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Development of Tripedalia Binata Moore, 1988 (Cubozoa

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Development of Tripedalia Binata Moore, 1988 (Cubozoa Hydrobiologia (2017) 792:37–51 DOI 10.1007/s10750-016-3022-1 PRIMARY RESEARCH PAPER Development of Tripedalia binata Moore, 1988 (Cubozoa: Carybdeida: Tripedaliidae) collected from the eastern Gulf of Thailand with implications for the phylogeny of the Cubozoa Sho Toshino . Hiroshi Miyake . Khwanruan Srinui . Nattawut Luangoon . Vorathep Muthuwan . Saowapa Sawatpeera . Shiho Honda . Haruka Shibata Received: 17 March 2016 / Revised: 27 September 2016 / Accepted: 8 October 2016 / Published online: 28 October 2016 Ó Springer International Publishing Switzerland 2016 Abstract Box jellyfishes are considered among the of budding. Complete metamorphosis of a whole most dangerous sea creatures due to the lethal polyp into a single medusa occurred. Newly detached poisonous stings to humans. In order to predict the medusae were distinguished from those of other occurrences of box jellyfishes, it is necessary to cubozoans by the pattern of nematocyst warts on the understand their ecology and life cycle. The small box exumbrella and red chromatophores. The develop- jellyfish Tripedalia binata was collected from eastern mental features of T. binata resemble most closely Thailand, in order to observe its life history, to those of T. cystophora and Copula sivickisi. The compare its morphological characters with other similarities in all early life cycle stages of those cubozoans, and to discuss ecology and phylogeny in species support the close relationship of these species the class Cubozoa. Fertilization occurred internally, in the family Tripedaliidae. blastulae developed into planulae. Planulae were bred in the gastral pocket of the female medusa and Keywords Copulation Á Cyst Á Polyp formation Á released into the water. Free swimming planulae Medusa Á Metamorphosis settled and metamorphosed into polyps. Adult polyps formed cysts at temperatures below 20°C water deterioration or starvation. Budding occurred in adult polyps, and buds were released after commencement Introduction Box jellyfishes are considered among the most dan- Handling editor: Jo¨rg Dutz gerous sea creatures due to the lethal poisonous stings to humans (Cunningham & Goetz, 1996; Fenner & S. Toshino (&) Á H. Miyake Á S. Honda Á H. Shibata Graduate School of Fisheries Sciences, Kitasato Williamson, 1996). In order to predict to occurrences University, 1-15-1 Kitasato, Sagamihara, of box jellyfishes, it is necessary to understand their Kanagawa 252-0373, Japan ecology and life cycle. Research on the development e-mail: [email protected] of Cubozoa was first reported by Conant (1898). He S. Toshino found mature eggs of Tripedalia cystophora Conant, Kuroshio Biological Research Foundation, Nishidomari, 1897, in stomach pouches of the female medusa which Otsuki, Hata, Kochi 788-0333, Japan developed into swimming planulae. The planulae settled and developed into small polyps with three to K. Srinui Á N. Luangoon Á V. Muthuwan Á S. Sawatpeera Institute of Marine Science, Burapha University, Mueang, five tentacles. Unfortunately, the polyps died after Chon Buri, Chon Buri 20131, Thailand three weeks in aquaria without undergoing further 123 38 Hydrobiologia (2017) 792:37–51 development. Okada (1927) observed the segmenta- suggested that T. binata likely shows copulation tion of eggs of Carybdea brevipedalia Kishinouye, behavior because both sexes possess stomach purses, 1891 (as Carybdea rastonii), and reared the resulting and a male specimen was shown to have sper- planulae to three-tentacled polyps but they died of matophores in its purse (Straehler-Pohl et al., 2014). starvation within a few weeks. Tripedalia binata has been reported from eastern Werner et al. (1971) first succeeded rearing T. India and northern Australia (Moore, 1988; Under- cystophora and showed an entire life cycle of this wood et al., 2013). Medusae of this species were found species. Cubozoa has alternation of generations, in creeks, aquaculture pond, and sandy beaches, near between a sexually planktonic medusa and an asex- the mangroves during the rainy season (Moore, 1988; ually benthic polyp (Werner et al., 1971). Cubopolyps Underwood et al., 2013). However, the life cycle of possess a clear radial-symmetrical body that lacks all this species has never been studied. The present paper inner structures, including the four gastric septae, four describes its life history from fertilized eggs to polyp gastric pockets, four longitudinal muscle strands, and formation to metamorphosis into a medusa and four septal funnels present in scyphopolyps (Werner, compares morphological characters between other 1973, 1976, 1993; Chapman, 1978). Additionally, cubozoans to discuss ecology and phylogeny in the solitary cubopolyp metamorphose completely into a class Cubozoa. single juvenile medusa without any remaining regen- erative residuum on the substrata (Werner et al., 1971; Cutress & Studebaker, 1973; Arneson & Cutress, Materials and methods 1976; Yamaguchi & Hartwick, 1980; Straehler-Pohl & Jarms, 2011; Carrette et al., 2014; Toshino