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The genus Chiropsoides (Chirodropida: Chiropsalmidae) from the Andaman Sea, Thai waters
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Charatsee AUNGTONYA1, *, Jie XIAO2, Xuelei ZHANG2, Nattanon WUTTHITUNTISIL3
Acta Oceanologica Sinica | 2018, 37(10) : 119 - 125
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Acta Oceanologica Sinica | 2018, 37(10): 119-125
• Articles •
The genus Chiropsoides (Chirodropida: Chiropsalmidae) from the Andaman Sea, Thai waters
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Charatsee AUNGTONYA1, *, Jie XIAO2, Xuelei ZHANG2, Nattanon WUTTHITUNTISIL3
Affiliations
  • 1 Phuket Marine Biological Center, Phuket 83000, Thailand
  • 2 The First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China
  • 3 Animal Systematics and Molecular Ecology Laboratory, Department of Biology, Faculty of Science, Mahidol University, Bangkok 10400, Thailand
Published: 2018-10-25 doi: 10.1007/s13131-018-1311-4
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Box jellyfish Chiropsoides buitendijki from the coastal zone along the Andaman Sea, southwestern Thailand are characterized by a box-shaped body with unilateral branched tentacles and lack of interradial furrows. Tentacular banding was first reported in the present study with 1-3-2-3-2-3-2-3-1 patterns (1-major band, 2-thicker minor band and 3-thinner minor band). The DNA sequences of 18 S ribosomal RNA genes indicated that the specimen examined were genetically similar to C. buitendijki that was previously identified from the Nam Bor Bay, Phuket, Thailand, and distinct to the other known taxa in the order Chirodropida. In addition, a significant genetic divergence based on 16S mitochondrial gene was observed within the C. buitendijki samples. This indicates a population genetic differentiation but needs further confirmation.

Chiropsoides  /  Cubozoa  /  Andaman Sea  /  jellyfish  /  tentacular banding
Charatsee AUNGTONYA, Jie XIAO, Xuelei ZHANG, Nattanon WUTTHITUNTISIL. The genus Chiropsoides (Chirodropida: Chiropsalmidae) from the Andaman Sea, Thai waters[J]. Acta Oceanologica Sinica, 2018 , 37 (10) : 119 -125 . DOI: 10.1007/s13131-018-1311-4
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1 Introduction
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The genus Chiropsoides Southcott (1956) replaced Drepanochirus Krumbach (1925) because this generic name was preoccupied (Southcott, 1956). The distinctive characters of Chiropsoides is having abaxially branched pedalia in a sequential linear form.
Gershwin (2006) revised the genus Chiropsoides and recognized 2 species of Chiropsoides, viz., C. quadrigatus (Haeckel, 1880) and C. buitendijki (Horst, 1907). The latter Indonesian species has a conspicuous, unilateral pedalia fork with knobs in a conspicuous unilateral manner and flat, ribbon-like tentacles. The main canal of C. buitendijki has a series of knobs between the forks, whereas C. quadrigatus has knobs on the forks themselves but not between.
The type of C. quadrigatus is immature, in a poor condition, and considered a nomendubium. However, Gershwin (2006) mentioned that it should be maintained as a separate species, but if C. buitendijki and C. quadrigatus are found to be identical, then C. quadrigatus would have priority.
C. buitendijki has been reported from India, Malay Archipelago and Indochina, whereas the distribution of C. quadrigatus is widely debated. Gershwin (2006) mentioned that all Chirodropida from Australia, Philippines, Japan, and throughout Southeast Asia should belong to other species than C. quadrigatus. Aungtonya and Chanachon (2012) found 4 cubozoan families with 5 species in coastal areas of Phuket Province, southwestern Thailand. Chiropsoides buitendijki was the only species of this genus. Sucharitakul et al. (2016) studied sequences of C. buitendijki from the Nam Bor Bay, Phuket, southwest Thailand (submitted to the National Center for Biotechnology Information (NCBI) with regard to KJ135023).
Chiropsoides buitendijki was reported to cause the rapid demise of two teenagers in Pulau Langkawi off the southwest coast of Malaysia bordering Thailand, the Andaman Sea (Fenner et al., 2010). The characteristic skin wound markings of the victims implied stung by Chirodropid. Chiropsoides buitendijki was blamed to be cause of these skin markings. However, Fenner et al. (2010) did not report the size of this box jellyfish.
