Hemiscyllium Michaeli, a New Species of Bamboo Shark (Hemiscyllidae) from Papua New Guinea

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aqua, International Journal of Ichthyology

Hemiscyllium michaeli, a new species of Bamboo Shark (Hemiscyllidae) from Papua New Guinea

Gerald R. Allen1 and Christine L. Dudgeon2

1) Department of Aquatic Zoology, Western Australian Museum, Locked Bag 49, Welshpool DC, Perth, Western Australia 6986, Australia. Email: [email protected] 2) University of Queensland, School of Biological Sciences, Brisbane, Queensland 4072, Australia

Received: 25 November 2009 – Accepted: 7 January 2010

Abstract gezählt). Der Unterschied in den Fleckenmustern zwischen Hemiscyllium michaeli new species is described from six den beiden Arten ist in der Kopfgegend besonders augenfäl- specimens, 257-695 mm TL, collected at eastern Papua lig. Außerdem weist H. michaeli n. sp. hinter dem Kopf einen New Guinea. The species was previously confused with H. markanten schwarzen Augenfleck auf, während bei H. freycineti, which is restricted to Papua Barat Province freycineti der schwarze Fleck gewöhnlich nicht besonders gut (western New Guinea), Indonesia. The two species differ abgegrenzt ist. Der Vergleich der mitochondrialen ND4 primarily in colour pattern, which provides the best means unterstützt die Auffassung einer Trennung auf Arten-Ebene. of separating the various members of the genus. Both species have a profuse covering of brown spots with a large Résumé black or brown ocellated marking on the middle of the Hemiscyllium michaeli, nouvelle espèce, est décrit sur base side, just behind the head. The spots of H. michaeli n. sp. de six spécimens, 257-695 mm de LT, collectés en are generally denser, larger, and distinctly polygonal, Papouasie-Nouvelle-Guinée orientale. L’espèce avait été remarkably similar to the spots of a leopard. In contrast confondue auparavant avec H. freycineti qui n’est réparti those of H. freycineti are round to transversely elongate and qu’en province de Papua Barat (Nouvelle-Guinée occiden- are darkened at regular intervals to form 8-9 bars or sad- tale), Indonésie. Les deux espèces se distinguent d’abord dle-like markings (including those on the tail). The differ- par le patron de coloration qui fournit la meilleure base ence in spot pattern between the two species is particularly pour délimiter les différents membres du genre. Les deux evident in the head region. In addition, H. michaeli n. sp. espèces présentent une abondance de taches brunes avec possesses a vivid ocellate black spot behind the head, une grande marque ocellée noire ou brune au milieu du whereas the black spot of H. freycineti is generally not well corps, juste derrière la tête. Les taches de H. michaeli n. sp. defined. Comparison of the mitochondrial ND4 gene also sont généralement plus denses, plus grandes et clairement supports the species-level separation of these species. polygonales, remarquablement semblables aux taches d’un léopard. En contraste, celles de H. freycineti sont rondes à Zusammenfassung transversalement allongées et sont assombries à intervalles Hemiscyllium michaeli wird auf der Grundlage von sechs réguliers òpour former 8-9 barres ou marques en forme de Exemplaren mit 257-695 mm TL beschrieben, die am selle (y compris celles de la queue). La différence du patron östlichen Papua-Neuguinea gefangen wurden. Die neue Art des taches entre les deux espèces est surtout évidente dans wurde bisher mit H. freycineti verwechselt, die aber auf die la région de la tête, alors que la tache noire de H. freycineti Provinz Papua Barat (westliches Neuguinea), Indonesien, n’est généralement pas bien définie. Une comparaison du beschränkt ist. Die zwei Arten unterscheiden sich hauptsäch- gène mitochondrial ND4 confirme aussi le niveau de dif- lich durch die Farbmuster, die als Unterscheidungsmerkmal férenciation entre ces espèces. zwischen den Angehörigen der Gattung am besten geeignet sind. Beide Arten sind reichlich mit braunen Flecken übersät; Sommario gleich hinter dem Kopf zeigt sich ein großer schwarzer oder Hemiscyllium michaeli nuova specie è descritta sulla base di brauner Augenfleck in Höhe der Flankenmitte. Bei H. mi - sei esemplari, 257-695 mm TL, raccolti nella regione orien- c ha eli n. sp. sind die Flecken im allgemeinen dichter, größer tale di Papua Nuova Guinea. La specie era precedentemente und deutlich vieleckig und erinnern stark an Leoparden- confusa con H. freycineti, circoscritta alla provincia di Papua flecken. Im Gegensatz dazu sind die Flecken bei H. freycineti Barat (Nuova Guinea occidentale), Indonesia. Le due specie rundlich bis quer-länglich und in regelmäßigen Abständen differiscono principalmente per la colorazione, che rappre- abgedunkelt, sodass sie 8 bis 9 Streifen oder sattelähnliche senta il criterio migliore per separare i vari membri del Markierungen bilden (diejenigen auf dem Schwanz mit- genere. Entrambe le specie hanno una diffusa copertura di

