Skip to main content
Log in

Physiological effects of the lunar cycle on the spawning of a coral reef fish, Abudefduf Vaigiensis: in vivo and in vitro trait

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

The aim of the present study was to investigate the lunar cycle effects of the spawning of Audefduf vaigiensis through in vivo and in vitro analysis. For this purpose, the indices of GSI, serum levels of sex steroids, including testosterone (T), 17α-hydroxyprogesterone (OHP), 17α, 20β-dihydroxyprogesterone (DHP), and 11-keto-testosterone (11-KT) as well as the germinal vesicle breakdown (GVBD) were measured. The sampling pattern was weekly, based on the moon cycles as the new moon (NM), the first quarter (FQ), the full moon (FM), and the last quarter (LQ). In females, the highest in vivo values of the GSI index were obtained in FQ and LQ, and in males, this value was significantly higher in LQ than NM. The highest in vivo level of OHP in females was observed in FQ, whereas in males was obtained in FM. In both sexes, the in vivo serum levels of DHP were obtained in LQ. In males, the level of 11-KT were at the peak in NM. In vitro analysis showed the highest rate of GVBD in LQ. Moreover, the in vitro levels of T, OHP, and DHP were significantly higher in LQ compare to NM in both sexes. However, in males, the in vitro levels of 11-KT was significantly higher in NM than LQ. These cyclical changes obtained from in vivo plasma steroid hormones and in vitro data on GVBD suggested that lunar periodicity is a major external regulator that synchronized ovarian and testicular activity of A. vaigiensis with emphasis on spawning phenomenon.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agahama YN, Yamashita M (2008) Regulation of oocyte maturation in fish. Dev Growth Differ 50:S195–S219

    Google Scholar 

  • Allen GR (1991) Damselfishes of the World. Mergus

  • Asahina K, Kambegawa A, Higashi T (1995) Development of a microtiter plate enzyme-linked immunosorbent assay for 17 α, 20 β-21-trihydroxy-4-pregnen-3-one, a teleost gondadal steroid. Fish Sci 61:491–494

    CAS  Google Scholar 

  • Babatunde TA, Amin SMN, Romano N, Yusoff FM, Arshad A, Esa YB, Ebrahimi M (2018) Gonad maturation and spawning of cobia, Rachycentron canadum (Linnaeus, 1766) off the Dungun coast, Malaysia. J Appl Ichthyol 34:638–645

    Google Scholar 

  • Baggerman B (1980) Photoperiodic and endogenous control of the annual reproductive cycle in teleost fishes. In: Ali MA (ed) Environmental physiology of fishes. Springer, pp 533–567

    Google Scholar 

  • Bayarri MJ, Rodrıguez L, Zanuy S, Madrid JA, Sanchez-Vazquez FJ, Kagawa H, Okuzawa K, Carrillo M (2004) Effect of photoperiod manipulation on the daily rhythms of melatonin and reproductive hormones in caged European sea bass (Dicentrarchus labrax). Gen Comp Endocrinol 136:72–81

    CAS  PubMed  Google Scholar 

  • Bhattacharya S, Chattoraj A, Maitra SK (2007) Melatonin in the regulation of annual testicular events in carp Catla catla: evidence from the studies on the effects of exogenous melatonin, continuous light, and continuous darkness. Chronobiol Int 24:629–650

    CAS  PubMed  Google Scholar 

  • Billard R, Fostier A, Weil C, Breton B (1982) Endocrine control of spermatogenesis in teleost fish. Can J Fish Aquat Sci 39:65–79

    CAS  Google Scholar 

  • Borg B, Schmitz M, Hellqvist A, Bornestaf C, Mayer I (2004) Mechanisms in the photoperiodic control of reproduction in the stickleback. Behaviour 141:1521

    Google Scholar 

  • Brummett RE (1995) Environmental regulation of sexual maturation and reproduction in tilapia. Rev Fish Sci 3:231–248

    Google Scholar 

  • Burgerhout E, Lokman PM, van den Thillart GEEJM, Dirks RP (2019) The time-keeping hormone melatonin: a possible key cue for puberty in freshwater eels (Anguilla spp.). Rev Fish Biol Fish 29:1–21

