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Biogeography 20. 73–77. Sep. 20, 2018

A rare record of the bump-head sunfish, alexandrini (: ) with a 117 kg ovary from Hualien,

Etsuro Sawai1 and Yung Chou Chang2*

1 Ocean Sunfishes Information Storage Museum, C-102 Plaisir Kazui APT, 13-6 Miho, Shimizu-ku, Shizuoka, Shizuoka 424-0901, 2 Center for General Education, Tzu Chi University, No.701, Sec. 3, Jhongyang Rd., Hualien City, Hualien County 97004, Taiwan, R.O.C.

Abstract: A female specimen of (Ranzani, 1839) was captured off the waters of Hualien, Taiwan on March 2008, representing the third record of this from Taiwanese waters. To date, this specimen (1380 kg body weight) is the heaviest M. alexandrini on record in Taiwan. Its ovarian weight (117 kg) and gonadosomatic index (8.5) are also the heaviest and highest respectively recorded values for the Mola .

Key words: gonadsomatic index, Mola alexandrini, ovary, rare record, Taiwan

Some species of the ocean sunfishes of the Taiwanese waters (especially in eastern Taiwan) is Molidae (Tetraodontiformes) grow to more than 3 significantly lower for Mola (10% of total ocean sun- m total length (TL) and 2000 kg body weight (BW) catch) than forMa. lanceolatus (ca. 90 %) (Liu (e.g., Sawai et al., 2018). They have a clavus instead et al., 2009), this fact is relatively unknown among of a caudal (e.g., Fraser-Brunner, 1951). Ocean Taiwanese people and accurate knowledge on Mola sunfishes have a long history of taxonomic confu- in Taiwan is limited. Mola in the Taiwanese waters sion in the world. There are five currently recognized are generally recognized as being from only one species in the family Molidae: Mola species, M. mola (e.g., Shen & Wu, 2011). However, mola (Linnaeus, 1758), bump-head sunfish M. al- two species, M. mola and M. alexandrini (Yoshita exandrini (Ranzani, 1839), hoodwinker sunfish M. et al., 2009; Sawai et al., 2018), have recently been tecta Nyegaard, Sawai, Gemmell, Gillum, Loner- confirmed. Of the two Mola species, M. alexandri- agan, Yamanoue and Stewart, 2017, sharptail sunfish ni from Taiwanese waters was reported based only Masturus lanceolatus (Liénard, 1840), and slender on two specimens until now (sample code TW-3 in sunfish Ranzania laevis (Pennant, 1776) (Nyegaard Yoshita et al., 2009 and TaHMo-2 in Sawai et al., et al., 2018; Sawai et al., 2018). 2018). Here we report a huge specimen of M. alex- Mola sunfishes are sometimes confused with andrini from the waters off Hualien (eastern Taiwan) Ma. lanceolatus by the similarity of their external as the third record from the Taiwanese waters. This morphology. For example, the photograph of Ma. specimen also represents the heaviest M. alexandrini lanceolatus is used in some Taiwanese picture record in Taiwan, and the heaviest ovarian record in books as M. mola (e.g., Shen & Wu, 2011; Zheng Mola. et al., 2011). Although ocean sunfishes catch rate in A female specimen was caught by Chaojin set net ——————————————————————— off the coast of Hualien, Taiwan (24°2'N, 121°37'E), *Corresponding author:[email protected] on 27 March 2008. This specimen was brought to

− 73 − Rare record of Mola alexandrini with 117 kg ovary Etsuro Sawai and Yung Chou Chang the fishing port and sold after which the whole body and ovary were weighed to the nearest 1 kg. Unfor- tunately, the TL of the specimen was not formally measured but is estimated to exceed 2 m TL from the photograph (Fig. 1). No ovarian tissue samples were obtained. Species identification followed Sawai et al. (2018). This specimen was identified as M. alexandrini through three key characters: bumped head (arrow in Fig. 1A), bumped chin (arrow in Fig. 1A), and rounded clavus (arrow in Fig. 1B). The shape of the gonads of Mola significantly differs between male and female: the ovary is singular and ball shaped, the testis is paired, elongated and rod-like (Nakatsubo et al., 2007a; Nyegaard et al., 2018; Sawai et al., 2018). The gonad of this specimen was determined as an ovary because it was singular and ball shaped

