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Fisheries
Research
164
(2015)
130–134
Contents
lists
available
at
ScienceDirect
Fisheries
Research
j
ourna
l
ho
me
pa
ge:
www.elsevier.com/locate/fishres
Short
Communication
DNA
barcoding
reveals
targeted
fisheries
for
endangered
sharks
in
Indonesia
Andrianus
Sembiringa,g,
Ni
Putu
Dian
Pertiwia,
Angka
Mahardinia,
Rizki
Wulandaria,
Eka
Maya
Kurniasihb,
Andri
Wahyu
Kuncoroc,
N.K.
Dita
Cahyania,
Aji
Wahyu
Anggoroa,
Maria
Ulfad,
Hawis
Madduppab,
Kent
E.
Carpentere,
Paul
H.
Barberf,
Gusti
Ngurah
Mahardikaa,∗
aThe
Indonesian
Biodiversity
Research
Centre,
The
Animal
Biomedical
and
Molecular
Biology
Laboratory
of
Udayana
University,
Jl
Sesetan-Markisa
6,
Denpasar,
Bali,
Indonesia
bFaculty
of
Fishery
and
Marine
Science,
Bogor
Agricultural
Institute,
Jl
Rasamala,
Bogor,
West
Java,
Indonesia
cMarine
Science
Department,
Faculty
of
Husbandry,
Fisheries,
and
Marine
Science,
University
State
of
Papua,
Jalan
Gunung
Salju
Amban,
Manokwari,
Papua,
Indonesia
dFlora
and
Fauna
International,
Jl
Cumi-Cumi
15,
Banda
Aceh,
Sumatra,
Indonesia
eDepartment
of
Biological
Sciences,
Old
Dominion
University,
Norfolk,
VA
23529,
USA
fDepartment
of
Ecology
and
Evolutionary
Biology,
University
of
California
Los
Angeles,
Los
Angeles,
CA
90095-7239,
USA
gMaster
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
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
rar-
ity
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
multi-
billion
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).
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
over-
utilization).
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
prod-
ucts,
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
bod-
ies
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
typ-
ically
lack
key
diagnostic
features,
making
identification
of
fins
to
species,
and
therefore
regulation
of
trade
in
fins,
extremely
chal-
lenging.
While
DNA
barcoding
based
on
a
short
fragment
of
the
mitochondrial
cytochrome
oxidase
I
(COI)
gene
has
been
used
to
http://dx.doi.org/10.1016/j.fishres.2014.11.003
0165-7836/©
2014
Elsevier
B.V.
All
rights
reserved.
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
mix-
ture
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
lev-
els,
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
num-
bers
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
compar-
ing
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
suc-
cessfully
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
“endan-
gered”
(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
mar-
kets
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
sam-
ples)
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,
scal-
loped
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
dis-
turbing,
this
high
frequency
of
scalloped
hammerheads
was
seen
across
sampling
locations,
including
Aceh,
Java,
Lombok,
Sulawesi,
Kalimantan
and
Papua,
indicating
that
fisherman
are
likely
specif-
ically
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
small-
scale
artisanal
fisheries,
but
instead
result
from
large-scale
targeted
shark
fisheries.
Another
disturbing
finding
of
our
study
was
that
the
vast
major-
ity
(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
sam-
pling
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.
com-
mun.).
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
black-
tip
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
popu-
lations
are
heavily
depressed,
requiring
special
conservation
status
within
Indonesia.
Although
this
study
only
provides
a
snapshot
of
the
Indone-
sian
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
Indone-
sian
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
abun-
dance
across
the
archipelago.
A.
Sembiring
et
al.
/
Fisheries
Research
164
(2015)
130–134
133
Table
1
Distribution,
catch
frequency,
IUCN/CITES
status
of
various
shark
species
harvested
in
different
geographical
areas
in
Indonesia.