19 aqua vol. 16 no. 1 - 20 January 2010 Hemiscyllium michaeli, a new species of Bamboo Shark (Hemiscyllidae) from Papua New Guinea macchie marroni e una larga macchia ocellata di colore nero there is no information for the species of Hemiscyl- o marrone centralmente sul fianco, appena dietro la testa. Le lium except H. ocellatum, which is also oviparous macchie di H. michaeli n. sp. sono generalmente più dense, (Compagno 2001). Assuming that all species are larghe e distintamente poligonali, notevolmente simili a oviparous, it would appear that dispersal opportu- quelle di un leopardo. Invece, quelle di H. freycineti sono tonde o allungate trasversalmente e sono più scure ad inter- nities are limited and the New Guinea species in valli regolari così da formare 8-9 barre o bande a sella (incluse particular exhibit very restricted geographic ranges quelle sulla coda). Le differenze tra le due specie nel motivo (Allen & Erdmann 2008). della macchiettatura è particolarmente evidente nella regione Over the past decade the first author has con- della testa. In aggiunta, H. michaeli n. sp. possiede una mac- ducted several coral reef fish surveys at the Raja chia ocellata nera brillante dietro la testa, mentre in H. Ampat Islands and Milne Bay Province, at the freycineti questa macchia non è generalmente ben definita. respective western and eastern ends of New L’analisi del gene mitocondriale ND4 conferma che le due Guinea. During the course of this work two species forme rappresentano specie distinte. of bamboo sharks were collected/observed and photographed. Although the two species are clearly INTRODUCTION separable on the basis of colour pattern, they have The family Hemiscylliidae, commonly known as been lumped under a single name, Hemiscyllium bamboo or epaulette sharks, contains small, slen- freycineti Quoy & Gaimard, 1824, in recent litera- der sharks characterised by nasoral and perioral ture (e.g. Dingerkus & DeFino 1983; Compagno grooves, short barbels, a small transverse mouth 2001). This species was originally described from below the eyes, two similar-sized dorsal fins, and a Waigeo in the Raja Ampat Islands, now part of long slender tail. The family was last revised by Papua Barat Province, Indonesia. The present Dingerkus & DeFino (1983). Other recent publi- paper provides evidence for the separation of the cations containing keys and accounts of the known two populations, which are geographically sepa- species include Compagno (1984, 2001), Last & rated by approximately 1,200 km (Fig. 1), includ- Stevens (2009) and Compagno & Niem (1998). ing the description of the Papua New Guinea shark The family contains two genera, Chiloscyllium as a new species. and Hemiscyllium, both described by Müller & Henle (1837, 1838). Chiloscyllium contains six MATERIALS AND METHODS species that range widely from Madagascar to the Technical terms and measurements mainly follow western Pacific. In contrast, the eight species of those explained and illustrated by Compagno Hemiscyllium are confined to shallow reefs of Aus- (2001). Snout length is the distance from the snout tralia and New Guinea, including two recent dis- tip to the anterior edge of the mouth. Subcaudal coveries from the Bird’s Head Peninsula of West length (as used by Dingerkus & DeFino 1983) is Papua (Allen & Erdmann 2008). The two genera the combined measurement of the upper postven- are similar in general apperance, but differ in the tral caudal-fin margin and terminal caudal-fin position of the nostrils on the snout (terminal in margin. Total length and head length are abbrevi- Hemiscyllium and subterminal in Chiloscyllium), ated as TL and HL respectively. Vertebral counts position of the mouth in relation to the snout tip were obtained from radiographs. Vertebral counts and eyes (closer to snout tip than eyes in Hemiscyl- and