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Cited by 111Circadian rhythm and melatoninPhysiological and biochemical adaptationsLight effects on plants

The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks

Open access
Andreatta, Gabriele, Tessmar-Raible, Kristin·2020·Journal of Molecular Biology
DOI 10.1016/j.jmb.2020.03.009PMC PMC7322537
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Abstract

Starting with the beginning of the last century, a multitude of scientific studies has documented that the lunar cycle times behaviors and physiology in many organisms. It is plausible that even the first life forms adapted to the different rhythms controlled by the moon. Consistently, many marine species exhibit lunar rhythms, and also the number of documented "lunar-rhythmic" terrestrial species is increasing. Organisms follow diverse lunar geophysical/astronomical rhythms, which differ significantly in terms of period length: from hours (circalunidian and circatidal rhythms) to days (circasemilunar and circalunar cycles). Evidence for internal circatital and circalunar oscillators exists for a range of species based on past behavioral studies, but those species with well-documented behaviorally free-running lunar rhythms are not typically used for molecular studies. Thus, the underlying molecular mechanisms are largely obscure: the dark side of the moon. Here we review findings that start to connect molecular pathways with moon-controlled physiology and behaviors. The present data indicate connections between metabolic/endocrine pathways and moon-controlled rhythms, as well as interactions between circadian and circatidal/circalunar rhythms. Moreover, recent high-throughput analyses provide useful leads toward pathways, as well as molecular markers. However, for each interpretation, it is important to carefully consider the, partly substantially differing, conditions used in each experimental paradigm. In the future, it will be important to use lab experiments to delineate the specific mechanisms of the different solar- and lunar-controlled rhythms, but to also start integrating them together, as life has evolved equally long under rhythms of both sun and moon.

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Written from the paper’s full text.

TL;DR

This review synthesizes evidence that lunar-controlled rhythms, from circatidal to circalunar periods, are widespread and that molecular links are emerging with circadian clock genes, metabolic/endocrine pathways, and high-throughput markers. It argues that mechanisms remain largely obscure because species with well-documented behavioral free-running lunar rhythms are rarely used for molecular work and experimental conditions vary widely.

Key findings

  • Lunar geophysical cycles span hours to days: lunidian ~24.8 h, semilunar ~14.8 days, synodic ~29.5 days; other lunar months include sidereal 27.32166 days, anomalistic 27.55 days, draconic 27.212220 days, and tropical 27.321582 days.
  • Circadian clock genes interact with lunar rhythms but not uniformly: in *Platynereis dumerilii*, free-running FM showed significantly higher mRNA for *pdp1*, *period*, *clock*, and *tim*; the CK1δ/ε inhibitor PF-670462 rendered clock gene transcription and locomotor activity arrhythmic but left monthly spawning unaffected. In *Eurydice pulchra*, circatidal timekeeping was independent of PER and TIM cycles, no circatidal oscillations were found in core clock genes, only *tim* showed a clear circadian profile, and peroxiredoxin plus 10 of 11 detected mitochondrial genes followed circatidal patterns.
  • Endocrine and metabolic pathways are implicated: melatonin levels were reduced around FM in several fish, melatonin receptors and *aanat* showed lunar-phase-dependent expression, and *Platynereis* GnRH-like/corazonin1 was differentially expressed across the circalunar cycle.
  • High-throughput studies provide candidate markers: coral spawning transcriptomes showed downregulation of clock genes and upregulation of GPCR, calcium signaling, and respiratory genes; in *Platynereis* heads, about 25% of the analyzed proteome was differentially regulated between NM and free-running FM, a much higher circalunar regulation than at the transcript level.

Methods

  • Narrative review, not a primary experimental study; it synthesizes behavioral, molecular, pharmacological, genetic linkage, transcriptomic, and proteomic findings across marine and terrestrial organisms.
  • Data/sample: published literature on corals, *Platynereis dumerilii*, *Eurydice pulchra*, *Clunio marinus*, fish, mollusks, *Drosophila*, rodents, and humans, among others.
  • Main analysis: compares experimental paradigms—natural versus artificial moonlight, free-running versus entrainment, field versus laboratory conditions—and highlights candidate pathways and molecular markers.