    Google Scholar 

  • Campbell CM, Walsh JM, Idler DR (1976) Steroids in the plasma of the winter flounder (Pseudopleuronectes americanus walbaum). a seasonal study and investigation of steroid involvement in oocyte maturation. Gen Comp Endocrinol 29:14–20

    CAS  PubMed  Google Scholar 

  • Campbell CM, Fostier A, Jalabert B, Truscott B (1980) Identification and quantification of steroids in the serum of rainbow trout during spermiation and oocyte maturation. J Endocrinol 85:371

    CAS  PubMed  Google Scholar 

  • Cardinaletti G, Franzoni MF, Palermo F, Cottone E, Mosconi G, Guastalla A, Campantico E, Tibaldi E, Polzonetti-Magni A (2010) Environmental and neuroendocrine control of fish reproduction. Recent Adv Fish Reprod Biol Kerala: Res Signpost 3:65–87

    Google Scholar 

  • Carnevali O, Gioacchini G, Piccinetti CC, Maradonna F, Lombardo F, Giorgini E, Tosi G (2010) Melatonin control of oogenesis and metabolic resources in Zebrafish. J Appl Ichthyol 26:826–830

    CAS  Google Scholar 

  • Chakraborty U (2018) Effects of different phases of the lunar month on living organisms. Biol Rhythm Res 51(2):1–29

    Google Scholar 

  • Cochran RC, Zabludoff SD, Paynter KT, DiMichele L, Palmer RE (1988) Serum hormone levels associated with spawning activity in the mummichog, Fundulus heteroclitus. Gen Comp Endocrinol 70:345–354

    CAS  PubMed  Google Scholar 

  • Craig GR, Baksi WF (1977) The effects of depressed pH on flagfish reproduction, growth and survival. Water Res 11:621–626

    CAS  Google Scholar 

  • Cunha AAP, Partridge CG, Knapp R, Neff BD (2019) Androgen and prolactin manipulation induces changes in aggressive and nurturing behavior in a fish with male parental care. Horm Behav 116:104582

    CAS  PubMed  Google Scholar 

  • Dadras H, Dzyuba B, Cosson J, Golpour A, Siddique MAM, Linhart O (2017) Effect of water temperature on the physiology of fish spermatozoon function: a brief review. Aquacult Res 48:729–740

    Google Scholar 

  • Donelson JM, Munday PL, McCormick MI, Pankhurst NW, Pankhurst PM (2010) Effects of elevated water temperature and food availability on the reproductive performance of a coral reef fish. Mar Ecol Prog Ser 401:233–243

    Google Scholar 

  • Edwards TM, Miller HD, Guillette LJ (2006) Water quality influences reproduction in female mosquitofish (gambusia holbrooki) from eight florida springs. Environ Health Persp 114:69–75

    Google Scholar 

  • Emata AC, Meier AH, Hsiao S-M (1991) Daily variations in plasma hormone concentrations during the semilunar spawning cycle of the gulf killifish, Fundulus grandis. J Exp Zool 259:343–354

    CAS  Google Scholar 

  • Falcón J, Besseau L, Sauzet S, Boeuf G (2007) Melatonin effects on the hypothalamo–pituitary axis in fish. Trends Endocrinol Metab 18:81–88

    PubMed  Google Scholar 

  • Fiszbein A, Cánepa M, Vázquez GR, Maggese C, Pandolfi M (2010) Photoperiodic modulation of reproductive physiology and behaviour in the cichlid fish Cichlasoma dimerus. Physiol Behav 99:425–432

    CAS  PubMed  Google Scholar 

  • Foster SA (1987) Diel and lunar patterns of reproduction in the Caribbean and Pacific sergeant major damselfishes Abudefduf saxatilis and A. troschelii. Mar Biol 95:333–343

    Google Scholar 

  • Fraser GS, Bestgen KR, Winkelman DL, Thompson KG (2019) Temperature—not flow—predicts native fish reproduction with implications for climate change. Trans Am Fish Soc 148:509–527

