Hemiscyllium halmahera, a new species of Bamboo Shark (Hemiscyllidae) from Indonesia

Abstract

Hemiscyllium halmahera new species is described from
two specimens, 656-681 mm TL, collected at Ternate,
Halmahera, Indonesia. The new species is clearly differentiated
on the basis of colour pattern. Its features include a
general brown colouration with numerous clusters of
mainly 2-3 dark polygonal spots, widely scattered white
spots in the matrix between dark clusters, relatively few (<
10), large dark spots on the interorbital/snout region, a
pair of large dark marks on the ventral surface of the head,
and a fragmented post-cephalic mark consisting of a large
U-shaped dark spot with a more or less continuous white
margin on the lower half, followed by a vertical row of
three, smaller clusters of 2-3 polygonal dark marks. The
new species is most similar in general appearance to H.
galei from Cenderawasih Bay, West Papua, which differs in
having 7-8 large, horizontally elongate dark spots on the
lower side between the abdomen and caudal-fin base, a
cluster of solid dark post-cephalic spots, and usually about
25 dark spots on the upper surface of the head.

Full text

Abstract
Hemiscyllium halmahera new species is described from
two specimens, 656-681 mm TL, collected at Ternate,
Halmahera, Indonesia. The new species is clearly differen-
tiated on the basis of colour pattern. Its features include a
general brown colouration with numerous clusters of
mainly 2-3 dark polygonal spots, widely scattered white
spots in the matrix between dark clusters, relatively few (<
10), large dark spots on the interorbital/snout region, a
pair of large dark marks on the ventral surface of the head,
and a fragmented post-cephalic mark consisting of a large
U-shaped dark spot with a more or less continuous white
margin on the lower half, followed by a vertical row of
three, smaller clusters of 2-3 polygonal dark marks. The
new species is most similar in general appearance to H.
galei from Cenderawasih Bay, West Papua, which differs in
having 7-8 large, horizontally elongate dark spots on the
lower side between the abdomen and caudal-fin base, a
cluster of solid dark post-cephalic spots, and usually about
25 dark spots on the upper surface of the head.
Zusammenfassung
Beschrieben wird die neue Art Hemiscyllium halmahera
auf der Grundlage von zwei Exemplaren mit 656-681 mm
TL (Gesamtlänge), die bei Ternate, Halmahera, in Indone-
sien gefangen wurden. Sie sind durch ihr Farbmuster ein-
deutig unterscheidbar. Zu den Merkmalen der neuen Art
gehören eine allgemein bräunliche Farbgebung mit zahlre-
ichen Gruppen von meist 2-3 dunklen vieleckigen
Flecken, weit verteilte weiße Flecken in der Grundfarbe
zwischen den schwarzen Fleckengruppen, relativ wenige (<
10) große dunkle Flecken in der Zwischen-Augen- und
Schnauzenregion, ein Paar großer dunkler Zeichen an der
bauchwärtigen Oberfläche des Kopfes sowie ein zusam-
mengesetztes Zeichen hinter dem Kopf, das aus einem
großen dunklen U-förmigen Fleck mit mehr oder weniger
durchgehendem weißen Rand im unteren Teil und einer
senkrechten Reihe von drei kleineren Gruppen aus 2-3
dunklen vieleckigen Markierungen besteht. Im allge-
meinen Erscheinungsbild ähnelt die neue Art stark H. galei
von der Cenderawasih-Bucht, West-Papua, deren Vertreter
sich aber durch 7-8 große, waagerecht längliche dunkle
Flecken an der Unterseite zwischen Abdomen und Basis
der Schwanzflosse unterscheiden, sowie durch eine
Gruppe einheitlich dunkler Flecken hinter dem Kopf und
gewöhnlich 25 dunkle Flecken auf der Kopfoberseite.
Résumé
Hemiscyllium halmahera, une nouvelle espèce, est décrit sur
base de deux spécimens, 656-681 mm de LT, collectés à Ter-
nate, Halmahera, Indonésie. La nouvelle espèce se distingue
clairement par le patron de coloration. Ses caractéristiques
comprennent une coloration d’ensemble brune avec nombre
de groupes de généralement 2-3 taches polygona les som-
bres, des taches blanches largement disséminées sur la
matrice parmi des groupes sombres, relativement peu
(moins de 10) de grandes taches foncées dans la région in te -
ror bitale/rostrale, une paire de grandes marques sombres sur
la partie ventrale de la tête et une marque fragmentée po st -
céphalique qui consiste en une grande tache sombre en for -
me de U avec une marge blanche plus ou moins continue
sur la moitié inférieure, suivie d’une rangée verticale de trois
amas plus petits de 2-3 marques polygonales foncées. En ap -
parence générale, la nouvelle espèce évoque le plus H. galei
de Cenderawasih Bay, West Papua, qui diffère par la pré -
sence de 7-8 grandes taches sombres étalées à l’horizontale
sur le côté inférieur, entre l’abdomen et la base de la caudale,
par un ensemble de taches postcéphaliques foncées et, gé -
néralement, d’environ 25 taches sombres sur la partie
supérieure de la tête.
aqua vol. 19 no. 3 - 19 July 2013
123
aqua, International Journal of Ichthyology
Hemiscyllium halmahera, a new species of Bamboo Shark (Hemiscylliidae)
from Indonesia
Gerald R. Allen1, Mark V. Erdmann2, 4 and Christine L. Dudgeon3
1) Department of Aquatic Zoology, Western Australian Museum, Locked Bag 49, Welshpool DC,
Perth, Western Australia 6986. Email: tropical_reef@bigpond.com
2) Conservation International Marine Program, Jl. Dr. Muwardi No. 17, Renon,
Denpasar 80235, Bali, Indonesia
3) University of Queensland, School of Veterinary Sciences, Gatton, Queensland, 4343, Australia
4) California Academy of Sciences, Golden Gate Park, San Francisco, CA 94118, USA
Received: 28 April 2013 – Accepted: 21 June 2013