measurements for the holotype are given first lium, and closer to eyes than snout tip in Chiloscyl- followed by the range for paratypes (in parenthe- lium), and lastly the supraorbital ridges are promi- ses) in the description below. Museum abbrevia- nently elevated in Hemiscyllium, but scarcely ele- tions used in this paper are as follows: Australian vated in Chiloscyllium. Museum, Sydney (AMS), Cornell University, Hemiscyllium are small (usually under about 80 Ithaca, New York (CU), Muséum National d’His- cm), nocturnally active, bottom-living sharks toire Naturelle, Paris (MNHN), United States which exhibit a peculiar “walking” gait while for- National Museum of Natural History, Washing- aging for benthic invertebrates and fishes. Some ton, D.C. (USNM), and the Western Australian and most probably all members of the genus are Museum, Perth (WAM). oviparous, depositing eggs on the bottom in oval A tissue sample was obtained for a single speci- egg cases (Compagno 2001). Although this repro- men of the new taxon from Milne Bay Province, ductive mode was reported for nearly all except one Papua New Guinea (specimen not retained but (with unknown biology) species of Chiloscyllium, identity verified later from photographs). This was aqua vol. 16 no. 1 - 20 January 2010 20 Gerald R. Allen and Christine L. Dudgeon compared with samples of H. freycineti, H. galei ducted in the forward direction using Big Dye Ter- Allen & Erdmann, 2008, H. henryi Allen & Erd- minator v3.1 Cycle Sequencing Kit (Applied mann, 2008, and H. ocellatum (Bonnaterre, 1788), Biosystems) following manufacturer’s instructions. which had been previously analysed (Allen and Sequencing products were precipitated by adding 4 Erdmann 2008). Total genomic DNA was µL sodium acetate (3M, pH 5.2) and 50 µL 100% extracted from 25 mg of fin tissue using the ethanol and centrifuged for 30 min at 13000 rpm. DNeasy Tissue Extraction Kit (Qiagen) following The pellet was washed twice with 500 µL 70% the instructions of the supplier. A fragment includ- ethanol and then products resolved on a 3730xl ing partial mitochondrial NADH Dehydrogenase Genetic Analyser (Applied Biosystems). subunit 4 gene (ND4), tRNA-His and tRNA-Ser Sequences were aligned using Sequencher soft- genes was amplified through polymerase chain ware (GeneCodes). The program Modeltest ver- reaction (PCR) using the primers: ND4-F: 5’ - sion 3.7 (Posada & Crandall 1998) was used to CACCTATGACTACCAAAAGCTCATGTA- assess the best-fit model for the nucleotide substi- GAAGC - 3’ (Arevalo et al. 1994) and H12293- tution. The hierarchical likelihood ratio test ranked Leu-R: 5’ – TTGCACCAAGAGTTTTTG- the TrN + G substitution model (gamma distribu- GTTCCTAAGACC - 3’ (Inoue et al. 2001). Reac- tion = 0.3388) as having the best fit to the data. tions were conducted in 30 µl total amounts and The Tamura-Nei (Tamura & Nei 1993) substitu- consisted of: 10 µM each primer, 400 µM of each tion model accounts for variable base frequencies, dNTP, 3 units Taq polymerase, 1 x PCR Buffer transition rates and rate variation among sites. (Qiagen) and 30-50 ng extracted DNA. PCRs Akaike’s Information Criterion ranked the general were conducted on 9700 Perkin Elmer thermocy- time reversible model with invariable sites (GTR + clers and consisted of an initial denaturation step at I model as having best fit. Phylogenetic trees were 95 °C for 5 min, followed by 30 cycles of 95 °C for constructed in PAUP version 4.0b (Swofford 15 sec, 56 °C for 30 sec and 72 °C for 1 min, and 1998) using both models. Maximum likelihood, a final extension at 72 °C for 7 min. The PCR maximum parsimony and neighbour-joining trees products were cleaned using QIAquick PCR were constructed with a specimen of Chiloscyllium Purification Kit (Qiagen). Sequences were con- punctatum as the outgroup taxon. Confidence in

