Systematic Distribution of Bioluminescence in Marine Animals: A Species-Level Inventory
Abstract
:1. Introduction
2. Materials and Methods
2.1. Catalogue of Marine Luminescent Animals
2.2. Taxonomy and Phylogenetic Tree Building
3. Results
3.1. Catalogue of Marine Luminescent Animals
3.2. Generic Distribution of Luminescence across Marine Taxonomic Groups
3.3. Specific Distribution of Bioluminescence across Marine Taxonomic Groups
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Roda, A. A History of Bioluminescence and Chemiluminescence from Ancient Times to the Present, 1st ed.; Royal Society of Chemistry: Cambridge, UK, 2011; pp. 1–50. [Google Scholar]
- Anctil, M. Luminous Creatures: The History and Science of Light Production in Living Organisms, 1st ed.; McGill-Queen’s Press-MQUP: Montreal, QC, Canada, 2018; pp. 34–37. [Google Scholar]
- Oba, Y.; Stevani, C.V.; Oliveira, A.G.; Tsarkova, A.S.; Chepurnykh, T.V.; Yampolsky, I.V. Selected least studied but not forgotten bioluminescent systems. Photochem. Photobiol. 2017, 93, 405–415. [Google Scholar] [CrossRef]
- Herring, P.J. Aspects of the bioluminescence of fishes. Oceanogr. Mar. Biol. 1982, 20, 415–470. [Google Scholar]
- Herring, P.J. Bioluminescent signals and the role of reflectors. J. Opt. A Pure Appl. Opt. 2000, 2, R29–R38. [Google Scholar] [CrossRef]
- Dewael, Y.; Mallefet, J. Luminescence in ophiuroids (Echinodermata) does not share a common nervous control in all species. J. Exp. Biol. 2002, 205, 799–806. [Google Scholar] [CrossRef]
- Krönström, J.; Dupont, S.; Mallefet, J.; Thorndyke, M.; Holmgren, S. Serotonin and nitric oxide interaction in the control of bioluminescence in northern krill, Meganyctiphanes norvegica (M. Sars). J. Exp. Biol. 2007, 210, 3179–3187. [Google Scholar] [CrossRef]
- Claes, J.M.; Mallefet, J. Hormonal control of luminescence from lantern shark (Etmopterus spinax) photophores. J. Exp. Biol. 2009, 212, 3684–3692. [Google Scholar] [CrossRef] [PubMed]
- Gouveneaux, A.; Mallefet, J. Physiological control of bioluminescence in a deep-sea planktonic worm, Tomopteris helgolandica. J. Exp. Biol. 2013, 216, 4285–4289. [Google Scholar] [CrossRef]
- Paitio, J.; Oba, Y. Luminous fishes: Endocrine and neuronal regulation of bioluminescence. Aquac. Fish. 2023, in press. [Google Scholar] [CrossRef]
- Duchatelet, L.; Coubris, C.; Pels, C.; Dupont, S.T.; Mallefet, J. Catecholamine involvement in the bioluminescence control of two species of anthozoans. Life 2023, 13, 1798. [Google Scholar] [CrossRef]
- Tong, D.; Rozas, N.S.; Oakley, T.H.; Mitchell, J.; Colley, N.J.; McFall-Ngai, M.J. Evidence for light perception in a bioluminescent organ. Proc. Natl. Acad. Sci. USA 2009, 106, 9836–9841. [Google Scholar] [CrossRef]
- Duchatelet, L.; Sugihara, T.; Delroisse, J.; Koyanagi, M.; Rezsohazy, R.; Terakita, A.; Mallefet, J. From extraocular photoreception to pigment movement regulation: A new control mechanism of the lanternshark luminescence. Sci. Rep. 2020, 10, 10195. [Google Scholar] [CrossRef] [PubMed]
- Frank, T.; Sickles, J.; DeLeo, D.; Blackwelder, P.; Bracken-Grissom, H. Putative photosensitivity in internal light organs (organs of Pesta) of deep-sea sergestid shrimps. Sci. Rep. 2023, 13, 16113. [Google Scholar] [CrossRef] [PubMed]