Sommario
Hemiscyllium halmahera nuova specie è descritta sulla
base di due esemplari, di 656-681 mm TL, raccolti a Ter-
nate, Halmahera, Indonesia. La nuova specie è chiara-
mente distinguibile sulla base della colorazione. Questa
include una tonalità bruna diffusa con numerosi grappoli
di 2-3 macchie poligonali scure, macchie bianche spar -
pagliate nella matrice tra i grappoli scuri, relativamente
poche (<10) grandi macchie scure sulla regione interor-
bitale/muso, un paio di grandi screziature scure sulla
superficie ventrale della testa e una in sede post-cefalica,
frammentata, composta da una grande macchia scura a
forma di U con un margine bianco più o meno continuo
nella metà inferiore, seguita da una fila verticale di tre
grappoli minori di 2-3 macchie poligonali scure. La nuova
specie è molto simile nell’aspetto generale a H. galei della
Cenderawasih Bay, Papua occidentale, che si distingue per
avere 7-8 grandi macchie scure, allungate orizzontalmente
sul lato inferiore tra l'addome e la base della pinna caudale,
un gruppo di ben definite macchie scure post-cefaliche e di
solito per circa 25 macchie scure sulla superficie superiore
della testa.
INTRODUCTION
The family Hemiscylliidae, commonly known as
bamboo, epaulette, or walking sharks, contains
small, slender sharks characterised by nasoral and
perioral grooves, short barbels, a small transverse
mouth below the eyes, two similar-sized dorsal fins,
and a long slender tail. Only two genera are known,
both described by Müller & Henle (1837 & 1838),
Chiloscyllium with seven Indo-Pacific species, and
Hemiscyllium with nine species, including the new
taxon described herein. The family was last
reviewed by Compagno (2002), who recognized
five Hemiscyllium: H. freycineti (Quoy & Gaimard,
1824), H. hallstromi Whitley, 1967, H. ocellatum
(Bonnaterre, 1788), H. strahani Whitley, 1967, and
H. trispeculare Richardson, 1843. Two additional
species, H. galei and H. henryi were described by
Allen & Erdmann (2008) from the Bird’s Head
Peninsula of western New Guinea (West Papua
Province, Indonesia), and a third addition, H.
michaeli was described by Allen & Dudgeon (2010)
from eastern Papua New Guinea. The members of
the genus are morphologically very similar, and
unfortunately most species are poorly represented
in museum collections, precluding detailed mor-
phological/meristic comparisons. Therefore, colour
patterns and genetic differences remain the most
valuable “tools” for distinguishing species.
Sharks of the genus Hemiscyllium are small (usu-
ally under about 80 cm), nocturnally active, bot-
tom-living animals, which exhibit a peculiar “walk-
ing” gait while foraging for benthic invertebrates
and fishes. Although biological data is sparse for
most species, they are generally oviparous with
elliptical egg capsules being deposited on the reef.
Hatchlings are rarely encountered, but the few
reported specimens were about 15 cm TL (Com-
pagno, 2001).
Due to their reproductive mode, limited swim-
ming ability, and poor dispersal capability most
species have restricted distributions. The two Aus-
tralian species, H. ocellatum and H. trispeculare, are
the most widespread, ranging around most of the
northern half of the continent. The remaining
species, with the exception of the new species
described below, have restricted regional New
Guinea distributions (indicated in parentheses;
also see Fig. 1): H. freycineti (Raja Ampat Islands,
and possibly adjacent West Papua mainland), H.
galei (Cenderawasih Bay, West Papua), H. hall-
stromi (Gulf of Papua to Milne Bay Province,
Papua New Guinea), H. henryi (Kaimana coastline
and Triton Bay, West Papua), H michaeli (Milne
Bay and Oro provinces, Papua New Guinea), and
H. strahani (Madang along north coast of Papua
New Guinea to Jayapura, Papua Province, Indone-
sia). All of these species were illustrated and dis-
cussed by Allen & Erdmann (2012).
The current paper describes a new species from
Halmahera, the first record for the genus from
beyond the Australia-New Guinea region. Two
specimens and tissue samples of each were col-
lected by M. Erdmann during a night dive at the
island of Ternate in the Halmahera group of
islands, Indonesia. Subsequent DNA analysis indi-
cates it is a separate species.
MATERIALS AND METHODS
Technical terms and measurements mainly follow
those explained and illustrated by Compagno
(2001). Snout length is the distance from the snout
tip to the anterior edge of the mouth. Subcaudal
length is the combined measurement of the upper
postventral caudal-fin margin and terminal caudal-
fin margin. Total length and head length are abbre-
viated as TL and HL respectively. Vertebral counts
were obtained from radiographs. Vertebral counts
and measurements for the holotype are given first
followed by the range for paratypes (in parenthe-
ses) in the description below. Type specimens are
deposited at Museum Zoologicum Bogoriense,
Cibinong, Indonesia (MZB) and the Western Aus-
tralian Museum, Perth (WAM).
aqua vol. 19 no. 3 - 19 July 2013 124
Hemiscyllium halmahera, a new species of Bamboo Shark (Hemiscylliidae) from Indonesia

