,
Kalimantan and Papua, indicating that fisherman are likely specifically targeting these endangered sharks across the Indonesian
archipelago. Similarly, the vulnerable thresher and big eye thresher
sharks comprised nearly 15% of the total catch, while the nearly
threatened silky and blue sharks represented 19.10% and 8.20%
respectively. The high frequency of these species across Indonesia
strongly suggests that they are not the result of by-catch or smallscale artisanal fisheries, but instead result from large-scale targeted
shark fisheries.
Another disturbing finding of our study was that the vast majority (83%) of the species recovered were pelagic sharks, while
common Carcharhiniformes such as Galapagos (0.52%), grey reef
(01.20%), black-tip reef (3.61%), and white-tip reef shark (0.86%)
that typically dominate coral reef ecosystems were extremely rare
as were common reef Orectolobiformes, such as tawny nurse (1.37%)
and brown-banded bamboo (0.86%) sharks. On pristine coral reefs,
reef sharks make up a nearly 63% of total fish biomass (Sandin
et al., 2008). Because the greatest fishing pressure in Indonesian
waters is in shallow coastal areas where reef sharks typically thrive,
the alarmingly low number of reef sharks recovered in our sampling strongly indicates that reef-shark populations in Indonesia
have collapsed, most like due to overfishing (Allen and Erdmann,
2012) as happened in the Great Barrier Reef (Robbins et al., 2006),
and/or reef degradation (Burke et al., 2011). Low incidence of reef
sharks is consistent with the rarity of shark sightings during scuba
activities across most of Indonesia, with the exception of regions
of Eastern Indonesia such as Raja Ampat (M. Erdmann, pers. commun.). Indeed results show that 18 reef shark fins were identified
from samples in Western Indonesia and 19 in Java, whereas 32 and
36 were identified from Eastern Indonesia and Central Indonesia.
Even the most common reef shark in our sampling, the blacktip,
was not observed in 75% of sampling locations and 59% of blacktip fins came from one locality in Papua. These data suggest that
many reef sharks may be ecologically extinct in parts of Indonesian
waters.
While sampling revealed that a diversity of sharks entering
the Indonesian shark fin trade, three species represented new
records for Indonesia, including the western spotted gummy,
galapagos, and whitecreek sharks. It is not clear whether these
sharks were caught while migrating through Indonesian waters or
whether there are resident populations. If the former is true, fishing
pressures within Indonesian waters could have a negative impact
on resident populations outside Indonesia. If the latter is true, the
rarity of these species in our sample may indicate that their populations are heavily depressed, requiring special conservation status
within Indonesia.
Although this study only provides a snapshot of the Indonesian shark fishery, our study does provide some critical insight
into changes in fishing effort. Previous research published in 2009
indicated that the most common commercially harvested sharks
in this region were, in order, dusky, spot-tail, blue, and scalloped
hammerhead sharks (Ovenden et al., 2009). However, while blue
and scalloped hammerhead sharks were common in our sample,
spot-tail sharks were less common and no dusky sharks were
recovered despite extensive sampling across the entire Indonesian archipelago. This sharp discrepancy between studies four years
apart may signal that even some pelagic shark species may be
heavily overfished, resulting in a precipitous drop in species abundance across the archipelago.
A. Sembiring et al. / Fisheries Research 164 (2015) 130–134
Table 1
Distribution, catch frequency, IUCN/CITES status of various shark species harvested
in different geographical areas in Indonesia.
