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Annual Review of Marine Science

Volume 15, 2023

Rhythms and Clocks in Marine Organisms

Abstract

The regular movements of waves and tides are obvious representations of the oceans’ rhythmicity. But the rhythms of marine life span across ecological niches and timescales, including short (in the range of hours) and long (in the range of days and months) periods. These rhythms regulate the physiology and behavior of individuals, as well as their interactions with each other and with the environment. This review highlights examples of rhythmicity in marine animals and algae that represent important groups of marine life across different habitats. The examples cover ecologically highly relevant species and a growing number of laboratory model systems that are used to disentangle key mechanistic principles. The review introduces fundamental concepts of chronobiology, such as the distinction between rhythmic and endogenous oscillator–driven processes. It also addresses the relevance of studying diverse rhythms and oscillators, as well as their interconnection, for making better predictions of how species will respond to environmental perturbations, including climate change. As the review aims to address scientists from the diverse fields of marine biology, ecology, and molecular chronobiology, all of which have their own scientific terms, we provide definitions of key terms throughout the article.

Keyword(s): algae, animals, circadian, circalunar, circannual, circatidal, climate change, endogenous oscillators, environmental cycles
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/content/journals/10.1146/annurev-marine-030422-113038
2023-01-16
2024-04-25
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Literature Cited

  1. Aguzzi J, Company JB, Costa C, Menesatti P, Garcia JA et al. 2011. Activity rhythms in the deep-sea: a chronobiological approach. Front. Biosci. Landmark Ed. 16:131–50
     [Google Scholar]
  2. Andersson S, Kautsky L, Kalvas A. 1994. Circadian and lunar gamete release in Fucus vesiculosus in the atidal Baltic Sea. Mar. Ecol. Prog. Ser. 110:195–201
     [Google Scholar]
  3. Andreatta G, Tessmar-Raible K. 2020. The still dark side of the moon: molecular mechanisms of lunar-controlled rhythms and clocks. J. Mol. Biol. 432:3525–46
     [Google Scholar]
  4. Andrzejaczek S, Vély M, Jouannet D, Rowat D, Fossette S. 2021. Regional movements of satellite-tagged whale sharks Rhincodon typus in the Gulf of Aden. Ecol. Evol. 11:4920–34
     [Google Scholar]
  5. Annunziata R, Ritter A, Fortunato AE, Manzotti A, Cheminant-Navarro S et al. 2019. bHLH-PAS protein RITMO1 regulates diel biological rhythms in the marine diatom Phaeodactylum tricornutum. PNAS 116:13137–42
     [Google Scholar]
  6. Arboleda E, Hartenstein V, Martinez P, Reichert H, Sen S et al. 2018. An emerging system to study photosymbiosis, brain regeneration, chronobiology, and behavior: the marine acoel Symsagittifera roscoffensis. BioEssays 40:e1800107
     [Google Scholar]
  7. Arboleda E, Zurl M, Waldherr M, Tessmar-Raible K. 2019. Differential impacts of the head on Platynereis dumerilii peripheral circadian rhythms. Front. Physiol. 10:900
     [Google Scholar]
  8. Aschoff J. 1960. Exogenous and endogenous components in circadian rhythms. Cold Spring Harb. Symp. Quant. Biol. 25:11–28
     [Google Scholar]
  9. Aschoff J. 1965. Circadian rhythms in man. Science 148:1427–32
     [Google Scholar]
  10. Asher G, Sassone-Corsi P. 2015. Time for food: the intimate interplay between nutrition, metabolism, and the circadian clock. Cell 161:84–92
     [Google Scholar]
  11. Atkinson A, Harmer RA, Widdicombe CE, McEvoy AJ, Smyth TJ et al. 2015. Questioning the role of phenology shifts and trophic mismatching in a planktonic food web. Prog. Oceanogr. 137:498–512
     [Google Scholar]
  12. Atkinson A, Hill SL, Pakhomov EA, Siegel V, Reiss CS et al. 2019. Krill (Euphausia superba) distribution contracts southward during rapid regional warming. Nat. Clim. Change 9:142–47
     [Google Scholar]
  13. Austin RW, Petzold TJ. 1986. Spectral dependence of the diffuse attenuation coefficient of light in ocean waters. Opt. Eng. 25:471–79
     [Google Scholar]
  14. Ayalon I, Rosenberg Y, Benichou JIC, Campos CLD, Sayco SLG et al. 2020. Coral gametogenesis collapse under artificial light pollution. Curr. Biol. 31:413–19
     [Google Scholar]
  15. Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK et al. 1986. Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Mar. Biol. 90:379–94
     [Google Scholar]
  16. Baghel KK, Pati AK. 2015. Pheromones as time cues for circadian rhythms in fish. Biol. Rhythm Res. 46:659–69
     [Google Scholar]
  17. Baillon S, Hamel J-F, Mercier A. 2014. Diversity, distribution and nature of faunal associations with deep-sea pennatulacean corals in the Northwest Atlantic. PLOS ONE 9:e111519
     [Google Scholar]
  18. Baumgartner MF, Tarrant AM. 2017. The physiology and ecology of diapause in marine copepods. Annu. Rev. Mar. Sci. 9:387–411
     [Google Scholar]
  19. Berge J, Cottier F, Last KS, Varpe Ø, Leu E et al. 2009. Diel vertical migration of Arctic zooplankton during the polar night. Biol. Lett. 5:69–72
     [Google Scholar]
  20. Berge J, Geoffroy M, Daase M, Cottier F, Priou P et al. 2020. Artificial light during the polar night disrupts Arctic fish and zooplankton behaviour down to 200 m depth. Commun. Biol. 3:102
     [Google Scholar]
  21. Berge J, Renaud PE, Darnis G, Cottier F, Last K et al. 2015. In the dark: a review of ecosystem processes during the Arctic polar night. Prog. Oceanogr. 139:258–71
     [Google Scholar]
  22. Bilcke G, Osuna-Cruz CM, Silva MS, Poulsen N, Bulankova P et al. 2021. Diurnal transcript profiling of the diatom Seminavis robusta reveals adaptations to a benthic lifestyle. Plant J 107:315–36
     [Google Scholar]
  23. Biscontin A, Martini P, Costa R, Kramer A, Meyer B et al. 2019. Analysis of the circadian transcriptome of the Antarctic krill Euphausia superba. Sci. Rep. 9:13894
     [Google Scholar]
  24. Biscontin A, Wallach T, Sales G, Grudziecki A, Janke L et al. 2017. Functional characterization of the circadian clock in the Antarctic krill. Euphausia superba. Sci. Rep. 7:17742
     [Google Scholar]
  25. Blaby-Haas CE, Merchant SS 2019. Comparative and functional algal genomics. Annu. Rev. Plant Biol. 70:605–38
