Research Article |
Corresponding author: Sho Toshino ( mf09008y@st.kitasato-u.ac.jp ) Academic editor: Leen van Ofwegen
© 2015 Sho Toshino, Hiroshi Miyake, Haruka Shibata.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Toshino S, Miyake H, Shibata H (2015) Meteorona kishinouyei, a new family, genus and species (Cnidaria, Cubozoa, Chirodropida) from Japanese Waters. ZooKeys 503: 1-21. https://doi.org/10.3897/zookeys.503.9047
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A new family, genus and species of cubozoan box jellyfish belonging to the order Chirodropida is reported from the eastern Japan. Meteorona kishinouyei gen. et sp. n. possesses the following unique morphological characters with respect to other known species in the Chirodropida: having one tentacle per scalpel-like unbranched pedalium and slightly raised unbranched gastric saccules. A comparative table of the primary diagnostic characters of genus and order in the Chirodropida is given. The order Chirodropida is redefined. The family Chiropsellidae is established. Discussion is provided on the implications for these findings on our current understanding of Cubozoan systematics.
Box jellyfish, Chiropsellidae , Japan, taxonomy
The order Chirodropida currently comprises 13 species in two families, Chirodropidae and Chiropsalmidae (
Chirodropids have been reported from a range of tropical, sub-tropical, and mild temperature localities in the Pacific and Atlantic (
Five species of Japanese cubozoans have been reported, Carybdea brevipedalia Kishinouye, 1891, Copula sivickisi (Stiasny, 1926), Tripedalia cystophora Conant, 1897, Morbakka virulenta (Kishinouye, 1910), and Chironex yamaguchii Lewis & Bentlage, 2009 (
List of Japanese Cubozoa. a
Current name | Former name | Japanese name | Reference |
---|---|---|---|
Carybdea brevipedalia Kishinouye, 1891 | Carybdea rastonii | Andon-kurage | a, b, c |
Copula sivickisi (Stiasny, 1926) | Carybdea sivickisi | Himeandon–kurage | a, b, c |
Tripedalia cystophora Conant, 1897 | Tripedalia cystophora | Mitsuderippo–kurage | b, d |
Morbakka virulenta (Kishinouye, 1910) | Tamoya haplonema | Hi–kurage | a, b, c, e |
Chironex yamaguchii Lewis & Bentlage, 2009 | Chiropsalmus quadrigatus | Habu–kurage | f, g |
Specimens were collected using a scoop, 170 mm in diameter, at Souma, Onahama and Fujisawa, eastern Japan between 24 August 2011 and 18 October 2013 (Fig.
Taxonomic observation and measurements were made on preserved specimens. Measurements were made with digital calipers (CD-20CPX, Mitsutoyo Corporation, Japan) to the nearest 0.01 mm. The following measurements were made according to
Key characters for identification and measurement of parts of the Cubozoa. A lateral view B pedalium C oral view. BH = Bell height; DBW = Diagonal bell width; DEW = Diagonal exumbrella width; DSW = Diagonal subumbrella width; IKL = Inner keel length; IKW = Inner keel width; IRW = Interrhopalial width; ML = manubrium length; OKL = Outer keel length; OKW = Outer keel width; PCW = Pedalial canal width; PW = Pedalial width; RH = Rhopalium height; TBW = Tentacle base width; VW = Velarial width.
For nematocyst identification in the medusae, squashes prepared from fresh tissues were examined under a compound microscope. Nematocysts were identified according to
Near complete sequences of the nuclear 18S rDNA genes (approximately 1800 bp) were used for molecular phylogenetic analysis. Genomic DNA was extracted from the 99.5 % ethanol preserved subsampled tentacle tissue of NSMT-Co1569, NSMT-Co1571 and NSMT-Co1572 using the DNeasy Blood and Tissue Kits (Qiagen, Germany) following the manufacturers protocol. 18S rDNA was PCR amplified and sequenced using primers and protocols outlined in
Taxa included in the phylogenetic analyses and GenBank accession numbers for sequences. Sequences obtained in this study are in bold.