Fig. 1. Map of New Guinea 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. strahani (red squares) and H. michaeli (red circles).

21 aqua vol. 16 no. 1 - 20 January 2010 Hemiscyllium michaeli, a new species of Bamboo Shark (Hemiscyllidae) from Papua New Guinea tree topology was evaluated by bootstrapping wharf at Samarai Island, 10° 36.633’S, across 1000 bootstrap replicates (Felsenstein 150°39.690’E, Milne Bay Province, Papua New 1985). Pairwise distances within and between Guinea, 6 m, spear, R. Vanderloos, 10 April 2003. putative taxa were calculated using the TrN + G Diagnosis: A species of bamboo shark belonging model with 500 bootstrap replicates, implemented to the genus Hemiscyllium, distinguished from in Mega version 3.1 (Kumar et al. 2004). related species by a unique colour pattern, particularly the combination of dense leopard-like spot- ting on the body and a large black ocellate spot on Hemiscyllium michaeli n. sp. the middle of the side, just behind the head. It Michael’s Epaulette Shark lacks diagnostic colour pattern features that typify (Figs 2-4 and 5; Tables I-III) the other known species in the genus including: black hood or face-mask marking on the head (H. Holotype: USNM 218602, female, 610 mm TL, strahani), large intensely black ovate spots on body coral reef in Harvey Bay, 08°54.440’S, (H. hallstromi), ocellate shoulder spot and numer- 148°30.306’E, east of Oro Bay, Papua New ous small black spots on body (H. ocellatum), ocel- Guinea, 0-10 m, T. Roberts, 6-7 August 1975. late shoulder spot with two curved black marks on Paratypes: AMS IA.5741-2, 2 specimens, 282-262 posterior edge and numerous diffuse dark spots on mm TL, vicinity of Samarai, 10° 36.633’S, head body and fins (H. trispeculare), row of 7-8 150°39.690’E, Milne Bay Province, Papua New large, horizontally ovate spots on lower side Guinea; CU 24992, 695 mm TL, Milne Bay, between abdomen and caudal-fin base (H. galei), Papua New Guinea (no other data); USNM “double-ocellus” shoulder marking (H. henryi) and 221705, 257 mm TL, Kuia Island, 08°35.350’S, a fragmented or diffuse shoulder marking and 150°51.332’E, Trobriand Islands, Papua New sparse spot pattern on dorsal surface of snout (H. Guinea, 1 m depth, B.B. Collette, 11 June 1970; freycineti). WAM P. 32840-001, female, 544 mm TL, under Description: Vertebral centrum 203 (197-204);

Fig. 2. Underwater photograph of male Hemiscyllium michaeli, approximately 600 mm TL, Sullivan Patches, Milne Bay Province, Papua New Guinea at depth of 12 m. Pale blue arrow indicates clasper. Photo by B. Halstead. aqua vol. 16 no. 1 - 20 January 2010 22 Gerald R. Allen and Christine L. Dudgeon body and tail relatively slender, tapering posteri- like, composed of numerous rows; individual teeth orly; precaudal-fin length 1.2 (1.2-1.3), HL 6.7 broad-based with single posteriorly-directed cusp, (6.7-7.5), both in TL; head height (at pectoral fin cusps of innermost rows more developed. origin) about equal to width of head at level of eye; Pre-first dorsal fin length 2.5 (2.4-2.9), pre-pelvic eye length 3.8 (3.0-4.1) in snout length; the eye fin length 3.3 (3.3-3.7), snout to vent length 3.3 height 3.1 (2.4-3.0) in eye length; fleshy interor- (3.2-3.6), vent to anal fin origin 2.3 (2.0-2.4), vent bital space 2.3 (1.2-1.9), bony interorbital space to caudal fin length 1.5 (1.3-1.5), all in TL. Pec- 1.7 (1.7-2.5), both in snout length; snout blunt toral fins below gill openings, their length 1.4 (1.2- and short, snout tip to eye 2.3 (2.2-3.4), snout tip 1.7) in HL; pelvic fins immediately anterior to ver- to mouth 6.8 (5.1-7.2), snout tip to spiracle 2.1 tical line passing through first dorsal fin origin, (1.9-2.3), snout tip to first gill slit 1.2 (1.2-1.3), all their length 1.4 (1.3-1.7) in HL; dorsal fins posi- in head length; gill slits on rear part of head, above tioned well back on body, first dorsal fin slightly to slightly anterior of pectoral-fin base; distance higher than second; first dorsal fin base 2.0 (1.9- between first and fifth gill slit 2.3 (2.4-3.2) in head 2.3) in head length, first dorsal fin height 0.9 (0.8- length; height of gill slits gradually increasing pos- 1.2) in first dorsal fin base; first dorsal fin inner teriorly, the first 3.2 (3.3-5.8) and fifth 2.8 (2.5- margin 1.8 (1.6-2.0) in first dorsal fin height; 3.9), both in snout length. interdorsal space 1.3 (0.9-1.4) in HL; second dor- Mouth small and transverse, positioned well for- sal fin base 2.0 (1.7-2.2) in head length; second ward on ventral surface of head, its width 1.2 (1.0- dorsal fin height 1.0 (0.8-1.4) in second dorsal fin 1.4) in snout length; short barbel on each side of base; second dorsal fin inner margin 2.2 (1.5-2.2) ventral snout, its length 4.4 (4.1-5.8) in snout in second dorsal fin height; long and low anal fin length; maximum width of lower labial flap 4.4 just anterior to caudal fin; anal fin base 2.4 (1.5- (3.6-5.6), length of postoral fold (upper labial fur- 2.0) in head length, anal fin height 2.6 (3.3-4.5) in row) 3.3 (2.8-3.7), length of lower labial furrow anal fin base; anal fin inner margin 1.7 (1.2-1.8) in 3.5 (3.5-5.3), all in snout length; teeth pavement- anal fin height; elongate and thick precaudal tail

Fig. 3. Underwater photograph of Hemiscyllium michaeli, approximately 200 mm TL, Milne Bay Province, Papua New Guinea. Photo by B. Halstead.