     [Google Scholar]
  26. Bouget F-Y, Lefranc M, Thommen Q, Pfeuty B, Lozano J-C et al. 2014. Transcriptional versus non-transcriptional clocks: a case study in Ostreococcus. Mar. Genom. 14:17–22
     [Google Scholar]
  27. Bradshaw WE, Holzapfel CM. 2001. Genetic shift in photoperiodic response correlated with global warming. PNAS 98:14509–11
     [Google Scholar]
  28. Brawley SH, Johnson LE. 1992. Gametogenesis, gametes and zygotes: an ecological perspective on sexual reproduction in the algae. Br. Phycol. J. 27:233–52
     [Google Scholar]
  29. Brenna A, Albrecht U 2020. Phosphorylation and circadian molecular timing. Front. Physiol. 11:612510
     [Google Scholar]
  30. Brierley AS. 2014. Diel vertical migration. Curr. Biol. 24:R1074–76
     [Google Scholar]
  31. Brodie J, Chan CX, De Clerck O, Cock JM, Coelho SM et al. 2017. The algal revolution. Trends Plant Sci. 22:726–38
     [Google Scholar]
  32. Brun P, Stamieszkin K, Visser AW, Licandro P, Payne MR, Kiørboe T. 2019. Climate change has altered zooplankton-fuelled carbon export in the North Atlantic. Nat. Ecol. Evol. 3:416–23
     [Google Scholar]
  33. Buhr ED, Yoo S-H, Takahashi JS. 2010. Temperature as a universal resetting cue for mammalian circadian oscillators. Science 330:379–85
     [Google Scholar]
  34. Caballes CF, Pratchett MS. 2017. Environmental and biological cues for spawning in the crown-of-thorns starfish. PLOS ONE 12:e0173964
     [Google Scholar]
  35. Chabot CC, Ramberg-Pihl NC, Watson WH 2016. Circalunidian clocks control tidal rhythms of locomotion in the American horseshoe crab, Limulus polyphemus. Mar. Freshw. Behav. Physiol. 49:75–91
     [Google Scholar]
  36. Chabot CC, Watson WH III. 2010. Circatidal rhythms of locomotion in the American horseshoe crab Limulus polyphemus: underlying mechanisms and cues that influence them. Curr. Zool. 56:499–517
     [Google Scholar]
  37. Chambault P, Fossette S, Heide-Jørgensen MP, Jouannet D, Vély M. 2021. Predicting seasonal movements and distribution of the sperm whale using machine learning algorithms. Ecol. Evol. 11:1432–45
     [Google Scholar]
  38. Chang Y, Dall'Olmo G, Schabetsberger R 2020. Tracking the marine migration routes of South Pacific silver eels. Mar. Ecol. Prog. Ser. 646:1–12
     [Google Scholar]
  39. Chen C, Buhl E, Xu M, Croset V, Rees JS et al. 2015. Drosophila Ionotropic Receptor 25a mediates circadian clock resetting by temperature. Nature 527:516–20
     [Google Scholar]
  40. Chivers WJ, Walne AW, Hays GC. 2017. Mismatch between marine plankton range movements and the velocity of climate change. Nat. Commun. 8:14434
     [Google Scholar]
  41. Choquet M, Hatlebakk M, Dhanasiri AKS, Kosobokova K, Smolina I et al. 2017. Genetics redraws pelagic biogeography of Calanus. Biol. Lett. 13:20170588
     [Google Scholar]
  42. Choquet M, Smolina I, Dhanasiri AKS, Blanco-Bercial L, Kopp K et al. 2019. Towards population genomics in non-model species with large genomes: a case study of the marine zooplankton Calanus finmarchicus. R. Soc. Open Sci. 6:180608
     [Google Scholar]
  43. Choquet M, Smolina I, Hoarau G. 2021. No evidence for hybridization in Calanus: reply to the comment by Parent et al. Limnol. Oceanogr. 66:3603–6
     [Google Scholar]
  44. Chow S, Okazaki M, Watanabe T, Segawa K, Yamamoto T et al. 2015. Light-sensitive vertical migration of the Japanese eel Anguilla japonica revealed by real-time tracking and its utilization for geolocation. PLOS ONE 10:e0121801
     [Google Scholar]
  45. Christiansen S, Titelman J, Kaartvedt S. 2019. Nighttime swimming behavior of a mesopelagic fish. Front. Mar. Sci. 6:787
     [Google Scholar]
  46. Coelho R, Fernandez-Carvalho J, Santos M. 2015. Habitat use and diel vertical migration of bigeye thresher shark: overlap with pelagic longline fishing gear. Mar. Environ. Res. 112:91–99
     [Google Scholar]
  47. Coesel SN, Durham BP, Groussman RD, Hu SK, Caron DA et al. 2021. Diel transcriptional oscillations of light-sensitive regulatory elements in open-ocean eukaryotic plankton communities. PNAS 118:e2011038118
     [Google Scholar]
  48. Coesel SN, Mangogna M, Ishikawa T, Heijde M, Rogato A et al. 2009. Diatom PtCPF1 is a new cryptochrome/photolyase family member with DNA repair and transcription regulation activity. EMBO Rep. 10:655–61
     [Google Scholar]
  49. Coffey DM, Royer MA, Meyer CG, Holland KN. 2020. Diel patterns in swimming behavior of a vertically migrating deepwater shark, the bluntnose sixgill (Hexanchus griseus). PLOS ONE 15:e0228253
     [Google Scholar]
  50. Cohen JH, Last KS, Charpentier CL, Cottier F, Daase M et al. 2021. Photophysiological cycles in Arctic krill are entrained by weak midday twilight during the Polar Night. PLOS Biol 19:e3001413
     [Google Scholar]
  51. Cohen JH, Screen JA, Furtado JC, Barlow M, Whittleston D et al. 2014. Recent Arctic amplification and extreme mid-latitude weather. Nat. Geosci. 7:627–37
     [Google Scholar]
  52. Connor KM, Gracey AY. 2011. Circadian cycles are the dominant transcriptional rhythm in the intertidal mussel Mytilus californianus. PNAS 108:16110–15
     [Google Scholar]
  53. Conover RJ. 1965. Notes on the molting cycle, development of sexual characters and sex ratio in Calanus hyperboreus. Crustaceana 8:308–20
     [Google Scholar]
  54. Corellou F, Schwartz C, Motta J-P, Djouani-Tahri EB, Sanchez F, Bouget F-Y. 2009. Clocks in the green lineage: comparative functional analysis of the circadian architecture of the picoeukaryote Ostreococcus. Plant Cell 21:3436–49
     [Google Scholar]
  55. Courties C, Vaquer A, Troussellier M, Lautier J. 1994. Smallest eukaryotic organism. Nature 370:255
     [Google Scholar]
  56. Creux N, Harmer S. 2019. Circadian rhythms in plants. Cold Spring Harb. Perspect. Biol. 11:a034611
     [Google Scholar]
  57. Cuvelier D, Legendre P, Laës-Huon A, Sarradin P-M, Sarrazin J. 2017. Biological and environmental rhythms in (dark) deep-sea hydrothermal ecosystems. Biogeosciences 14:2955–77
     [Google Scholar]
  58. d'Alcalà MR, Conversano F, Corato F, Licandro P, Mangoni O et al. 2004. Seasonal patterns in plankton communities in a pluriannual time series at a coastal Mediterranean site (Gulf of Naples): an attempt to discern recurrences and trends. Sci. Mar. 68:S165–83
     [Google Scholar]
