Dissociation of circadian and circatidal timekeeping in the marine crustacean Eurydice pulchra
Open accessAbstract
BACKGROUND: Tidal (12.4 hr) cycles of behavior and physiology adapt intertidal organisms to temporally complex coastal environments, yet their underlying mechanism is unknown. However, the very existence of an independent "circatidal" clock has been disputed, and it has been argued that tidal rhythms arise as a submultiple of a circadian clock, operating in dual oscillators whose outputs are held in antiphase i.e., ~12.4 hr apart. RESULTS: We demonstrate that the intertidal crustacean Eurydice pulchra (Leach) exhibits robust tidal cycles of swimming in parallel to circadian (24 hr) rhythms in behavioral, physiological and molecular phenotypes. Importantly, ~12.4 hr cycles of swimming are sustained in constant conditions, they can be entrained by suitable stimuli, and they are temperature compensated, thereby meeting the three criteria that define a biological clock. Unexpectedly, tidal rhythms (like circadian rhythms) are sensitive to pharmacological inhibition of Casein kinase 1, suggesting the possibility of shared clock substrates. However, cloning the canonical circadian genes of E. pulchra to provide molecular markers of circadian timing and also reagents to disrupt it by RNAi revealed that environmental and molecular manipulations that confound circadian timing do not affect tidal timing. Thus, competent circadian timing is neither an inevitable nor necessary element of tidal timekeeping. CONCLUSIONS: We demonstrate that tidal rhythms are driven by a dedicated circatidal pacemaker that is distinct from the circadian system of E. pulchra, thereby resolving a long-standing debate regarding the nature of the circatidal mechanism.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
RNAi experiments revealed that circatidal timekeeping in Eurydice pulchra is at least independent from PER and TIM cycles.
“RNAi experiments revealed that the circatidal timekeeping is at least independent from PER and TIM cycles.”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [10]
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.”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [10]
In Eurydice pulchra, pharmacological inhibition of CK1δ/ε by PF-670462 altered both circadian cycles (pigment dispersion in chromatophores) and circatidal swimming rhythms.
“In this species, the pharmacological inhibition of CK1δ/ε by PF-670462 altered both circadian cycles (pigment dispersion in chromatophores), as well as circatidal swimming rhythms [10].”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [10]
Vibrations mimicking water turbulence were effective in re-entraining Eurydice pulchra that became arrhythmic after spending more than a month in DD.
“Moreover, vibrations mimicking water turbulence were effective in re-entraining animals that became arrhythmic after spending more than a month in DD [10].”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [10]
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].”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [10]
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.”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [10]
Apart from timeless, Eurydice circadian clock genes also do not show a circadian expression pattern.
“However, it should be noted that apart from timeless, Eurydice circadian clock genes also do not show a circadian expression pattern [10] (Figure 3F).”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [10]
No circatidal oscillations have been found in Eurydice core clock genes.