Species | GenBank No. | Reference |
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Alatina moseri (Australia) | GQ849082 (as Alatina mordens) |
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Carybdea branchi (South Africa) | GQ849089 |
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Carybdea brevipedalia (Japan) | GQ849092 (as Carybdea mora) |
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Carybdea marsupialis | AF358106 |
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Carybdea rastonii | AF358108 | Collins et al. 2002 |
Carybdea xaymacana | AF358109 | Collins et al. 2002 |
Carybdea xaymacana (Panama) | GQ849090 |
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Carukia barnesi | AF358107 | Collins et al. 2002 |
Copula sivickisi | AF358110 (as Carybdea sivickisi) | Collins et al. 2002 |
Gerongia rifkinae | AF358105 (as Darwin carybdeid) | Collins et al. 2002 |
Meteorona kishinouyei (Fujisawa) | LC033478 | this study |
Meteorona kishinouyei (Onahama) | LC033479 | this study |
Meteorona kishinouyei (Souma) | LC033480 | this study |
Morbakka virulenta (Japan) | GQ849083 |
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Malo maxima (Australia) | GQ849084 (as Malo kingi) |
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Tripedalia cystophora (Indonesia) | GQ849088 |
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Chironex fleckeri (Australia) | GQ849073 |
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Chironex yamaguchii (Japan) | GQ849076 |
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Chiropsalmus quadrumanus (Brazil) | GQ849078 |
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Chiropsella bronzie | AF358103 (as Chiropsalmus sp.) | Collins et al. 2002 |
Chirodropida with unbranched gastric saccules. Gastric phacellae V-shaped or horseshoe shaped. Sensory niches U-shaped, with medial flap on upper rhopaliar scale. Pedalial canal bend slight volcano or knee-shaped. Pedalia four, branched with 5 to 11 tentacles or unbranched with one tentacle.
Chiropsella Gershwin, 2006.
Chiropsella bronzie Gershwin, 2006: 25–36, pl. 4–6.
Chiropsella bart Gershwin & Alderslade, 2006: 15–21, figs 1–4.
Chiropsella rudloei Bentlage, 2013: 1–7, figs 1–3.
Chiropsellidae with smooth, unbranched, slightly raised gastric saccules. Gonads leaf-shaped. Gastric phacellae horseshoe-shaped. Sensory niches U-shaped, with medial tongue-shape flap on upper rhopaliar scale. Pedalia four, unbranched, scalpel-like with one tentacle per pedalium.
Meteorona kishinouyei sp. n. here designated.
The genus name comes from the meteor-like appearance of the jellyfish shooting through the sea while swimming. The name Meteorona is taken from the Latin ‘Meteoron’, with the suffix -a. Gender is feminine.
Holotype: NSMT-Co1572. Eastern Japan, Fukushima Prefecture, Souma, Matsukawa-ura, 37°48'39.3"N, 140°58'3.3"E, 14 October 2013, collector: Ko Tomikawa, one adult male. Paratypes. NSMT-Co1568, 1569, 1570. Eastern Japan, Kanagawa Prefecture, Fujisawa, Enoshima, Shonan Port, 35°18'4.75"N, 139°28'61.0"E, 23 August 2011, collector: Haruka Shibata, one adult female. NSMT-Co1571. Eastern Japan, Fukushima Prefecture, Iwaki, Onahama Port, 36°56'29.1"N, 140°54'.32.9"E, 18 October 2013, collector: Shun Ishikawa, one adult female.
Adult medusae with smooth exumbrella, with evenly thick mesoglea of rigid consistency (Fig.
Meteorona kishinouyei sp. n., holotype. A gonad B mouth oral lips C gastric saccules D phacellae E gastric filaments F rhopaliar niche ostia, front view G rhopaliar niche ostia, side view H rhopaliar window I rhopalium, front view J rhopalium, rear view K rhopalium, side view L velarium; M pedalium N pedalial canal bend O tentacle. De: Depression; Fl: flap; GS: gastric saccule; LLE: lower lens eye; PCB: pedalial canal bend; PE: pit eye; Ph: phacella; PL: perradial lappet; RN: rhopaliar niche ostia; RW: rhopaliar window; SE: slit eye; St: statolith; ULE: upper lens eye. Scale bars: 1 cm (A–E, L), 5 mm (C), 2 mm (F–H, M–O), 1 mm (E), 0.5 mm (I–K).
Illustration of Meteorona kishinouyei sp. n., holotype. A gonad B gastric saccule C phacellae D gastric filaments E rhopaliar niche ostia and opening, front view F rhopaliar niche ostia and opening, side view G rhopalium, front view H rhopalium, side view I velarium J pedalium K pedalial canal bend L tentacle. Allows indicate gastric saccule. Scale bars: 1 cm (A–C, I), 2 mm (D, J–L), 1 mm (E–F, H), 0.5 mm (G).
Size (mm) of Meteorona kishinouyei. *: The holotype. Nos. Co1568-1571 are paratypes. BH = bell height; DBW = diagonal bell width; DEW = diagonal exumbrella width; DSW = diagonal subumbrella width; ML = manubrium length; IKL = inner keel length; IKW = inner keel width; IRW = interrhopalial width; OKL = outer keel length; OKW = outer keel width; RH = rhopalium height; PCW = pedalial canal width; PW = pedalial width; TBW = tentacle base width; VW = velarial width. All bars represent unavailable due to dissection.