Limitations

  • Stated: the underlying molecular mechanisms are largely obscure; species with well-documented behaviorally free-running lunar rhythms are not typically used for molecular studies; data variability likely arises from differing experimental regimes; current resolution may be insufficient to distinguish among different lunar cycles; laboratory versus field discrepancies exist; functional studies, knockouts, and transgenic models are needed.
  • Stated: many interpretations require careful consideration of partly substantially differing experimental conditions, and some analyses, such as those on the HPG axis and lunar rhythmicity, are inconclusive.
  • Evident: as a review, it reports no new primary data; cited studies show conflicting results, and many candidate mechanisms remain functionally untested.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1016/j.jmb.2020.03.009

Cites

142 of 142 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 83 cited sources checked · 0 supported · 0 flagged

  • Interpretationreasoning

    The underlying molecular mechanisms of lunar rhythms are largely obscure.

    “Thus, the underlying molecular mechanisms are largely obscure: the dark side of the moon.”
    Quote in the paperSubstantial claim
  • Premisecitation

    Lunar rhythms are widespread among marine species, especially those living in relatively shallow waters and coastal reef habitats.

    “In line with this, it is not surprising that lunar rhythms are widespread among marine species [3], especially those living in relatively shallow waters and coastal reef habitats.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [3] Raible F. Takekata H. Tessmar-Raible K. An overview of monthly rhythms and clocks Front. Neurol. 8 2017 1 14 10.3389/fneur.2017.00189 28553258 PMC5428424 source

      Not checked in the free run.

  • Premisenone given

    A multitude of scientific studies has documented that the lunar cycle times behaviors and physiology in many organisms.

    “Starting with the beginning of the last century, a multitude of scientific studies has documented that the lunar cycle times behaviors and physiology in many organisms.”
    Quote in the paperNot a substantial claim
  • Premisecitation

    Potential effects of the anomalistic cycle on biological rhythmicity approximating the synodic month have been shown in Crassostrea gigas, both at the behavioral and reproductive levels.

    “However, it is interesting to report that potential effects of the anomalistic cycle on biological rhythmicity approximating the synodic month have been shown in Crassostrea gigas, both at the behavioral and reproductive levels [6,9].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [6] Tran D. Nadau A. Durrieu G. Ciret P. Parisot J.P. Massabuau J.C. Field chronobiology of a molluscan bivalve: how the moon and sun cycles interact to drive oyster activity rhythms Chronobiol. Int. 28 2011 307 317 10.3109/07420528.2011.565897 21539422 source

      Not checked in the free run.

    • cites [9] Bernard I. Massabuau J.C. Ciret P. Sow M. Sottolichio A. Pouvreau S. Tran D. In situ spawning in a marine broadcast spawner, the Pacific oyster Crassostrea gigas: timing and environmental triggers Limnol. Oceanogr. 61 2016 635 647 10.1002/lno.10240 source

      Not checked in the free run.

  • Premisecitation

    In Odontosyllis enopla, reproductive swarming occurs precisely during the first nights after FM in summer and early autumn.

    “As witnessed by the crew on Colombo's caravel, also in the Bermuda fireworm, Odontosyllis enopla, reproductive swarming occurs precisely during the first nights after FM in summer and early autumn [20].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [20] Fischer A. Fischer U. On the life-style and life-cycle of the luminescent polychaete Odontosyllis enopla (Annelida: Polychaeta) Invert. Biol. 114 2019 236 247 10.2307/3226878 source

      Not checked in the free run.

  • May combine two claims. 26
  • Classified as probably not a substantial claim. 15
  • The quote only partly states this claim. 1

  • May combine two claims.

    Premisecitation

    Reef corals are losing this critical reproductive synchrony, likely due to anthropogenic impact.

    “Unfortunately, reef corals are losing this critical reproductive synchrony, likely due to anthropogenic impact [22,23].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [22] Fogarty N.D. Marhaver K.L. Coral spawning, unsynchronized Science. 365 2019 987 988 10.1126/science.aay7457 31488677 source

      Not checked in the free run.

    • cites [23] Shlesinger T. Loya Y. Breakdown in spawning synchrony: a silent threat to coral persistence Science. 365 2019 1002 1007 10.1126/science.aax0110 31488683 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    Species with well-documented behaviorally free-running lunar rhythms are not typically used for molecular studies.

    “but those species with well-documented behaviorally free-running lunar rhythms are not typically used for molecular studies.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Premisenone given

    Many marine species exhibit lunar rhythms, and the number of documented lunar-rhythmic terrestrial species is increasing.

