180
Views
0
CrossRef citations to date
0
Altmetric
Articles

Induction of spawning under artificial moonlight in the honeycomb grouper Epinephelus merra, a lunar-synchronized spawner

ORCID Icon, , &
Pages 1880-1893 | Received 25 Nov 2021, Accepted 21 Feb 2022, Published online: 28 Feb 2022

References

  • Aguilar-Perera A, Aguilar-Dávila W. 1996. A spawning aggregation of Nassau grouper Epinephelus striatus (Pisces: Serranidae) in the Mexican Caribbean. Environ Biol Fishes. 45(4):351–361. doi:10.1007/BF00002527.
  • Alvarado MV, Carrillo M, Felip A. 2015. Melatonin-induced changes in kiss/gnrh gene expression patterns in the brain of male sea bass during spermatogenesis. Comp Biochem Physiol Part A Mol Integr Physiol. 185:69–79. doi:10.1016/J.CBPA.2015.03.010.
  • Amagai T, Murata R, Soyano K. 2020. Spawning characteristics of a lunar-synchronized spawner, the honeycomb grouper Epinephelus merra, under artificial conditions. Aquac Sci. 68(3):235–242. doi:10.11233/aquaculturesci.68.235.
  • Andreatta G, Tessmar-Raible K. 2020. The still dark side of the moon: molecular mechanisms of lunar-controlled rhythms and clocks. J Mol Biol. 432(12):3525–3546. doi:10.1016/j.jmb.2020.03.009.
  • Ayodya FP, Wijayanti DP, Sabdono A. 2021. Lunar cycle and reproductive activity of Redbelly yellowtail fusilier, Caesio cuning in Karimunjawa National Park, Indonesia. Biodiversitas J Biol Divers. 22(7):3075–3082. doi:10.13057/biodiv/d220762.
  • Badruzzaman M, Ikegami T, Amin AKMR, Shahjahan M. 2020. Melatonin inhibits reproductive activity through changes of serotonergic activity in the brain of freshwater catfish (Mystus cavasius). Aquaculture. 526:735378. doi:10.1016/j.aquaculture.2020.735378.
  • Berlinsky DL, Kenter LW, Reading BJ, Goetz FW. 2020. Regulating reproductive cycles for captive spawning. Fish Physiol. 38:1–52. doi:10.1016/bs.fp.2020.09.001.
  • Chai K, Liu X, Zhang Y, Lin H. 2013. Day-night and reproductive cycle profiles of melatonin receptor, kiss, and gnrh expression in Orange-spotted grouper (Epinephelus coioides). Mol Reprod Dev. 80(7):535–548. doi:10.1002/mrd.22191.
  • Choi JY, Kim NN, Lee D-W, Choi Y-U, Choi CY. 2017. The reproductive cycle of the humbug damselfish Dascyllus aruanus according to the changes in lunar phase in Micronesia. Ocean Sci J. 52(3):439–446. doi:10.1007/s12601-017-0036-1.
  • Ciani E, Fontaine R, Maugars G, Mizrahi N, Mayer I, Levavi-Sivan B, Weltzien FA. 2019. Melatonin receptors in Atlantic salmon stimulate cAMP levels in heterologous cell lines and show season-dependent daily variations in pituitary expression levels. J Pineal Res. 67(3):e12590. doi:10.1111/jpi.12590.
  • Colin PL. 1992. Reproduction of the Nassau grouper, Epinephelus striatus (Pisces: serranidae) and its relationship to environmental conditions. Environ Biol Fishes. 34(4):357–377. doi:10.1007/BF00004740.
  • Domeier ML, Colin PL. 1997. Tropical reef fish spawning aggregations: defined and reviewed. Bull Mar Sci. 60(3):698–726. doi:10.1016/j.porgcoat.2012.10.013.
  • Falcón J, Besseau L, Sauzet S, Boeuf G. 2007. Melatonin effects on the hypothalamo–pituitary axis in fish. Trends Endocrinol Metab. 18(2):81–88. doi:10.1016/J.TEM.2007.01.002.
