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

ABSTRACT In the reproductive season, lunar-synchronized fish spawn during species-specific moon phases. It remains unknown how they perceive cues from the moon for initiating gonadal development and subsequent spawning. We hypothesized that fish use moonlight to synchronize reproductive events. Using the honeycomb grouper Epinephelus merra, a tropical Serranidae, spawns around the time of the full moon, we report the successful induction of spawning in this species by controlling light condition at night. Following 3 months of acclimatization under long days (14:10) at 28 ± 1.0°C, mature fish were reared under an artificial full (experimental group) or new (controls) moon during scotophase. Rearing fish under these conditions for 1 month resulted in successful spawning in the experimental group between 21h00 and 01h30. Similar results were obtained when control fish were subdivided into artificial full and new moon groups and reared for an additional month. Fish in the experimental group had a high gonadosomatic index and abundant yolk-laden oocytes in the ovary. Therefore, moonlight triggers gonadal development and subsequent spawning in lunar-synchronized fish with a full-moon preference.

[1]  Y. Takeuchi,et al.  Effect of short- and long-term melatonin treatments on the reproductive activity of the tropical damselfish Chrysiptera cyanea , 2021, Fish physiology and biochemistry.

[2]  Sung-Pyo Hur,et al.  Testis development in the Japanese eel is affected by photic signals through melatonin secretion , 2021, PeerJ.

[3]  A. Noori,et al.  Physiological effects of the lunar cycle on the spawning of a coral reef fish, Abudefduf Vaigiensis: in vivo and in vitro trait , 2021, Coral Reefs.

[4]  Y. Nozawa,et al.  Moonrise timing is key for synchronized spawning in coral Dipsastraea speciosa , 2021, Proceedings of the National Academy of Sciences.

[5]  A. Sabdono,et al.  Lunar cycle and reproductive activity of Redbelly yellowtail fusilier, Caesio cuning in Karimunjawa National Park, Indonesia , 2021, Biodiversitas Journal of Biological Diversity.

[6]  Yuji Mushirobira,et al.  Lunar-related maturation and spawning migration in the honeycomb grouper, Epinephelus merra , 2021, Galaxea, Journal of Coral Reef Studies.

[7]  F. Weltzien,et al.  New Insights Into the Evolutionary History of Melatonin Receptors in Vertebrates, With Particular Focus on Teleosts , 2020, Frontiers in Endocrinology.

[8]  M. Shahjahan,et al.  Melatonin inhibits reproductive activity through changes of serotonergic activity in the brain of freshwater catfish (Mystus cavasius) , 2020 .

[9]  C. Yamauchi,et al.  Moonlight is a key entrainer of lunar clock in the brain of the tropical grouper with full moon preference , 2020 .

[10]  R. J. Hamilton,et al.  Declining grouper spawning aggregations in Western Province, Solomon Islands, signal the need for a modified management approach , 2020, PloS one.

[11]  G. Andreatta,et al.  The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks , 2020, Journal of molecular biology.

[12]  F. Goetz,et al.  Regulating reproductive cycles for captive spawning , 2020 .

[13]  F. Weltzien,et al.  Melatonin receptors in Atlantic salmon stimulate cAMP levels in heterologous cell lines and show season‐dependent daily variations in pituitary expression levels , 2019, Journal of pineal research.

[14]  C. Yamauchi,et al.  Involvement of melatonin in transducing moon-related signals into the reproductive network of the female honeycomb grouper Epinephelus merra. , 2019, General and comparative endocrinology.

[15]  J. López-Olmeda,et al.  Environmental Cycles, Melatonin, and Circadian Control of Stress Response in Fish , 2019, Front. Endocrinol..

[16]  Y. Takeuchi,et al.  Expression profiles of types 2 and 3 iodothyronine deiodinase genes in relation to vitellogenesis in a tropical damselfish, Chrysiptera cyanea. , 2019, General and comparative endocrinology.

[17]  C. Yamauchi,et al.  Moonlight controls lunar-phase-dependency and regular oscillation of clock gene expressions in a lunar-synchronized spawner fish, Goldlined spinefoot , 2018, Scientific Reports.

[18]  Ji Yong Choi,et al.  The reproductive cycle of the humbug damselfish Dascyllus aruanus according to the changes in lunar phase in Micronesia , 2017, Ocean Science Journal.

[19]  Hitomi Ito-Takeuchi,et al.  Importance of sandy bottoms in coral reefs to the oscillation of daily rhythms in the tropical wrasse Halichoeres trimaculatus , 2017, Chronobiology international.

[20]  Taku Sato,et al.  Spawning aggregation of white-streaked grouper Epinephelus ongus: spatial distribution and annual variation in the fish density within a spawning ground , 2017, PeerJ.

[21]  E. Nelson,et al.  Thyroid hormone regulates vitellogenin by inducing estrogen receptor alpha in the goldfish liver , 2016, Molecular and Cellular Endocrinology.

[22]  M. Carrillo,et al.  Melatonin-induced changes in kiss/gnrh gene expression patterns in the brain of male sea bass during spermatogenesis. , 2015, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[23]  C. Yamauchi,et al.  Hypothalamic Expression and Moonlight-Independent Changes of Cry3 and Per4 Implicate Their Roles in Lunar Clock Oscillators of the Lunar-Responsive Goldlined Spinefoot , 2014, PloS one.

[24]  Y. Takeuchi,et al.  Impacts of moonlight on fish reproduction. , 2014, Marine genomics.