Tissue samples were obtained for both type spec-
imens of the new taxon from Ternate, Indonesia.
This was compared with samples of H. freycineti,
H. galei, H. henryi, H. michaeli, and H. ocellatum,
which had been previously analysed (Allen and
Erdmann 2008; Allen and Dudgeon, 2010). Total
genomic DNA was extracted from 25 mg of fin tis-
sue using the DNeasy Tissue Extraction Kit (Qia-
gen) following the instructions of the supplier. A
fragment including partial mitochondrial NADH
Dehydrogenase subunit 4 gene (ND4), tRNA-His
and tRNA-Ser genes was amplified through poly-
merase chain reaction (PCR) using the primers:
ND4-F: 5’ - CACCTATGACTACCAAAAGCT-
CATGTAGAAGC - 3’ (Arevalo et al. 1994) and
H12293-Leu-R: 5’ – TTGCACCAAGAG -
TTTTT GGTTCCTAAGACC - 3’ (Inoue et al.
2001). Reactions were conducted in 30 µl total
amounts and consisted of: 10 µM each primer, 400
µM of each dNTP, 3 units Taq polymerase, 1 x
PCR Buffer (Qiagen) and 30-50 ng extracted
DNA. PCRs were conducted on 9700 Perkin
Elmer thermocyclers and consisted of an initial
denaturation step at 95°C for 5 min, followed by
30 cycles of 95°C for 15 sec, 56°C for 30 sec and
72°C for 1 min, and a final extension at 72°C for
7 min. The PCR products were cleaned using Iso-
late PCR and Gel Kit (Bioline). Sequences were
conducted in both forward and reverse directions
using Big Dye Terminator v3.1 Cycle Sequencing
Kit (Applied Biosystems) following manufacturer’s
instructions. Sequencing products (20ul) were pre-
cipitated by adding 5 µl EDTA (125mM, pH8.0)
and 60 µl 100% ethanol and centrifuged for 45
min at 3000 rpm (30 cm diameter rotor). The pel-
let was washed with 60 µl 70% ethanol and cen-
trifuged for 15 min at 3000 rpm and then products
resolved on a 3730xl Genetic Analyser (Applied
Biosystems).
Sequences were aligned using Sequencher version
4.6 (Gene Codes). All molecular statistical analyses
were conducted using Mega version 5 (Tamura et
al. 2011). Maximum likelihood analysis was used
to assess the model of best fit for the nucleotide
substitution. Both Bayesian Information Criterion
(BIC) and Akaike’s Information Criterion cor-
rected for small sample sizes (AICc) ranked the
Tamura-Nei substitution model (Tamura & Nei
1993) with a discrete Gamma distribution
(TN93+G; G=0.38) as having the best fit to the
data. The Tamura-Nei (Tamura & Nei 1993) sub-
stitution model accounts for variable base frequen-
aqua vol. 19 no. 3 - 19 July 2013
125
Gerald R. Allen, Mark V. Erdmann and Christine L. Dudgeon
Fig. 1. Map of New Guinea and Halmahera showing collection/observation locations of resident species of Hemiscyllium:
H. freycineti (yellow circles), H. galei (white star), H. henryi (yellow star), H. hallstromi (white squares), H. halmahera (green
circles), H. strahani (red squares), and H. michaeli (red circles).

cies, transition rates and rate variation among sites.
The TN93+G model was used to construct phylo-
genetic trees with maximum likelihood analysis.
Maximum parsimony trees were also constructed
with a specimen of Chiloscyllium punctatum as the
outgroup taxon. Confidence in tree topology was
evaluated by bootstrapping across 1000 bootstrap
replicates (Felsenstein 1985). Pairwise distances
within and between putative taxa were calculated
using the TN93+G model with 1000 bootstrap
replicates.
Hemiscyllium halmahera n. sp.
Halmahera Epaulette Shark
(Figs 2-7; Tables I-II)
Holotype: MZB 21248, male, 681 mm TL, north-
western Ternate, 00°50.958’N, 127°18.717’E,
Halmahera, Indonesia, 10 m, captured by hand,
M. Erdmann, 1 May 2012.
Paratype: WAM P. 33784-001, female, 656 mm
TL, collected with holotype.
Diagnosis: A species of bamboo shark belonging
to the genus Hemiscyllium, distinguished from all
congeners by a unique colour pattern, particularly
a light brown background colour with numerous
clusters of mainly 2-3 dark polygonal spots, widely
scattered white spots in the matrix between dark
clusters, relatively few (< 10), large dark spots on
the interorbital/snout region, pair of large dark
marks on ventral surface of head, and fragmented
post-cephalic mark consisting of a large U-shaped
dark spot with more or less continuous white mar-
gin on lower half, followed posteriorly by vertical
row of three, smaller clusters of 2-3 polygonal dark
marks. It lacks diagnostic colour pattern features
that typify the other known species in the genus,
including a black hood or face-mask marking on
the head (H. strahani), large intensely black ovate
spots on body (H. hallstromi), ocellated shoulder
spot and numerous small black spots on body (H.
ocellatum), ocellated shoulder spot with two curved
black marks on posterior edge and numerous dif-
fuse dark spots on head body and fins (H. trispecu-
lare), row of 7-8 large, horizontally ovate dark spots
on lower side between abdomen and caudal-fin
base (H. galei), “double-ocellus” shoulder marking
(H. henryi), diffuse shoulder marking, numerous
dark spots on dorsal surface of head, and pair of
aqua vol. 19 no. 3 - 19 July 2013 126
Hemiscyllium halmahera, a new species of Bamboo Shark (Hemiscylliidae) from Indonesia
Fig. 2. Underwater photograph of Hemiscyllium halmahera, male holotype, Ternate Island, Halmahera, Indonesia at depth of
10 m. Photo by M. V. Erdmann.