  • Falcón J, Migaud H, Muñoz-Cueto JA, Carrillo M. 2010. Current knowledge on the melatonin system in teleost fish. Gen Comp Endocrinol. 165(3):469–482. doi:10.1016/j.ygcen.2009.04.026.
  • 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. doi:10.1016/j.ygcen.2019.113211.
  • Fukunaga K, Yamashina F, Takeuchi Y, Yamauchi C, Takemura A. 2020. Moonlight is a key entrainer of lunar clock in the brain of the tropical grouper with full moon preference. BMC Zool. 5(1):11. doi:10.1186/s40850-020-00060-8.
  • García-Allegue R, Madrid JA, Sánchez-Vázquez F. 2001. Melatonin rhythms in European sea bass plasma and eye: influence of seasonal photoperiod and water temperature. J Pineal Res. 31(1):68–75. doi:10.1034/J.1600-079X.2001.310110.X.
  • Golmoradizadeh A, Noori A, Amiri BM. 2021. 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(6):1757–1767. doi:10.1007/s00338-021-02183-x.
  • Hereu B, Diaz D, Pasqual J, Zabala M, Sala E. 2006. Temporal patterns of spawning of the dusky grouper Epinephelus marginatus in relation to environmental factors. Mar Ecol Prog Ser. 325:187–194. doi:10.3354/meps325187.
  • Hong LY, Hong WS, Zhu WB, Shi Q, You XX, Chen SX. 2014. Cloning and expression of melatonin receptors in the mudskipper Boleophthalmus pectinirostris: their role in synchronizing its semilunar spawning rhythm. Gen Comp Endocrinol. 195:138–150. doi:10.1016/j.ygcen.2013.11.004.
  • Hoque MM, Takemura A, Matsuyama M, Matsuura S, Takano K. 1999. Lunar spawning in Siganus canaliculatus. J Fish Biol. 55(6):1213–1222. doi:10.1111/j.1095-8649.1999.tb02071.x.
  • Hoque MM, Takemura A, Takano K. 1998. Annual changes in oocyte development and serum vitellogenin level in the rabbitfish Siganus canaliculatus (Park) in Okinawa, southern Japan. Fish Sci. 64(1):44–51. doi:10.2331/fishsci.64.44.
  • Hughes AT, Hamilton RJ, Choat JH, Rhodes KL. 2020. Declining grouper spawning aggregations in Western Province, Solomon Islands, signal the need for a modified management approach. PLoS One. 15(3):e0230485. doi:10.1371/JOURNAL.PONE.0230485.
  • Hur S-P, Mahardini A, Takeuchi Y, Imamura S, Wambiji N, Rizky D, Udagawa S, Kim S-J, Takemura A. 2020. Expression profiles of types 2 and 3 iodothyronine deiodinase genes in relation to vitellogenesis in a tropical damselfish, Chrysiptera cyanea. Gen Comp Endocrinol. 285:113264. doi:10.1016/j.ygcen.2019.113264.
  • Hyeon J-Y, Byun J-H, Kim E-S, Heo Y-S, Fukunaga K, Kim S-K, Imamura S, Kim S-J, Takemura A, Hur S-P. 2021. Testis development in the Japanese eel is affected by photic signals through melatonin secretion. PeerJ. 9:e12289. doi:10.7717/peerj.12289.
  • Ikegami T, Takeuchi Y, Hur S-P, Takemura A. 2014. Impacts of moonlight on fish reproduction. Mar Genomics. 14:59–66. doi:10.1016/j.margen.2013.11.007.
  • Imamura S, Hur S-P, Takeuchi Y, Badruzzaman M, Mahardini A, Rizky D, Takemura A. 2021. Effect of short- and long-term melatonin treatments on the reproductive activity of the tropical damselfish Chrysiptera cyanea. Res Sq. doi:10.21203/RS.3.RS-895393/V1.