No
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
Species
Total
Frequency
IUCN status
Carcharhinus
falciformis
Silky shark
Sphyrna lewini
Scalloped
hammerhead
Prionace glauca
Blue shark
Alopias
superciliosus
Thresher shark
Alopias pelagicus
Bigeye thresher
shark
Carcharhinus sorrah
Spottail shark
Carcharhinus
limbatus
Blacktip shark
Isurus oxyrinchus
Shortfin mako
Rhizoprionodon
acutus
White-eyed shark
Squalus hemipinnis
Indonesian
shortsnout spurdog
Galeocerdo cuvier
Tiger shark
Isurus paucus
Long fin mako
Carcharhinus
longimanus
Whitetip oceanic
shark
Centrophorus
niaukang
Taiwan gulper
shark
Carcharhinus
melanopterus
Blacktip reef shark
Carcharhinus sealei
Blackspot shark
Carcharhinus
brevipinna
Spinner shark
Hemipristis
elongata
Snaggletooth shark
Nebrius ferrugineus
Tawny nurse shark
Carcharhinus
amblyrhynchos
Grey reef shark
Hemitriakis falcata
Sicklefin hound
shark
Mustelus
lenticulatus
Spotted
smoothhound
Hemigaleus
microstoma
Sickle fin weasel
shark
Loxodon
macrorhinus
Jordan’s blue
dogshark
Sphyrna zygaena
Smooth
hammerhead
111
19.07%
Near threatened
61
10.48%
Near threatened
Table 1 (Continued)
No
Species
26
Chiloscyllium
punctatum
Brownbanded
bamboo shark
Triaenodon obesus
Whitetip reef shark
Hemitriakis
indroyonoi
Indonesian
houndshark
Carcharhinus
albimarginatus
Silvertip shark
Carcharhinus
galapagensis
Galapagos shark
Carcharhinus
plumbeus
Sandbar shark
Squalus montalbani
Philippines
spurdog
Squatina legnota
Indonesian
angleshark
Carcharhinus leucas
Bull shark
Carcharhinus
amboinensis
Pigeye shark
Carcharhinus
coatesi
Whitecreek shark
Heptranchias perlo
Sharpnose
sevengill shark
Pseudocarcharias
kamoharai
Crocodile shark
Atelomycterus
marmoratus
Coral catshark
Carcharhinus
obscurus
Dusky shark
27
28
48
8.25%
Endangered
44
7.56%
Vulnerable
29
42
7.22%
Vulnerable
30
39
6.70%
Near threatened
31
21
3.61%
Near threatened
32
21
3.61%
Vulnerable
18
3.09%
Least concern
17
2.92%
Near threatened
33
34
35
12
2.06%
Near threatened
11
1.89%
Vulnerable
10
1.72%
Vulnerable
10
1.72%
Near threatened
36
37
38
39
9
1.55
Near threatened
40
9
1.55%
Near threatened
9
1.55%
Near threatened
8
1.37%
Least concern
8
1.37%
Vulnerable
7
1.20%
Near threatened
7
1.20%
Least concern
7
1.20%
Least concern
6
1.03%
Vulnerable
6
1.03%
Least concern
133
Total
Frequency
IUCN status
5
0.86%
Near threatened
5
0.86%
Near threatened
4
0.69%
Data deficient
4
0.69%
Near threatened
3
0.52%
Vulnerable
3
0.52%
Vulnerable
2
0.34%
Vulnerable
2
0.34%
Data deficient
1
0.17%
Near threatened
1
0.17%
Data deficient
1
0.17%
Data deficient
1
0.17%
Near threatened
1
0.17%
Near threatened
1
0.17%
Near threatened
1
0.17%
Vulnerable
Indonesia’s marine ecosystems are an extremely valuable natural resource that contributes significantly to its GDP and food
needs of its people (Barber et al., 2014). Because of the importance
of sharks in maintaining healthy marine ecosystems, achieving
the biodiversity preservation and food security goals of the Coral
Triangle Initiative (www.coraltriangleinitiative.org) will require
enforcement of existing fisheries regulations and expanding the
management of shark fisheries to protect ecologically important, but highly threatened shark species. Recently, the West
Papua Province enacted regulations prohibiting the capture of
sharks, rays and certain other fish species in Raja Ampat waters
(www.rajaampatkab.go.id/index.php). This initiative serves as a
model that could be adopted and enforced by other districts in
Indonesia to prevent a further decline in Indonesia’s vulnerable shark population, further jeopardizing its already imperilled
marine ecosystems (Burke et al., 2011).
5. Conclusion
6
1.03%
Vulnerable
The high frequency of “endangered”, “vulnerable”, and “near
threatened” taxa, the predominance of pelagic sharks entering the
Indonesian shark markets, and absence of a once abundant shark
species should be a wakeup call to the Indonesian Government.
134
A. Sembiring et al. / Fisheries Research 164 (2015) 130–134
Acknowledgements
This study was funded by the Partnerships for Enhanced
Engagement in Research (PEER) Science Programme (AID-OAA-A11-00012) funded by the United States Agency for International
Development (USAID) and the National Science Foundation (NSF)
in partnership with NSF PIRE Programme (OISE-0730256). Facilities and training for this study were provided by UCLA and the
Smithsonian Institution under USAID (grant number 497-A-0010-00008-00). We thank B. Subhan, A.A. Wibowo, I.A. Putra, S.
Bahri, Rahmad, N. Akbar, P. Akna, WWF Indonesia, D. Suprapti,
Agri, Masriana, Reef Check Indonesia, P. Borsa, N. Putra, A. Yusmalinda, Ambariyanto, S. Indriawan, A.A. Tarekat, Stevanus, A. Arimbi,
C.A.K. Hardani, Ma’rufah, A. Kusuma for their assistance with sample and/or data collection.
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