Specimen No. | BH | DBW | DEW | DSW | IRW | PW | PCW | OKW |
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NSMT-Co1568 | 34,3 | 49,5 | 44,0 | 41,3 | 22,6 | 7,3 | 1,5 | 2,8 |
NSMT-Co1569 | 28,7 | 41,7 | – | – | 19,6 | 6,8 | 1,2 | 2,6 |
NSMT-Co1570 | 15,3 | 19,6 | 18,9 | 15,5 | 9,2 | 3,7 | 1,0 | 1,1 |
NSMT-Co1571 | 23,7 | 28,3 | 25,5 | 22,6 | 15,4 | 6,7 | 1,5 | 2,9 |
NSMT-Co1572* | 34,6 | 46,5 | 42,9 | 39,6 | 22,0 | 6,9 | 1,8 | 3,1 |
Specimen No. | IKW | OKL | IKL | TBW | RH | VW | ML | SEX |
NSMT-Co1568 | 3,0 | 17,2 | 11,2 | 2,6 | 5,6 | 5,5 | 15,2 | Male |
NSMT-Co1569 | 3,2 | 13,7 | 7,1 | 2,1 | 4,4 | 5,4 | 11,9 | Female |
NSMT-Co1570 | 1,3 | 7,5 | 4,9 | 0,9 | 2,3 | 2,8 | 3,6 | Female |
NSMT-Co1571 | 2,3 | 16,4 | 11,1 | 2,0 | 4,5 | 4,3 | 10,0 | Female |
NSMT-Co1572* | 2,1 | 17,7 | 11,1 | 2,7 | 5,1 | 6,0 | 12,5 | Female |
Gastric saccules unbranched, slightly raised and opaque (Fig.
The smallest young medusa (NSMT-Co 1570) had a BH of about 15 mm, DBW of about 20 mm (Fig.
Meteorona kishinouyei sp. n., young medusa, paratype NSMT-Co1570. A gonad B phacella C rhopaliar niche ostia, front view D rhopaliar niche ostia, side view E velarium F pedalium G pedalial canal bend H tentacle. Fl: Flap; PCB: Pedalial canal bend Scale bars: 2 mm (A, E–F), 1 mm (C–D, G–H), 0.5 mm (B).
Cnidome. Six different nematocyst types identified and measured in the paratype specimen (NSMT-Co1571) (Table
Nematocysts of Meteorona kishinouyei, paratype NSMT-Co1571. A, B Large microbasic p-rhopaloids. Intact (A), discharged (B) C, D Banana-shaped p-mastigophores. Intact (C), discharged (D) E, F Small oval beehive isorhizas. Intact (E), discharged (F) G, H Rod-shaped isorhizas. Intact (G), discharged (H) I, J Small sub-spherical p-rhopaloids. Intact (I), discharged (J) K, L Tiny microbasic euryteles. Intact (K), discharged (L). All bars represent 10 µm.
Cnidomes of Meteorona kishinouyei, paratype (NSMT-Co1571). D, L represent capsule diameter and length, respectively, in µm.
Part | Type | Min | Max | Mean | SD | N | |
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Tentacle | banana-shaped microbasic p-mastigophore | D | 11,58 | 15,49 | 13,62 | 1,06 | 21 |
L | 58,22 | 67,85 | 62,60 | 2,54 | 21 | ||
large microbasic p-rhopaloid | D | 15,64 | 20,61 | 17,64 | 1,21 | 30 | |
L | 26,05 | 33,02 | 29,27 | 1,65 | 30 | ||
small sub-spherical p-rhopaloid | D | 11,63 | 15,49 | 13,57 | 1,08 | 25 | |
L | 15,09 | 19,96 | 17,37 | 1,31 | 25 | ||
small oval beehive isorhiza | D | 9,77 | 11,86 | 10,67 | 0,56 | 30 | |
L | 12,36 | 15,12 | 13,38 | 0,72 | 30 | ||
rod-shaped isorhiza | D | 3,38 | 5,92 | 4,56 | 0,62 | 30 | |
L | 9,92 | 18,31 | 15,11 | 1,45 | 30 | ||
Exumbrella | N/A | D | – | – | – | – | – |
L | – | – | – | – | – | ||
Manubrium | small sub-spherical p-rhopaloid | D | 12,45 | 16,67 | 14,50 | 0,97 | 30 |
L | 16,15 | 19,35 | 17,79 | 0,90 | 30 | ||
tiny microbasic eurytele | D | 9,80 | 12,19 | 11,06 | 0,61 | 30 | |
L | 14,29 | 18,69 | 16,22 | 0,98 | 30 | ||
Phacella | small sub-spherical p-rhopaloid | D | 11,73 | 14,39 | 13,27 | 0,63 | 30 |
L | 14,03 | 18,42 | 16,37 | 1,00 | 30 | ||
tiny microbasic eurytele | D | 9,63 | 12,49 | 10,82 | 0,83 | 15 | |
L | 12,56 | 19,79 | 15,82 | 1,91 | 15 |
In the resulting ML tree (Fig.