  59. D'Alelio D, d'Alcalà MR, Dubroca L, Sarn D, Zingone A, Montresor M. 2010. The time for sex: a biennial life cycle in a marine planktonic diatom. Limnol. Oceanogr. 55:106–14
     [Google Scholar]
  60. Davies TW, Duffy JP, Bennie J, Gaston KJ 2014. The nature, extent, and ecological implications of marine light pollution. Front. Ecol. Environ. 12:347–55
     [Google Scholar]
  61. de Lima CDM, Göndör A. 2018. Circadian organization of the genome. Science 359:1212–13
     [Google Scholar]
  62. De Pontual H, Jolivet A, Bertignac M, Fablet R. 2012. Diel vertical migration of European hake Merluccius merluccius and associated temperature histories: insights from a pilot data-storage tagging (DST) experiment. J. Fish Biol. 81:728–34
     [Google Scholar]
  63. Deagle BE, Faux C, Kawaguchi S, Meyer B, Jarman SN. 2015. Antarctic krill population genomics: apparent panmixia, but genome complexity and large population size muddy the water. Mol. Ecol. 24:4943–59
     [Google Scholar]
  64. Deutsch C, Ferrel A, Seibel B, Pörtner H-O, Huey RB. 2015. Climate change tightens a metabolic constraint on marine habitats. Science 348:1132–35
     [Google Scholar]
  65. Dixson DL, Munday PL, Jones GP. 2010. Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol. Lett. 13:68–75
     [Google Scholar]
  66. Dodd AN, Salathia N, Hall A, Kévei E, Tóth R et al. 2005. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–33
     [Google Scholar]
  67. Ducklow HW, Baker K, Martinson DG, Quetin LB, Ross RM et al. 2007. Marine pelagic ecosystems: the West Antarctic Peninsula. Philos. Trans. R. Soc. B 362:67–94
     [Google Scholar]
  68. Durant JM, Molinero J-C, Ottersen G, Reygondeau G, Stige LC, Langangen Ø. 2019. Contrasting effects of rising temperatures on trophic interactions in marine ecosystems. Sci. Rep. 9:15213
     [Google Scholar]
  69. Dypvik E, Klevjer TA, Kaartvedt S. 2012a. Inverse vertical migration and feeding in glacier lanternfish (Benthosema glaciale). Mar. Biol. 159:443–53
     [Google Scholar]
  70. Dypvik E, Røstad A, Kaartvedt S. 2012b. Seasonal variations in vertical migration of glacier lanternfish, Benthosema glaciale. Mar. Biol. 159:1673–83
     [Google Scholar]
  71. Edgar RS, Green EW, Zhao Y, van Ooijen G, Olmedo M et al. 2012. Peroxiredoxins are conserved markers of circadian rhythms. Nature 485:459–64
     [Google Scholar]
  72. Elowe C, Tomanek L. 2021. Circadian and circatidal rhythms of protein abundance in the California mussel (Mytilus californianus). Mol. Ecol. 30:5151–63
     [Google Scholar]
  73. Enright JT. 1976. Plasticity in an isopod's clockworks: Shaking shapes form and affects phase and frequency. J. Comp. Physiol. 107:13–37
     [Google Scholar]
  74. Evans WG. 1976. Circadian and circatidal locomotory rhythms in the intertidal beetle Thalassotrechus barbarae (Horn): Carabidae. J. Exp. Mar. Biol. Ecol. 22:79–90
     [Google Scholar]
  75. Fabry VJ, McClintock JB, Mathis JT, Grebmeier J. 2009. Ocean acidification at high latitudes: the bellwether. Oceanography 22:4160–71
     [Google Scholar]
  76. Falciatore A, Jaubert M, Bouly J-P, Bailleul B, Mock T. 2020. Diatom molecular research comes of age: model species for studying phytoplankton biology and diversity. Plant Cell 32:547–72
     [Google Scholar]
  77. Falk-Petersen S, Mayzaud P, Kattner G, Sargent JR. 2009. Lipids and life strategy of Arctic Calanus. Mar. Biol. Res. 5:18–39
     [Google Scholar]
  78. Farré EM. 2020. The brown clock: circadian rhythms in stramenopiles. Physiol. Plant. 169:430–41
     [Google Scholar]
  79. Feng Z, Ji R, Ashjian C, Campbell R, Zhang J 2017. Biogeographic responses of the copepod Calanus glacialis to a changing Arctic marine environment. Glob. Change Biol. 24:e159–70
     [Google Scholar]
  80. Field CB, Behrenfeld MJ, Randerson JT, Falkowski P. 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–40
     [Google Scholar]
  81. Fogarty ND, Marhaver KL. 2019. Coral spawning, unsynchronized. Science 365:987–88
     [Google Scholar]
  82. Fortier M, Fortier L, Hattori H, Saito H, Legendre L. 2001. Visual predators and the diel vertical migration of copepods under Arctic sea ice during the midnight sun. J. Plankton Res. 23:1263–78
     [Google Scholar]
  83. Fortunato AE, Jaubert M, Enomoto G, Bouly J-P, Raniello R et al. 2016. Diatom phytochromes reveal the existence of far-red-light-based sensing in the ocean. Plant Cell 28:616–28
     [Google Scholar]
  84. Foster WA, Moreton RB. 1981. Synchronization of activity rhythms with the tide in a saltmarsh collembolan Anurida maritima. Oecologia 50:265–70
     [Google Scholar]
  85. Fulton J. 1973. Some aspects of the life history of Calanus plumchrus in the Strait of Georgia. J. Fish. Res. Board Can. 30:811–15
     [Google Scholar]
  86. Fung-Uceda J, Lee K, Seo PJ, Polyn S, De Veylder L, Mas P. 2018. The circadian clock sets the time of DNA replication licensing to regulate growth in Arabidopsis. Dev. Cell 45:101–113.e4
     [Google Scholar]
  87. Gardner JPA. 1997. Hybridization in the sea. Advances in Marine Biology, Vol. 31 JHS Blaxter, AJ Southward 1–78 San Diego, CA: Academic
     [Google Scholar]
  88. Garrett C. 2003. Internal tides and ocean mixing. Science 301:1858–59
     [Google Scholar]
  89. Gekakis N. 1998. Role of the CLOCK protein in the mammalian circadian mechanism. Science 280:1564–69
     [Google Scholar]
  90. Gerkema MP, Davies WIL, Foster RG, Menaker M, Hut RA. 2013. The nocturnal bottleneck and the evolution of activity patterns in mammals. Proc. R. Soc. B 280:20130508
     [Google Scholar]
  91. Gilly WF, Markaida U, Baxter CH, Block BA, Boustany A et al. 2006. Vertical and horizontal migrations by the jumbo squid Dosidicus gigas revealed by electronic tagging. Mar. Ecol. Prog. Ser. 324:1–17
     [Google Scholar]
  92. Goldman B, Gwinner E, Karsch FJ, Saunders D, Zucker I, Gall GF. 2004. Circannual rhythms and photoperiodism. Chronobiology: Biological Timekeeping JC Dunlap, JJ Loros, PJ DeCoursey 107–42 Sunderland, MA: Sinauer
     [Google Scholar]
  93. Häfker NS, Meyer B, Last KS, Pond DW, Hüppe L, Teschke M. 2017. Circadian clock involvement in zooplankton diel vertical migration. Curr. Biol. 27:2194–201.e3
     [Google Scholar]
  94. Häfker NS, Teschke M, Hüppe L, Meyer B. 2018a. Calanus finmarchicus diel and seasonal rhythmicity in relation to endogenous timing under extreme polar photoperiods. Mar. Ecol. Prog. Ser. 603:79–92
