Toshiaki Shitamitsu

須之部 友基

須之部, 友基

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Notes on protandry in the creediid fishes Limnichthys fasciatus and L. nitidus (Teleostei: Creediidae)

Sunobe, Tomoki

スノベ, トモキ

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TUMSAT-OACIS Repository - Tokyo University of Marine Science and Technology (東京海洋大学)Notes on protandry in the creediid fishesLimnichthys fasciatus and L. nitidus(Teleostei: Creediidae)著者 Toshiaki Shitamitsu, 須之部 友基journal orpublication titleIchthyological Researchvolume 64number 3page range 365-367year 2017-07科学研究費研究課題 魚類における配偶システムの系統進化と脳内神経葉ホルモン遺伝子に関する研究研究課題番号 16K07507URL http://id.nii.ac.jp/1342/00001580/doi: 10.1007/s10228-016-0566-z1   1  2  3  4 Notes on protandry in the creediid fishes Limnichthys fasciatus  and L. nitidus 5 (Teleostei: Creediidae) 6  7 Toshiaki Shitamitsu・Tomoki Sunobe 8  9 T. Shitamitsu・T. Sunobe 10 Laboratory of Fish Behavioral Ecology, Tateyama Station,  Field Science Center,  11 Tokyo University of Marine Science  and Technology, 670 Banda, Tateyama 12 294–0308, Japan 13  14 Present Address: 15 T. Shitamitsu (✉)  16 Marine Fisheries Research and Development Center, Japan Fisheries Research 17 and Education Agency, 15F Queen’s Tower B, 2–3–3 Minatomirai, Nishi–ku, 18 Yokohama–city, Kanagawa 220–6115, Japan 19 E-mail: shitamitsu@affrc.go.jp  20  21 Running title: Protandry in Limnichthys  22  23 News and Comments 24  25 Six pages 26  27 Two figures  28 2  Fishes of the family Creediidae occur mainly on sandy bottom of tropical and 29 temperate shallow waters in Indo–West Pacific Ocean. Eight genera and 18 valid 30 species are known (Fricke and Golani 2012; Nelson et al . 2016). For ecological 31 information, Leis (1982) and Reader et al . (2000) describe egg and larval 32 development of L. fasciatus and L. nitidus, respectively. Cozzi and Clark (1995)  33 reports darting behavior, exhibited by L. nitidus as quick movements out and 34 back in the sand, suggesting that it  was an escape behavior  when they were 35 disturbed. 36 Biological information on reproduction of Creediidae has been very limited. 37 Langston (2004) histologically studies sexuality of 10 species of creediids and 38 shows that Crystallodytes cookei  and Limnichthys nitidus,  identified as L. 39 donaldsoni  in the original paper, which is a junior synonym of L. nitidus  40 (Yoshino et al . 1999; Shimada 2013), are regarded as protandry (sex change 41 from male to female) by histological observation of gonads and size 42 distributions of both sexes  (female>male). In addition to these two species,  43 Chalixodytes tauensis , Crystallodytes pauciradiatus  and L. fasciatus have 44 gonads comprised of ovarian and testicular parts divided by connective tissue  in  45 functional males, whereas those of females consist of only ovarian part .  46 Sadovy de Mitcheson and Liu (2008) indicates that functional 47 hermaphroditism is confirmed in 27 families of teleost fishes in their review  on 48 hermaphrodite fishes. However, Creediidae is not included among these families. 49 Namely, hermaphroditism of Creediidae has been overlooked for a long time. In 50 order to provide evidential data of  functional hermaphroditism, we made 51 histological observations on gonads of the two creediid fishes L. fasciatus  and L.  52 nitidus.  53 Forty–two specimens of L. fasciatus  were collected by hand net using SCUBA 54 at Banda Beach, Tateyama, Chiba , Japan (34 58′ N, 139 46′ E) on 13 April (n = 55 1), 14–15 May (n = 7), 17 June (n = 9), 18–16 July (n = 13) and 18–21 August (n 56 3  = 12), 2013. The fish were brought to the laboratory, anesthetized in 100 ppm 57 MS-222, measured for standard length (SL) to the nearest 0.1 mm with a digital 58 caliper, fixed in Bouin’s solution for 24 hours, and then preserved in 70 % 59 ethanol. The abdominal parts of the specimens were embedded in paraffin, 60 sectioned to 5 μm, and stained with haematoxylin and eosin.  61   We also examined gonads of seven L. nitidus  specimens deposited at the 62 National Science Museum, Tokyo: NSMT–P 71438 (n = 4, 16.0–20.5 mm SL, 63 collected at Ambon Isl ., Indonesia on 5 December 1998) and NSMT–P 77532 (n 64 = 3, 14.9–26.8 mm SL, Okinoshima Isl.,  Kochi, Japan on 24 July 2007). We 65 dissected and extracted the abdominal organs containing the gonads and 66 prepared the tissues following the methods outlined above.   67 The gonads of 21 specimens of L. fasciatus were comprised of both testis and 68 ovary (Fig. 1a), which were apparently divided  by connective tissue. The 69 oocytes of all 21 hermaphroditic specimens  were immature, while the testicular 70 parts of seven specimens collected in July and August were developed and 71 sperm and spermatids were detected.  Therefore, those individuals were regarded 72 as functional male. The gonads of other 21 specimens were comprised of only 73 vitellogenic oocytes (Fig. 1b).  