Fig. 2. An ovary (117 kg) of Mola alexandrini from Hualien, Taiwan. A: the ovary and some oocytes inside the peritoneal cavity. B: the ovary at weighing. This ovary was weighed with a blue basket (3 kg), and the needle of the green weighing scale was rotated one time (arrow) and showed 120 kg. A jin (Taiwanese traditional unit of weight) equals to 0.6 kg. Photographs by W. Z. Liu.

(Fig. 2). This specimen was 1380 kg in BW, 117 kg in go- nad weight (GW). Two specimens of M. alexandrini in the previous study (Yoshita et al., 2009; Sawai et al., 2018) have not been recorded for their body weight. Therefore, this present specimen represents the heaviest M. alexandrini on record in Taiwan. The Fig. 1. A female specimen of Mola alexandrini (1380 kg body ovary was weighed with a blue basket (3 kg, 40.7 cm weight, 117 kg gonad weight) was caught by Chaojin set net off the coast of Hualien, Taiwan (24°2'N, 121°37'E), × 66.2 cm × 35.0 cm), and shown to be 120 kg (the on 27 March 2008. A: head. B: posterior dorsal part of needle of the green weighing scale was rotated one body. Arrows indicate taxonomic key characters (bumped head, bumped chin, and rounded clavus) by Sawai et al. time; Fig. 2B). Although two persons supported the (2018). Photographs by W. Z. Liu. blue basket, the weighing was not almost affected.

− 74 − Rare record of Mola alexandrini with 117 kg ovary Etsuro Sawai and Yung Chou Chang

The only additional information on ovarian weight specimen (0.35). Maturity stage of Kamogawa spec- from M. alexandrini is only from a Kamogawa imen was determined to be the yolk globule stage specimen (2300 kg BW, ca. 8 kg GW, 272 cm TL) by histological observations of oocyte (Nakatsubo et in Nakatsubo et al. (2007b) (Table 1). Therefore, al., 2007b). Oocytes from the ovary of Hualien spec- we collected the ovarian data from the literature and imen are visible Fig. 2A. They are macroscopically compared it at the genus level. A literature survey translucent and orange or reddish orange (Fig. 2A). of available ovarian data from fish genera (Lidth de Referring to the other fishes, these macroscopic fea- Jeude, 1890; Martin & Drewry, 1978; Nakatsubo et tures of oocyte are presumed to be the stage between al., 2007b; Soichi, 2009; Yamanoue & Sawai, 2012; ‘developing’ and ‘spawning’ (e.g., Mackie et al., Kang et al., 2015; Sawai et al., 2015) shows Hualien 2009; Thulasitha & Sivashanthini, 2013). Although specimen to have the heaviest Mola ovary on record the level of GSI does not necessarily match the level (Table 1). of maturity stage (Nakatsubo et al., 2007a, b), the Mola alexandrini is currently the world's heavi- maturity stage of the Hualien specimen was likely est bony fish species (Sawai et al., 2018) but does more advanced than Kamogawa specimen. These not hold the record of the heaviest bony fish ovary. data from a huge ovary may suggest that the Taiwan- The current record belongs to a beluga sturgeon ese waters are an important place for maturity and Huso huso (Linnaeus, 1758) which was caught in reproduction of this species. Further studies of large the northern Caspian region in Russia in 1924. It gravid individuals are necessary to clarify the repro- weighed 1228.5 kg BW and had a 245.7 kg ovary ductive biology of M. alexandrini. containing an estimated 7729700 (Babushkin, 1947; Dettlaff et al., 1993; Helfman et al., 2009). Acknowledgments The values for gonadosomatic index (GSI, the gonad weight in percent of body weight) were calcu- We would like to thank the following persons lated for the estimation of maturation: GSI = gonad and institutions for assistance: G. Shinohara, Y. Ya- weight (GW, in g) / body weight (BW, in g) × 100 manoue, M. Nyegaard, W. Z. Liu, the staff of Dong (Nakatsubo et al., 2007a). Although BW of the Hual- Chang set net fishery farm, and the fishermen oper- ien specimen in this study was lighter than BW of ating the Chaojin set net. We also thank anonymous above-mentioned Kamogawa specimen in Nakatsu- reviewers for their valuable comments, which helped bo et al. (2007b), the GSI of Hualien specimen (8.5) us to improve the manuscript. The research was sup- was significantly higher than the GSI of Kamogawa ported by the Sasakawa Scientific Research Grant