    “Consistently, many marine species exhibit lunar rhythms, and also the number of documented “lunar-rhythmic” terrestrial species is increasing.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationreasoning

    Synchronization of external fertilization with a reliable environmental cycle maximizes the probability that eggs and sperms encounter, and hence is critical for the survival of these species.

    “As external fertilization is frequent among these animals, its synchronization with a reliable environmental cycle maximizes the probability that eggs and sperms encounter, and hence is critical for the survival of these species.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationreasoning

    In animals where the gonads contribute to a large proportion of the body mass, such as sea urchins or mussels, the lunar synchronization effect is particularly prominent, leading to significant changes in body mass.

    “In animals where the gonads contribute to a large proportion of the body mass, such as sea urchins or mussels, this effect is particularly prominent, leading indeed to significant changes in body mass”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    In Gecarcoidea natalis, spawning occurs 17-18 days after mating, in a precise lunar phase between LQM and NM.

    “In this case, the spawning occurred 17–18 days after mating, in a precise lunar phase, between LQM and NM [19].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [19] A.M. Adamczewska, S. Morris, Ecology and behavior of Gecarcoidea natalis, the Christmas Island red crab, during the annual breeding migration, (2001) 305–320. 11441973 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Interpretationnone given

    Recent high-throughput analyses provide useful leads toward pathways, as well as molecular markers.

    “Moreover, recent high-throughput analyses provide useful leads toward pathways, as well as molecular markers.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The anomalistic cycle can impact tides amplitude during the synodic month, although slightly out of phase.

    “The anomalistic cycle, modulating the proximity of our satellite to earth, can impact for instance on tides amplitude during the synodic month (spring–neap tides cycle, 14.76 days), although slightly out of phase (13.78 days from perigee to apogee) [5,7].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [5] Coughenour C.L. Archer A.W. Lacovara K.J. Tides, tidalites, and secular changes in the earth–moon system Earth-Science Rev. 97 2009 59 79 10.1016/j.earscirev.2009.09.002 source

      Not checked in the free run.

    • cites [7] Kvale E.P. The origin of neap–spring tidal cycles Mar. Geol. 235 2006 5 18 10.1016/j.margeo.2006.10.001 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisenone given

    Organisms follow diverse lunar geophysical/astronomical rhythms that differ significantly in period length, from hours (circalunidian and circatidal rhythms) to days (circasemilunar and circalunar cycles).

    “Organisms follow diverse lunar geophysical/astronomical rhythms, which differ significantly in terms of period length: from hours (circalunidian and circatidal rhythms) to days (circasemilunar and circalunar cycles).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Interpretationnone given

    While for short and long lunar period lengths marine examples are very well established, this is less clear for terrestrial organisms.

    “While for short and long lunar period lengths marine examples are very well established, this is less clear for terrestrial organisms.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    In Platynereis dumerilii, most analyzed circadian clock genes showed similar circadian expression profiles in NM and FR-FM, but pdp1, period, clock, and tim had significantly higher mRNA levels during FR-FM.

    “Most of the genes analyzed showed similar circadian expression profiles in the two different lunar phases, but significantly higher mRNA levels during FR-FM were found for pdp1, period, clock, and tim (see Figure 2), suggesting that a subset of circadian clock transcripts is affected by the circalunar clock, independently of nocturnal light cues.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [28] Zantke J. Ishikawa-Fujiwara T. Arboleda E. Lohs C. Schipany K. Hallay N. Straw A.D. Todo T. Circadian and circalunar clock interactions in a marine annelid Cell Rep. 5 2013 99 113 10.1016/j.celrep.2013.08.031 24075994 PMC3913041 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    These data suggest that the integration of multiple environmental features and/or the specific light spectrum of sunlight and moonlight might affect the expression of these genes.

    “These data suggest that the integration of multiple environmental features and/or the specific light spectrum of sunlight and moonlight might affect the expression of these genes.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given

    The elucidation of the mechanisms underlying circalunar/circasemilunar and circatidal/circalunidian rhythms is still at an early stage.

    “In spite of the increasing literature, the elucidation of the mechanisms underlying circalunar/circasemilunar and circatidal/circalunidian rhythms is still at an early stage.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    In Platynereis dumerilii, the circalunar clock seems to also affect locomotor activity levels, with worms showing a weaker circadian rhythmicity during free-running FM compared to NM.