    Google Scholar 

  • Frisch AJ, McCormick MI, Pankhurst NW (2007) Reproductive periodicity and steroid hormone profiles in the sex-changing coral-reef fish, Plectropomus leopardus. Coral Reefs 26:189–197

    Google Scholar 

  • Fukunaga K, Yamashina F, Ohta N, Mizuno H, Takeuchi Y, Yamauchi C, Takemura A (2019) Involvement of melatonin in transducing moon-related signals into the reproductive network of the female honeycomb grouper Epinephelus merra. Gen Comp Endocrinol 282:113211

    CAS  PubMed  Google Scholar 

  • Fukushiro M, Takeuchi T, Takeuchi Y, Hur S-P, Sugama N, Takemura A, Kubo Y, Okano K, Okano T (2011) Lunar phase-dependent expression of cryptochrome and a photoperiodic mechanism for lunar phase-recognition in a reef fish Goldlined Spinefoot. PLoS One 6:e28643

    CAS  PubMed  PubMed Central  Google Scholar 

  • Greeley MS, Calder DR, Taylor MH, Hols H, Wallace RA (1986) Oocyte maturation in the mummichog (Fundulus heteroclitus): Effects of steroids on germinal vesicle breakdown of intact follicles in vitro. Gen Comp Endocrinol 62:281–289

    CAS  PubMed  Google Scholar 

  • Greeley JRMS, MacGregor R III, Marion KR (1988) Variation in plasma oestrogens and androgens during the seasonal and semilunar spawning cycles of female gulf killifish, Fundulus grandis (Baird and Girard). J Fish Biol 33:419–429

    CAS  Google Scholar 

  • Hachero-Cruzado I, Forniés A, Herrera M, Mancera JM, Martínez-Rodríguez G (2013) Sperm production and quality in brill Scophthalmus rhombus L.: relation to circulating sex steroid levels. Fish Physiol Biochem 39:215–220

    CAS  PubMed  Google Scholar 

  • Harahap AP, Takemura A, Nakamura S, Rahman S, Takano K (2001) Histological evidence of lunar-synchronized ovarian development and spawning in the spiny rabbitfish Siganus spinus (Linnaeus) around the Ryukyus. Fish Sci 67:888–893

    CAS  Google Scholar 

  • Harahap AP, Takemura A, Rahman MS, Nakamura S, Takano K (2002) Lunar synchronization of sperm motility in the spiny rabbitfish Siganus spinus (Linnaeus). Fish Sci 68:706–708

    CAS  Google Scholar 

  • Hoque MM, Takemura A, Matsuyama M, Matsuura S, Takano K (1999) Lunar spawning in Siganus canaliculatus. J Fish Biol 55:1213–1222

    Google Scholar 

  • Hsiao S-M, Limesand SW, Wallace RA (1996) Semilunar follicular cycle of an intertidal fish: the fundulus model1. Biol Reprod 54:809–818

    CAS  PubMed  Google Scholar 

  • Ijiri S, Shibata Y, Takezawa N, Kazeto Y, Takatsuka N, Kato E, Hagihara S, Ozaki Y, Adachi S, Yamauchi K, Nagahama Y (2016) 17β-HSD type 12-like is responsible for maturation-inducing hormone synthesis during oocyte maturation in masu salmon. Endocrinology 158:627–639

    Google Scholar 

  • Inbaraj RM, Haider S, Baqri SSR (2001) Dynamics of 17α,20β-dihydroxy-4-pregnen-3-one and 17α,20β,21-trihydroxy-4-pregnen-3-one in plasma and oocyte incubation media of catfish (Clarias batrachus) in response to. Curr Sci 80:455–458

    CAS  Google Scholar 

  • Iwamatsu T (1978) Studies on oocyte maturation of the medaka, Oryzias latipes; V. on the structure of steroids that induce maturation in vitro. J Exp Zool 204:401–408

    CAS  PubMed  Google Scholar 

  • Jackson MW, Nieland DL, Cowan JH Jr (2006) Diel spawning periodicity of red snapper Lutjanus campechanus in the northern Gulf of Mexico. J Fish Biol 68:695–706