These individuals were identified as functional 74 female. The females (mean ± SD = 39.8 ± 7.0 mm SL, range = 25.4–47.5 mm SL) 75 were significantly larger than the males (31.3 ± 5.1 mm SL, 24.3–39.1 mm SL) 76 (t-test, t  = –4.4, df = 40, P < 0.01) (Fig. 2). These results strongly suggest that L. 77 fasciatus is protandrous. 78 The gonadal structure of  L. nitidus also indicated bisexuality (Fig. 1c, d), as 79 in L. fasciatus. The gonads of the three individuals (14.9, 16.4 and 17.8 mm SL) 80 were comprised of both testicular ovarian parts . However, only ovarian tissue 81 was detected in the other four specimens (16.0, 20.5,  23.5 and 26.8 mm SL). The 82 former and latter samples were regarded as males and females, respectively. 83 Although we did not have enough data on sizes for a statistical analysis, there 84 4  was a tendency that the females were larger than the males.  These results 85 suggest that L. nitidus is also protandrous. 86 The gonadal structure of L. fasciatus and L. nitidus are well corresponded 87 with the previous study by Langston (2004), being divided into testicular and 88 ovarian parts by the connective tissue in functional male and comprised of only 89 ovarian part in functional female. In some protandrous species, the structure of 90 ovotestis is divided by connective t issue (Sadovy and Shapiro 1987). This type 91 of gonad structure is similar to those of the other protandrous species like 92 Thysanophrys celebica  (Platycephalidae) (Sunobe et al.  2015), genus 93 Amphiprion  (Pomacentridae)  (Moyer and Nakazono 1978) and Acanthopagrus 94 schlegelii (Sparidae) (Chang and Yueh 1990). 95 Protandry has been known in Centropomidae, Gonostomidae, Latidae, 96 Muraenidae, Platycephalidae, Pomacentridae and Sparidae (Sadovy de 97 Mitcheson and Liu 2008). Creediidae is the eighth family, which protandry is 98 confirmed. 99  100 Acknowledgements  We are deeply indebted to E. Katayama and G. Shinohara 101 (NSMT) for giving us the opportunity to examine L. nitidus specimens and for 102 providing important basic knowledge. This study is supported by JSPS 103 KAKENHI Grant to T.Sunobe (no. 19570016 and 24370006) from Japan Society 104 for Promotion of Science.  105  106 References 107  108 Chang CF, Yueh WS (1990) Annual cycle of gonadal histology and steroid 109 profiles in the juvenile males and adult females of the protandrous black 110 porgy, Acanthopagrus schlegeli . Aquaculture 91:179–196 111 Cozzi J,  Clark E (1995) Darting behavior sandburrower fish, Limnichthys 112 5  nitidus (Creediidae), in the Red Sea. Env Biol Fish 44:327–336 113 Fricke R, Golani E (2012) Limnichthys marisrubri , a new species of sand diver 114 (Teleostei: Creediidae) from the Red Sea. Stuttgater Beiträge zur Naturkunde 115 A, Neue Serie 5: 287–292 116 Langston RC (2004) Gonad morphology and sex change in sandburrowers 117 (Teleostei: Creediidae). Doctoral  dissertation, UNIVERSITY OF HAWAI’I  118 Leis JM (1982) Hawaiian creediid fishes (Crystallodytes cookei  and Limnichthys 119 donaldsoni): Development of eggs and larvae and use of pelagic eggs to trace 120 coastal water movement. Bul Mar Sci 32:166–180 121 Moyer JT and Nakazono (1978) Protandrous hermaphroditism  in six species of 122 the anemonefish genus Amphiprion  in Japan. Japan J Ichthyol 25: 101–106 123 Nelson JS, TC Grande, MVH Wilson (2016) Fishes of the world, 5th edition. 124 John Wiley & Sons, Inco., New Jersey 125 Reader SE, JM Leis, DS Rennis (2000) Creediidae : In Leis JM, Carson–Ewart 126 BM (eds) The larvae of Indo–Pacific coastal fishes: An identification guide to 127 marine fish larvae. BRILL, Netherlands, pp 575–578 128 Sadovy Y, Shapiro DY (1987) Criteria for the diagnosis of he rmaphroditism in 129 fishes. Copeia 1987:136–156 130 Sadovy de Mitcheson Y, Liu M (2008) Functional hermaphroditism in teleosts. 131 Fish and Fisheries 9: 1–43 132 Shimada K (2013) Creediidae. In: Nakabo T (ed) Fishes of Japan with pictorial 133 keys to the species, 3rd edition. Tokai Univ Press, Tokyo, pp 1270–1271, 134 2093–2094 135 Sunobe T, Sakaida S, Kuwamura T (2015) Random mating and protandrous sex 136 change of the platycephalid fish Thysanophrys celebica  (Platycephalidae). J 137 Ethol 34: 15–21 138 Yoshino T, Kon T, Okabe S (1999) Review of the genus Limnichthys 139 (Perciformes: Creediidae) from Japan with description of a new species. 140 6  Ichthyol Res 46:73–83 141   142 7  Figure legends 143  144 Fig. 1 Gonad structure of Limnichthys fasciatus (male: a,  female: b) and L. 145 nitidus (c ,  d).  O–ovarian tissue; T–testicular tissue. Scale bars  100 μm (a) and  146 300 μm (b, c, d) 147  148 Fig. 2 Size frequencies of male and female Limnichthys fasciatus   149 Fig. 1Fig. 2

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Notes on protandry in the creediid fishes Limnichthys fasciatus and L. nitidus (Teleostei: Creediidae)

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