closely spaced dark post-cephalic ocelli surrounded
by white halo (H. freycineti), and dense pattern of
leopard-like dark spots (H. michaeli).
Description: Total vertebral centra 195 (includes
39-40 monospondylous centra, 101-102 diplos -
pondylous precaudal centra, and 54 caudal centra);
body and tail relatively slender, tapering posteri-
orly; precaudal length 1.3 and HL 6.7 (7.5-8.0) in
TL; head height (at pectoral-fin origin) 1.2 in
greatest width of head; eye length 3.4 (3.2) in
snout length, eye height 1.9 (2.7) in eye length;
fleshy interorbital space 1.4 and bony interorbital
space 1.7 in snout length; snout blunt and short,
snout tip to eye 2.2 (2.4), snout tip to mouth 4.6
aqua vol. 19 no. 3 - 19 July 2013
127
Gerald R. Allen, Mark V. Erdmann and Christine L. Dudgeon
Fig. 3. Underwater photographs of Hemiscyllium halmahera: upper – approximately 650 mm TL, Bacan Island, Halmahera,
Indonesia at depth of 10 m. Photo by J. Yonover. Lower – approximately 700 mm TL, Weda Bay, Halmahera, at depth of
5 m. Photo by T. Mulder.

(5.8), snout tip to spiracle 1.8 (2.0), snout tip to
first gill slit 1.1, all in HL; gill slits on rear part of
head, above to slightly anterior of pectoral-fin base;
distance between first and fifth gill slit 2.5 (2.7) in
HL; height of gill slits gradually increasing posteri-
orly, the first 3.9 and fifth 2.7 (2.8) in snout
length.
Mouth small and transverse, positioned well for-
ward on ventral surface of head, its width 1.2 (1.3)
in snout length; short barbel on each side of ven-
tral snout, its length 5.2 (4.6) in snout length;
maximum width of lower labial flap 5.0 (5.3),
length of postoral fold (upper labial furrow) 3.4
(3.1), length of lower labial furrow 4.5 (5.3), all in
snout length; teeth pavement-like, composed of
numerous rows; individual teeth broad-based with
single posteriorly-directed cusp, the cusps of inner-
most rows more developed.
Pre-first dorsal length 2.6 (2.5), prepelvic length
3.4 (3.2), snout to vent length 3.1 (3.0), vent to
anal-fin origin 2.3 (2.4), vent to caudal-fin length
1.3, all in TL. Pectoral fins below gill openings,
their length 1.1 (1.2) in HL; pelvic fins immedi-
ately anterior to vertical line passing through first
dorsal-fin origin, their length 1.2 (1.4) in HL; dor-
sal fins positioned well back on body, first and sec-
ond dorsal fins nearly equal in height; first dorsal-
fin base 1.5 (1.8) in HL, first dorsal-fin height 1.1
in first dorsal-fin base; free margin of first dorsal
fin 2.1 (1.4) in first dorsal-fin height; interdorsal
space 1.1 in HL; second dorsal-fin base 1.6 (1.7) in
HL; second dorsal-fin height 1.0 (1.1) in second
dorsal-fin base; free margin of second dorsal fin 2.0
(1.9) in second dorsal-fin height; long and low anal
fin just anterior to caudal fin; anal-fin base 1.4
(1.7) in HL, anal-fin height 3.3 (2.7) in anal-fin
base; free margin of anal fin 1.5 (1.8) in anal-fin
height; elongate and thick precaudal tail (section of
body between anus and caudal fin), its depth at
level of anal-fin origin 2.2 (2.6) in head length;
subcaudal length 6.2 (5.7) in TL.
Clasper of adult male holotype (Fig. 4A) relatively
stout and elongate, its length greater than first dor-
sal-fin height.
Colour in life (Figs. 2-3): generally brown
on snout, dorsally on head and body, grading to
golden brown on lower side of body, and white on
ventral surface; numerous clusters of mainly 2-3
dark polygonal spots (largest about equal to eye)
and widely scattered, much smaller, white spots in
brownish matrix between dark clusters; two
(paratype) or three (holotype), progressively
smaller dark grey brown saddles across back from
rear edge of head to dorsal-fin base, a similar sad-
dle between dorsal fins, and 4-5 additional dark
saddles on dorsal edge of tail; four large saddles on
body with narrow white or pale grey anterior and
aqua vol. 19 no. 3 - 19 July 2013 128
Hemiscyllium halmahera, a new species of Bamboo Shark (Hemiscylliidae) from Indonesia
Holotype Paratype
Measurement MZB WAM
21248 P. 33784
Sex male female
Total length (mm) 681 656
Precaudal length 78.4 76.5
Head width 8.8 8.3
Head depth 7.3 6.7
Preanal body depth 5.3 5.2
Snout - pectoral-fin origin (HL) 12.5 13.4
Snout - 1st gill slit 11.5 11.9
1st to 5th gill slit 5.0 4.9
First gill slit height 1.5 1.4
Fifth gill slit height 2.1 2.0
Eye diameter (horizontal) 1.7 1.8
Eye diameter (vertical) 0.9 0.7
Bony interorbital width 3.5 3.3
Fleshy interorbital width 4.1 3.9
Snout to eye (snout length) 5.8 5.7
Snout to spiracle 6.8 6.6
Snout to mouth 2.7 2.3
Lower labial furrow length 1.3 1.1
Maximum width lower labial flap 1.1 1.1
Postoral fold 1.7 1.8
Mouth width 4.9 4.2
Barbel length 1.1 1.2
Snout -1st dorsal origin 37.9 40.2
Snout - pelvic origin 29.0 31.2
Snout - anal opening 32.2 33.6
Anal opening - anal-fin origin 42.9 40.8
Anal opening - tail tip 68.8 67.1
Interdorsal distance 11.3 11.8
Pectoral-fin length 11.7 11.0
Pelvic-fin length 10.4 9.9
1WAM dorsal fin base 8.5 7.4
1st dorsal-fin height 8.1 6.5
1st dorsal-fin free margin 4.9 4.5
2nd dorsal-fin base 8.1 7.7
2nd dorsal-fin height 7.4 7.4
2nd dorsal-fin free margin 3.7 4.0
Anal-fin base 9.2 7.8
Anal-fin height 2.8 2.9
Anal-fin free margin 1.9 1.6
Subcaudal 16.2 17.6
Clasper length (inner) 8.9 -
Clasper length (outer) 6.3 -
Table I. Proportional measurements (as percentage of total
length) for type specimens of Hemiscyllium halmahera.