    Google Scholar 

  • Jeng S-R, Yueh W-S, Lee Y-H, Yen H-F, Chang C-F (2012) 17,20β,21-Trihydroxy-4-pregnen-3-one biosynthesis and 20β-hydroxysteroid dehydrogenase expression during final oocyte maturation in the protandrous yellowfin porgy, Acanthopagrus latus. Gen Comp Endocrinol 176:192–200

    CAS  PubMed  Google Scholar 

  • Jiang J-Q, Kobayashi T, Ge W, Kobayashi H, Tanaka M, Okamoto M, Nonaka Y, Nagahama Y (1996) Fish testicular 11β-hydroxylase : cDNA cloning and mRNA expression during spermatogenesis. FEBS Lett 397:250–252

    CAS  PubMed  Google Scholar 

  • Jiang J, Wang D, Senthilkumaran B, Kobayashi T, Kobayashi H, Yamaguchi A, Ge W, Young G, Nagahama Y (2003) Isolation, characterization and expression of 11beta-hydroxysteroid dehydrogenase type 2 cDNAs from the testes of Japanese eel (Anguilla japonica) and Nile tilapia (Oreochromis niloticus). J Mol Endocrinol 31:305–315

    CAS  PubMed  Google Scholar 

  • Jumawan-Nanual B, Metillo EB (2008) Population structure and reproductive biology of Siganus fuscescens Houttuyn 1782 (Perciformes, Siganidae) in Pujada Bay, Southeastern Mindanao, Philippines. Philippine Scientist 45:62–79

    Google Scholar 

  • Kashiwagi T, Park YJ, Park JG, Imamura S, Takeuchi Y, Hur SP, Takemura A (2013) Moonlight affects mRNA abundance of arylalkylamine N-acetyltransferase in the retina of a lunar-synchronized spawner, the Goldlined Spinefoot. J Exp Zool A Ecol Genet Physiol 319:505–516

    CAS  PubMed  Google Scholar 

  • Kazeto Y, Adachi S, Yamauchi K (2001) 20β-Hydroxysteroid dehydrogenase of the Japanese eel ovary: its cellular localization and changes in the enzymatic activity during sexual maturation. Gen Comp Endocrinol 122:109–115

    CAS  PubMed  Google Scholar 

  • Kazeto Y, Tosaka R, Matsubara H, Ijiri S, Adachi S (2011) Ovarian steroidogenesis and the role of sex steroid hormones on ovarian growth and maturation of the Japanese eel. J Steroid Biochem Mol Biol 127:149–154

    CAS  PubMed  Google Scholar 

  • Kerr Lobel L, Drown DM, Barber PH, Lobel PS (2019) A genetic assessment of parentage in the blackspot sergeant damselfish, abudefduf sordidus (Pisces: Pomacentridae). Fishes 4:53–67

    Google Scholar 

  • Kerr Lobel L, Lobel PS (2013) Junkyard damselfishes: Spawning behavior and nest site selection. In: Proceedings of the 2013 AAUS/ESDP curaçao joint international scientific diving symposium (pp 167–178)

  • King W, Thomas P, Harrell RM, Hodson RG, Sullivan CV (1994) Plasma levels of gonadal steroids during final oocyte maturation of striped bass, morone saxatilis L. Gen Comp Endocrinol 95:178–191

    CAS  PubMed  Google Scholar 

  • King W, Berlinsky DL, Sullivan CV (1995) Involvement of gonadal steroids in final oocyte maturation of white perch (Morone americana) and white bass (M. chrysops): in vivo and in vitro studies. Fish Physiol Biochem 14:489–500

    CAS  PubMed  Google Scholar 

  • Knapp R, Wingfield JC, Bass AH (1999) Steroid hormones and paternal care in the plainfin midshipman fish (Porichthys notatus). Horm Behav 35:81–89

    CAS  PubMed  Google Scholar 

  • Kusakabe M, Nakamura I, Young G (2003) 11β-Hydroxysteroid dehydrogenase complementary deoxyribonucleic acid in rainbow trout: cloning, sites of expression, and seasonal changes in gonads. Endocrinology 144:2534–2545