Table 1. List of the published ovarian weights in the genus Mola.

Ovarian weight Body weight Total length Species Locality Literature (kg)* (kg) (cm) 4.5 no data 223 Mola tecta (?)** Ameland, the Netherlands Lidth de Jeude (1890); Martin & Drewry (1978) 7.999*** 2300 272 Mola alexandrini**** off Kamogawa, Chiba, Japan Nakatsubo et al. (2007b) 2.982 no data 210 Mola sp. off Kamogawa, Chiba, Japan Soichi (2009) ca. 36 1150 275 Mola mola off Yunotsu, Shimane, Japan Yamanoue & Sawai (2012); Sawai et al. (2015) 3.47 no data 250 Mola mola***** off Jeju island, Kang et al. (2015) 117 1380 no data Mola alexandrini off Hualien, Taiwan This study *A specimen with maximum ovarian weight in each literature. **This specimen was re-identified by Nyegaardet al. (2018). ***The ovarian weight in this specimen was calculated backward from the equation for obtaining the gonad index [GI = gonad weight (g) / total length (cm)3 × 10000] in Nakatsubo et al. (2007b: table 2). ****This specimen was re-identified by Sawaiet al. (2018). *****This specimen was re-identified from a taxonomic key character (wavy clavus) of fig. 2 in Kanget al. (2015) by this study.