- Herring, P.J. Systematic distribution of bioluminescence in living organisms. J. Biolumin. Chemilumin. 1987, 1, 147–163. [Google Scholar] [CrossRef] [PubMed]
- Haddock, S.H.; Moline, M.A.; Case, J.F. Bioluminescence in the sea. Annu. Rev. Mar. Sci. 2010, 2, 443–493. [Google Scholar] [CrossRef]
- Widder, E.A. Bioluminescence in the ocean: Origins of biological, chemical, and ecological diversity. Science 2010, 328, 704–708. [Google Scholar] [CrossRef]
- Martini, S.; Haddock, S.H. Quantification of bioluminescence from the surface to the deep sea demonstrates its predominance as an ecological trait. Sci. Rep. 2017, 7, 45750. [Google Scholar] [CrossRef]
- Martini, S.; Kuhnz, L.; Mallefet, J.; Haddock, S.H. Distribution and quantification of bioluminescence as an ecological trait in the deep-sea benthos. Sci. Rep. 2019, 9, 14654. [Google Scholar] [CrossRef]
- Irigoien, X.; Klevjer, T.A.; Røstad, A.; Martinez, U.; Boyra, G.; Acuña, J.L.; Bode, A.; Echevarria, F.; Gonzalez-Gordillo, J.I.; Hernandez-Leon, S.; et al. Large mesopelagic fishes biomass and trophic efficiency in the open ocean. Nat. Commun. 2014, 5, 3271. [Google Scholar] [CrossRef]
- Johnsen, S.; Widder, E.A.; Mobley, C.D. Propagation and perception of bioluminescence: Factors affecting counterillumination as a cryptic strategy. Biol. Bull. 2004, 207, 1–16. [Google Scholar] [CrossRef]
- Deheyn, D.; Mallefet, J.; Jangoux, M. Evidence of seasonal variation in bioluminescence of Amphipholis squamata (Ophiuroidea, Echinodermata): Effects of environmental factors. J. Exp. Mar. Biol. Ecol. 2000, 245, 245–264. [Google Scholar] [CrossRef] [PubMed]
- Claes, J.M.; Mallefet, J. Functional physiology of lantern shark (Etmopterus spinax) luminescent pattern: Differential hormonal regulation of luminous zones. J. Exp. Biol. 2010, 213, 1852–1858. [Google Scholar] [CrossRef] [PubMed]
- Giesbrecht, W. Mitteilungen über Copepoden. 8. Über das Leuchten der pelagischen Copepoden und das tierische Leuchten im Allgemeinen. Mitt. Zool. Stn. Neapel. 1895, 11, 648–689. [Google Scholar]
- Herring, P.J. Sex with the lights on? A review of bioluminescent sexual dimorphism in the sea. J. Mar. Biol. Assoc. UK 2007, 87, 829–842. [Google Scholar] [CrossRef]
- Roper, C.F.E.; Jereb, P. Family Thysanoteuthidae. In Cephalopods of the World. An Annotated and Illustrated Catalogue of Species Known to Date, 2nd ed.; Jereb, P., Roper, C.F.E., Eds.; Myopsid an Oegopsid Squids; FAO: Rome, Italy, 2010; Volume 2, pp. 384–387. [Google Scholar]
- Warner, J.A.; Case, J.F. The zoogeography and dietary induction of bioluminescence in the midshipman fish, Porichthys notatus. Biol. Bull. 1980, 159, 231–246. [Google Scholar] [CrossRef]
- Frank, T.M.; Widder, E.A.; Latz, M.I.; Case, J.F. Dietary maintenance of bioluminescence in a deep-sea mysid. J. Exp. Biol. 1984, 109, 385–389. [Google Scholar] [CrossRef]
- Haddock, S.H.; Rivers, T.J.; Robison, B.H. Can coelenterates make coelenterazine? Dietary requirement for luciferin in cnidarian bioluminescence. Proc. Natl. Acad. Sci. USA 2001, 98, 11148–11151. [Google Scholar] [CrossRef]