2 Materials and methods
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2.1 Specimens collection and treatment
Samples from the Andaman Sea in this study were collected during the surveys of distribution of venomous jellyfish project during 2009–2014. The surveys were conducted on the coast of Ranong, Phang-nga, Phuket, Krabi, Trang and Satun for 6, 12, 12, 8, 5 and 6 times during the northeast monsoon (November–April) and 3, 11, 9, 10, 4 and 4 times during the southwest monsoon (May–October), respectively. The trapped jellyfish were collected from shrimp trammel net. Additional specimens were occasionally received from fishermen. The specimens were examined, photographed, bell height measured and the amount of branching pedalia counted.
Means and standard deviations of bell height and number of tentacles of C. buitendijki were calculated and compared by box plots.
2.2 DNA extraction, PCR amplification and sequencing
A small piece (about 0.5 cm) of tentacle or rhopalia or mesoglea was cut off from the selected samples, and preserved in 99% EtOH at a ratio of 10–acl: 1 tissue (v:v). The fixed tissues were stored at 4°C for DNA analysis.
The genomic DNA was extracted using the commercial animal tissue extraction kit or a CTAB/chloroform method described by Dawson et al. (1998). The nuclear 18S and mitochondrial 16S gene fragments were amplified using the primer pairsL18S: 5′–CGGAAGGGCACCACCAGGAG–3′, 18Sb: 5′–GATCCTTCTGCAGGTTCACCTAC–3′ and BRDGP–1: 5′–TCGACTGTTTACCAAAAACATAGC–3′, BRDGP–2: 5′–ACGGAATGAACTCAAATCATGTAAG–3′, respectively (Bayha, 2005; Bayha et al., 2010). PCR reactions were performed on the thermal cycler following the optimized protocol (Liu et al., 2016). The amplicons were directly sequenced bi-directionally on the ABI3130XL genetic analyzer. In cases where direct sequencing was not applicable, amplicons were cloned using the TA cloning kits and then sequenced.
2.3 Sequence analysis
The resulting sequences were cleaned for vectors, primers and ambiguous nucleotides and subsequently aligned with the reference sequences downloaded from GenBank using Clustal W algorithm (Thompson et al., 1994). The phylogenetic relationship between unknown specimen and references was analyzed using maximum likelihood (ML) and neighbor joining (NJ) methods. Robustness of resulting phylogenetic trees was assessed by boostrapping for 1 000 replicates. The best assignment of the unknown specimen was hypothesized, and the results from different genes were compared to evaluate the consistency of the conclusions.
3 Results and discussion
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3.1 Sample measurements
Average bell height sizes from Ranong (n=29): 38.37±8.92, Phang-nga (n=401): 40.84±7.09, Phuket (n=171): 42.40±9.05, Krabi (n=48): 44.31±8.22, Trang (n=66): 32.75±5.76 and Satun (n=99): 44.33±11.09. The values are not significantly different (Fig. 1 and Table 1). However, the number of tentacle of C. buitendijki in Trang is significant different from that of Phuket and Krabi (Fig. 2 and Table 1).
3.2 Systematic account
Order Chirodropida
Family Chiropsalmidae Thiel, 1936
Genus Chiropsoides Southcott, 1956
Chiropsoides Southcott, 1956
Type species: Chiropsalmus buitendijki Horst, 1907 (by monotypy).
Diagnosis: Chirodropida with smooth, unbranched, finger-like gastic saccules, lacking filaments, unilaterally branching pedalia (Gershwin, 2006).
Remarks: Chiropsoides quadrigatus is a nomen dubium species, meaning a species commonly in doubt and debate. Although it best resides in Genus Chiropsoides, a new genus may soon be necessary.
Chiropsoides buitendijki (Horst, 1907)
(Figs 1, 2, 3a–h and Table 1)
Chiropsalmus buitendijki Horst, 1907: 101–106, Pl. 2, Figs 1–5.
Chiropsoides buitendijki – Gershwin, 2006: 18–22, Pls 3a–d, 5b, c, with synonymy; – Sucharitakul et al., 2016: 7–14.