“Furthermore, no circatidal oscillations have been found in Eurydice core clock genes.”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [10]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr121 · Cited by 39,795 · see citing works
Post-translational modifications regulate the ticking of the circadian clock
Gallego, M., & Virshup, D. M. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2106 · Cited by 863 · see citing works
Regulation of circadian behaviour and metabolism by synthetic REV-ERB agonists
Solt, L. A., Wang, Y., Banerjee, S., Hughes, T., Kojetin, D. J., Lundåsen, T., Shin, Y., Liu, J., Cameron, M. D., Noël, R., et al. (2012) · Nature · doi:10.1038/nature11030 · Cited by 835 · see citing works
Coupled oscillators control morning and evening locomotor behaviour of Drosophila
Stoleru, D., Peng, Y., Agosto, J. L., & Rosbash, M. (2004) · Nature · doi:10.1038/nature02926 · Cited by 700 · see citing works
Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain
Grima, B., Chélot, E., Xia, R., & Rouyer, F. (2004) · Nature · doi:10.1038/nature02935 · Cited by 684 · see citing works
Hogben, L. T., & Slome, D. (1931) · Proceedings of the Royal Society of London Series B Containing Papers of a Biological Character · doi:10.1098/rspb.1931.0020 · Cited by 613 · see citing works
Circadian topology of metabolism
Bass, J. T. (2012) · Nature · doi:10.1038/nature11704 · Cited by 610 · see citing works
Circadian orchestration of the hepatic proteome
Reddy, A. B., Karp, N. A., Maywood, E. S., Sage, E. A., Deery, M., O'Neill, J. S., Wong, G. K. Y., Chesham, J., Odell, M., Lilley, K. S., et al. (2006) · Current Biology · doi:10.1016/j.cub.2006.04.026 · Cited by 548 · see citing works
Self-citationIdentification of Small Molecule Activators of Cryptochrome
Hirota, T., Lee, J. W., John, P. C. S., Sawa, M., Iwaisako, K., Noguchi, T., Pongsawakul, P. Y., Sonntag, T., Welsh, D. K., Brenner, D. A., et al. (2012) · Science · doi:10.1126/science.1223710 · Cited by 500 · see citing works
Gaunt, M. W., & Miles, M. A. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004133 · Cited by 435 · see citing works
Zerr, D., Hall, J. C., Rosbash, M., & Siwicki, K. K. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-08-02749.1990 · Cited by 401 · see citing works
Sehgal, A., Rothenfluh, A., Hunter-Ensor, M., Chen, Y.-F., Myers, M. P., & Young, M. W. (1995) · Science · doi:10.1126/science.270.5237.808 · Cited by 370 · see citing works
Zhu, H., Šauman, I., Yuan, Q., Casselman, A. L., Emery-Le, M., Emery, P., & Reppert, S. M. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060004 · Cited by 321 · see citing works
Circadian Control of Global Gene Expression Patterns
Doherty, C. J., & Kay, S. A. (2010) · Annual Review of Genetics · doi:10.1146/annurev-genet-102209-163432 · Cited by 288 · see citing works
Casein kinase 1: Complexity in the family
Cheong, J. K., & Virshup, D. M. (2010) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2010.12.004 · Cited by 256 · see citing works
Šauman, I., & Reppert, S. M. (1996) · Neuron · doi:10.1016/s0896-6273(00)80220-2 · Cited by 238 · see citing works
Zimmerman, W. F., Pittendrigh, C. S., & Pavlidis, T. (1968) · Journal of Insect Physiology · doi:10.1016/0022-1910(68)90226-6 · Cited by 216 · see citing works
Another place, another timer: marine species and the rhythms of life
Tessmar‐Raible, K., Raible, F., & Arboleda, E. (2011) · BioEssays · doi:10.1002/bies.201000096 · Cited by 208 · see citing works
Selective Inhibition of Casein Kinase 1ϵ Minimally Alters Circadian Clock Period
Walton, K. M., Fisher, K., Rubitski, D., Marconi, M., Meng, Q.-J., Sládek, M., Adams, J., Bass, M., Chandrasekaran, R., Butler, T., et al. (2009) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.109.151415 · Cited by 184 · see citing works