    “In this species, the circalunar clock seems to also affect locomotor activity levels, with worms showing a weaker circadian rhythmicity during free-running FM (FR-FM) compared to NM.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [28] Zantke J. Ishikawa-Fujiwara T. Arboleda E. Lohs C. Schipany K. Hallay N. Straw A.D. Todo T. Circadian and circalunar clock interactions in a marine annelid Cell Rep. 5 2013 99 113 10.1016/j.celrep.2013.08.031 24075994 PMC3913041 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Before the 1970s, the scientific literature is rich in examples of other rhythms, including tidal and monthly, mainly focused on behavioral observations and including many studies that provide evidence for free-running rhythms.

    “Before this time, the scientific literature is rich in examples of other rhythms, including tidal and monthly. Those were mainly focused on behavioral observations and include many studies that provide evidence for free-running rhythms (for overviews, see [24,25]).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [24] Fingerman M. Lunar rhythmicity in marine organisms Am. Nat. 91 1957 167 178 source

      Not checked in the free run.

    • cites [25] Numata H. Helm B. Annual, Lunar, and Tidal Clocks: Patterns and Mechanisms of Nature’s Enigmatic Rhythms 2014 Springer

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In Acropora millepora, natural FM, as well as artificial night illumination mimicking FM, impact on clock genes expression.

    “In the reef-building coral Acropora millepora, which reproduces once every year integrating both seasonal, lunar and daily cues, natural FM, as well as artificial night illumination mimicking FM, have been shown to impact on clock genes expression.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [26] Levy O. Appelbaum L. Leggat W. Gothlif Y. Hayward D.C. Miller D.J. Hoegh-Guldberg O. Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora Science. 318 2007 467 470 10.1126/science.1145432 17947585 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In Acropora millepora, both cry1 and cry2 were expressed in the ectodermal layer of larvae and adults, and their mRNA levels peaked during daylight phases.

    “Both cry1 and cry2 were expressed in the ectodermal layer of larvae and adults, and their mRNA levels peaked during daylight phases.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [26] Levy O. Appelbaum L. Leggat W. Gothlif Y. Hayward D.C. Miller D.J. Hoegh-Guldberg O. Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora Science. 318 2007 467 470 10.1126/science.1145432 17947585 source

      Not checked in the free run.

  • May combine two claims. The quote only partly states this claim.

    Premisecitation

    In Acropora millepora, only cry1 (but not cry2) was affected by exposure to DD, whereas cry2 increased under natural moonlight compared to artificial one during both LQM and FM.

    “For instance, only cry1 (but not cry2) was affected by exposure to DD, whereas, although not significantly, cry2 increased under natural moonlight compared to the artificial one during both LQM and FM [27,31].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [27] Brady A.K. Willis B.L. Harder L.D. Vize P.D. Lunar phase modulates circadian gene expression cycles in the broadcast spawning coral Acropora millepora Biol. Bull. 230 2016 130 142 10.1086/BBLv230n2p130 27132135 source

      Not checked in the free run.

    • cites [31] Brady A.K. Snyder K.A. Vize P.D. Circadian cycles of gene expression in the coral, Acropora millepora PLoS One 6 2011 10.1371/journal.pone.0025072 PMC3176305 21949855 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    This loss of reproductive synchrony threatens several species, not only corals, but entire reef communities.

    “This phenomenon threatens several species, not only corals, but entire reef communities.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    These and other data suggest a high level of data variability, likely due to differences in experimental regimes, as well as strong environmental and possibly population variability.

    “These and other data reported in this review suggest a high level of data variability, likely due to differences in experimental regimes, as well as strong environmental and possibly population variability.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Eurydice pulchra showed robust tidal rhythmicity after being caught in the wild and released in DD, suggesting the existence of a true circatidal endogenous oscillator.

    “This intertidal isopod showed robust tidal rhythmicity after being caught in the wild and released in DD, suggesting the existence of a true circatidal endogenous oscillator.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [10] Zhang L. Hastings M.H. Green E.W. Tauber E. Sladek M. Webster S.G. Kyriacou C.P. Wilcockson D.C. Dissociation of circadian and circatidal timekeeping in the marine crustacean Eurydice pulchra Curr. Biol. 23 2013 1863 1873 10.1016/j.cub.2013.08.038 24076244 PMC3793863 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Circadian rhythm disruption through LL exposure affected neither the tidal swimming period nor overall activity levels in Eurydice pulchra.