3.2.1 Morphological study
Description: A total of 814 specimens were collected and examined. A set of specimens preserved in a good condition was selected for registration (Appendix Table A1). Cuboidal bell, with a rounded dome-shape apex; smooth exumbrellar surface without nematocyst warts. Thick mesoglea at bell apical and interradial pillars. Adradial body walls have thinner mesoglea layer; becoming thicker in upper-half of the bell. Adradial furrows shallow in lower-half bell and disappear in upper bell. Interradial furrows absent.
Eight gastric saccules attach to upper subumbrellar cavity; 2 pouches each pillar, unbranched, finger-like in shape, longer than 2/3 of the bell height. Single rooted phacellae arrange itself in a horseshoe-shape, attaching to each corner. Each filament is short and unbranched (Figs 3d, e).
Four pedalia present, interradial, with 3–6 tentacular branches abaxially, aligned and size reduced downward; terminal branch is the smallest. Main pedalia curve into oral direction below the bell. Pedalial canals with a long, narrow spike shape (Fig. 3b),point into each pillar mesoglea. Abaxial ridge of pedalial canals have a short spike between 2 tentacular canals while adaxial side is fine without any spike. Pedalial canals radially flat as ribbon-like tentacles but smaller in diameter. Tentacular banding comes with 1–3–2–3–2–3–2–3–1 patterns (1–major band, 2–thicker minor band and 3–thinner minor band; Fig. 3h).
Four rhopalial niches present, perradial, with a tiny upper scale; lower edge is slightly concave. Ostia oval shaped and shallow, without rhopaliar horns. Six eyes in each rhopalium, with 2 median lensed eyes and 4 lateral pigment spots (Fig. 3g).
Velarium wide; 2 velarial canals per octant then dendritically branched into countless canals in highly complex form. Perradial lappets pyramidal shape, about equal in each side, with lateral and distal branches, complex dendritic form (Fig. 3f). Transparent and colourless living body, with yellowish-white tentacles.
Remarks: The character of rhopalium agrees with that described by Gershwin (2006) and Sucharitakul et al. (2016, Figs 2A, B). Gershwin (2006) found that C. buitendijki has a phacellae arranged in V-shape as a typical Chirodropida being, but all specimens examined in this study show a conspicuous horseshoe-shaped phacellae. The tentacular banding pattern was revealed in this study because of the good specimen condition, as well as the staining technique. A preserved tentacle in formalin normally has a yellowish-white color.
Even though the number of specimens varys in each province, the range and mean of bell height from Ranong, Phang-nga, Phuket, Krabi and Satun show an increasing trend (Table 1). The specimens from Trang, however, were slightly lower in bell height.
Distribution: India, Thailand (Andaman Sea), Malay Archipelago, and Indochina.
3.2.2 Phylogeny
The partial sequences of 16S and 18S genes were generated from eight samples. The 18S sequences of the eight samples were 100% identical from each other, and showed two nucleotide differences from the deposited sequence of C. buitendijki (accession No. KJ135023) from Sucharitakul et al. (2016). Due to the length variation, KJ135023 was excluded from the following phylogenetic analysis.
These eight 18S gene sequences formed a monophyletic clade sister to Meteorona (LC033478, LC033479 and LC033480), a new genus observed in Japan (Toshino et al., 2015, Fig. 4).
The 16S gene sequences, on the other hand, showed significant divergence within the eight samples and formed two reciprocally monophyletic clades, one enclosed specimens of PMBC 25893 (accession No. KY980651–2) and PMBC 27976 (accession No. KT982728), the other consisted of the five specimens of PMBC 27985 (accession No. KT982726), PMBC 27972 (accession No. KT982727), PMBC 27986 (accession No. KT982729), PMBC 27989 (accession No. KT982730) and PMBC 27971 (accession No. KT982725) (Fig. 5).
Above all, these eight samples were genetically similar to C. buitendijki identified by Sucharitakul et al. (2016), and distinct to the other known taxa in Order Chirodropidae, including Chironex, Chiropsella, Chiropsalmus and Meteorona.
Acknowledgements
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The authors thank Sukthong Piyawut and Chanachon Krittaya, former staff from the Reference Collection, Phuket Marine Biological Center, for their kind assistance in sample measurement. Thanks also go to Hyllebergemer Jorgen and anonymous reviewers for providing valuable comments on the manuscript.