et al., Tripedalia binata medusae (Fig. 1A, B) were col- 2014). Werner (1973) established the class Cubozoa lected using an underwater fish-luring lamp (YF-500, based on these unique features. However, cubopolyps Hapyson, Japan) at Mangrove swamp, Trat Province, of Carybdea marsupialis (Linnaeus, 1758) and Mor- the eastern Gulf of Thailand (Fig. 2), between 21:00 bakka virulenta (Kishinouye, 1910) have been shown and 23:30 on March 17, 2014 (water temperature to undergo something akin to a modified strobilation 32.3°C, salinity 21.8). Two mature medusae, one (Straehler-Pohl & Jarms, 2005; Toshino et al., 2015). female and one male, were taken by a dip net (mesh The family Tripedaliidae currently comprises three size 0.2 mm). Male and female medusae were kept in a species in two genera, Tripedalia and Copula (Bent- bottle (diameter 72 mm, height 97 mm, water volume lage et al., 2010; Straehler-Pohl et al., 2014). 1000 ml) with fresh seawater (salinity 33) at about 25 Tripedaliids are characterized by their display of to 30°C in the laboratory at Burapha University, sexual dimorphism of the gonads, production of Thailand. These medusae were fed with mysid or spermatophores, and males and females possessing subgastral sacs, pockets, or purses which function as seminal vesicles or spermathecae (Straehler-Pohl et al., 2014). In addition, recent molecular phyloge- netic analyses suggest that Copula sivickisi (Stiasny, 1926) is more closely related to T. cystophora than any other species (Bentlage et al., 2010). Tripedalia binata Moore, 1988, is a small species in the class Cubozoa, with a maximum bell height of 11 mm and maximum bell diameter (interpedalial distance) of 14.5 mm, that possesses two pedalia per corner of the bell margin instead of the three characteristic of T. cystophora (Moore, 1988). This species displays sexual dimorphism of the gonads in which mature males possess stick-shaped testes while Fig. 1 Tripedalia binata Moore, 1988, live, lateral view, in laboratory. A Mature female, B mature male. GF gastric mature female possess butterfly-shaped ovaries filaments, P pedalium, Rh rhopalium, T tentacle. Scale bars (Straehler-Pohl et al., 2014). Additionally, it was 5mm 123 Hydrobiologia (2017) 792:37–51 39 For nematocyst identification in polyps and medu- sae, fresh tissue was squashed under a cover slip and examined under an optical microscope (CX 21, Olympus, Japan). Nematocysts were identified according to Gershwin (2006) and Collins et al. (2011). For determination of the respective abundance of nematocyst types in multiple areas on the tentacles of polyps and medusae, at least 200 nematocysts were counted. Results Fertilization and polyp formation On the night of collection, gonads of female and male medusae were transparent. Spermatophores were not observed in the stomach purse of both male and female medusae. Three days after medusae were collected, and fertilization was observed in the laboratory. The gonads of female became yellow, while male testis withered. Three days after fertilization, hundreds of Fig. 2 Map of the sampling site, Trat, Eastern Thailand free-swimming planulae (Figs. 1A, 3A, B) were bred in gastric cavity of the female. Two days later, all planulae were released from the female’s gastric Artemia nauplii on a daily basis. Rearing water was cavity. Planulae (Fig. 3C, D) were about 100 lmin replaced with fresh seawater twice or thrice a week. diameter and about 130 lm in length and had about Planulae obtained from these medusae in the twenty dark reddish larval ocelli at the part of aboral. laboratory were incubated in petri-dishes (diameter Two to four days after planula formation, planulae 75 mm, height 45 mm) filled with filtered seawater settled on the bottom of petri-dishes or water surface (0.22 lm filter pore size) at 30°C (temperature of the (Fig. 4A). Planulae developed into primary polyps, sampling site) in an incubator. Primary polyps were and larval ocelli faded out within 2 days. Primary transferred to petri-dishes (diameter 78 mm, height polyps were either settled (Fig. 4B–D) or actively 24 mm) filled with filtered seawater (1 lm filter pore detached to start a creeping phase (Fig. 4B, E). The size) and kept at 30°C. Chopped Artemia nauplii were shape of the settled primary polyps resembled a pouch fed directly to polyps using a fine needle on a daily with a very short stalk, with one to four tentacles basis. Rearing water was completely replaced with protruding from the ovoid calyx around the mouth filtered seawater (1 lm filter pore size) about 3 h after cone. At a body length of about 0.28 mm the mouth feeding. During metamorphosis from polyp to disc diameter of the polyps was about 0.08 mm. The medusa, the cultures were not fed nor the water primary creeping polyps had elastic worm-shaped changed. Several polyps were separated and exposed body with one to four outstretched tentacles. They to a wide range of temperatures (15 to 30°C) to crept to change location using their body and tentacles. observe polyp reaction. At a body length of about 0.44 mm, the mouth disc Newly detached medusae were kept in a disposable diameter of the polyps was about 0.07 mm.
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