23 aqua vol. 16 no. 1 - 20 January 2010 Hemiscyllium michaeli, a new species of Bamboo Shark (Hemiscyllidae) from Papua New Guinea

Table I. Proportional measurements (as percentage of total length) for selected type specimens of Hemiscyllium michaeli.

Holotype Paratype Paratype Paratype USNM WAM USNM CU 218602 P. 32840 221705 24992 Sex female female male female Total length 610.0 544.0 257.2 695.0 Precaudal length 82.0 81.8 82.5 81.6 Head width (eye) 7.8 7.3 7.0 6.3 Head width (max) 9.3 9.3 8.0 7.9 Head depth 8.3 7.5 7.3 7.7 Preanal body depth 3.5 3.5 3.7 3.5 Snout – pectoral fin origin (HL) 15.0 13.5 14.7 15.5 Snout – 1st gill slit 12.1 11.5 11.7 11.8 1st to 5th gill slit 6.6 4.2 4.9 6.1 First gill slit height 2.1 1.7 1.6 1.7 Fifth gill slit height 2.4 2.2 2.3 2.2 Eye diameter (horizontal) 1.7 1.5 1.4 1.4 Eye diameter (vertical) 0.5 0.5 0.5 0.6 Bony interorbital width 2.8 2.9 3.7 3.1 Fleshy interorbital width 4.5 3.7 4.8 3.6 Snout to eye (snout length) 6.4 5.5 4.3 5.8 Snout to spiracle 7.0 6.6 7.1 6.7 Snout to mouth 2.2 1.9 2.4 2.2 Lower labial furrow length 1.2 0.9 1.9 1.2 Maximum width lower labial flap 1.4 1.1 1.2 1.2 Postoral fold 1.9 1.6 1.6 1.8 Mouth width 5.2 4.4 4.3 4.5 Barbel length 1.5 1.4 1.0 1.1 Snout – 1st dorsal origin 39.3 36.6 38.7 41.3 Snout – pelvic origin 30.3 27.6 29.9 26.8 Snout – anal opening 30.4 29.3 31.3 27.6 Anal opening – anal fin origin 44.2 43.4 43.7 49.4 Anal opening – tail tip 67.9 71.5 69.0 75.7 Interdorsal distance 11.1 11.9 10.5 12.3 Postdorsal distance 35.7 35.8 35.5 35.7 Pectoral fin length 10.7 10.7 9.6 12.3 Pelvic fin length 11.0 10.1 8.6 9.8 1st dorsal fin base 7.7 6.8 6.4 6.8 1st dorsal fin height 8.5 8.5 5.2 8.9 1st dorsal fin free margin 4.8 4.2 2.8 5.3 2nd dorsal fin base 7.4 7.9 6.8 6.6 2nd dorsal fin height 7.3 7.8 4.9 8.1 2nd dorsal fin free margin 3.3 3.5 2.6 4.1 Anal fin base 6.4 8.8 7.2 8.5 Anal fin height 2.4 2.1 1.6 2.1 Anal fin free margin 1.4 1.3 1.2 1.8 Subcaudal 19.2 – 17.5 17.7 Clasper length (inner) – – 3.5 – Clasper length (outer) – – 1.0 –