posterior margins; fragmented post-cephalic mark
(Fig. 4B), consisting of a large U-shaped dark spot
with more or less continuous white margin on
lower half, followed by vertical row of three,
smaller clusters of 2-3 polygonal dark marks; pair
of large round to oval dark marks (Fig. 4C) on ven-
tral surface of head at about level of spiracle; lower
side of head, below and slightly posterior to spira-
cle with 2-3 large, irregular dark spots; relatively
few (< 10) large (smaller than eye, Fig. 4D), dark
spots on interorbital/snout region; each dorsal fin
with few poorly defined brown spots and pair of
prominent blackish saddles on anterior edge, the
lowermost ocellus-like with white margin around
lower edge; pectoral and pelvic fins with 8-10 and
6-11 variable-sized brown spots respectively on
dorsal surface and narrow white posterior margin.
Colour in alcohol (Figs 5-7) similar to the
aqua vol. 19 no. 3 - 19 July 2013
129
Gerald R. Allen, Mark V. Erdmann and Christine L. Dudgeon
H. halmahera H. michaeli H. freycineti H. galei H. henryi H. ocellatum C. punctatum
H. halmahera - 0.0052 0.0058 0.0066 0.0059 0.0065 0.0219
H. michaeli 0.0201 - 0.0056 0.0060 0.0057 0.0068 0.0237
H. freycineti 0.0229 0.0226 - 0.0043 0.0036 0.0072 0.0202
H. galei 0.0286 0.0254 0.0130 - 0.0047 0.0077 0.0209
H. henryi 0.0229 0.0227 0.0103 0.0184 - 0.0073 0.0203
H. ocellatum 0.0314 0.0329 0.0372 0.0401 0.0371 - 0.0215
C. punctatum 0.1627 0.1747 0.1545 0.1588 0.1547 0.1572 -
Table II. Inter-specific pairwise distance matrix (below diagonal) calculated from the TN93+G model with
corresponding matrix (above diagonal) of SE estimates (bootstrap method, 1000 replicates).
Fig. 4A-D. Diagnostic features of Hemiscyllium halmahera: A. claspers of male holotype; B. post-cephalic marking of holo-
type; C. ventral surface of head of female paratype; D. dorsal surface of head of male holotype. Photos by G. R. Allen.

aqua vol. 19 no. 3 - 19 July 2013 130
Hemiscyllium halmahera, a new species of Bamboo Shark (Hemiscylliidae) from Indonesia
Fig. 5. Hemiscyllium halmahera, preserved male holotype, 681 mm TL, Ternate, Halmahera, Indonesia. Photo by G. R. Allen.
Fig. 7. Hemiscyllium halmahera, preserved female paratype, 656 mm TL, Ternate, Halmahera, Indonesia. Photo by G. R. Allen.
Fig. 6. Hemiscyllium halmahera, dorsal view of preserved holotype, 681 mm TL, Ternate, Halmahera, Indonesia. Photo by
G. R. Allen.

aqua vol. 19 no. 3 - 19 July 2013
131
Gerald R. Allen, Mark V. Erdmann and Christine L. Dudgeon
Fig. 8. Underwater photograph of Hemiscyllium michaeli, approximately 600 mm TL, Milne Bay Province, Papua New
Guinea. Photo by B. Halstead.
Fig. 9. Underwater photograph of Hemiscyllium freycineti, approximately 600 mm TL, Kri Island, Raja Ampat Islands, West
Papua Province, Indonesia. Photo by G. R. Allen.