  • Ito-Takeuchi H, Takahashi K, Bouchekioua S, Yamauchi C, Takeuchi Y, Hur S-P, Lee Y-D, Takemura A. 2017. Importance of sandy bottoms in coral reefs to the oscillation of daily rhythms in the tropical wrasse Halichoeres trimaculatus. Chronobiol Int. 34(8):1014–1025. doi:10.1080/07420528.2017.1335747.
  • Johannes RE. 1978. Reproductive strategies of coastal marine fishes in the tropics. Environ Biol Fishes. 3(1):65–84. doi:10.1007/BF00006309.
  • Kaiser TS, Neumann D, Heckel DG. 2011. Timing the tides: genetic control of diurnal and lunar emergence times is correlated in the marine midge Clunio marinus. BMC Genet. 12(1):49. doi:10.1186/1471-2156-12-49.
  • Kline RJ, Khan IA, Holt GJ, Osorio D. 2011. Behavior, color change and time for sexual inversion in the protogynous grouper (Epinephelus adscensionis). PLoS One. 6(5):e19576. doi:10.1371/journal.pone.0019576.
  • Lee YD, Park SH, Takemura A, Takano K. 2002. Histological observations of seasonal reproductive and lunar-related spawning cycles in the female honeycomb grouper Epinephelus merra in Okinawan waters. Fish Sci. 68(4):872–877. doi:10.1046/j.1444-2906.2002.00505.x.
  • Lin C-H, Takahashi S, Mulla AJ, Nozawa Y. 2021. Moonrise timing is key for synchronized spawning in coral Dipsastraea speciosa. Proc Natl Acad Sci. 118(34):e2101985118. doi:10.1073/pnas.2101985118.
  • Maugars G, Nourizadeh-Lillabadi R, Weltzien F-A. 2020. New insights into the evolutionary history of melatonin receptors in vertebrates, with particular focus on teleosts. Front Endocrinol. 11:538196. doi:10.3389/fendo.2020.538196.
  • Murata R, Amagai T, Izumida D, Mushirobira Y, Nozu R, Soyano K. 2021. Lunar-related maturation and spawning migration in the honeycomb grouper, Epinephelus merra. Galaxea, J Coral Reef Stud. G2021_S4R. 10.3755/GALAXEA.G2021_S4R.
  • Murata R, Kobayashi Y, Karimata H, Kishimoto K, Kimura M, Shimizu A, and Nakamura M. 2012. The role of pituitary gonadotropins in gonadal sex differentiation in the protogynous Malabar grouper, Epinephelus malabaricus. General and comparative endocrinology. 178(3):587–92. https://doi.org/10.1016/j.ygcen.2012.07.012
  • Nanami A, Sato T, Kawabata Y, Okuyama J. 2017. Spawning aggregation of white-streaked grouper Epinephelus ongus: spatial distribution and annual variation in the fish density within a spawning ground. PeerJ. 2017(2):e3000. doi:10.7717/peerj.3000.
  • Nelson ER, Habibi HR. 2016. Thyroid hormone regulates vitellogenin by inducing estrogen receptor alpha in the goldfish liver. Mol Cell Endocrinol. 436:259–267. doi:10.1016/j.mce.2016.08.045.
  • Okumura S, Okamoto K, Oomori R, Nakazono A. 2002. Spawning behavior and artificial fertilization in captive reared red spotted grouper, Epinephelus akaara. Aquaculture. 206(3–4):165–173. doi:10.1016/S0044-8486(01)00722-0.
  • Park YJ, Takemura A, Lee YD. 2006. Annual and lunar-synchronized ovarian activity in two rabbitfish species in the Chuuk lagoon, Micronesia. Fish Sci. 72(1):166–172. doi:10.1111/j.1444-2906.2006.01131.x.
  • Rahman MS, Kim B-H, Takemura A, Park C-B, Lee Y-D. 2004. Effects of moonlight exposure on plasma melatonin rhythms in the seagrass rabbitfish, Siganus canaliculatus. J Biol Rhythms. 19(4):325–334. doi:10.1177/0748730404266712.
  • Rahman MS, Takemura A, Takano K. 2000. Correlation between plasma steroid hormones and vitellogenin profiles and lunar periodicity in the female golden rabbitfish, Siganus guttatus (Bloch). Comp Biochem Physiol Part B Biochem Mol Biol. 127(1):113–122. doi:10.1016/S0305-0491(00)00240-6.