    CAS  PubMed  Google Scholar 

  • Lam TJ (1983) Environmental Influences on gonadal activity in fish. In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish Physiology. Academic Press, pp 65–116

    Google Scholar 

  • Leatherland JF, Ogasawara K, Rahman MS, Renaud R, Yamashiro H, Takemura A (2003) In vitro steroidogenesis of the gonads of the protogynous Pacific wrasse Haliochoeres trimaculatus. J Fish Biol 62(1414):1434

    Google Scholar 

  • Lee ST, Lam TJ, Tan CH (2002) Increased 21-hydroxylase and shutdown of C17,20 lyase activities in testicular tissues of the grouper (Epinephelus coioides) during 17α-methyltestosterone-induced sex inversion. Gen Comp Endocrinol 126:298–309

    CAS  PubMed  Google Scholar 

  • Maitra SK, Hasan KN (2016) The role of melatonin as a hormone and an antioxidant in the control of fish reproduction. Front Endocrinol. https://doi.org/10.3389/fendo.2016.00038

    Article  Google Scholar 

  • Maruska KP, Peyton KA (2007) Interspecific spawning between a recent immigrant and an endemic damselfish (pisces: pomacentridae) in the Hawaiian Islands. Pac Sci 61(211–221):211

    Google Scholar 

  • Matsuyama M, Adachi S, Nagahama Y, Matsuura S (1988) Diurnal rhythm of oocyte development and plasma steroid hormone levels in the female red sea bream, Pagrus major, during the spawning season. Aquaculture 73:357–372

    CAS  Google Scholar 

  • Matsuyama M, Ohta K, Morita S, Hoque MM, Kagawa H, Kambegawa A (1998) Circulating levels and in vitro production of two maturation-inducing hormones in teleost: 17α,20β-dihydroxy-4-pregnen-3-one and 17α,20β,21-trihydroxy-4-pregnen-3-one, in a daily spawning wrasse, Pseudolabrus japonicus. Fish Physiol Biochem 19:1–11

    CAS  Google Scholar 

  • Meseguer C, Ramos J, Bayarri MJ, Oliveira C, Sánchez-Vázquez FJ (2008) Light Synchronization of the Daily Spawning Rhythms of Gilthead Sea bream (Sparus aurata L) Kept under Different Photoperiod and after Shifting the LD Cycle. Chronobiol Int 25:666–679

    PubMed  Google Scholar 

  • Miura S, Horiguchi R, Nakamura M (2008) Immunohistochemical evidence for 11β-hydroxylase (P45011β) and androgen production in the gonad during sex differentiation and in adults in the protandrous anemonefish Amphiprion clarkii. Zoolog Sci 25(212–219):218

    Google Scholar 

  • Mojazi Amiri B, Maebayashi M, Adachi S, Moberg G, Doroshov S, Yamauchi K (1999) In vitro steroidogenesis by testicular fragments and ovarian follicles in a hybrid sturgeon, Bester. Fish Physiol Biochem 21:1–14

    Google Scholar 

  • Mojazi Amiri B, Maebayashi M, Omoto N, Adachi S, Yamauchi K (2001) In Vitro oocyte maturation in a hybrid sturgeon, bester: changes in the germinal vesicle breakdown and 17, 20β- dihydroxy-4-pregnen-3-one production. J Agric Sci Technol 3:199–207

    Google Scholar 

  • Mugnier C, Gaignon J-L, Fostier A (1997) In Vitro synthesis of 17,20β,21-trihydroxy-4-pregnen-3-one by ovaries of turbot (Scophthalmus maximus L.) during oocyte maturation. Gen Comp Endocrinol 107:63–73

    CAS  PubMed  Google Scholar 

  • Nagahama Y (1994) Endocrine regulation of gametogenesis in fish. Int J Dev Biol 38:217–229

    CAS  PubMed  Google Scholar 

  • Nagahama Y (1997) 17α,20β-Dihydroxy-4-pregnen-3-one, a maturation-inducing hormone in fish oocytes: mechanisms of synthesis and action. Steroids 62:190–196