live colour provided above, except the ground
colour is tan to reddish brown and the dark spot-
ting on the head, body, and fins is less intense.
DNA Analysis: In total, we analysed a 792 base
pair (bp) alignment of the mitochondrial ND4
gene from 18 Hemiscyllium individuals and one
Chiloscyllium punctatum individual. There were
two new samples for H. halmahera that were com-
pared with the 16 sequences included in the previ-
ous genetic analyses from Allen and Erdmann
(2008) (H. henryi = 4; H. ocellatum = 5; H.
freycineti = 4; H. galei = 2) and Allen and Dudgeon
(2010) (H. michaeli = 1). The two H. halmahera
samples had identical sequences. A total of 6 hap-
lotypes were detected for all Hemiscyllium species
with all species having one haplotype, except for H.
ocellatum with two haplotypes. In the total Hemi -
scyllium alignment there were 50 variable sites and
43 parsimony-informative characters. Nucleotide
frequencies of H. halmahera were similar to the
other species and average frequencies for the com-
bined Hemiscyllium samples were as follows: A =
32, C = 24, G = 0.11, T = 32. Pairwise distances
(d) between the Hemiscyllium species ranged from
0.0103-0.0401. The H. halmahera samples clearly
differed from all the other Hemiscyllium species
with pairwise distances ranging from 0.0201-
0.0314 which fall within the range of inter-species
differences for the other members of the genus.
Pairwise distances between the Hemiscyllium
species and the outgroup Chiloscyllium punctatum
(dave= 0.1559) were over an order of magnitude
higher than some of the intra-genus distances.
Only H. ocellatum showed intra-species distance
(d = 0.0013) which was an order of magnitude
lower than the intra genus distances.
The maximum likelihood (ML) and maximum
parsimony (MP) trees both clearly separated out
H. halmahera from the morphologically similar H.
galei. H. halmahera was positioned in a basal posi-
tion of the Hemiscyllium samples with H. michaeli.
The phylogenetic analyses produced identical trees
for most of taxa, but could not resolve the relative
positioning of H. halmahera and H. michaeli with
ML analyses placing H. michaeli in the most basal
position (with low bootstrap support = 49%) and
MP analyses reversing this relationship (bootstrap
support = 62%; Fig. 11).
Distribution and habitat: The new species is
known with certainty from satellite islands off the
west coast of Halmahera, Indonesia and in Weda
Bay in South Halmahera. The type specimens were
collected at night in 10 m depth, nestling under
coral heads that were sparsely scattered on a steep,
black volcanic sand slope off northwestern Ternate
Island. It has also been photographed off south-
aqua vol. 19 no. 3 - 19 July 2013 132
Hemiscyllium halmahera, a new species of Bamboo Shark (Hemiscylliidae) from Indonesia
Fig.10. Underwater photograph of Hemiscyllium galei, approximately 600 mm TL, Cenderawasih Bay, West Papua Province,
Indonesia. Photo by G. R. Allen.

western Halmahera at Proco Island (00°25.264’S,
127°44.264’E), which lies in the Proco Strait
between Bacan and mainland Halmahera; at Bacan
Island (00°20.371’S, 127°18.153’E); and in Weda
Bay in southern Halmahera (00°27.935’N, 127°
56.753’E) .
Etymology: The species is named H. halmahera
with reference to the type locality. The name is
treated as a noun in apposition.
Remarks: The new species is the first record for
Hemiscyllium beyond the Australia/New Guinea
region. Although Halmahera lies in close proxim-
ity to New Guinea, the current study extends the
known boundary for the genus approximately 300
km further west. As mentioned previously, Hemi -
scyllium species appear to have limited dispersal
capabilities, including an apparent inability to
cross significant deep-water barriers. For example,
the genus is unknown from the island of New
Britain, which lies only about 80 km from the
aqua vol. 19 no. 3 - 19 July 2013
133
Gerald R. Allen, Mark V. Erdmann and Christine L. Dudgeon
Fig. 11. Maximum likelihood (ML) tree (TN93+G) of the ND4 data for six Hemiscyllium species. Bootstrap support for
1000 replicates are shown for ML and Maximum Parsimony (MP) trees respectively. ML and MP trees are identical except
for the relative positions of H. halmahera and H. michaeli, which are reversed in the MP phylogeny with bootstrap support
of 62% (indicated by *). The outgroup is Chiloscyllium punctatum Müller & Henle, 1838, a member of the other genus in
the family Hemiscylliidae.