− 75 − Rare record of Mola alexandrini with 117 kg ovary Etsuro Sawai and Yung Chou Chang from The Japan Science Society (23-512, 24-506 Wildl. Serv., Washington D. C. and 25-504). The English in our manuscript was re- Nakatsubo, T., Kawachi, M., Mano, N. & Hirose, H., viewed by Dr. Lawrence M. Liao (Graduate School 2007a. Estimation of maturation in wild and cap- of Biosphere Science, Hiroshima University). tive ocean sunfish Mola mola. Aquacul. Sci., 55: 259–264. (In Japanese with English abstract) Reference Nakatsubo, T., Kawachi, M., Mano, N. & Hirose, H., 2007b. Spawning period of ocean sunfish Babushkin, N. J., 1947. The fertility of the Caspian Mola mola in waters of the eastern Kanto Region, beluga (Huso huso). Zool. Zh., 26: 339–345. (In Japan. Aquacul. Sci., 55: 613–618. (In Japanese Russian with English summary) with English abstract) Dettlaff, T. A., Ginsburg, A. S. & Schmalhausen, O. Nyegaard, M., Sawai, E., Gemmell, N., Gillum, J., I., 1993. Sturgeon Fishes: Developmental Biology Loneragan, N. R., Yamanoue, Y. & Stewart A. and Aquaculture. Springer-Verlag, Berlin. L., 2018., Hiding in broad daylight: molecular Fraser-Brunner, A., 1951. The ocean sunfishes (Fam- and morphological data reveal a new ocean sun- ily Molidae). Bull. Br. Mus. (Nat. Hist.) Zool., 1: fish species (Tetraodontiformes: Molidae) that 89–121. has eluded recognition. Zool. J. Linn. Soc., 182: Helfman, G. S., Collette, B. B., Facey, D. E. & Bow- 631–658. en, B. W., 2009. The Diversity of Fishes: Biology, Sawai, E., Yamanoue, Y., Mochizuki, T. & Sakai, Y., Evolution, and Ecology, 2nd edition. Wiley-Black- 2015. Notes on the morphological characteristics well, Oxford. of extremely large specimens of Mola sunfishes Kang, M. J., Baek, H. J., Lee, D. W. & Choi, J. H., (Tetraodontiformes, Molidae) in Japanese mu- 2015. Sexual maturity and spawning of ocean seum collections. Bull. Ibaraki Nat. Mus., 18: sunfish Mola mola in Korean waters. Korean J. 65–70. (In Japanese with English abstract) Fish. Aquat. Sci., 48: 739–744. (In Korean with Sawai, E., Yamanoue, Y., Nyegaard, M. & Sakai, English abstract) Y., 2018. Redescription of the bump-head sunfish Lidth de Jeude, T. W. V., 1890. On a large specimen Mola alexandrini (Ranzani 1839), senior of Orthragoriscus on the Dutch coast. Notes Ley- of Mola ramsayi (Giglioli 1883), with designa- den Museum, 12: 189–195. tion of a neotype for Mola mola (Linnaeus 1758) Liu, K. M., Lee, M. L., Joung, S. J. & Chang, Y. C., (Tetraodontiformes: Molidae). Ichthyol. Res., 65: 2009. Age and growth estimates of the sharptail 142–160. mola, Masturus lanceolatus, in waters of eastern Shen, S. C. & Wu, K. Y. (Eds.), 2011. Fishes of Tai- Taiwan. Fish. Res., 95: 154–160. wan. National Museum of Marine Biology and Mackie, M., Jackson, G., Tapp, N., Norriss, J. & Aquarium, Taiwan. (In Chinese) Thomson, A., 2009. Macroscopic and microscopic Soichi, M., 2009. A gentle giant of the ocean, Mola description of snapper (Pagrus auratus) gonads mola, this mysterious fella. In: Saruwatari, T. & from Bay, Western . Fisheries Re- Nishi, G. (Eds.), Research activities at aquari- search Report No. 184. Department of Fisheries, ums: an intelligent world not limited to aquarium Western Australia. exhibits: 197–210. Tokai Univ. Press, Hadano. (In Martin, F. D. & Drewry, G. E., 1978. Development Japanese) of fishes of the mid-Atlantic Bight: an atlas of Thulasitha, W. S. & Sivashanthini, K., 2013. Micro- , larval and juvenile stages. VI. Stromateidae scopic staging system used in the identification through Ogcocephalidae. U. S. Dept. Int., Fish of gonad developmental stages of Scomberoides

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lysan. J. Fish. Aquat. Sci., 8: 355–366. Molidae) occurring around the coasts of Japan, Yamanoue, Y. & Sawai, E., 2012. The forefront of with notes on their geographical distribution and the study of ocean sunfishes—, ecology morphological characteristics. Ichthyol. Res., 56: and biogeography. In: Matsuura, K. (Ed.), Fishes 232–244. in the Kuroshio Current: 165–182. Tokai Univ. Zheng, M., Haung, S. & Lin, X., 2011. Marine Tai- Press, Kanagawa. (In Japanese) wan: Ecological Conservation Special Exhibition. Yoshita, Y., Yamanoue, Y., Sagara, K., Nishibori, M., National Taiwan Museum, Taipei. (In Chinese) Kuniyoshi, H., Umino, T., Sakai, Y., Hashimoto, H. & Gushima, K., 2009. Phylogenetic relation- (Received June 30, 2018; Accepted July 21, 2018) ships of two Mola sunfishes (Tetraodontiformes:

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