    CAS  PubMed  Google Scholar 

  • Nagahama Y, Yoshikuni M, Yamashita M, Tokumoto T, Katsu Y (1995) Regulation of oocyte growth and maturation in Fish. In: Pedersen RA, Schatten GP (eds) Current Topics in Developmental Biology. Academic Press, pp 103–145

    Google Scholar 

  • Ndobe S, Herawati EY, Setyohadi D, Moore A, Palomares ML, Pauly D (2013) Life history of Banggai cardinalfish, Pterapogon kauderni (Actinopterygii: Perciformes: Apogonidae), from Banggai Islands and Palu Bay, Sulawesi Indonesia. Acta Ichthyol Piscat 43:237

    Google Scholar 

  • Noori A, Mojazi Amiri B, Mirvaghefi A, Rafiee G, Kalvani Neitali B (2015) Enhanced growth and retarded gonadal development of farmed rainbow trout, Oncorhynchus mykiss (Walbaum) following a long-day photoperiod. Aquacult Res 46:2398–2406

    Google Scholar 

  • Oliveira C, Dinis MT, Soares F, Cabrita E, Pousão-Ferreira P, Sánchez-Vázquez FJ (2009) Lunar and daily spawning rhythms of Senegal sole Solea senegalensis. J Fish Biol 75:61–74

    CAS  PubMed  Google Scholar 

  • Oliveira C, Duncan NJ, Pousão-Ferreira P, Mañanós E, Sánchez-Vázquez FJ (2010) Influence of the lunar cycle on plasma melatonin, vitellogenin and sex steroids rhythms in Senegal sole, Solea senegalensis. Aquaculture 306:343–347

    CAS  Google Scholar 

  • Pankhurst NW (1990) Changes in plasma levels of gonadal steroids during spawning behaviour in territorial male demoiselles Chromis dispilus (Pisces: Pomacentridae) sampled underwater. Gen Comp Endocrinol 79:215–225

    CAS  PubMed  Google Scholar 

  • Pankhurst NW, Munday PL (2011) Effects of climate change on fish reproduction and early life history stages. Mar Freshwater Res 62:1015–1026

    CAS  Google Scholar 

  • Park YJ, Takemura A, Lee YD (2006a) Annual and lunar-synchronized ovarian activity in two rabbitfish species in the Chuuk lagoon, Micronesia. Fish Sci 72:166–172

    CAS  Google Scholar 

  • Park YJ, Takemura A, Lee YD (2006b) Lunar-synchronized reproductive activity in the pencil-streaked rabbitfish Siganus doliatus in the Chuuk Lagoon, Micronesia. Ichthyol Res 53:179–181

    Google Scholar 

  • Petrino TR, Lin YWP, Netherton JC, Powell DH, Wallace RA (1993) Steroidogenesis in Fundulus heteroclitus V.: purification, characterization, and metabolism of 17α,20β-dihydroxy-4-pregnen-3-one by intact follicles and its role in oocyte maturation. Gen Comp Endocrinol 92:1–15

    CAS  PubMed  Google Scholar 

  • Pisingan RS, Takemura A (2007) Apparent semi-lunar spawning rhythmicity in a brackish cardinalfish. J Fish Biol 70:1512–1522

    Google Scholar 

  • Pisingan RS, Harnadi L, Takemura A (2006) Semilunar spawning periodicity in brackish damsel Pomacentrus taeniometopon. Fish Sci 72:1256–1260

    CAS  Google Scholar 

  • Rahman MS, Takemura A, Takano K (2000a) Correlation between plasma steroid hormones and vitellogenin profiles and lunar periodicity in the female golden rabbitfish, Siganus guttatus (Bloch). Comp Biochem Physiol b: Biochem Mol Biol 127:113–122

    CAS  Google Scholar 

  • Rahman MS, Takemura A, Takano K (2000b) Lunar synchronization of testicular development and plasma steroid hormone profiles in the golden rabbitfish. J Fish Biol 57:1065–1074