     [Google Scholar]
  95. Häfker NS, Teschke M, Last KS, Pond DW, Hüppe L, Meyer B. 2018b. Calanus finmarchicus seasonal cycle and diapause in relation to gene expression, physiology, and endogenous clocks. Limnol. Oceanogr. 63:2815–38
     [Google Scholar]
  96. Häfker NS, Tessmar-Raible K. 2020. Rhythms of behavior: Are the times changin’?. Curr. Opin. Neurobiol. 60:55–66
     [Google Scholar]
  97. Hairston NG, Kearns CM. 1995. The interaction of photoperiod and temperature in diapause timing: a copepod example. Biol. Bull. 189:42–48
     [Google Scholar]
  98. Hastings JW. 2007. The Gonyaulax clock at 50: translational control of circadian expression. Cold Spring Harb. Symp. Quant. Biol. 72:141–44
     [Google Scholar]
  99. Hastings JW, Sweeney BM. 1957. On the mechanism of temperature independence in a biological clock. PNAS 43:804–11
     [Google Scholar]
  100. Hauenschild C. 1960. Lunar periodicity. Cold Spring Harb. Symp. Quant. Biol. 25:491–97
     [Google Scholar]
  101. Haydon MJ, Mielczarek O, Frank A, Román Á, Webb AAR. 2017. Sucrose and ethylene signaling interact to modulate the circadian clock. Plant Physiol 175:947–58
     [Google Scholar]
  102. Heijde M, Zabulon G, Corellou F, Ishikawa T, Brazard J et al. 2010. Characterization of two members of the cryptochrome/photolyase family from Ostreococcus tauri provides insights into the origin and evolution of cryptochromes. Plant Cell Environ 33:1614–26
     [Google Scholar]
  103. Hendricks WD, Byrum CA, Meyer-Bernstein EL. 2012. Characterization of circadian behavior in the starlet sea anemone, Nematostella vectensis. PLOS ONE 7:e46843
     [Google Scholar]
  104. Hewson-Browne RC. 1973. Magnetic effects of sea tides. Phys. Earth Planet. Inter. 7:167–86
     [Google Scholar]
  105. Hölker F, Bolliger J, Davies TW, Giavi S, Jechow A et al. 2021. 11 pressing research questions on how light pollution affects biodiversity. Front. Ecol. Evol. 9:896
     [Google Scholar]
  106. Höring F, Biscontin A, Harms L, Sales G, Reiss CS et al. 2021. Seasonal gene expression profiling of Antarctic krill in three different latitudinal regions. Mar. Genom. 56:100806
     [Google Scholar]
  107. Höring F, Teschke M, Suberg L, Kawaguchi S, Meyer B. 2018. Light regime affects the seasonal cycle of Antarctic krill (Euphausia superba): impacts on growth, feeding, lipid metabolism, and maturity. Can. J. Zool. 96:1203–13
     [Google Scholar]
  108. Horn M, Mitesser O, Hovestadt T, Yoshii T, Rieger D, Helfrich-Förster C. 2019. The circadian clock improves fitness in the fruit fly, Drosophila melanogaster. Front. Physiol. 10:1374
     [Google Scholar]
  109. Howard EM, Penn JL, Frenzel H, Seibel BA, Bianchi D et al. 2020. Climate-driven aerobic habitat loss in the California Current System. Sci. Adv. 6:eaay3188
     [Google Scholar]
  110. Huffeldt NP. 2020. Photic barriers to poleward range-shifts. Trends Ecol. Evol. 35:652–55
     [Google Scholar]
  111. Hughes AR, Hanley TC, Moore AF, Ramsay-Newton C, Zerebecki RA, Sotka EE. 2019. Predicting the sensitivity of marine populations to rising temperatures. Front. Ecol. Environ. 17:17–24
     [Google Scholar]
  112. Hui M, Song C, Liu Y, Li C, Cui Z. 2017. Exploring the molecular basis of adaptive evolution in hydrothermal vent crab Austinograea alayseae by transcriptome analysis. PLOS ONE 12:e0178417
     [Google Scholar]
  113. Hunt BJ. 2016. Advancing molecular crustacean chronobiology through the characterisation of the circadian clock in two malacostracan species Euphausia superba and Parhyale hawaiensis. PhD Thesis Univ. Leicester Liecester, UK:
  114. Hüppe L, Payton L, Last K, Wilcockson D, Ershova E, Meyer B. 2020. Evidence for oscillating circadian clock genes in the copepod Calanus finmarchicus during the summer solstice in the high Arctic. Biol. Lett. 16:20200257
     [Google Scholar]
  115. IPCC (Intergov. Panel Clim. Change) 2014. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change Geneva, Switz: IPCC
  116. Jenouvrier S, Caswell H, Barbraud C, Holland M, Strøeve J, Weimerskirch H. 2009. Demographic models and IPCC climate projections predict the decline of an emperor penguin population. PNAS 106:1844–47
     [Google Scholar]
  117. Jesus TF, Moreno JM, Repolho T, Athanasiadis A, Rosa R et al. 2017. Protein analysis and gene expression indicate differential vulnerability of Iberian fish species under a climate change scenario. PLOS ONE 12:e0181325
     [Google Scholar]
  118. Johnson CH, Golden SS. 1999. Circadian programs in cyanobacteria: adaptiveness and mechanism. Annu. Rev. Microbiol. 53:389–409
     [Google Scholar]
  119. Jónasdóttir SH, Visser AW, Richardson K, Heath MR. 2015. Seasonal copepod lipid pump promotes carbon sequestration in the deep North Atlantic. PNAS 112:12122–26
     [Google Scholar]
  120. Jorda G, Marbà N, Bennett S, Santana-Garcon J, Agusti S, Duarte CM. 2020. Ocean warming compresses the three-dimensional habitat of marine life. Nat. Ecol. Evol. 4:109–14
     [Google Scholar]
  121. Kaartvedt S. 2010. Diel vertical migration behaviour of the northern krill (Meganyctiphanes norvegica Sars). Advances in Marine Biology, Vol. 57 GA Tarling 255–75 San Diego, CA: Academic
     [Google Scholar]
  122. Kaartvedt S, Titelman J. 2018. Planktivorous fish in a future Arctic Ocean of changing ice and unchanged photoperiod. ICES J. Mar. Sci. 75:2312–18
     [Google Scholar]
  123. Kahru M, Brotas V, Manzano-Sarabia M, Mitchell BG. 2010. Are phytoplankton blooms occurring earlier in the Arctic?. Glob. Change Biol. 17:1733–39
     [Google Scholar]
  124. Kaiser TS, Neumann D, Heckel DG, Berendonk TU. 2010. Strong genetic differentiation and postglacial origin of populations in the marine midge Clunio marinus (Chironomidae, Diptera). Mol. Ecol. 19:2845–57
     [Google Scholar]
  125. Kaiser TS, Neumann J. 2021. Circalunar clocks—old experiments for a new era. BioEssays 43:2100074
     [Google Scholar]
  126. Kaiser TS, Poehn B, Szkiba D, Preussner M, Sedlazeck FJ et al. 2016. The genomic basis of circadian and circalunar timing adaptations in a midge. Nature 540:69–73
     [Google Scholar]
  127. Kaiser TS, von Haeseler A, Tessmar-Raible K, Heckel DG. 2021. Timing strains of the marine insect Clunio marinus diverged and persist with gene flow. Mol. Ecol. 30:1264–80
