First Record of the Crowned Jellyfish Netrostoma Coerulescens (Cnidaria

Marine Biodiversity Records, page 1 of 4. # Marine Biological Association of the United Kingdom, 2015 doi:10.1017/S1755267215001268; Vol. 8; e156; 2015 Published online First record of the crowned jellyfish Netrostoma coerulescens (Cnidaria: Scyphozoa) from Pakistani waters shahnawaz gul1, andre’ c. morandini2 and mohammad moazzam3 1Department of Zoology, Jamia Millia Government Degree College, Malir, Karachi, Pakistan, 2Departamento de Zoologia, Instituto de Biocieˆncias, Universidade de Saõ Paulo, Rua do Mataõ, trav. 14, n. 101, Cidade Universita´ria, Saõ Paulo, SP, 05508-090, Brazil, 3WWF-Pakistan, 46-K, Block 6, PECHS, Karachi 75400, Pakistan

This report presents the first record of the crowned jellyfish Netrostoma coerulescens from Pakistani waters and establishes its first confirmed record from the Arabian Sea. The jellyfish is briefly described and compared with its congeners. In the region, this is the second record of the genus; the first was Netrostoma setouchianum.

Keywords: Rhizostomeae, Cepheidae, crowned jellyﬁsh, Arabian Sea, Indo-Paciﬁc

Submitted 27 March 2015; accepted 24 September 2015

INTRODUCTION of its branching was photographed microscopically; filaments at the centre of the arm disc were also photographed. This spe- The cnidarian fauna of the Pakistani waters is poorly known, cimen was identified as Netrostoma coerulescens Maas, 1903 but a recent compilation of literature data is available (Gul and is briefly described here. The specimen is now deposited et al., 2015b). Jellyfishes, although abundant in certain in the Museum of Department of Zoology, Jamia Millia periods, were only rarely reported in the scientific literature. Government Degree College (JMGDC MDZ), Malir, In the past, only three species were mentioned for the Karachi, Pakistan. We also found one medium-sized crab region: Cephea sp., Pelagia noctiluca (Forska˚l, 1775) and inside the subumbrella of this jellyfish. Sanderia malayensis Goette, 1887 (Stiasny, 1937a). Additionally, one specimen was previously collected as So far, recent efforts have increased the knowledge, reach- by-catch on 11 November 2010 during trawling off the coast ing a number of eight scyphomedusae from the Pakistani of Pakistan (24859.03′N65843.62′E); the specimen was photo- waters: Catostylus perezi Ranson, 1945, Cephea coerulea graphed and examined on board, but due the absence of Vanho¨ffen, 1902, Marivagia stellata Galil & Gershwin, 2010, technical facilities it could not be preserved. As we had no Netrostoma setouchianum (Kishinouye, 1902) and opportunity to further study the specimen, we present it Rhopilema hispidum (Vanho¨ffen, 1888) (Gul & Morandini, here as Netrostoma sp. 2013, 2015;Gulet al., 2014, 2015a). Interestingly, four of Identification follows Kramp (Maas, 1903; Stiasny, 1937b; the aforementioned species belong to the family Cepheidae Kramp, 1961). We assumed that the number of warts/ Agassiz, 1862, which has a higher richness in Indo-Pacific protuberances on the exumbrellar dome of the crowned jelly- waters (Kramp, 1970). fishes (Cephea and Netrostoma) may vary with growth The goal of this report is to register one more cepheid jelly- and thus, is not considered here as a diagnostic character. fish, Netrostoma coerulescens Maas, 1903, from the coast of Differentiation between genera of the family Cepheidae Pakistan, presenting a brief description and comparison Agassiz, 1862 and comparison of key morphological features with other members of the genus. of the valid species within the genus Netrostoma Schultze, 1898 are also provided (Tables 1 & 2).

MATERIALS AND METHODS RESULTS On 20 March 2014, during ﬁshing activities at Pitiani creek (24826.23853′N67817.44481′E), one crowned jellyﬁsh was collected as by-catch, brought to the laboratory and preserved systematics in 4% formaldehyde solution in sea water. The morphology Class SCYPHOZOA Goette, 1887 and canal system of the specimen was studied, a small piece Subclass DISCOMEDUSAE Haeckel, 1880 of the mouth arm was cut and the surface view plus detail Order RHIZOSTOMEAE Cuvier, 1800 Family CEPHEIDAE Agassiz, 1862

Corresponding author: Genus Netrostoma Schultze, 1898 S. Gul Netrostoma coerulescens Maas, 1903 Email: [email protected] (Figure 1A–F)

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Table 1. Differentiation between genera of the family Cepheidae Agassiz, 1862. Data from Mayer (1910), Kramp (1961), Gershwin & Zeidler (2008) and Galil et al. (2010). AD, arm disc; EU, exumbrella; MA, mouth arms.