  • Robinson J, Aumeeruddy R, Jörgensen TL, Öhman MC. 2008. Dynamics of camouflage (Epinephelus polyphekadion) and brown marbled grouper (Epinephelus fuscoguttatus) spawning aggregations at a remote reef site, Seychelles. Bull Mar Sci. 83(2):415–431.
  • Sánchez-Vázquez FJ, Iigo M, Madrid JA, Zamora S, Tabata M. 1997. Daily cycles in plasma and ocular melatonin in demand-fed sea bass, Dicentrarchus labrax L. J Comp Physiol B Biochem Syst Environ Physiol. 167(6):409–415. doi:10.1007/s003600050090.
  • Sánchez-Vázquez FJ, López-Olmeda JF, Vera LM, Migaud H, López-Patiño MA, Míguez JM. 2019. Environmental cycles, melatonin, and circadian control of stress response in fish. Front Endocrinol. 10:279. doi:10.3389/fendo.2019.00279.
  • Sébert M-E, Legros C, Weltzien F-A, Malpaux B, Chemineau P, Dufour S. 2008. Melatonin activates brain dopaminergic systems in the eel with an inhibitory impact on reproductive function. J Neuroendocrinol. 20(7):917–929. doi:10.1111/j.1365-2826.2008.01744.x.
  • Soyano K, Masumoto T, Tanaka H, Takushima M, Nakamura M. 2003. Lunar-related spawning in honeycomb grouper, Epinephelus merra. Fish Physiol Biochem. 28(1–4):447–448. doi:10.1023/B:FISH.0000030625.40402.18.
  • Sugama N, Park J-G, Park Y-J, Takeuchi Y, Kim S-J, Takemura A. 2008. Moonlight affects nocturnal Period2 transcript levels in the pineal gland of the reef fish Siganus guttatus. J Pineal Res. 45(2):133–141. doi:10.1111/j.1600-079X.2008.00566.x.
  • Takemura A, Susilo ES, Rahman MS, Morita M. 2004. Perception and possible utilization of moonlight intensity for reproductive activities in a lunar-synchronized spawner, the golden rabbitfish. J Exp Zool. 301(10):844–851. doi:10.1002/jez.a.105.
  • Takemura A, Ueda S, Hiyakawa N, Nikaido Y. 2006. A direct influence of moonlight intensity on changes in melatonin production by cultured pineal glands of the golden rabbitfish, Siganus guttatus. J Pineal Res. 40(3):236–241. doi:10.1111/j.1600-079X.2005.00306.x.
  • 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):1–12. doi:10.1038/s41598-018-24538-1.
  • Toda R, Okano K, Takeuchi Y, Yamauchi C, Fukushiro M, Takemura A, Okano T, Mintz EM. 2014. Hypothalamic expression and moonlight-independent changes of Cry3 and Per4 implicate their roles in lunar clock oscillators of the lunar-responsive goldlined spinefoot. PLoS One. 9(10):e109119. doi:10.1371/journal.pone.0109119.
  • Whaylen L, Pattengill-Semmens CV, Semmens BX, Bush PG, Boardman MR. 2004. Observations of a Nassau grouper, Epinephelus striatus, spawning aggregation site in Little Cayman, Cayman Islands, including multi-species spawning information. Environ Biol Fishes. 70(3):305–313. doi:10.1023/B:EBFI.0000033341.57920.a8.
  • Yasuo S, Yoshimura T, Ebihara S, Korf HW. 2007. Temporal dynamics of type 2 deiodinase expression after melatonin injections in Syrian hamsters. Endocrinology. 148(9):4385–4392. doi:10.1210/en.2007-0497.
  • Zeller D. 1998. Spawning aggregations:patterns of movement of the coral trout Plectropomus leopardus (Serranidae) as determined by ultrasonic telemetry. Mar Ecol Prog Ser. 162:253–263. doi:10.3354/meps162253.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.