     [Google Scholar]
  128. Keith SA, Maynard JA, Edwards AJ, Guest JR, Bauman AG et al. 2016. Coral mass spawning predicted by rapid seasonal rise in ocean temperature. Proc. R. Soc. B 283:20160011
     [Google Scholar]
  129. Kolody BC, McCrow JP, Allen LZ, Aylward FO, Fontanez KM et al. 2019. Diel transcriptional response of a California Current plankton microbiome to light, low iron, and enduring viral infection. ISME J 13:2817–33
     [Google Scholar]
  130. Krittika S, Yadav P. 2020. Circadian clocks: an overview on its adaptive significance. Biol. Rhythm Res. 51:1109–32
     [Google Scholar]
  131. Lambert S, Tragin M, Lozano J-C, Ghiglione J-F, Vaulot D et al. 2019. Rhythmicity of coastal marine picoeukaryotes, bacteria and archaea despite irregular environmental perturbations. ISME J 13:388–401
     [Google Scholar]
  132. Last KS, Bailhache T, Kramer C, Kyriacou CP, Rosato E, Olive PJW 2009. Tidal, daily, and lunar-day activity cycles in the marine polychaete Nereis virens. Chronobiol. Int. 26:167–83
     [Google Scholar]
  133. Last KS, Häfker NS, Hendrick VJ, Meyer B, Tran D, Piccolin F 2020. Biological clocks and rhythms in polar organisms. Polar Night Marine Ecology: Life and Light in the Dead of Night J Berge, G Johnsen, JH Cohen 217–40 Cham, Switz: Springer
     [Google Scholar]
  134. Last KS, Hobbs L, Berge J, Brierley AS, Cottier F. 2016. Moonlight drives ocean-scale mass vertical migration of zooplankton during the Arctic winter. Curr. Biol. 26:244–51
     [Google Scholar]
  135. Leach WB, Reitzel AM. 2020. Decoupling behavioral and transcriptional responses to color in an eyeless cnidarian. BMC Genom. 21:361
     [Google Scholar]
  136. Lenz PH, Roncalli V. 2019. Diapause within the context of life-history strategies in calanid copepods (Calanoida: Crustacea). Biol. Bull. 237:170–79
     [Google Scholar]
  137. Levy O, Appelbaum L, Leggat W, Gothlif Y, Hayward DC et al. 2007. Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora. Science 318:467–70
     [Google Scholar]
  138. Liberman R, Fine M, Benayahu Y. 2021. Simulated climate change scenarios impact the reproduction and early life stages of a soft coral. Mar. Environ. Res. 163:105215
     [Google Scholar]
  139. Maor R, Dayan T, Ferguson-Gow H, Jones KE. 2017. Temporal niche expansion in mammals from a nocturnal ancestor after dinosaur extinction. Nat. Ecol. Evol. 1:1889–95
     [Google Scholar]
  140. Mat AM, Massabuau J-C, Ciret P, Tran D. 2014. Looking for the clock mechanism responsible for circatidal behavior in the oyster Crassostrea gigas. Mar. Biol. 161:89–99
     [Google Scholar]
  141. Mat AM, Sarrazin J, Markov GV, Apremont V, Dubreuil C et al. 2020. Biological rhythms in the deep-sea hydrothermal mussel Bathymodiolus azoricus. Nat. Commun. 11:3454
     [Google Scholar]
  142. Matrai P, Thompson B, Keller M. 2005. Circannual excystment of resting cysts of Alexandrium spp. from eastern Gulf of Maine populations. Deep-Sea Res. II 52:2560–68
     [Google Scholar]
  143. Matsuo T. 2003. Control mechanism of the circadian clock for timing of cell division in vivo. Science 302:255–59
     [Google Scholar]
  144. Mehta TS, Lewis RD. 2000. Quantitative tests of a dual circalunidian clock model for tidal rhythmicity in the sand beach isopod Cirolana cookii. Chronobiol. Int. 17:29–41
     [Google Scholar]
  145. Melle W, Runge J, Head E, Plourde S, Castellani C et al. 2014. The North Atlantic Ocean as habitat for Calanus finmarchicus: environmental factors and life history traits. Prog. Oceanogr. 129:244–84
     [Google Scholar]
  146. Menegazzi P, Dalla Benetta E, Beauchamp M, Schlichting M, Steffan-Dewenter I, Helfrich-Förster C 2017. Adaptation of circadian neuronal network to photoperiod in high-latitude European drosophilids. Curr. Biol. 27:833–39
     [Google Scholar]
  147. Mercier A, Sun Z, Baillon S, Hamel J-F. 2011. Lunar rhythms in the deep sea: evidence from the reproductive periodicity of several marine invertebrates. J. Biol. Rhythms 26:82–86
     [Google Scholar]
  148. Mergenhagen D, Schweiger HG. 1975. Circadian rhythm of oxygen evolution in cell fragments of Acetabularia mediterranea. Exp. Cell. Res. 92:127–30
     [Google Scholar]
  149. Meyer B, Freier U, Grimm V, Groeneveld J, Hunt BPV et al. 2017. The winter pack-ice zone provides a sheltered but food-poor habitat for larval Antarctic krill. Nat. Ecol. Evol. 1:1853–61
     [Google Scholar]
  150. Mitbavkar S, Anil AC. 2004. Vertical migratory rhythms of benthic diatoms in a tropical intertidal sand flat: influence of irradiance and tides. Mar. Biol. 145:9–20
     [Google Scholar]
  151. Mittag M, Lee DH, Hastings JW. 1994. Circadian expression of the luciferin-binding protein correlates with the binding of a protein to the 3′ untranslated region of its mRNA. PNAS 91:5257–61
     [Google Scholar]
  152. Miyagishima S, Fujiwara T, Sumiya N, Hirooka S, Nakano A et al. 2014. Translation-independent circadian control of the cell cycle in a unicellular photosynthetic eukaryote. Nat. Commun. 5:3807
     [Google Scholar]
  153. Montanari SR, Hobbs J-PA, Pratchett MS, van Herwerden L. 2016. The importance of ecological and behavioural data in studies of hybridisation among marine fishes. Rev. Fish Biol. Fish. 26:181–98
     [Google Scholar]
  154. Morse D, Milos PM, Roux E, Hastings JW. 1989a. Circadian regulation of bioluminescence in Gonyaulax involves translational control. PNAS 86:172–76
     [Google Scholar]
  155. Morse D, Pappenheimer AM, Hastings JW. 1989b. Role of a luciferin-binding protein in the circadian bioluminescent reaction of Gonyaulax polyedra. J. Biol. Chem. 264:11822–26
     [Google Scholar]
  156. Moum JN. 2021. Variations in ocean mixing from seconds to years. Annu. Rev. Mar. Sci. 13:201–26
     [Google Scholar]
  157. Muller EB, Kooijman SALM, Edmunds PJ, Doyle FJ, Nisbet RM. 2009. Dynamic energy budgets in syntrophic symbiotic relationships between heterotrophic hosts and photoautotrophic symbionts. J. Theor. Biol. 259:44–57
     [Google Scholar]
  158. Narasimamurthy R, Virshup DM. 2021. The phosphorylation switch that regulates ticking of the circadian clock. Mol. Cell 81:1133–46
     [Google Scholar]
  159. Naylor E. 1996. Crab clockwork: the case for interactive circatidal and circadian oscillators controlling rhythmic locomotor activity of Carcinus maenas. Chronobiol. Int. 13:153–61