aqua vol. 16 no. 1 - 20 January 2010 24 Gerald R. Allen and Christine L. Dudgeon

(section of body between anus and caudal fin), its and three on the caudal fin. There are a few small depth at level of anal fin origin 4.0 (3.6-4.5) in brown spots on the head and anterior body within head length; subcaudal length 5.2 (5.4-5.7) in TL. the pale interspaces and the characteristic large Adult male (approximately 600 mm TL, see Fig. ocellus is evident, although partially merged with 2, inset) clasper relatively large, its length about the second dark bar. equal to first dorsal fin height. Clasper of imma- Colour in alcohol (Fig. 4): similar to live ture 257 mm paratype rudimentary and barely coloration, although pattern is less intense and reaching ventral edge of pelvic fin. whitish areas are pale brown to tannish. A juvenile Colour in life (Fig. 2): overall whitish to paratype (USNM 221705), 257.2 mm TL, has a pale grey brown with dense network of leopard- greatly reduced spot pattern, primarily consisting like, brown spots covering head, body, and fins; of about nine light brown bars on the side and tail, large white-rimmed, dark brown spot on middle of those on the side with a large dark brown mid-lat- side, its anterior edge about level with posterior eral spot, a pair of large dark brown spots on the edge of pectoral fin; series of about 9-10 bars some- cheek region and a large brown spot (precursor of times apparent, faint on sides, but more conspi- the characteristic pale-rimmed marking of adult) cuous on tail; 2-3 prominent dark brown saddle- behind the head. like markings along dorsal edge of both dorsal fins. DNA Analysis: We analysed a 792 base pair (bp) This pattern was consistent in additional images of fragment from the ND4 gene in 16 individuals from four different individuals that were photographed Hemiscyllium species: there was one new sample for at Milne Bay Province and sent to the authors. A H. michaeli that was compared with the 15 individ- small juvenile (estimated size of 200 mm TL) pho- uals included in the previous phylogenetic analysis tographed by R. Halstead (Fig. 3) is mainly white from Allen and Erdmann (2008) (H. henryi = 4; H. with 10 dark brown bars including one on the head ocellatum = 5; H. freycineti = 4; H. galei = 2). In the

Fig. 4. Hemiscyllium michaeli, holotype, 610 mm TL, Harvey Bay, Papua New Guinea. Photo by G. R. Allen.

25 aqua vol. 16 no. 1 - 20 January 2010 Hemiscyllium michaeli, a new species of Bamboo Shark (Hemiscyllidae) from Papua New Guinea

Table II. Comparison of mean values for selected proportional measurements (as percentage of total length) of species of Hemiscyllium. Data for H. galei and H. henryi, H. freycineti, and H. michaeli were obtained by the authors, remaining data are from Dingerkus & DeFino (1983). The data for H. freycineti were taken by the authors from type specimens at MNHN.

H. michaeli H. freycineti H. galei H. hallstromi H. henryi H. ocellatum H. strahani H. trispeculare Number of specimens 6 3 2 9 3 20 2 7 Snout to first dorsal fin 37.99 36.02 37.28 35.98 38.43 36.18 36.96 36.13 Snout to pelvic fin 28.62 28.01 27.91 25.93 28.75 28.58 28.63 29.39 Snout to vent 29.52 30.13 29.94 30.07 31.04 30.32 29.36 31.51 Vent to anal fin 43.87 45.34 41.05 42.67 42.69 43.11 43.82 39.96 Vent to tail tip 69.62 69.15 69.24 68.59 68.55 68.37 68.67 67.26 Interdorsal distance 13.02 13.39 11.56 12.06 13.29 12.48 12.33 11.60 Pelvic fin length 9.69 9.95 11.35 9.70 10.20 9.59 10.19 10.50 First dorsal fin base 7.00 7.69 8.88 8.64 7.23 8.39 7.67 8.90 First dorsal fin height 7.20 6.36 6.94 6.97 9.12 6.48 6.92 8.42 Second dorsal fin base 7.24 8.24 7.92 7.79 7.76 7.81 7.65 7.67 Second dorsal fin height 6.53 6.02 7.36 6.55 7.59 6.45 6.31 7.65 Anal fin base 7.77 8.00 9.31 9.02 9.31 9.02 9.17 10.25 Anal fin height 2.08 3.10 2.90 2.33 3.17 2.28 2.66 2.91

Fig. 5. Maximum likelihood tree (TrN + G) of the ND4 data for five Hemiscyllium species. ML, MP and NJ bootstrap support of 1000 replicates are shown respectively. The outgroup is Chiloscyllium punctatum Müller & Henle, 1838, a member of the other genus in the family Hemiscyllidae. aqua vol. 16 no. 1 - 20 January 2010 26 Gerald R. Allen and Christine L. Dudgeon total Hemiscyllium alignment there were 44 variable resulted in identical tree topologies (Fig. 5) reveal- sites with 37 parsimony-informative characters. ing reciprocal monophyly for the five Hemiscyllium Nucleotide frequencies were highly similar amongst species with high bootstrap support. Further, all all the species and the average frequencies for the analyses clearly separated the one H. michaeli indi- combined Hemiscyllium samples were as follows: A = vidual from the H. freycineti samples. 0.32, C = 0.25, G = 0.11, T = 0.32. A total of six Distribution and habitat: The new species is haplotypes was detected. All species showed only known only from eastern Papua New Guinea (Fig. one haplotype except for H. ocellatum that showed 1) with observation and collecting records from two haplotypes, one found in four individuals and Samarai Island, Milne Bay (vicinity of Alotau and the other from one individual. Pairwise distances (d) Sullivan Patches), vicinity of Harvey Bay (Oro between the Hemiscyllium species ranged from Province), and the Trobriand Islands. It is typically 0.0106 - 0.0436 with H. ocellatum differing from encountered on coastal fringing reefs and patch the other species by at least twice the distance (Table reefs while diving at night, although it is some- III). The H. michaeli sample clearly differed from all times seen during the day, sheltering under rocky the other Hemiscyllium species with pairwise differ- outcrops or tabular corals. The known depth range ences ranging from 0.0239-0.0355. Pairwise dis- is approximately 2-20 m. tances between the Hemiscyllium species and the Etymology: The species is named H. michaeli in outgroup Chiloscyllium punctatum were over an honour of Scott W. Michael, who first brought the order of magnitude higher (dave = 0.23844). Only difference between this species and H. freycineti to H. ocellatum showed within-species distances which our attention. In addition, he has contributed a was over two orders of magnitude lower than the wealth of information, including valuable pho- within genus distances, d = 0.00052. tographs, for the first author’s research on Indo- Maximum likelihood, maximum parsimony and Pacific fishes. neighbour-joining analyses for both model types Remarks: The new species was previously con-