    CAS  Google Scholar 

  • Rahman MS, Takemura A, Takano K (2001) Lunar synchronization of testicular development and steroidogenesis in rabbitfish. Comp Biochem Physiol b: Biochem Mol Biol 129:367–373

    CAS  Google Scholar 

  • Rahman MS, Takemura A, Takano K (2002) Lunar synchronization of in vitro steroidogenesis in ovaries of the golden rabbitfish, Siganus guttatus (Bloch). Gen Comp Endocrinol 125:1–8

    CAS  PubMed  Google Scholar 

  • Rahman M, Takemura A, Park Y, Takano K (2003a) Lunar cycle in the reproductive activity in the forktail rabbitfish. Fish Physiol Biochem 28:443–444

    CAS  Google Scholar 

  • Rahman MS, Morita M, Takemura A, Takano K (2003b) Hormonal changes in relation to lunar periodicity in the testis of the forktail rabbitfish, Siganus argenteus. Gen Comp Endocrinol 131:302–309

    PubMed  Google Scholar 

  • Rahman MS, Takemura A, Nakamura S, Takano K (2003c) Rhythmic changes in testicular activity with lunar cycle in the forktail rabbitfish. J Fish Biol 62:495–499

    Google Scholar 

  • Sangalang GB, Freeman HC (1988) In vitro biosynthesis of 17α,20β-dihydroxy-4-pregnen-3-one by the ovaries, testes, and head kidneys of the Atlantic salmon Salmo salar. Gen Comp Endocrinol 69:406–415

    CAS  PubMed  Google Scholar 

  • Sarkar UK, Naskar M, Roy K, Sudheesan D, Gupta S, Bose AK, Srivastava PK, Nandy SK, Verma VK, Sarkar SD, Karnatak G (2018) Baseline information of reproduction parameters of an amphidromous croaker Johnius coitor (Hamilton, 1822) from Ganga river basin, India with special reference to potential influence of climatic variability. Aquat Living Resour 31:4

    Google Scholar 

  • Schulz RW, De França LR, Lareyre J-J, LeGac F, Chiarini-Garcia H, Nobrega RH, Miura T (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165:390–411

    CAS  PubMed  Google Scholar 

  • Scott AP, Canario AVM, Prat F (1990) Radioimmunoassay of ovarian steroids in plasmas of ovulating female sea bass (Dicentrarchus labrax). Gen Comp Endocrinol 78:299–302

    CAS  PubMed  Google Scholar 

  • Senthilkumaran B, Yoshikuni M, Nagahama Y (2004) A shift in steroidogenesis occurring in ovarian follicles prior to oocyte maturation. Mol Cell Endocrinol 215:11–18

    CAS  PubMed  Google Scholar 

  • Shimizu A (1997) Reproductive cycles in a reared strain of the mummichog, a daily spawner. J Fish Biol 51:724–737

    CAS  Google Scholar 

  • Sisneros JA, Forlano PM, Knapp R, Bass AH (2004) Seasonal variation of steroid hormone levels in an intertidal-nesting fish, the vocal plainfin midshipman. Gen Comp Endocrinol 136:101–116

    CAS  PubMed  Google Scholar 

  • Soltanzadeh Z, Noori A, Sajjadi M (2013) A study of changes in plasma testosterone in Abudefduf vaigiensis at the northern coast of Qeshm Island, Persian Gulf. (Abstract in English). J Aquat Ecol 3:1–7

    Google Scholar 

  • Sumpter JP (1997) Environmental control of fish reproduction: a different perspective. Fish Physiol Biochem 17:25–31

    CAS  Google Scholar 

  • Suzuki K, Asahina K, Tamaru CS, Lee C-S, Inano H (1991) Biosynthesis of 17α,20β-dihydroxy-4-pregnen-3-one in the ovaries of grey mullet (Mugil cephalus) during induced ovulation by carp pituitary homogenates and an LHRH analogue. Gen Comp Endocrinol 84:215–221