     [Google Scholar]
  160. Naylor E. 2010. Chronobiology of Marine Organisms Cambridge, UK: Cambridge Univ. Press
  161. Neumann D. 1966. Die lunare und tägliche Schlüpfperiodik der Mücke Clunio: Steuerung und Abstimmung auf die Gezeitenperiodik. Z. Vgl. Physiol. 53:1–61
     [Google Scholar]
  162. Neumann D. 1967. Genetic adaptation in emergence time of Clunio populations to different tidal conditions. Helgol. Wiss. Meeresunters. 15:163–71
     [Google Scholar]
  163. Neumann D. 1968. Die Steuerung einer semilunaren Schlüpfperiodik mit Hilfe eines künstlichen Gezeitenzyklus. Z. Vgl. Physiol. 60:63–78
     [Google Scholar]
  164. Neumann D 1988. The timing of reproduction to distinct spring tide situations in the intertidal insect Clunio. Behavioral Adaptation to Intertidal Life G Chelazzi, M Vannini 45–54 Boston: Springer
     [Google Scholar]
  165. Nichol DG, Kotwicki S, Zimmermann M. 2013. Diel vertical migration of adult Pacific cod Gadus macrocephalus in Alaska. J. Fish Biol. 83:170–89
     [Google Scholar]
  166. Niehoff B, Madsen S, Hansen B, Nielsen T. 2002. Reproductive cycles of three dominant Calanus species in Disko Bay, West Greenland. Mar. Biol. 140:567–76
     [Google Scholar]
  167. Oldach MJ, Workentine M, Matz MV, Fan T-Y, Vize PD. 2017. Transcriptome dynamics over a lunar month in a broadcast spawning acroporid coral. Mol. Ecol. 26:2514–26
     [Google Scholar]
  168. Omand MM, Steinberg DK, Stamieszkin K. 2021. Cloud shadows drive vertical migrations of deep-dwelling marine life. PNAS 118:e2022977118
     [Google Scholar]
  169. O'Neill JS, Lee KD, Zhang L, Feeney K, Webster SG et al. 2015. Metabolic molecular markers of the tidal clock in the marine crustacean Eurydice pulchra. Curr. Biol. 25:R326–27
     [Google Scholar]
  170. O'Neill JS, van Ooijen G, Dixon LE, Troein C, Corellou F et al. 2011. Circadian rhythms persist without transcription in a eukaryote. Nature 469:554–58
     [Google Scholar]
  171. Oren M, Tarrant AM, Alon S, Simon-Blecher N, Elbaz I et al. 2015. Profiling molecular and behavioral circadian rhythms in the non-symbiotic sea anemone Nematostella vectensis. Sci. Rep. 5:11418
     [Google Scholar]
  172. Palmer JD. 1991. Contributions made to chronobiology by studies of fiddler crab rhythms. Chronobiol. Int. 8:110–30
     [Google Scholar]
  173. Palmer JD. 2000. The clocks controlling the tide-associated rhythms of intertidal animals. BioEssays 22:32–37
     [Google Scholar]
  174. Payton L, Noirot C, Hoede C, Hüppe L, Last K et al. 2020. Daily transcriptomes of the copepod Calanus finmarchicus during the summer solstice at high Arctic latitudes. Sci. Data 7:415
     [Google Scholar]
  175. Peijnenburg KTCA, Goetze E. 2013. High evolutionary potential of marine zooplankton. Ecol. Evol. 3:2765–81
     [Google Scholar]
  176. Perrigault M, Andrade H, Bellec L, Ballantine C, Camus L, Tran D. 2020. Rhythms during the polar night: evidence of clock-gene oscillations in the Arctic scallop Chlamys islandica. Proc. R. Soc. B 287:20201001
     [Google Scholar]
  177. Perrigault M, Tran D. 2017. Identification of the molecular clockwork of the oyster Crassostrea gigas. PLOS ONE 12:e0169790
     [Google Scholar]
  178. Petersen J, Rredhi A, Szyttenholm J, Mittag M. 2022. Evolution of circadian clocks along the green lineage. Plant Physiol 190:924–37
     [Google Scholar]
  179. Pfeuty B, Thommen Q, Corellou F, Djouani-Tahri EB, Bouget F-Y, Lefranc M. 2012. Circadian clocks in changing weather and seasons: lessons from the picoalga Ostreococcus tauri. BioEssays 34:781–90
     [Google Scholar]
  180. Piccolin F, Meyer B, Biscontin A, De Pittà C, Kawaguchi S, Teschke M. 2018. Photoperiodic modulation of circadian functions in Antarctic krill Euphausia superba Dana, 1850 (Euphausiacea). J. Crustac. Biol. 38:707–15
     [Google Scholar]
  181. Piccolin F, Pitzschler L, Biscontin A, Kawaguchi S, Meyer B. 2020. Circadian regulation of diel vertical migration (DVM) and metabolism in Antarctic krill Euphausia superba. Sci. Rep. 10:16796
     [Google Scholar]
  182. Poehn B, Krishnan S, Zurl M, Coric A, Rokvic D et al. 2022. A Cryptochrome adopts distinct moon- and sunlight states and functions as sun- versus moonlight interpreter in monthly oscillator entrainment. Nat. Commun. 13:5220
     [Google Scholar]
  183. Poliner E, Cummings C, Newton L, Farré EM 2019. Identification of circadian rhythms in Nannochloropsis species using bioluminescence reporter lines. Plant J. 99:112–27
     [Google Scholar]
  184. Provan J, Beatty GE, Keating SL, Maggs CA, Savidge G. 2009. High dispersal potential has maintained long-term population stability in the North Atlantic copepod Calanus finmarchicus. Proc. R. Soc. B 276:301–7
     [Google Scholar]
  185. Pülmanns N, Castellanos-Galindo GA, Krumme U. 2018. Tidal-diel patterns in feeding and abundance of armed snook Centropomus armatus from macrotidal mangrove creeks of the tropical eastern Pacific Ocean. J. Fish Biol. 93:850–59
     [Google Scholar]
  186. Raible F, Takekata H, Tessmar-Raible K. 2017. An overview of monthly rhythms and clocks. Front. Neurol. 8:189
     [Google Scholar]
  187. Ramos AP, Gustafsson O, Labert N, Salecker I, Nilsson D-E, Averof M. 2019. Analysis of the genetically tractable crustacean Parhyale hawaiensis reveals the organisation of a sensory system for low-resolution vision. BMC Biol 17:67
     [Google Scholar]
  188. Régnier T, Gibb FM, Wright PJ. 2019. Understanding temperature effects on recruitment in the context of trophic mismatch. Sci. Rep. 9:15179
     [Google Scholar]
  189. Renaud PE, Daase M, Banas NS, Gabrielsen TM, Søreide JE et al. 2018. Pelagic food-webs in a changing Arctic: a trait-based perspective suggests a mode of resilience. ICES J. Mar. Sci. 75:1871–81
     [Google Scholar]
  190. Reynolds C. 2006. Ecology of Phytoplankton Cambridge, UK: Cambridge Univ. Press
  191. Rock A, Wilcockson D, Last KS. 2022. Towards an understanding of circatidal clocks. Front. Physiol. 13:830107
     [Google Scholar]
  192. Roenneberg T, Colfax GN, Hastings JW. 1989. A circadian rhythm of population behavior in Gonyaulax polyedra. J. Biol. Rhythms 4:89–104
     [Google Scholar]
  193. Roenneberg T, Hastings JW. 1988. Two photoreceptors control the circadian clock of a unicellular alga. Sci. Nat. 75:206–7
     [Google Scholar]