[25]  Q. Shi,et al.  Cloning and expression of melatonin receptors in the mudskipper Boleophthalmus pectinirostris: their role in synchronizing its semilunar spawning rhythm. , 2014, General and comparative endocrinology.

[26]  Yong Zhang,et al.  Day‐night and reproductive cycle profiles of melatonin receptor, kiss, and gnrh expression in orange‐spotted grouper (Epinephelus coioides) , 2013, Molecular reproduction and development.

[27]  A. Shimizu,et al.  The role of pituitary gonadotropins in gonadal sex differentiation in the protogynous Malabar grouper, Epinephelus malabaricus. , 2012, General and comparative endocrinology.

[28]  I. Khan,et al.  Behavior, Color Change and Time for Sexual Inversion in the Protogynous Grouper (Epinephelus adscensionis) , 2011, PloS one.

[29]  D. Heckel,et al.  Timing the tides: Genetic control of diurnal and lunar emergence times is correlated in the marine midge Clunio marinus , 2011, BMC Genetics.

[30]  H. Migaud,et al.  Current knowledge on the melatonin system in teleost fish. , 2010, General and comparative endocrinology.

[31]  A. Takemura,et al.  Annual and lunar-synchronized ovarian activity in two rabbitfish species in the Chuuk lagoon, Micronesia , 2006, Fisheries Science.

[32]  Y. Takeuchi,et al.  Moonlight affects nocturnal Period2 transcript levels in the pineal gland of the reef fish Siganus guttatus , 2008, Journal of pineal research.

[33]  F. Weltzien,et al.  Melatonin Activates Brain Dopaminergic Systems in the Eel with an Inhibitory Impact on Reproductive Function , 2008, Journal of neuroendocrinology.

[34]  M. Öhman,et al.  Dynamics of Camouflage (Epinephelus Polyphekadion) and Brown Marbled Grouper (Epinephelus Fuscoguttatus) Spawning Aggregations at a Remote Reef Site, Seychelles , 2008 .

[35]  H. Korf,et al.  Temporal dynamics of type 2 deiodinase expression after melatonin injections in Syrian hamsters. , 2007, Endocrinology.

[36]  G. Boeuf,et al.  Melatonin effects on the hypothalamo–pituitary axis in fish , 2007, Trends in Endocrinology & Metabolism.

[37]  E. Sala,et al.  Temporal patterns of spawning of the dusky grouper Epinephelus marginatus in relation to environmental factors , 2006 .

[38]  A. Takemura,et al.  A direct influence of moonlight intensity on changes in melatonin production by cultured pineal glands of the golden rabbitfish, Siganus guttatus , 2006, Journal of pineal research.

[39]  A. Takemura,et al.  Perception and possible utilization of moonlight intensity for reproductive activities in a lunar-synchronized spawner, the golden rabbitfish. , 2004, Journal of experimental zoology. Part A, Comparative experimental biology.

[40]  Md Saydur Rahman,et al.  Effects of Moonlight Exposure on Plasma Melatonin Rhythms in the Seagrass Rabbitfish, Siganus Canaliculatus , 2004, Journal of biological rhythms.

[41]  B. Semmens,et al.  Observations of a Nassau grouper, Epinephelus striatus, Spawning Aggregation Site in Little Cayman, Cayman Islands, Including Multi-Species Spawning Information , 2004, Environmental Biology of Fishes.

[42]  K. Soyano,et al.  Lunar-related spawning in honeycomb grouper, Epinephelus merra , 2003, Fish Physiology and Biochemistry.

[43]  A. Aguilar-Perera,et al.  A spawning aggregation of Nassau grouperEpinephelus striatus (Pisces: Serranidae) in the Mexican Caribbean , 1996, Environmental Biology of Fishes.

[44]  P. Colin Reproduction of the Nassau grouper, Epinephelus striatus (Pisces: Serranidae) and its relationship to environmental conditions , 1992, Environmental Biology of Fishes.

[45]  R. E. Johannes Reproductive strategies of coastal marine fishes in the tropics , 1978, Environmental Biology of Fishes.

[46]  A. Takemura,et al.  Histological observations of seasonal reproductive and lunar‐related spawning cycles in the female honeycomb grouper Epinephelus merra in Okinawan waters , 2002 .

[47]  A. Nakazono,et al.  Spawning behavior and artificial fertilization in captive reared red spotted grouper, Epinephelus akaara , 2002 .

[48]  J. A. Madrid,et al.  Melatonin rhythms in European sea bass plasma and eye: influence of seasonal photoperiod and water temperature , 2001, Journal of pineal research.

[49]  A. Takemura,et al.  Correlation between plasma steroid hormones and vitellogenin profiles and lunar periodicity in the female golden rabbitfish, Siganus guttatus (Bloch). , 2000, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[50]  A. Takemura,et al.  Lunar spawning in Siganus canaliculatus , 1999 .

[51]  D. Zeller Spawning aggregations: patterns of movement of the coral trout Plectropomus leopardus (Serranidae) as determined by ultrasonic telemetry , 1998 .

[52]  A. Takemura,et al.  Annual Changes in Oocyte Development and Serum Vitellogenin Level in the Rabbitfish Siganus canaliculatus (Park) in Okinawa, Southern Japan , 1998 .

[53]  S. Zamora,et al.  Daily cycles in plasma and ocular melatonin in demand-fed sea bass, Dicentrarchus labrax L. , 1997, Journal of Comparative Physiology B.

[54]  M. Domeier,et al.  Tropical reef fish spawning aggregations : Defined and reviewed , 1997 .