    CAS  PubMed  Google Scholar 

  • Takemura A, Rahman MS, Nakamura S, Park YJ, Takano K (2004) Lunar cycles and reproductive activity in reef fishes with particular attention to rabbitfishes. Fish Fish 5:317–328

    Google Scholar 

  • Takeuchi Y, Kabutomori R, Yamauchi C, Miyagi H, Takemura A, Okano K, Okano T (2018) Moonlight controls lunar-phase-dependency and regular oscillation of clock gene expressions in a lunar-synchronized spawner fish, Goldlined spinefoot. Sci Rep 8:1–12

    Google Scholar 

  • Teruya K, Masuma S, Hondo Y, Hamasaki K (2008) Spawning season, lunar-related spawning and mating systems in the camouflage grouper Epinephelus polyphekadion at Ishigaki Island, Japan. Aquac Sci 56:359–368

    Google Scholar 

  • Thomas P, Trant JM (1989) Evidence that 17α,20β,21-trihydroxy-4-pregnen-3-one is a maturation-inducing steroid in spotted seatrout. Fish Physiol Biochem 7:185

    CAS  PubMed  Google Scholar 

  • Todo T, Ikeuchi T, Kobayashi T, Kajiura-Kobayashi H, Suzuki K, Yoshikuni M, Yamauchi K, Nagahama Y (2000) Characterization of a testicular 17α,20β-dihydroxy-4-pregnen-3-one (a spermiation-inducing steroid in fish) receptor from a teleost, Japanese eel (Anguilla japonica) 1. FEBS Lett 465:12–17

    CAS  PubMed  Google Scholar 

  • Trant JM, Thomas P (1989) Isolation of a novel maturation-inducing steroid produced in vitro by ovaries of Atlantic croaker. Gen Comp Endocrinol 75:397–404

    CAS  PubMed  Google Scholar 

  • Van Der Kraak G, Pankhurst N (1997) Temperature effects on the reproductive performance of fish. In: Wood CM, McDonald DG (eds) Global warming: implications for freshwater and marine fish. Cambridge University Press, pp 159–176

    Google Scholar 

  • Wang Q, Hong W, Chen S, Zhang Q (2008) Variation with semilunar periodicity of plasma steroid hormone production in the mudskipper Boleophthalmus pectinirostris. Gen Comp Endocrinol 155:821–826

    CAS  PubMed  Google Scholar 

  • Wang N, Teletchea F, Kestemont P, Milla S, Fontaine P (2010) Photothermal control of the reproductive cycle in temperate fishes. Rev Aquacult 2:209–222

    Google Scholar 

  • Wu RSS (2009) Effects of hypoxia on fish reproduction and development. In: Richards JG, Farrell AP, Brauner CJ (eds) Fish Physiology. Academic Press, pp 79–141

    Google Scholar 

  • Young G, Kusakabe M, Nakamura I, Lokman PM, Goetz FW (2005) Gonadal steroidogenesis in teleost fish. In: Melamed P, Sherwood N (eds) Hormones and their receptors in fish reproduction. World Scientific Publishing Co, pp 155–223

    Google Scholar 

  • Zhang L-L, Liu M, Fang L-P, Xu Q, Lin J-J (2019) Reproductive biology of Johnius taiwanensis (Perciformes: Sciaenidae) in Fujian Waters, Southern China. Zool Stud 58:e38–e38

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to the editor and anonymous reviewers for their insightful comments, which greatly improved the manuscript. The authors are thankful to the University of Hormozgan for providing us with laboratory facilities. We are grateful to Alireza Razi for his assistance in the field. This work was performed according to the Iranian Society for the Animal Welfare.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ahmad Noori.

Ethics declarations

Conflicts of interest

The authors claim that there is no conflict of interest in this manuscript.

Data availability statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topic Editor Morgan S. Pratchett

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Golmoradizadeh, A., Noori, A. & Amiri, B.M. Physiological effects of the lunar cycle on the spawning of a coral reef fish, Abudefduf Vaigiensis: in vivo and in vitro trait. Coral Reefs 40, 1757–1767 (2021). https://doi.org/10.1007/s00338-021-02183-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-021-02183-x

Keywords

Navigation