Genera/ Exumbrellar morphology Subumbrellar appendages Inter-rhopalar canals characters per octant

Cephea EU with a dome bearing warts/protuberances MA and AD with long, pointed ﬁlaments Numerous (more than 3) Marivagia EU smooth; without dome, warts/protuberances or knobs No appendages 3 Netrostoma EU with a dome bearing warts/protuberances or a large MA with short spindle-shaped while, 3 smooth central knob AD with long ﬁlaments Cotylorhiza EU with a smooth dome without warts/protuberances Filaments with expanded ends/suckers Numerous (up to 13)

material examined DISCUSSION One specimen, 20 March 2014, Pitiani creek (24826.23853′N 67817.44481′E), bell width 300 mm (JMGDC MDZ CN 21). Cephea Pe´ron & Lesueur, 1810 and Netrostoma Schultze, 1898 are two closely related genera of the family Cepheidae, com- monly known as crowned jellyfishes. The main features that description are used to differentiate the genera are the exumbrellar Umbrella thinner at margin, bearing a low exumbrellar central morphology and the presence/absence of subumbrellar dome with a distinct furrow around it (Figure 1A). Dome appendages and their shape. Cephea can be easily distin- completely ornamented with about 20 wart-like protuber- guished by having numerous long, pointed ‘lash-like fila- ances; outer ones relatively loosely set, inner ones raised and ments’ on mouth arms (Menon, 1930) besides other greatly fused (Figure 1B). Eight distinct, round velar lappets morphological features (see Table 1). per octant; rhopalar lappets also distinct, small and pointed The unique character of Netrostoma is the presence of (Figure 1C). short appendages on mouth arms (Kramp, 1961; Gul et al., Mouth arms eight, short, laterally compressed, bifurcated 2015a). Kramp (1961) mentioned two types of appendages distally, bearing numerous tiny, lateral branches, each on the mouth arms of Netrostoma coerulescens – the having several minute tubular appendages (Figure 1D, E); tubular and the spindle ones; however, the former are most surface of mouth arms with numerous short, spindle-shaped likely the digitata, which help the rhizostome medusae in appendages (Figure 1E); both having microscopic warts. feeding (Arai, 1997). Surprisingly, we also noticed numerous Centre of arm disc with a cluster of mostly thin, transparent, similar whitish, spindle-shaped appendages on the surface of small filaments of varying length (Figure 1F). Three inter- mouth arms in an underwater image of a live specimen of rhopalar canals per octant forming a wide-meshed network Marivagia stellata Galil & Gershwin, 2010 provided by Galil reaching into the velar lappets. Subumbrellar radial muscles et al.(2010: Figure 4). strongly developed. Maas (1903: Figures 41 & 42) illustrated one large wart in the middle of the central dome surrounded by about ten smaller ones and the dome appears completely ornamented. remarks However, in the specimen at hand (Figure 1A, B) no such Netrostoma coerulescens Maas, 1903 can be distinguished by single large wart was noticed in the centre. Menon (1930) its wart-like protuberances completely covering the exumbrel- reported numerous gelatinous warts on the exumbrellar lar dome; 6–8 distinct, round-edged velar lappets in each dome of this species in specimens examined from India. octant; small, pointed rhopalar lappets; short, laterally com- The same author (Menon, 1936) stated that this middle, pressed, distally bifurcated mouth arms having numerous large wart can be formed by the coalescence of a number short, spindle-shaped appendages, and the centre of arm of smaller ones. Stiasny (1937b) considered Netrostoma typh- disc with long filaments (Maas, 1903; Stiasny, 1937b; lodendrium, which had (80) round warts with no middle Kramp, 1961; present study). A comparison of N. coerulescens larger one, identical with the discussed species. Kramp with other species is provided in Table 2. (1961) also seems at doubt about the presence of one large

Table 2. Comparison of key morphological features of the valid species within the genus Netrostoma Schultze, 1898; type localities are also shown. Data from original descriptions: Mayer (1910), Kramp (1961) and Gershwin & Zeidler (2008). AD, arm disc; ED, exumbrellar dome; MA, mouth arms.