    “Furthermore, circadian rhythm disruption through LL exposure affected neither the tidal swimming period nor overall activity levels [10].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [10] Zhang L. Hastings M.H. Green E.W. Tauber E. Sladek M. Webster S.G. Kyriacou C.P. Wilcockson D.C. Dissociation of circadian and circatidal timekeeping in the marine crustacean Eurydice pulchra Curr. Biol. 23 2013 1863 1873 10.1016/j.cub.2013.08.038 24076244 PMC3793863 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisereasoning

    Circatidal clocks and their relation with circadian clocks are particularly interesting because a 12.4 h period is just half of 24.8 h.

    “Circatidal clocks and their relation with circadian clocks are particularly interesting, because in essence a 12.4 h period is just half of 24.8 h, i.e. a period covered by the conventional core circadian clock network.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Genetic linkage analysis identified two specific chromosomal regions responsible for diurnal emergence and two related to lunar timing in Clunio marinus.

    “Genetic linkage analysis identified two specific chromosomal regions responsible for diurnal emergence and two related to lunar timing.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [46] Kaiser T.S. Poehn B. Szkiba D. Preussner M. Sedlazeck F.J. Zrim A. Neumann T. Nguyen L.T. The genomic basis of circadian and circalunar timing adaptations in a midge Nature. 540 2016 69 73 10.1038/nature20151 27871090 PMC5133387 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    The data presented might actually suggest the presence of both a photo-repressive mechanism and an endogenous clock contributing together to the circalunar timing in Siganus guttatus.

    “Thus, the data presented might actually suggest the presence of both a photo-repressive mechanism and an endogenous clock contributing together to the circalunar timing.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    In Eurydice pulchra, despite the observed phase delay, the amplitude of tidal oscillations was robust and comparable to the untreated control.

    “In spite of the observed phase delay, the amplitude of tidal oscillations was robust and comparable to the untreated control.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [10] Zhang L. Hastings M.H. Green E.W. Tauber E. Sladek M. Webster S.G. Kyriacou C.P. Wilcockson D.C. Dissociation of circadian and circatidal timekeeping in the marine crustacean Eurydice pulchra Curr. Biol. 23 2013 1863 1873 10.1016/j.cub.2013.08.038 24076244 PMC3793863 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In Siganus guttatus, per4 showed a robust oscillation over the lunar cycle under all the light regimes, but in antiphase compared to cry3.

    “Moreover, per4 showed a robust oscillation over the lunar cycle under all the light regimes, but in antiphase compared to cry3.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [50] Toda R. Okano K. Takeuchi Y. Yamauchi C. Fukushiro M. Takemura A. Okano T. 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 2014 10.1371/journal.pone.0109119 PMC4182804 25272159 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    The data potentially indicate the existence of a circatidal clock in the grass puffer brain, which, together with the circadian clock, might contribute to set daily and lunar-related reproductive rhythms.

    “These data potentially indicate the existence of a circatidal clock in the grass puffer brain, which, together with the circadian clock, might contribute to set the proper daily and lunar-related reproductive rhythms.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Interpretationcitation

    Peaks of PRX activity and mitochondrially encoded transcript levels might anticipate changes in the energy demand and reactive oxygen species production originating from the prevailing metabolic program, following a circatidal rest/activity rhythm.

    “Thus, the authors suggested that peaks of PRX activity and mitochondrially encoded transcript levels might anticipate changes in the energy demand and reactive oxygen species production originating from the prevailing metabolic program, following in this case a circatidal rest/activity rhythm.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [54] O’Neill J.S. Lee K.D. Zhang L. Feeney K. Webster S.G. Blades M.J. Kyriacou C.P. Hastings M.H. Metabolic molecular markers of the tidal clock in the marine crustacean Eurydice pulchra Curr. Biol. 25 2015 R326 R327 10.1016/j.cub.2015.02.052 25898100 PMC4406942 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Melatonin synthesis is exquisitely light sensitive, inhibited by light exposure, and fueled in the dark.