No
Species
Total
Frequency
IUCN
status
1
Carcharhinus
falciformis
111
19.07%
Near
threatened
Silky
shark
2
Sphyrna
lewini
61
10.48%
Near
threatened
Scalloped
hammerhead
3
Prionace
glauca 48
8.25%
Endangered
Blue
shark
4
Alopias
superciliosus
44
7.56%
Vulnerable
Thresher
shark
5
Alopias
pelagicus
42
7.22%
Vulnerable
Bigeye
thresher
shark
6
Carcharhinus
sorrah
39
6.70%
Near
threatened
Spottail
shark
7
Carcharhinus
limbatus
21
3.61%
Near
threatened
Blacktip
shark
8
Isurus
oxyrinchus
21
3.61%
Vulnerable
Shortfin
mako
9
Rhizoprionodon
acutus
18
3.09% Least
concern
White-eyed
shark
10
Squalus
hemipinnis
17
2.92%
Near
threatened
Indonesian
shortsnout
spurdog
11
Galeocerdo
cuvier
12
2.06%
Near
threatened
Tiger
shark
12
Isurus
paucus
11
1.89%
Vulnerable
Long
fin
mako
13
Carcharhinus
longimanus
10
1.72%
Vulnerable
Whitetip
oceanic
shark
14
Centrophorus
niaukang
10
1.72%
Near
threatened
Taiwan
gulper
shark
15
Carcharhinus
melanopterus
9
1.55
Near
threatened
Blacktip
reef
shark
16
Carcharhinus
sealei
9
1.55%
Near
threatened
Blackspot
shark
17
Carcharhinus
brevipinna
9
1.55%
Near
threatened
Spinner
shark
18
Hemipristis
elongata
8
1.37%
Least
concern
Snaggletooth
shark
19
Nebrius
ferrugineus
8
1.37%
Vulnerable
Tawny
nurse
shark
20
Carcharhinus
amblyrhynchos
7
1.20%
Near
threatened
Grey
reef
shark
21
Hemitriakis
falcata
7
1.20%
Least
concern
Sicklefin
hound
shark
22
Mustelus
lenticulatus
7
1.20%
Least
concern
Spotted
smoothhound
23
Hemigaleus
microstoma
6
1.03%
Vulnerable
Sickle
fin
weasel
shark
24
Loxodon
macrorhinus
6
1.03%
Least
concern
Jordan’s
blue
dogshark
25
Sphyrna
zygaena
6
1.03%
Vulnerable
Smooth
hammerhead
Table
1
(Continued)
No
Species
Total
Frequency
IUCN
status
26
Chiloscyllium
punctatum
5
0.86%
Near
threatened
Brownbanded
bamboo
shark
27
Triaenodon
obesus
5
0.86%
Near
threatened
Whitetip
reef
shark
28
Hemitriakis
indroyonoi
4
0.69%
Data
deficient
Indonesian
houndshark
29
Carcharhinus
albimarginatus
4
0.69%
Near
threatened
Silvertip
shark
30
Carcharhinus
galapagensis
3
0.52%
Vulnerable
Galapagos
shark
31
Carcharhinus
plumbeus
3
0.52%
Vulnerable
Sandbar
shark
32
Squalus
montalbani
2
0.34%
Vulnerable
Philippines
spurdog
33
Squatina
legnota
2
0.34%
Data
deficient
Data
deficient
34
Carcharhinus
leucas
1
0.17%
Near
threatened
Bull
shark
35
Carcharhinus
amboinensis
1
0.17%
Data
deficient
Pigeye
shark
36
Carcharhinus
coatesi
1
0.17%
Data
deficient
Whitecreek
shark
37
Heptranchias
perlo
1
0.17%
Near
threatened
Sharpnose
sevengill
shark
38
Pseudocarcharias
kamoharai
1
0.17%
Near
threatened
Crocodile
shark
39
Atelomycterus
marmoratus
1
0.17%
Near
threatened
Coral
catshark
40
Carcharhinus
obscurus
1
0.17%
Vulnerable
Dusky
shark
Indonesia’s
marine
ecosystems
are
an
extremely
valuable
nat-
ural
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
impor-
tant,
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
vulnera-
ble
shark
population,
further
jeopardizing
its
already
imperilled
marine
ecosystems
(Burke
et
al.,
2011).
5.
Conclusion
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-A-
11-00012)
funded
by
the
United
States
Agency
for
International
Development
(USAID)
and
the
National
Science
Foundation
(NSF)
in
partnership
with
NSF
PIRE
Programme
(OISE-0730256).
Facil-
ities
and
training
for
this
study
were
provided
by
UCLA
and
the
Smithsonian
Institution
under
USAID
(grant
number
497-A-00-
10-00008-00).
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.
Yusma-
linda,
Ambariyanto,
S.
Indriawan,
A.A.
Tarekat,
Stevanus,
A.
Arimbi,
C.A.K.
Hardani,
Ma’rufah,
A.
Kusuma
for
their
assistance
with
sam-
ple
and/or
data
collection.
References
Afonso,
A.S.,
Santiago,
R.,
Hazin,
H.,
Hazin,
F.H.V.,
2012.
Shark
bycatch
and
mortality
and
hook
bite-offs
in
pelagic
longlines:
interactions
between
hook
types
and
leader
materials.
Fish.
Res.
131–133,
9–14.
Allen,
G.R.,
Erdmann,
M.V.,
2012.
Reef
Fishes
of
the
East
Indies.
Tropical
Reef
Research,
vol.
I.
University
of
Hawaii
Press,
Perth,
Australia.
Baldwin,
C.C.,
Mounts,
J.H.,
Smith,
D.G.,
Weigt,
L.A.,
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
2008,
1–22.