Fig. 6. Underwater photograph of Hemiscyllium freycineti, approximately 600 mm TL, Cri Island, Raja Ampat Islands, Papua Province, Indonesia, at depth of 2 m. Photo by G. R. Allen.

27 aqua vol. 16 no. 1 - 20 January 2010 Hemiscyllium michaeli, a new species of Bamboo Shark (Hemiscyllidae) from Papua New Guinea

Table III. Inter-specific pairwise distance matrix calculated from the TrN + G model with corresponding matrix (above diag- onal) of SE estimates (bootstrap method, 500 replicates).

H. michaeli H. freycineti H. galei H. henryi H. ocellatum C. punctatum H. michaeli – 0.0060 0.0065 0.0063 0.0082 0.0542 H. freycineti 0.0239 – 0.0046 0.0038 0.0084 0.0428 H. galei 0.0269 0.0134 – 0.0051 0.0094 0.0449 H. henryi 0.0239 0.0106 0.0191 – 0.0086 0.0423 H. ocellatum 0.0355 0.0402 0.0402 0.0402 – 0.0450 C. punctatum 0.2739 0.2255 0.2332 0.2261 0.2335 – fused with H. freycineti (Fig. 6), which is appar- larly evident on the dorsal surface of the head. The ently restricted to the West Papua Province (far spots of H. michaeli remain leopard-like in this western New Guinea), Indonesia. Our comparison region and are more densely arranged compared with H. freycineti includes several underwater pho- with the relatively sparse arrangement of spots on tographs by the author and colleagues as well as H. freycineti. In addition, H. michaeli possesses a examination of the following type specimens at vivid ocellate spot behind the head, whereas that of MNHN: A.7792, 308.5 mm TL, male lectotype H. freycineti is comparatively ill defined and often (designated by Dingerkus & DeFino 1983); fragmented. B.2962, 285.0 mm TL, male paralectotype; 7767, The only known juvenile specimen of H. freycineti, 663.0 mm TL, type of Scyllium malaisianum Les- a specimen (CAS 26798) from Waigeo, 214 mm son, 1831 (a junior synonym of H. freycineti). TL, was illustrated by Dingerkus & DeFino (1983) The two species differ primarily in colour pattern and is reproduced here as Fig. 7. Comparison with a (compare Figs 2 and 6), which provides the best similar-sized juvenile of H. michaeli (Fig. 3) reveals means of separating the various members of the less pronounced bars and a more ornate pattern con- genus. Both species have a profuse covering of sisting of a number of large spots between the pec- brown spots with a large black or dark brown ocel- toral and pelvic fins and smaller ocellate spots on the late marking on the middle of the side, just behind head and body of H. freycineti. the head. The leopard-like spots of H. michaeli are At present, the genus is poorly represented in generally larger and distinctly polygonal. In con- museum collections and therefore morphometric trast the spots of H. freycineti are round to trans- data is of limited value in separating the various versely elongate and are darkened at regular inter- species. A comparison of selected features (Table vals to form 8-9 dorsal bars or saddle-like markings II) reveals that H. michaeli differs from the other (including those on tail). Moreover, the markings members of the genus in having shorter first dorsal of H. freycineti are more diffuse and less dense fin and anal fin bases and a lower anal fin. How- compared to those of H. michaeli. The difference ever, more specimens are required for most species in spot pattern between the two species is particu- to fully evaluate these differences.