Allebrandt, K. V., Amin, N., Müller‐Myhsok, B., Esko, T., Teder‐Laving, M., Azevedo, R. V. D. M., Hayward, C., van Mill, J., Vogelzangs, N., Green, E. W., et al. (2011) · Molecular Psychiatry · doi:10.1038/mp.2011.142 · Cited by 153 · see citing works
Self-citationCircadian and circalunar clock interactions in a marine annelid
Zantke, J., Ishikawa-Fujiwara, T., Arboleda, E., Lohs, C., Schipany, K., Hallay, N., Straw, A. D., Todo, T., & Tessmar-Raible, K. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.08.031 · Cited by 148 · see citing works
The swimming rhythm of the sand beach isopod Eurydice pulchra
Jones, D. A., & Naylor, E. (1970) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/0022-0981(70)90024-9 · Cited by 128 · see citing works
Deery, M. J., Maywood, E. S., Chesham, J. E., Sládek, M., Karp, N. A., Green, E. W., Charles, P. D., Reddy, A. B., Kyriacou, C. P., Lilley, K. S., et al. (2009) · Current Biology · doi:10.1016/j.cub.2009.10.024 · Cited by 125 · see citing works
Self-citationThe Cyanobacterial Circadian System: From Biophysics to Bioevolution
Johnson, C. H., Stewart, P. L., & Egli, M. (2011) · Annual Review of Biophysics · doi:10.1146/annurev-biophys-042910-155317 · Cited by 124 · see citing works
Marrus, S. B., Zeng, H., & Rosbash, M. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb01080.x · Cited by 123 · see citing works
Kim, E. Y., Ko, H. W., Yu, W., Hardin, P. E., & Edery, I. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02339-06 · Cited by 112 · see citing works
Neuroanatomical studies of period gene expression in the hawkmoth, Manduca sexta
Wise, S. K., Davis, N. T., Tyndale, E., Noveral, J., Folwell, M. G., Bedian, V., Emery, I. F., & Siwicki, K. K. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10242 · Cited by 109 · see citing works
Ikeno, T., Numata, H., & Goto, S. G. (2011) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2011.04.006 · Cited by 107 · see citing works
Naylor, E. (1996) · Chronobiology International · doi:10.3109/07420529609012649 · Cited by 103 · see citing works
Závodská, R., Šauman, I., & Sehnal, F. (2003) · Journal of Biological Rhythms · doi:10.1177/0748730403251711 · Cited by 102 · see citing works
The Circadian Clock of the Fly: A Neurogenetics Journey Through Time
Özkaya, Ö., & Rosato, E. (2012) · Advances in genetics · doi:10.1016/b978-0-12-387687-4.00004-0 · Cited by 86 · see citing works
Moriyama, Y., Sakamoto, T., Karpova, S. G., et al. (2008) · Journal of Biological Rhythms · doi:10.1177/0748730408320486 · Cited by 86 · see citing works
Qiu, J., & Hardin, P. E. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.8.4182 · Cited by 85 · see citing works
Palmer, J. D. (1995) · Chronobiology International · doi:10.3109/07420529509057279 · Cited by 71 · see citing works
Takekata, H., Matsuura, Y., Goto, S. G., Satoh, A. O., & Numata, H. (2012) · Biology Letters · doi:10.1098/rsbl.2012.0079 · Cited by 71 · see citing works
Bloch, G., Solomon, S. M., Robinson, G. E., et al. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10778 · Cited by 70 · see citing works
Nawathean, P., Stoleru, D., & Rosbash, M. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02338-06 · Cited by 62 · see citing works
Organization of endogenous clocks in insects
Helfrich‐Förster, C. (2005) · Biochemical Society Transactions · doi:10.1042/bst20050957 · Cited by 44 · see citing works
Wilcockson, D. C., Zhang, L., Hastings, M. H., et al. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22533 · Cited by 35 · see citing works
Self-citationOntogeny of an endogenous rhythm in Eurydice pulchra
Hastings, M. H., & Naylor, E. (1980) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/0022-0981(80)90027-1 · Cited by 31 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Circadian and circalunar clock interactions in a marine annelid
Zantke, J., Ishikawa-Fujiwara, T., Arboleda, E., Lohs, C., Schipany, K., Hallay, N., Straw, A. D., Todo, T., & Tessmar-Raible, K. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.08.031 · Cited by 148 · see citing works