Barber,
P.H.,
Ablan-lagman,
M.C.A.,
Ambariyanto
Berlinck,
R.G.S.,
Cahyani,
D.,
Cran-
dall,
E.D.,
Ravago-gotanco,
R.,
Juinio-me˜
nez,
M.A.,
Mahardika,
I.G.N.,
Shanker,
K.,
Starger,
C.J.,
Toha,
A.H.A.,
Anggoro,
A.W.,
Willette,
D.A.,
2014.
Advancing
biodi-
versity
research
in
developing
countries:
the
need
for
changing
paradigms.
Bull.
Mar.
Sci.
90,
187–210.
Barnett,
A.,
Abrantes,
K.G.,
Seymour,
J.,
Fitzpatrick,
R.,
2012.
Residency
and
spatial
use
by
reef
sharks
of
an
isolated
seamount
and
its
implications
for
conservation.
PLoS
One
7,
e36574.
Baum,
J.K.,
Myers,
R.A.,
Kehler,
D.G.,
Worm,
B.,
Harley,
S.J.,
Doherty,
P.A.,
2003.
Col-
lapse
and
conservation
of
shark
populations
in
the
Northwest
Atlantic.
Science
299,
389–392.
Bond,
M.E.,
Babcock,
E.A.,
Pikitch,
E.K.,
Abercrombie,
D.L.,
Lamb,
N.F.,
Chapman,
D.D.,
2012.
Reef
sharks
exhibit
site-fidelity
and
higher
relative
abundance
in
marine
reserves
on
the
Mesoamerican
Barrier
reef.
PLoS
One
7,
e32983.
Burke,
L.,
Reytar,
K.,
Spalding,
M.D.,
Perry,
A.,
2011.
Reefs
at
Risk
Revisited.
World
Resource
Institute,
Washington,
DC.
Camhi,
M.D.,
Valenti,
S.V.,
Fordham,
S.V.,
Fowler,
S.L.,
Gibson,
C.,
2009.
The
Conser-
vation
Status
of
Pelagic
Sharks
and
Rays:
Report
of
the
IUCN
Shark
Specialist
Group
Pelagic
Shark
Red
List
Workshop.
IUCN
Species
Survival
Commission
Shark
Specialist
Group,
Newbury,
UK,
x
+
78
p.
Campana,
S.E.,
Dorey,
A.,
Fowler,
M.,
Joyce,
W.,
Wang,
Z.,
Wright,
D.,
Yashayaev,
I.,
2011.
Migration
pathways,
behavioural
thermoregulation
and
overwintering
grounds
of
blue
sharks
in
the
Northwest
Atlantic.
PLoS
One
6,
e16854.
Carpenter,
K.E.,
Barber,
P.H.,
Crandall,
E.D.,
Ablan-Lagman,
M.C.A.,
Ambariyanto
Mahardika,
G.N.,
Manjaji-Matsumoto,
B.M.,
Juinio-Me˜
nez,
M.A.,
Santos,
M.D.,
Starger,
C.J.,
Toha,
A.H.A.,
2011.
Comparative
phylogeography
of
the
coral
trian-
gle
and
implications
for
marine
management.
J.
Mar.
Biol.
2011,
1–14.
Chapman,
D.D.,
Frisk,
M.G.,
Abercrombie,
D.L.,
Safina,
C.,
Gruber,
S.H.,
Babcock,
E.A.,
Feldheim,
K.A.,
Pikitch,
E.K.,
Ward-Paige,
C.,
Davis,
B.,
Kessel,
S.,
Hei-
thaus,
M.,
Worm,
B.,
2013.
Give
shark
sanctuaries
a
chance.
Science
339,
757.
Clarke,
S.C.,
Magnussen,
J.E.,
Abercrombie,
D.L.,
McAllister,
M.K.,
Shivji,
M.S.,
2006.
Identification
of
shark
species
composition
and
proportion
in
the
Hong
Kong
shark
fin
market
based
on
molecular
genetics
and
trade
records.
Conserv.
Biol.
20,
201–211.
Dubinsky,
Z.,
Stambler,
N.,
2011.
Coral
Reefs:
An
Ecosystem
in
Transition.
Springer
Science
+
Business
Media
B.V.
Ferretti,
F.,
Worm,
B.,
Britten,
G.L.,
Heithaus,
M.R.,
Lotze,
H.K.,
2010.
Patterns
and
ecosystem
consequences
of
shark
declines
in
the
ocean.
Ecol.
Lett.
13,
1055–1071.
Holmes,
B.H.,
Steinke,
D.,
Ward,
R.D.,
2009.
Identification
of
shark
and
ray
fins
using
DNA
barcoding.
Fish.
Res.
95,
280–288.