    “Moreover, melatonin synthesis is exquisitely light sensitive, inhibited by light exposure, and fueled in the dark [48,58,59]”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [48] Takemura A. Susilo E.S. Rahman M.D.S. Morita M. Perception and possible utilization of moonlight intensity for reproductive activities in a lunar-synchronized spawner, the golden rabbitfish J. Exp. Zool. Part A Comp. Exp. Biol. 301 2004 844 851 10.1002/jez.a.105 15449345 source

      Not checked in the free run.

    • cites [58] Rahman M.S. Kim B.H. Takemura A. Park C.B. Lee Y.D. Effects of moonlight exposure on plasma melatonin rhythms in the seagrass rabbitfish, Siganus canaliculatus J. Biol. Rhythm. 19 2004 325 334 10.1177/0748730404266712 15245651 source

      Not checked in the free run.

    • cites [59] Rahman M.S. Kim B.H. Takemura A. Park C.B. Lee Y.D. Influence of light-dark and lunar cycles on the ocular melatonin rhythms in the seagrass rabbitfish, a lunar-synchronized spawner J. Pineal Res. 37 2004 122 128 10.1111/j.1600-079X.2004.00147.x 15298671 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisereasoning

    Melatonin has been suggested as a potential component of the molecular mechanisms contributing to lunar-regulated rhythms.

    “Given its role as an endocrine mediator of other light-dependent rhythms (daily/circadian, i.e. daily sleep–wake cycle) in vertebrates, also melatonin has been suggested as a potential component of the molecular mechanisms contributing to lunar-regulated rhythms.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    The period of these oscillations was consistent with swimming activity and respiratory rate tidal cycles, which peak around high tides.

    “The period of these oscillations was consistent with swimming activity and respiratory rate tidal cycles, which peak around high tides [54,56].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [54] O’Neill J.S. Lee K.D. Zhang L. Feeney K. Webster S.G. Blades M.J. Kyriacou C.P. Hastings M.H. Metabolic molecular markers of the tidal clock in the marine crustacean Eurydice pulchra Curr. Biol. 25 2015 R326 R327 10.1016/j.cub.2015.02.052 25898100 PMC4406942 source

      Not checked in the free run.

    • cites [56] Hastings M.H. Semi-lunar variations of endogenous circa-tidal rhythms of activity and respiration in the isopod Eurydice pulchra Mar. Ecol Prog Ser. 4 1981 85 90 10.3354/meps004085 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Taking all above findings together might start to indicate that the circadian clockwork could be more plastic than previously thought and capable to adjust to the environmental cycle(s) most relevant for a given species.

    “Taking all above findings together might start to indicate that the circadian clockwork could be more plastic than previously thought and capable to adjust to the environmental cycle(s) most relevant for a given species [53,54,57].”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [53] Tran D. Perrigault M. Ciret P. Payton L. Bivalve mollusc circadian clock genes can run at tidal frequency Proc. Biol. Sci. 287 2020 20192440 10.1098/rspb.2019.2440 31910786 PMC7003461

      Not checked in the free run.

    • cites [54] O’Neill J.S. Lee K.D. Zhang L. Feeney K. Webster S.G. Blades M.J. Kyriacou C.P. Hastings M.H. Metabolic molecular markers of the tidal clock in the marine crustacean Eurydice pulchra Curr. Biol. 25 2015 R326 R327 10.1016/j.cub.2015.02.052 25898100 PMC4406942 source

      Not checked in the free run.

    • cites [57] Schnytzer Y. Simon-Blecher N. Li J. Ben-Asher H.W. Salmon-Divon M. Achituv Y. Hughes M.E. Levy O. Tidal and diel orchestration of behaviour and gene expression in an intertidal mollusc Sci. Rep. 8 2018 1 13 10.1038/s41598-018-23167-y 29559663 PMC5861051 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    The lack of both circatidal and circadian rhythmicity in clock gene expression is conceivable with the idea that specific subsets of the core circadian clock might be differentially recruited in a tissue-dependent manner, and depending on cellular context form circadian, circatidal, or circalunidian clocks.

    “This lack of both circatidal and circadian rhythmicity in clock gene expression is also conceivable with the idea that specific subsets of the core circadian clock might be differentially recruited in a tissue-dependent manner, and depending on cellular context form circadian, circatidal, or circalunidian clocks.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given

    Laboratory studies provide better control of the multitude of environmental variables present in nature, allowing investigation of the single contributions of a certain cue.