Papua New Guinea mainland. Based on paleogeo-
graphic reconstructions presented by Hall (2002)
and Hill & Hall (2003) it seems likely that the
ancestral population may have colonized Halma-
hera sometime after 25 MYA when its island-arc
fragments precursor came within close proximity
of the northern New Guinea mainland. Then
according to these reconstructions, the component
parts of Halmahera underwent a long, slow west-
ward drift during the Miocene and Pliocene, arriv-
ing at their present position over the past few mil-
lion years. Therefore, it seems highly likely that the
ancestral population of H. halmahera was rafted
from a distant colonization point to its current
location. Similar scenarios involving dispersal of
New Guinea freshwater Heteroptera (water strid-
ers) via island arc fragments were discussed by Pol-
hemus & Polhemus (1998), and may also explain
the presence of the bird-of-paradise Semioptera
wallacii on Halmahera, despite the family Paradis-
aeidae otherwise being considered endemic to the
island of New Guinea and Australia (Irestedt et al.,
2009). We moreover note that there are a number
of examples of restricted range New Guinea reef
fish species whose ranges just penetrate into
Halmahera, including Pseudochromis ammeri Gill,
Allen and Erdmann, 2012, P. matahari Gill, Erd-
mann and Allen, 2009, P. pylei Randall and
McCosker, 1989, and Pentapodus numberii Allen
and Erdmann, 2009, as well as a blenny (Ecsenius
randalli Springer, 1991) considered endemic to
Halmahera that is found occasionally in Raja
Ampat, West Papua.
The new species is most similar in colour pattern
to H. galei (Fig. 10) from Cenderawasih Bay, West
Papua. Both species have characteristic broad dark
saddles with narrow, white anterior and posterior
margins on the dorsal surface of the body, as well
as similar post-cephalic markings. However, there
are significant differences between the two species.
Hemiscyllium galei differs in having a row of 7-8
large, horizontally ovate spots on the lower side
between the abdomen and caudal-fin base and has
more spots (usually about 25) on the dorsal surface
of the head. In contrast, H. halmahera differs in
having far fewer head spots (usually less than 10)
and possesses a pair of large dark spots on the ven-
tral surface of the head. Although the general con-
figuration of the post-cephalic spot is similar, that
of H. halmahera consists of clusters of fragmented
spots (with a U-shaped main spot) compared to
the solid spots of H. galei.
At present, the genus is poorly represented in
museum collections and therefore morphometric
data is of limited value in separating the various
species. However, the new species appears to have
an unusually thick tail base (preanal body depth)
compared to its congeners. For example, the pre-
anal depth for H. halmahera is 2.3-2.6 in the head
length compared with values of 3.5-4.5 for H.
galei, H. henryi, and H. michaeli. However, more
specimens are required for most species to fully
evaluate these differences.
The species of Hemiscyllium are distinguished
mainly on the basis of colour pattern. The follow-
ing key will serve to identify the nine known
species.
Key to the Species of Hemiscyllium
1a. Head and snout with an abrupt black hood;
body covered with conspicuous large white
spots (northern New Guinea).........................
.....................................................H. strahani
1b. Head and snout light in colour, without a black
hood but with conspicuous black spots above
pectoral fins; body with inconspicuous light
spots or spots absent.................................... 2
2a. Dark spot behind gills relatively small, forming
a weak ocellus (or semi-ocellate dark spot) and
followed posteriorly by dark brown bar (con-
sisting of 2-3 merged spots in vertical row or 2-
3 clusters of fragmented spots)..................... 3
2b. Dark spot behind gills large, forming 1-2 con-
spicuous white-rimmed ocelli or merged dou-
ble ocelli without dark brown bar immediately
behind ......................................................... 5
3a. Lower side with conspicuous horizontal row of
row of 7-8 large, horizontally-oval, dark spots
(Cenderawasih Bay, West Papua)....... H. galei
3b. Lower side without row of large, horizontally-
oval, dark spots along lower side.................. 4
4a. Ventral surface of head with pair of large dark
spots; snout region of adult with only a few
small dark spots (Halmahera)..........................
..................................................H. halmahera
4b. Ventral surface of head without pair of large
dark spots; snout region of adult with numer-
ous small dark spots (Raja Ampat Islands, West
Papua)........................................ H. freycineti
5a. Head, body, and fins covered with polygonal,
leopard-like spots (eastern Papua New Guinea)
.................................................... H. michaeli
5b. Head body, and fins covered with numerous
aqua vol. 19 no. 3 - 19 July 2013 134
Hemiscyllium halmahera, a new species of Bamboo Shark (Hemiscylliidae) from Indonesia