A cell-autonomous mammalian 12 hr clock coordinates metabolic and stress rhythms
Zhu, B., Zhang, Q., Pan, Y., Mace, E. M., York, B., Antoulas, A. C., Dacso, C. C., & O’Malley, B. W. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.05.004 · Cited by 146 · see citing works
An Overview of Monthly Rhythms and Clocks
Raible, F., Takekata, H., & Tessmar-Raible, K. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00189 · Cited by 121 · see citing works
The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks
Andreatta, G., & Tessmar-Raible, K. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2020.03.009 · Cited by 111 · see citing works
The cryptochrome/photolyase family in aquatic organisms
Oliveri, P., Fortunato, A. E., Petrone, L., Ishikawa-Fujiwara, T., Kobayashi, Y., Todo, T., Antonova, O., Arboleda, E., Zantke, J., Tessmar-Raible, K., et al. (2014) · Marine Genomics · doi:10.1016/j.margen.2014.02.001 · Cited by 90 · see citing works
Tidal and diel orchestration of behaviour and gene expression in an intertidal mollusc
Schnytzer, Y., Simon-Blecher, N., Li, J., Waldman Ben-Asher, H., Salmon-Divon, M., Achituv, Y., Hughes, M. E., & Levy, O. (2018) · Scientific Reports · doi:10.1038/s41598-018-23167-y · Cited by 58 · see citing works
Metabolic molecular markers of the tidal clock in the marine crustacean Eurydice pulchra
O’Neill, J. S., Lee, K. D., Zhang, L., Feeney, K., Webster, S. G., Blades, M. J., Kyriacou, C. P., Hastings, M. H., & Wilcockson, D. C. (2015) · Current Biology · doi:10.1016/j.cub.2015.02.052 · Cited by 43 · see citing works
Self-citationTranscriptome dynamics over a lunar month in a broadcast spawning acroporid coral
Oldach, M. J., Workentine, M., Matz, M. V., Fan, T., & Vize, P. D. (2017) · Molecular Ecology · doi:10.1111/mec.14043 · Cited by 39 · see citing works
- Authors
- Zhang, L., Hastings, M. H., Green, E. W., Tauber, E., Sladek, M., Webster, S. G., Kyriacou, C. P., & Wilcockson, D. C.
- Affiliations
- University of Leicester (GB)
- MRC Laboratory of Molecular Biology (GB)
- Bangor University (GB)
- Aberystwyth University (GB)
- Corresponding author
- Webster, Simon G.
- Kyriacou, Charalambos P.
- ORCID
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2013-10
- Volume
- 23
- Issue
- 19
- Pages
- 1863-1873
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC3793863
- OpenAlex
- W2111762174
- Cited by
- 187
- References
- 40
- Citations by year
- 2026: 12 · 2025: 11 · 2024: 10 · 2023: 14 · 2022: 20 · 2021: 14 · 2020: 15 · 2019: 8 · 2018: 15 · 2017: 25 · 2016: 17 · 2015: 11 · 2014: 10 · 2013: 4
- FWCI
- 7.56
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Current Biology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- ASEP (submittedVersion, public-domain)
- Figshare (submittedVersion, cc-by)
- Leicester Research Archive (University of Leicester) (submittedVersion, cc-by)
- Funders
- University of Leicester
- Medical Research Council
- Biotechnology and Biological Sciences Research Council (BB/G02085X/1, BB/K009702/1, 91/517172, BB/E001750/1, BB/E000835/1, S17172)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
- Physical Sciences › Environmental Science › Ecology › Crustacean biology and ecology
- Keywords
- circatidal rhythm, circadian rhythm, Eurydice pulchra, intertidal crustaceans, biological clock, tidal rhythms, swimming behavior, casein kinase 1, clock genes, RNA interference, entrainment, temperature compensation
- MeSH terms
- Animals, Behavior, Animal, Cell Line, Circadian Rhythm, Drosophila, Molecular Sequence Data, Periodicity, Pyrazoles, Pyrimidines, Swimming, Isopoda, RNA Interference, RNA, Small Interfering, Casein Kinase I, Tidal Waves, CLOCK Proteins, ARNTL Transcription Factors, Cryptochromes, 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.
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 ›
Are you an author, or do you see a problem with this page? Request a review