Last,
P.R.,
Stevens,
J.D.,
1994.
Sharks
and
Rays
of
Australia.
CSIRO
Publishing,
Victoria,
Australia.
Liu,
S.Y.V.,
Chan,
C.L.C.,
Lin,
O.,
Hu,
C.S.,
Chen,
C.A.,
2013.
DNA
barcoding
of
shark
meats
identify
species
composition
and
CITES-listed
species
from
the
markets
in
Taiwan.
PLoS
One
8,
e79373.
Moftah,
M.,
Aziz,
S.H.A.,
El
Ramah,
S.,
Favereaux,
A.,
2011.
Classification
of
sharks
in
the
Egyptian
Mediterranean
waters
using
morphological
and
DNA
barcoding
approaches.
PLoS
One
6,
e27001.
Myers,
R.A.,
Baum,
J.K.,
Shepherd,
T.D.,
Powers,
S.P.,
Peterson,
C.H.,
2007.
Cascading
effects
of
the
loss
of
apex
predatory
sharks
from
a
coastal
ocean.
Science
315,
1846–1850.
Nadon,
M.O.,
Baum,
J.K.,
Williams,
I.D.,
Mcpherson,
J.M.,
Zgliczynski,
B.J.,
Richards,
B.L.,
Schroeder,
R.E.,
Brainard,
R.E.,
2012.
Re-creating
missing
population
base-
lines
for
pacific
reef
sharks.
Conserv.
Biol.
26,
493–503.
Oliver,
S.P.,
Hussey,
N.E.,
Turner,
J.R.,
Beckett,
A.J.,
2011.
Oceanic
sharks
clean
at
coastal
seamount.
PLoS
One
6,
e14755.
Ovenden,
J.R.,
Kashiwagi,
T.,
Broderick,
D.,
Giles,
J.,
Salini,
J.,
2009.
The
extent
of
population
genetic
subdivision
differs
among
four
co-distributed
shark
species
in
the
Indo-Australian
archipelago.
BMC
Evol.
Biol.
9,
40.
Pinhal,
D.,
Shivji,
M.S.,
Nachtigall,
P.G.,
Chapman,
D.D.,
Martins,
C.,
2012.
A
stream-
lined
DNA
tool
for
global
identification
of
heavily
exploited
coastal
shark
species
(genus
rhizoprionodon).
PLoS
One
7,
e34797.
Robbins,
W.D.,
Hisano,
M.,
Connolly,
S.R.,
Choat,
J.H.,
2006.
Ongoing
collapse
of
coral-
reef
shark
populations.
Curr.
Biol.
16,
2314–2319.
Roberts,
C.M.,
McClean,
C.J.,
Veron,
J.E.N.,
Hawkins,
J.P.,
Allen,
G.R.,
McAllister,
D.E.,
Mittermeier,
C.G.,
Schueler,
F.W.,
Spalding,
M.,
Wells,
F.,
Vynne,
C.,
Werner,
T.B.,
2002.
Marine
biodiversity
hotspots
and
conservation
priorities
for
tropical
reefs.
Science
295,
1280–1284.
Sandin,
S.A.,
Smith,
J.E.,
Demartini,
E.E.,
Dinsdale,
E.A.,
Donner,
S.D.,
Friedlander,
A.M.,
Konotchick,
T.,
Malay,
M.,
Maragos,
J.E.,
Obura,
D.,
Pantos,
O.,
Paulay,
G.,
Richie,
M.,
Rohwer,
F.,
Schroeder,
R.E.,
Walsh,
S.,
Jackson,
J.B.C.,
Knowlton,
N.,
Sala,
E.,
2008.
Baselines
and
degradation
of
coral
reefs
in
the
Northern
Line
Islands.
PLoS
One
3,
e1548.
Tamura,
K.,
Dudley,
J.,
Nei,
M.,
Kumar,
S.,
2007.
MEGA4:
molecular
evolution-
ary
genetics
analysis
(MEGA)
software
version
4.0.
Mol.
Biol.
Evol.
24,
1596–
1599.
Tull,
M.,
2009.
The
History
of
Shark
Fishing
in
Indonesia.
Asia
Research
Centre,
Murdoch
University,
Perth,
Australia,
pp.
1–24.
Walsh,
P.S.,
Metzger,
D.A.,
Higuchi,
R.,
1991.
Chelex
100
as
a
medium
for
simple
extraction
of
DNA
for
PCR-based
typing
from
forensic
material.
Biotechniques
10,
506–513.
Wong,
E.H.K.,
Shivji,
M.S.,
Hanner,
R.H.,
2009.
Identifying
sharks
with
DNA
barcodes:
assessing
the
utility
of
a
nucleotide
diagnostic
approach.
Mol.
Ecol.
Resour.
9,
243–256.