    “Laboratory studies provide a better control of the multitude of environmental variables present in nature, allowing the investigation of the single contributions of a certain cue”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    Generation of knockouts and transgenic animals allows for a detailed functional dissection that is difficult to meet with other methods.

    “the generation of knockouts and transgenic animals clearly allow for a detailed functional dissection that is difficult to meet with other methods”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Anthropogenic impacts (light pollution, temperature changes, architectural barriers) likely cause complex chronobiological changes that are endangering the world's ecosystems as we know them, and possibly human health.

    “complex chronobiological changes likely caused by anthropogenic impacts (i.e. light pollution, temperature changes, architectural barriers) that are endangering the world's ecosystems as we know them [22,23], and possibly human health”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [22] Fogarty N.D. Marhaver K.L. Coral spawning, unsynchronized Science. 365 2019 987 988 10.1126/science.aay7457 31488677 source

      Not checked in the free run.

    • cites [23] Shlesinger T. Loya Y. Breakdown in spawning synchrony: a silent threat to coral persistence Science. 365 2019 1002 1007 10.1126/science.aax0110 31488683 source

      Not checked in the free run.

37 of 37

  • The paper relies on this without support.

    Life has evolved equally long under both lunar and solar influences.

    “As the moon formed about 4.51 billion years ago, life evolved equally long under both lunar and solar influences”

  • The paper relies on this without support.

    The lunar cycle is a reliable and steady environmental cue.

    “Animals exploit reliable and steady environmental cues to synchronize crucial events of their life”
2 of 2

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • The cited retinal melatonin study names a different fish

    Minor

    The text attributes the retinal aanat result to the grass puffer, but reference 62 identifies the fish studied as the goldlined spinefoot.

  • Tropical-month discussion points to the draconic-month panel

    Minor

    The tropical-month explanation cites Figure 1(f), which the figure caption labels as the draconic month; the caption labels Figure 1(g) as the tropical month.

  • Limpet oxygen-consumption citation names a different species

    Minor

    The text attributes the cited oxygen-consumption finding to Cellana rota, while reference 99 names Cellana radiata.

3 of 3

Cites

Flagged first, then by citations

6 of the 148 references couldn’t be matched to a known paper.

Research works printed but not linked: 3

  1. Szmant-Froelich, 1985, Sexual reproduction of Favia fragum (ESPER): lunar patterns of gametogenesis, embryogenesis and planulation in Puerto Rico, Bull. Mar. Sci., 37, 880
  2. Ranzi, 1931, Ricerche sulla biologia sessuale degli Anellidi, Pubbl. Del Stn. Zool. Napoli., 11, 271
  3. Decoursey, 1990, Circadian photoentrainment in nocturnal mammals—ecological overtones, Biol. Behav., 15, 213

Cited by

Sorted by citations

Related

Authors
Andreatta, G., & Tessmar-Raible, K.
Affiliations
University of Vienna (AT)
ORCID
Andreatta, Gabriele
Venue
Journal of Molecular Biology
Publisher
Elsevier BV
Published
2020-05
Volume
432
Issue
12
Pages
3525-3546
ISSN
0022-2836 (ISSN-L)
DOI
10.1016/j.jmb.2020.03.009
PMC
PMC7322537
OpenAlex
W3012359533
Semantic Scholar
b671c083737034100dfd60550f2e16af2f3a5b0a
Cited by
111
References
148
Citations by year
2026: 16 · 2025: 22 · 2024: 20 · 2023: 17 · 2022: 20 · 2021: 12 · 2020: 4
FWCI
1.79
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Molecular Biology (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Padua Research Archive (University of Padova) (submittedVersion, cc-by-nc-nd)
Funders
  • Seventh Framework Programme
  • Horizon 2020 Framework Programme (819952)
  • European Research Council (337011)
  • Austrian Science Fund (P28970, SFB F78)
  • Universität Wien
Topics
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
  • Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Light effects on plants
Keywords
lunar rhythms, circatidal rhythm, circalunar rhythm, circadian rhythm, molecular clock mechanisms, metabolic pathways, endocrine pathways, molecular markers, free-running rhythm, marine organisms, terrestrial organisms
MeSH terms
Adaptation, Physiological, Animals, Circadian Rhythm, Light, Moon, Metabolic Networks and Pathways, Circadian Clocks

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-09.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-09.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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