  194. Roenneberg T, Morse D. 1993. Two circadian oscillators in one cell. Nature 362:362–64
     [Google Scholar]
  195. Rosa R, Seibel BA. 2008. Synergistic effects of climate-related variables suggest future physiological impairment in a top oceanic predator. PNAS 105:20776–80
     [Google Scholar]
  196. Round FE, Palmer JD. 1966. Persistent, vertical-migration rhythms in benthic microflora: II. Field and laboratory studies on diatoms from the banks of the River Avon. J. Mar. Biol. Assoc. UK 46:191–214
     [Google Scholar]
  197. Saikkonen K, Taulavuori K, Hyvönen T, Gundel PE, Hamilton CE et al. 2012. Climate change-driven species’ range shifts filtered by photoperiodism. Nat. Clim. Change 2:239–42
     [Google Scholar]
  198. Saini R, Jaskolski M, Davis SJ. 2019. Circadian oscillator proteins across the kingdoms of life: structural aspects. BMC Biol 17:13
     [Google Scholar]
  199. Sanchez A, Shin J, Davis SJ. 2011. Abiotic stress and the plant circadian clock. Plant Signal. Behav. 6:223–31
     [Google Scholar]
  200. Satoh A. 2017. Constant light disrupts the circadian but not the circatidal rhythm in mangrove crickets. Biol. Rhythm Res. 48:459–63
     [Google Scholar]
  201. Satoh A, Momoshita H, Hori M. 2006. Circatidal rhythmic behaviour in the coastal tiger beetle Callytron inspecularis in Japan. Biol. Rhythm Res. 37:147–55
     [Google Scholar]
  202. Satoh A, Terai Y. 2019. Circatidal gene expression in the mangrove cricket Apteronemobius asahinai. Sci. Rep. 9:3719
     [Google Scholar]
  203. Satoh A, Yoshioka E, Numata H. 2008. Circatidal activity rhythm in the mangrove cricket Apteronemobius asahinai. Biol. Lett. 4:233–36
     [Google Scholar]
  204. Schneck DT, Barreto FS. 2020. Phenotypic variation in growth and gene expression under different photoperiods in allopatric populations of the copepod Tigriopus californicus. Biol. Bull. 238:106–18
     [Google Scholar]
  205. Schnytzer Y, Simon-Blecher N, Li J, Ben-Asher HW, Salmon-Divon M et al. 2018. Tidal and diel orchestration of behaviour and gene expression in an intertidal mollusc. Sci. Rep. 8:4917
     [Google Scholar]
  206. Schunter C, Welch MJ, Nilsson GE, Rummer JL, Munday PL, Ravasi T. 2018. An interplay between plasticity and parental phenotype determines impacts of ocean acidification on a reef fish. Nat. Ecol. Evol. 2:334–42
     [Google Scholar]
  207. Schunter C, Welch MJ, Ryu T, Zhang H, Berumen ML et al. 2016. Molecular signatures of transgenerational response to ocean acidification in a species of reef fish. Nat. Clim. Change 6:1014–18
     [Google Scholar]
  208. Seibel BA, Häfker NS, Trübenbach K, Zhang J, Tessier SN et al. 2014. Metabolic suppression during protracted exposure to hypoxia in the jumbo squid, Dosidicus gigas, living in an oxygen minimum zone. J. Exp. Biol. 217:2555–68
     [Google Scholar]
  209. Sims DW, Southall EJ, Tarling GA, Metcalfe JD. 2005. Habitat-specific normal and reverse diel vertical migration in the plankton-feeding basking shark. J. Anim. Ecol. 74:755–61
     [Google Scholar]
  210. Søreide JE, Leu E, Berge J, Graeve M, Falk-Petersen S. 2010. Timing of blooms, algal food quality and Calanus glacialis reproduction and growth in a changing Arctic. Glob. Change Biol. 16:3154–63
     [Google Scholar]
  211. Sorek M, Díaz-Almeyda EM, Medina M, Levy O. 2014. Circadian clocks in symbiotic corals: the duet between Symbiodinium algae and their coral host. Mar. Genom. 14:47–57
     [Google Scholar]
  212. Sorek M, Levy O. 2012. Influence of the quantity and quality of light on photosynthetic periodicity in coral endosymbiotic algae. PLOS ONE 7:e43264
     [Google Scholar]
  213. Sorek M, Schnytzer Y, Waldman Ben-Asher H, Caspi VC, Chen C-S et al. 2018. Setting the pace: host rhythmic behaviour and gene expression patterns in the facultatively symbiotic cnidarian Aiptasia are determined largely by Symbiodinium. Microbiome 6:83
     [Google Scholar]
  214. Sorek M, Yacobi YZ, Roopin M, Berman-Frank I, Levy O. 2013. Photosynthetic circadian rhythmicity patterns of Symbiodium, the coral endosymbiotic algae. Proc. R. Soc. B 280:20122942
     [Google Scholar]
  215. Sournia A. 1975. Circadian periodicities in natural populations of marine phytoplankton. Advances in Marine Biology, Vol. 12 FS Russell, M Yonge 325–89 London: Academic
     [Google Scholar]
  216. Spoelstra K, Wikelski M, Daan S, Loudon ASI, Hau M. 2016. Natural selection against a circadian clock gene mutation in mice. PNAS 113:686–91
     [Google Scholar]
  217. Stevenson TJ, Lincoln GA 2017. Epigenetic mechanisms regulating circannual rhythms. Biological Timekeeping: Clocks, Rhythms and Behaviour V Kumar 607–23 New Delhi: Springer
     [Google Scholar]
  218. Stramma L, Prince ED, Schmidtko S, Luo J, Hoolihan JP et al. 2012. Expansion of oxygen minimum zones may reduce available habitat for tropical pelagic fishes. Nat. Clim. Change 2:33–37
     [Google Scholar]
  219. Strelkov P, Nikula R, Väinölä R. 2007. Macoma balthica in the White and Barents Seas: properties of a widespread marine hybrid swarm (Mollusca: Bivalvia). Mol. Ecol. 16:4110–27
     [Google Scholar]
  220. Strömberg J-O, Spicer JI, Liljebladh B, Thomasson MA. 2002. Northern krill, Meganyctiphanes norvegica, come up to see the last eclipse of the millennium?. J. Mar. Biol. Assoc. UK 82:919–20
     [Google Scholar]
  221. Sweeney BM, Hastings JW. 1958. Rhythmic cell division in populations of Gonyaulax polyedra. J. Protozool. 5:217–24
     [Google Scholar]
  222. Sweeney BM, Haxo FT. 1961. Persistence of a photosynthetic rhythm in enucleated Acetabularia. Science 134:1361–63
     [Google Scholar]
  223. Sweeney BM, Tuffli CF, Rubin RH. 1967. The circadian rhythm in photosynthesis in Acetabularia in the presence of actinomycin D, puromycin, and chloramphenicol. J. Gen. Physiol. 50:647–59
     [Google Scholar]
  224. Takekata H, Matsuura Y, Goto SG, Satoh A, Numata H. 2012. RNAi of the circadian clock gene period disrupts the circadian rhythm but not the circatidal rhythm in the mangrove cricket. Biol. Lett. 8:488–91
     [Google Scholar]
  225. Takekata H, Numata H, Shiga S, Goto SG. 2014. Silencing the circadian clock gene Clock using RNAi reveals dissociation of the circatidal clock from the circadian clock in the mangrove cricket. J. Insect Physiol. 68:16–22
     [Google Scholar]