Funding
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  • China-ASEAN Maritime Cooperation Fund; the Tropical Marine Ecosystem Collaborative Study (TiME) of the Thailand-China Joint Laboratory for Climate and Marine Ecosystem; the Public Science and Technology Research Funds Projects of Ocean under contract No. 201505004; the fund from Phuket Marine Biological Center; the Miscellaneous Contribution No. 60 from Phuket Marine Biological Center.
References
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Aungtonya C, Chanachon K. 2012. Species and distribution of venomous jellyfish in coastal areas of Phuket Province. Phuket: Phuket Marine Biological Center
Bayha K M. 2005. The molecular systematics and population genetics of four coastal ctenophores and scyphozoan jellyfish of the U.S. Atlantic and Gulf of Mexico [dissertation]. Newark: the University of Delaware
Bayha K M, Dawson M N, Collins A G, et al. 2010. Evolutionary relationships among scyphozoan jellyfish families based on complete taxon sampling and phylogenetic analyses of 18S and 28S ribosomal DNA. Integrative and Comparative Biology, 50(3): 436–455, doi: 10.1093/icb/icq074
Dawson M N, Raskoff K A, Jacobs D K. 1998. Field preservation of marine invertebrate tissue for DNA analyses. Molecular Marine Biology and Biotechnology, 7(2): 145–152
Fenner P J, Lippmann J, Gershwin L. 2010. Fatal and nonfatal severe jellyfish stings in Thai waters. Journal of Travel Medicine, 17(2): 133–138, doi: 10.1111/j.1708-8305.2009.00390.x
Gershwin L A. 2006. Comments on Chiropsalmus (Cnidaria: Cubozoa: Chirodropida): a preliminary revision of the Chiropsalmidae, with descriptions of two new genera and two new species. Zootaxa, 1231: 1–42
Haeckel E. 1880. System der Acraspeden. Zweite Halfte des System der Medusen. Jena: Verlag von Gustav Fischer, 361–672
Horst R. 1907. On a new cubomedusa from the Java-Sea: Chiropsalmus buitendijki. Notes from the Leyden Museum, 29: 101–106
Liu Ruijuan, Xiao Jie, Zhang Xuelei, et al. 2016. Genetic analysis of common venomous Cubozoa and Scyphozoa in Thailand waters. Haiyang Xuebao (in Chinese), 38(6): 51–61
Southcott R V. 1956. Studies on Australian cubomedusae, including a new genus and species apparently harmful to man. Australian Journal of Marine and Freshwater Research, 7(2): 254–280, doi: 10.1071/MF9560254
Sucharitakul P, Aungtonya C, Chomdej S. 2016. DNA sequencing complements morphological identification of Chiropsoides from Nam Bor Bay, Phuket, Thailand. Phuket Marine Biological Center Research Bulletin, 73: 7–14
Thompson J D, Higgins D G, GibsonT J. 1994. Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22(22): 4673–4680, doi: 10.1093/nar/22.22.4673
Toshino S, Miyake H, Shibata H. 2015. Meteorona kishinouyei, a new family, genus and species (Cnidaria, Cubozoa, Chirodropida) from Japanese waters. ZooKeys, 503(2): 1–21
Appendix
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Year 2018 volume 37 Issue 10
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Article Info
doi: 10.1007/s13131-018-1311-4
  • Receive Date：2017-09-19
  • Online Date：2026-04-14
  • Published：2018-10-25
Article Data
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History
  • Received：2017-09-19
  • Accepted：2018-02-16
Funding
China-ASEAN Maritime Cooperation Fund; the Tropical Marine Ecosystem Collaborative Study (TiME) of the Thailand-China Joint Laboratory for Climate and Marine Ecosystem; the Public Science and Technology Research Funds Projects of Ocean under contract No. 201505004; the fund from Phuket Marine Biological Center; the Miscellaneous Contribution No. 60 from Phuket Marine Biological Center.
Affiliations
    1 Phuket Marine Biological Center, Phuket 83000, Thailand
    2 The First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China
    3 Animal Systematics and Molecular Ecology Laboratory, Department of Biology, Faculty of Science, Mahidol University, Bangkok 10400, Thailand

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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