Fig. 7. Drawing of juvenile specimen, 214 mm TL, of Hemiscyllium freycineti from Waigeo, Raja Ampat Islands, Indonesia (from Dingerkus & DeFino 1983). aqua vol. 16 no. 1 - 20 January 2010 28 Gerald R. Allen and Christine L. Dudgeon

The species of Hemiscyllium are distinguished (south-eastern Papua New Guinea)...... mainly on the basis of colour pattern. The following ...... H. hallstromi key will serve to distinguish the eight known species. 6b. Lateral ocellus surrounded by relatively small spots; spots present on head in front and below Key to the Species of Hemiscyllium eyes...... 7 1a. Head and snout with an abrupt black hood; 7a. Lateral ocellus composed of single large, round body covered with conspicuous large white spot surrounded by distinct white halo; dark spots (eastern Papua New Guinea)...... spot absent at origin of pectoral and pelvic fins; ...... H. strahani numerous small dark spots usually present on 1b. Head and snout light in colour, without a black dorsal fins (northern Australia) ...... hood but with conspicuous black spots above ...... H. ocellatum pectoral fins; body with inconspicuous light 7b. Lateral ocellus usually composed of double, spots or spots absent ...... 2 merged ocelli surrounded by poorly defined 2a. Dark spot behind gills relatively small, forming white halo; dark spot present at origin of pec- a weak ocellus (or semi-ocellate dark spot) and toral and pelvic fins; dorsal fins usually without followed posteriorly by dark brown bar (con- small dark spots or if present they are restricted sisting of 2-3 merged spots in vertical row)..... to basal portion of fins (Triton Bay region, ...... 3 West Papua) ...... H. henryi 2b. Dark spot behind gills large, forming 1-2 conspicuous white-rimmed ocelli or merged dou- ACKNOWLEDGEMENTS ble ocelli without dark brown bar immediately We are especially grateful to Scott Michael of Lin- behind ...... 4 coln, Nebraska, who first brought the new species 3a. Network of white lines/spots mainly associated to our attention. Conservation International pro- with edge of large dark saddles on back; con- vided survey opportunities at Milne Bay Province, spicuous row of 7-8 large, horizontally-oval, Papua New Guinea and West Papua, Indonesia. I dark spots along lower side (Cenderawasih Bay, am particularly indebted to Mark Erdmann and West Papua)...... H. galei Roger Steene for their field assistance and espe- 3b. Network of white lines/spots mainly associated cially their help in obtaining vital tissue samples. with edge of large dark saddles on back absent; Rob Vanderloos, owner and operator of the live- row of dark spots along lower side relatively aboard vessel Chertan, provided valuable logistic inconspicuous and not well differentiated from assitance. Mary Jane Adams and Robert Halstead surrounding spots (Raja Ampat Islands, West generously provided underwater photographs of Papua) ...... H. freycineti the new taxon. Patrice Pruvost of MNHN and Jef- 4a. Head, body, and fins covered with polygonal, frey Williams of USNM facilitated the first leopard-like spots (eastern Papua New Guinea) author’s visits to their respective institutions for the ...... H. michaeli purpose of examining type specimens. John Friel of 4b. Head body, and fins covered with numerous CU kindly provided a specimen loan of a paratype spots, but more or less round in shape and not of H. michaeli. Finally, we are grateful to Raewyn polygonal and leopard like...... 5 Street, Queensland Department of Primary Indus- 5a. Body covered with numerous, densely clus- tries and Fisheries, for genetic sequencing. tered, dark small and large spots that form a reticular network of light base colour between them; dark cross-bands well defined on ventral REFERENCES surface of tail (northern Australia) ...... ALLEN, G. R. & ERDMANN, M. V. 2008. Two new species ...... H. trispeculare of bamboo sharks (Orectolobiformes: Hemiscyllidae) 5b. Body with fewer large spots that do not form a from western New Guinea. Aqua, International Journal of reticular network of light ground colour Ichthyology 13(3-4): 93-108. between them; dark cross-bands on tail rela- AREVALO, E., DAVIS, S. K. & SITES, J. W. 1994. Mito- chondrial-DNA sequence divergence and phylogenetic- tively weak or not reaching ventral surface ..... relationships among eight chromosome races of the Scelo- ...... 6 porus-Grammicus complex (Phrynosomatide) in central 6a. Lateral ocellus surrounded by large black spots; Mexico. Systematic Biology 43: 387-418. spots absent on head in front and below eyes COMPAGNO, L. J. V. 1984. FAO species catalogue. Volume 4.

29 aqua vol. 16 no. 1 - 20 January 2010 Hemiscyllium michaeli, a new species of Bamboo Shark (Hemiscyllidae) from Papua New Guinea

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