  226. Tankersley RA, Bullock TM, Forward RB, Rittschof D. 2002. Larval release behaviors in the blue crab Callinectes sapidus: role of chemical cues. J. Exp. Mar. Biol. Ecol. 273:1–14
     [Google Scholar]
  227. Tarling GA, Buchholz F, Matthews JBL. 1999. The effect of a lunar eclipse on the vertical migration behaviour of Meganyctiphanes norvegica (Crustacea: Euphausiacea) in the Ligurian Sea. J. Plankton Res. 21:1475–88
     [Google Scholar]
  228. Teschke M, Wendt S, Kawaguchi S, Kramer A, Meyer B. 2011. A circadian clock in Antarctic krill: an endogenous timing system governs metabolic output rhythms in the euphausid species Euphausia superba. PLOS ONE 6:e26090
     [Google Scholar]
  229. Tessmar-Raible K, Raible F, Arboleda E. 2011. Another place, another timer: marine species and the rhythms of life. BioEssays 33:165–72
     [Google Scholar]
  230. Teuber L, Schukat A, Hagen W, Auel H. 2013. Distribution and ecophysiology of calanoid copepods in relation to the oxygen minimum zone in the eastern tropical Atlantic. PLOS ONE 8:e77590
     [Google Scholar]
  231. Thorne LH, Nye JA. 2021. Trait-mediated shifts and climate velocity decouple an endothermic marine predator and its ectothermic prey. Sci. Rep. 11:18507
     [Google Scholar]
  232. Tomioka K, Matsumoto A. 2015. Circadian molecular clockworks in non-model insects. Curr. Opin. Insect Sci. 7:58–64
     [Google Scholar]
  233. Tougeron K. 2021. How constraining are photic barriers to poleward range-shifts?. Trends Ecol. Evol. 36:478–79
     [Google Scholar]
  234. Tran D, Perrigault M, Ciret P, Payton L. 2020. Bivalve mollusc circadian clock genes can run at tidal frequency. Proc. R. Soc. B 287:20192440
     [Google Scholar]
  235. van Haren H, Compton TJ. 2013. Diel vertical migration in deep sea plankton is finely tuned to latitudinal and seasonal day length. PLOS ONE 8:e64435
     [Google Scholar]
  236. Veedin Rajan VB, Häfker NS, Arboleda E, Poehn B, Gossenreiter T et al. 2021. Seasonal variation in UVA light drives hormonal and behavioural changes in a marine annelid via a ciliary opsin. Nat. Ecol. Evol. 5:204–18
     [Google Scholar]
  237. Villarino E, Irigoien X, Villate F, Iriarte A, Uriarte I et al. 2020. Response of copepod communities to ocean warming in three time-series across the North Atlantic and Mediterranean Sea. Mar. Ecol. Prog. Ser. 636:47–61
     [Google Scholar]
  238. Visser F, Hartman KL, Pierce GJ, Valavanis VD, Huisman J. 2011. Timing of migratory baleen whales at the Azores in relation to the North Atlantic spring bloom. Mar. Ecol. Prog. Ser. 440:267–79
     [Google Scholar]
  239. Wagner HJ, Kemp K, Mattheus U, Priede IG 2007. Rhythms at the bottom of the deep sea: cyclic current flow changes and melatonin patterns in two species of demersal fish. Deep-Sea Res. I 54:1944–56
     [Google Scholar]
  240. Wallace MI, Cottier FR, Berge J, Tarling GA, Griffiths C, Brierley AS. 2010. Comparison of zooplankton vertical migration in an ice-free and a seasonally ice-covered Arctic fjord: an insight into the influence of sea ice cover on zooplankton behavior. Limnol. Oceanogr. 55:831–45
     [Google Scholar]
  241. Watson GJ, Bentley MG, Gaudron SM, Hardege JD. 2003. The role of chemical signals in the spawning induction of polychaete worms and other marine invertebrates. J. Exp. Mar. Biol. Ecol. 294:169–87
     [Google Scholar]
  242. Watson NHF, Smallman BN. 1971. The role of photoperiod and temperature in the induction and termination of an arrested development in two species of freshwater cyclopid copepods. Can. J. Zool. 49:855–62
     [Google Scholar]
  243. Weizman EN, Tannenbaum M, Tarrant AM, Hakim O, Levy O 2019. Chromatin dynamics enable transcriptional rhythms in the cnidarian Nematostella vectensis. PLOS Genet 15:e1008397
     [Google Scholar]
  244. Weydmann A, Przyłucka A, Lubośny M, Walczyńska KS, Serrão EA et al. 2018. Postglacial expansion of the Arctic keystone copepod Calanus glacialis. Mar. Biodivers. 48:1027–35
     [Google Scholar]
  245. Williams BG. 1998. The lack of circadian timing in two intertidal invertebrates and its significance in the circatidal/circalunidian debate. Chronobiol. Int. 15:205–18
     [Google Scholar]
  246. Wuitchik DM, Wang D, Pells TJ, Karimi K, Ward S, Vize PD. 2019. Seasonal temperature, the lunar cycle and diurnal rhythms interact in a combinatorial manner to modulate genomic responses to the environment in a reef-building coral. Mol. Ecol. 28:3629–41
     [Google Scholar]
  247. Yan J, Kim YJ, Somers DE. 2021. Post-translational mechanisms of plant circadian regulation. Genes 12:325
     [Google Scholar]
  248. Yerushalmi S, Green RM. 2009. Evidence for the adaptive significance of circadian rhythms. Ecol. Lett. 12:970–81
     [Google Scholar]
  249. Yildirim E, Curtis R, Hwangbo D-S. 2022. Roles of peripheral clocks: lessons from the fly. FEBS Lett 596:263–93
     [Google Scholar]
  250. Yocum GD, Rinehart JP, Yocum IS, Kemp WP, Greenlee KJ. 2016. Thermoperiodism synchronizes emergence in the alfalfa leafcutting bee (Hymenoptera: Megachilidae). Environ. Entomol. 45:245–51
     [Google Scholar]
  251. Zbawicka M, Gardner JPA, Wenne R. 2019. Cryptic diversity in smooth-shelled mussels on Southern Ocean islands: connectivity, hybridisation and a marine invasion. Front. Zool. 16:32
     [Google Scholar]
  252. Zeidberg LD, Robison BH. 2007. Invasive range expansion by the Humboldt squid, Dosidicus gigas, in the eastern North Pacific. PNAS 104:12946–48
     [Google Scholar]
  253. Zhang L, Hastings MH, Green EW, Tauber E, Sladek M et al. 2013. Dissociation of circadian and circatidal timekeeping in the marine crustacean Eurydice pulchra. Curr. Biol. 23:1863–73
     [Google Scholar]
  254. Zheng P, Wang M, Li C, Sun X, Wang X et al. 2017. Insights into deep-sea adaptations and host-symbiont interactions: a comparative transcriptome study on Bathymodiolus mussels and their coastal relatives. Mol. Ecol. 26:5133–48
     [Google Scholar]
  255. Zurl M, Poehn B, Rieger D, Krishnan S, Rokvic D et al. 2022. Two light sensors decode moonlight versus sunlight to adjust a plastic circadian/circalunidian clock to moon phase. PNAS 119:e2115725119
     [Google Scholar]
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Rhythms and Clocks in Marine Organisms
Annual Review of Marine Science 15, 509 (2023); https://doi.org/10.1146/annurev-marine-030422-113038
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