spots, but more or less round in shape and not
polygonal and leopard like .......................... 6
6a. Body covered with numerous, densely clus-
tered, dark small and large spots that form a
reticular network of light base colour between
them; dark cross-bands well defined on ventral
surface of tail (northern Australia)...................
............................................... H. trispeculare
6b. Body with fewer large spots that do not form a
reticular network of light ground colour
between them; dark cross-bands on tail rela-
tively weak or not reaching ventral surface......
.................................................................... 7
7a. Lateral ocellus surrounded by large black spots;
spots absent on head in front and below eyes
(south-eastern Papua New Guinea).................
................................................. H. hallstromi
7b. Lateral ocellus surrounded by relatively small
spots; spots present on head in front and below
eyes.............................................................. 8
8a. Lateral ocellus composed of single large, round
spot surrounded by distinct white halo; dark
spot absent at origin of pectoral and pelvic fins;
numerous small dark spots usually present on
dorsal fins (northern Australia) .......................
.................................................. H. ocellatum
8b. Lateral ocellus usually composed of double,
merged ocelli surrounded by poorly defined
white halo; dark spot present at origin of pec-
toral and pelvic fins; dorsal fins usually without
small dark spots or if present they are restricted
to basal portion of fins (Triton Bay region,
West Papua).................................... H. henryi
ACKNOWLEDGEMENTS
We thank Graham Abbott for first calling our
attention to the presence of Hemiscyllium on
Halmahera with his photo from Proco Strait, and
Alberth Reija, Tony Rhodes and the outstanding
crew of the Damai II live-aboard for their dive sup-
port in collecting the type specimens; dive guide
Gusti in particular deserves mention for his sharp
eyes spotting the sharks at night. Thanks are due
Dita Cahyani and the Udayana University staff for
assistance in x-raying the holotype, and Renny
Hadiaty of LIPI for assistance in curating the holo-
type. We also thank Jeff Yonover and Tom Mulder
for the use of their excellent images of the new
species, and Rob Sinke for further information on
the species in Weda Bay. Finally, we thank the gov-
ernment of Maluku Utara for permitting our trip
and for their efforts to develop marine tourism and
conservation programs to protect this unique
species on the reefs of Halmahera.
REFERENCES
ALLEN, G. R. & DUDGEON, C. L. 2010. Hemiscyllium
michaeli, a new species of bamboo shark (Hemiscyllidae)
from Papua New Guinea. aqua, International Journal of
Ichthyology 16 (1): 19-30.
ALLEN, G. R. & ERDMANN, M. V. 2008. Two new species
of bamboo sharks (Orectolobiformes: Hemiscyllidae)
from western New Guinea. aqua, International Journal of
Ichthyology 13 (3-4): 93-108.
ALLEN, G. R. & ERDMANN, M. V. 2012. Reef Fishes of the
East Indies. Volume 1. Tropical Reef Research, Perth,
Australia, 424 pp.
AREVALO, E., DAVIS, S. K. & SITES, J. W. 1994. Mito-
chondrial-DNA sequence divergence and phylogenetic-
relationships among eight chromosome races of the Scelo-
porus-Grammicus complex (Phrynosomatide) in central
Mexico. Systematic Biology 43: 387-418.
BONNATERRE, J. P. 1788. Tableau encyclopédique et method-
ique des trois règnes de la nature... Ichthyologie. Panck-
oucke, Paris.
COMPAGNO, L. J. V. 2001. Sharks of the world. An anno-
tated and illustrated catalogue of shark species known to
date. Volume 2. Bullhead, mackerel and carpet sharks (Het-
erodontiformes, Lamniformes and Orectolobiformes). FAO
Species Catalogue for Fishery Purposes. No. 1, Vol. 2.
FAO, Rome, 269 pp.
FELSENSTEIN, J. 1985. Confidence limits on phylogenies:
an approach using the bootstrap. Evolution 39: 783-791.
HALL, R. 2003. Cenozoic geological and plate tectonic
evolution of SE Asia and the SW Pacific: computer-based
reconstructions, model, and animations. Journal of Asian
Earth Sciences 20: 353-434.
HILL, K. C. & HALL, R. 2003. Mesozoic-Cenozoic evolu-
tion of Australia’s New Guinea margin in a west Pacific
context. In Hillis R.R. & Müller, R.D. (eds.) Evolution
and Dynamics of the Australian Plate, pp. 265-290. Geo-
logical Society of Australia Special Publication 22 and
Geological Society of America Special Paper 372.
INOUE, J. G., MIYA, M., TSUKAMOTO, K. & NISHIDA, M.
2001. A mitogenomic perspective on the basal teleostean
phylogeny: Resolving higher-level relationships with
longer DNA sequences. Molecular Phylogenetics and Evo-
lution 20: 275-285.
IRESTEDT, M., JØNSSON, K. A., FJELDS, Å, J., CHRISTIDIS,
L. & ERICSON, P. G. 2009. An unexpectedly long history
of sexual selection in birds-of-paradise. BMC Evolution-
ary Biology 9: 235.
MÜLLER, J. & HENLE, F. G. J. 1837. Ueber die Gattun-
gen der Plagiostomen. Archiv für Naturgeschichte 3:
394-401, 434.
MÜLLER, J. & HENLE, F. G. J. 1838. On the generic char-
acters of cartilaginous fishes, with descriptions of new
genera. Magazine of Natural History (new series) 2: 33-
37, 88-91.
aqua vol. 19 no. 3 - 19 July 2013
135
Gerald R. Allen, Mark V. Erdmann and Christine L. Dudgeon

POLHEMUS, D. A. & POLHEMUS, J. T. 1998. Assembling
New Guinea: 40 million years of island arc accretion as
indicated by the distributions of aquatic Heteroptera
(Insecta). In Hall & Holloway (eds.) Biogeography and
Geological Evolution of SE Asia, pp. 327-340. Blackhuys
Publishers, Leiden, The Netherlands.
QUOY, J. R. C. & GAIMARD, J. P. 1824-25. Description des
Poissons. Chapter IX. In: Freycinet, L. de, Voyage autour
du Monde...exécuté sur les corvettes de L. M. “L’Uranie”
et “La Physicienne,” pendant les années 1817, 1818,
1819 et 1820. Paris.
RICHARDSON, J. 1843. Icones piscium, or plates of rare
fishes. Part I. Richard and John E. Taylor, London.
TAMURA, K., PETERSON, D., PETERSON, N., STECHER, G.,
NEI, M., KUMAR, S. 2011. MEGA5: Molecular evolu-
tionary genetics analysis using maximum likelihood, evo-
lutionary distance, and maximum parisomony methods.
Molecular Biology and Evolution 28: 2731-2739.
TAMURA, K. & NEI, M. 1993. Estimation of the number
of nucleotide substitutions in the contral region of mito-
chondrial DNA in humans and chimpanzees. Molecular
Biology and Evolution 10: 512-526.
WHITLEY, G. P. 1967. Sharks of the Australasian region.
Australian Zoologist 14 (2): 173-188.
aqua vol. 19 no. 3 - 19 July 2013 136
Hemiscyllium halmahera, a new species of Bamboo Shark (Hemiscylliidae) from Indonesia