Holotype specimen of Meteorona kishinouyei was collected near shore in shallow waters of the Matsukawa-ura lagoon, Fukushima prefecture, eastern Japan. Until March 2011, the north part of the lagoon extended to the sea via a man-made channel. However, the channel was destroyed and considerable sea water flowed into the lagoon as a result of the 2011 Tohoku earthquake and tsunami. M. kishinouyei medusae may have been brought into the lagoon on the high waves. Moreover, M. kishinouyei may be a neritic species. Young medusae appeared during August, while adult medusae appeared between August and November. Carybdea brevipedalia was collected together with M. kishinouyei along at Onahama port and Shonan at the water surface in a shallow area (water depth 3–10 m) port during daytime. Polyps of M. kishinouyei may metamorphose into young medusae during summer. However, the polyp stage and life history are unknown.
The species is named kishinouyei (noun in apposition) to honor Professor Kamakichi Kishinouye, zoologist and fishery scientist. Kishinouye’s meticulous studies and observations have led to many important contributions in the description of cubozoan zoology
A comparison of key features of the species of Chirodropida is presented in Table
Morphology of chirodropida medusae in previous and the present studies. All bars represent lacking data.
Family | Genus | Nematocysts on exumbrella | Gastric saccule shape | Gastric phacella shape | Rhopaliar covering scale | Number of tentacles | Pedalial branching pattern | Pedalial canal | Pedalial canal bend |
Chiropsellidae fam. n. | Meteorona gen. n. | – | Slightly raised | Horseshoe shaped | Tongue | 1 | Unbranching | Undivided | Slight volcano |
Chiropsella | – | Solid and spherical; sessile | V-shaped | Cigar/Banana/Tongue/Squarish to rounded | 5–11 | Usually but always opposite | Divided | Knee-shaped/ Slight volcano | |
Horseshoe shaped | |||||||||
Chirodropidae | Chirodropus | – | Elongate, tapered, with numerous axial processes, or absent | V-shaped | – | 9–21 | Bilateral with reduced ‘palm’ | Unknown | Spike |
Chirodectes | – | – | Arranged vertically along stomach wall | – | 9–11 | Bilateral with reduced ‘palm’ | Unknown | Spike | |
Chironex | – | cock’s-comb shaped/grape-cluster-like | V-shaped | – | 7–15 | Alternate | Divided | Spike/volcano | |
Chiropsalmidae | Chiropsalmus | Fine warts | Finger-like and short | Horseshoe shaped | – | 2–9 | Opposite | Undivided | Slight volcano |
Chiropsoides | – | Finger-like and long | V-shaped | – | 4–11 | Unilateral | Undivided | Spike |
Meteorona kishinouyei is most likely to be confused with the carybdeid Carybdea brevipedalia from eastern and northern Japan.
Two families, Chirodropidae and Chiropsalmidae are currently classified in the order Chirodropida (
Diagnosis.Cubozoa with or without gastric saccules; with branched or unbranched pedalium; with a triangular shaped depression of exumbrella surrounded rhopaliar niche; with a triangular shaped perradial lappet and highly divergent branching velarial canals.
Based on our maximum likelihood study, M. kishinouyei and Chiropsella bronzie appear to be the closest relatives in the currently understood cubozoan phylogenetic relationships. Moreover, Meteorona and Chiropsella have some common morphological characters such as the unbranched gastric saccule, rhopaliar flap and slight volcano-shaped pedalial canal bend. However, the shape of pedalium and number of tentacles differs between the two species.
Chiropsella has been classified as a genus in the family Chiropsalmidae (
We would like to express our sincere thanks to Ko Tomikawa, Yusuke Kondo (Hiroshima University) and Shun Ishikawa (Kitasato University) for providing the specimens and photos. The manuscript was greatly improved by the constructive comments Shin Kubota (Kyoto University) and Cheryl Lewis (National Museum of Natural History, Smithsonian Institution). The research was financially supported by the Sasakawa Scientific Research Grant from The Japan Science Society and the Research Institute of Marine Invertebrates Foundation by Research Institute of Marine Invertebrates.