Characters/species Netrostoma coerulescens Netrostoma Netrostoma nuda Netrostoma setouchianum dumokuroa

Exumbrellar Wart-like protuberances ED with protuberances A single, large, smooth, Pointed protuberances completely ornamentation completely covering ED only on the sides central knob on the covering ED exumbrella Velar lappets 6–8 per octant, round edged Scarcely distinguishable 7 per octant, round edged 6–8 per octant, flatly-round edged Subumbrellar MA with numerous short No appendages No appendages on MA MA with numerous short appendages spindle-shaped while, AD with while, AD with long spindle-shaped while, AD with long filaments filaments long filaments Type locality Malayan Archipelago Fiji Islands, Pacific Palm Cove, Cairns district, Japan north Queensland

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Fig. 1. Netrostoma coerulescens Maas, 1903 from Pitiani creek, Pakistan (JMGDC MDZ CN 21), bell width 300 mm. (A) Specimen in exumbrellar view; (B) Closer view of exumbrella showing wart-like protuberances on the central dome and a distinct furrow (arrow) around; (C) Closer view of bell margin highlighting round-edged velar and pointed rhopalar lappets; (D) Microscopic view showing mouth arms’ lateral branching and formation of tubular appendages (possibly digitata); (E) Surface of a mouth arm; note the numerous minute tubular appendages (arrows) and one spindle-shaped appendage; (F) Subumbrellar view showing ﬁlaments (arrow) at the centre of arm disc.

wart in the centre and thus, he does not mention it in the water environments. But the boundaries between the species diagnosis of Netrostoma coerulescens. We also collected a of Cephea and Netrostoma are based on a few characters – Netrostoma specimen as by-catch during trawling off the which may vary depending on development and the level of coast of Pakistan (24859.03′N65843.62′E), which had (80) damage to specimens – and are also based on a few observed round warts on the exumbrellar dome, but as it was not medusae individuals. The group needs an urgent approach retained, we could not study it in more detail and thus, it is that would combine detailed morphological studies of a present here as Netrostoma sp. (Figure 2A, B). large series of animals, the observation of developmental It is clear that the higher diversity of species of the family series and the use of molecular techniques in order to Cepheidae in the Indo-Paciﬁc waters presents an intriguing unravel the valid species. and exciting source of study. Following Kramp (1961) there Netrostoma coerulescens is an Indo-west Paciﬁc species are ten species out of 12 that inhabit such clear, shallow (Kramp, 1961). In the Arabian Sea, it was previously collected

Fig. 2. Netrostoma sp. freshly collected from off the Pakistani coast (24859.03’N 65843.62’E). (A) Exumbrellar view highlighting the numerous warts; (B) Subumbrellar view.

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from the Gulf of Oman during John Murray’s Expedition Gul S. and Morandini A.C. (2015) First record of the jellyfish Rhopilema (1933–34) as a single, badly damaged specimen (Stiasny, hispidum (Cnidaria: Scyphozoa) from the coast of Pakistan. Marine 1937a) and Nair (1951) later briefly mentioned this scypho- Biodiversity Records 8(e30), 1–4. medusa from the Trivandrum coast, India. Therefore, Gul S., Morandini A.C., Haüssermann V. and Po¨rschmann U. (2015b) present record is the first confirmed report of this species Checklist of cnidarians from Pakistani waters. Check List 11(1609), from the Arabian Sea, offering its first record from Pakistani 1–8, doi: http://dx.doi.org/10.15560/11.2.1609. waters. Kramp P.L. (1961) Synopsis of the medusae of the world. Journal of the Marine Biological Association of the United Kingdom 40, 7–469.

ACKNOWLEDGEMENTS Kramp P.L. (1970) Zoogeographical studies on Rhizostomeae (Scyphozoa). Videnskabelige Meddelelserfra Dansk Naturhistorisk We are grateful to the anonymous reviewers for their critical Forening 133, 7–30. evaluation of the manuscript. ACM was supported by grants Maas O. (1903) Die Scyphomedusen der Siboga Expedition. 2010/50174-7 and 2011/50242-5 from the Sa˜o Paulo Siboga-Expeditie XI, 1–91. Research Foundation (FAPESP), and by CNPq (301039/ 2013-5). This is a contribution of NP-BioMar, USP. Mayer A.G. (1910) The medusae of the world. Vol. III. The Scyphomedusae. Carnegie Institution of Washington Publication 109(III), 499–735.

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