- Mallefet, J.; Duchatelet, L.; Coubris, C. Bioluminescence induction in the ophiuroid Amphiura filiformis (Echinodermata). J. Exp. Biol. 2020, 223, jeb218719. [Google Scholar] [CrossRef]
- Bessho-Uehara, M.; Yamamoto, N.; Shigenobu, S.; Mori, H.; Kuwata, K.; Oba, Y. Kleptoprotein bioluminescence: Parapriacanthus fish obtain luciferase from ostracod prey. Sci. Adv. 2020, 6, eaax4942. [Google Scholar] [CrossRef]
- Meyer-Rochow, V.B. Loss of bioluminescence in Anomalops katoptron due to starvation. Experientia 1976, 32, 1175–1176. [Google Scholar] [CrossRef]
- Copilas-Ciocianu, D.; Pop, F.M. An account of bacterial-induced luminescence in the Ponto-Caspian amphipod Pontogammarus maeoticus (Sowinskyi, 1894), with an overview of amphipod bioluminescence. North-West. J. Zool. 2020, 16, 238–240. [Google Scholar]
- Chakrabarty, P.; Davis, M.P.; Smith, W.L.; Berquist, R.; Gledhill, K.M.; Frank, L.R.; Sparks, J.S. Evolution of the light organ system in ponyfishes (Teleostei: Leiognathidae). J. Morphol. 2011, 272, 704–721. [Google Scholar] [CrossRef] [PubMed]
- Morin, J.G. Luminaries of the reef: The history of luminescent ostracods and their courtship displays in the Caribbean. J. Crustac. Biol. 2019, 39, 227–243. [Google Scholar] [CrossRef]
- Straube, N.; Li, C.; Claes, J.M.; Corrigan, S.; Naylor, G.J. Molecular phylogeny of Squaliformes and first occurrence of bioluminescence in sharks. BMC Evol. Biol. 2015, 15, 162. [Google Scholar] [CrossRef]
- Davis, M.P.; Sparks, J.S.; Smith, W.L. Repeated and widespread evolution of bioluminescence in marine fishes. PLoS ONE 2016, 11, e0155154. [Google Scholar] [CrossRef] [PubMed]
- Sanchez, G.; Fernández-Álvarez, F.Á.; Taite, M.; Sugimoto, C.; Jolly, J.; Simakov, O.; Marlétaz, F.; Allock; Rokhsar, D.S. Phylogenomics illuminates the evolution of bobtail and bottletail squid (order Sepiolida). Commun. Biol. 2021, 4, 819. [Google Scholar] [CrossRef]
- Golightly, C.; DeLeo, D.M.; Perez, N.; Chan, T.Y.; Landeira, J.M.; Bracken-Grissom, H.D.; Wolfe, J. Tracing the evolution of bioluminescent light organs across the deep-sea shrimp family Sergestidae using a genomic skimming and phylogenetic approach. Invertebr. Syst. 2022, 36, 22–35. [Google Scholar] [CrossRef]
- Paitio, J.; Oba, Y.; Meyer-Rochow, V.B. Bioluminescent fishes and their eyes. In Luminescence—An Outlook on the Phenomena and Their Applications, 1st ed.; Thirumalai, J., Ed.; IntechOpen: Rijeka, Croatia, 2016; pp. 297–332. [Google Scholar] [CrossRef]
- Poupin, J.; Cussatlegras, A.S.; Geistdoerfer, P. Plancton Marin Bioluminescent: Inventaire Documenté des Espèces et Bilan des Formes les plus Communes de la mer D’Iroise. Ph.D. Thesis, Ecole Navale, Laboratoire d’Océanographie Brest, Brest, France, 1999. [Google Scholar]
- Duchatelet, L.; Claes, J.M.; Delroisse, J.; Flammang, P.; Mallefet, J. Glow on sharks: State of the art on bioluminescence research. Oceans 2021, 2, 822–842. [Google Scholar] [CrossRef]
- Moraes, G.V.; Hannon, M.C.; Soares, D.M.; Stevani, C.V.; Schulze, A.; Oliveira, A.G. Bioluminescence in polynoid scale worms (Annelida: Polynoidae). Front. Mar. Sci. 2021, 8, 643197. [Google Scholar] [CrossRef]
- Mallefet, J.; Martinez-Soares, P.; Eléaume, M.; O’hara, T.; Duchatelet, L. New insights on crinoid (Echinodermata; Crinoidea) bioluminescence. Front. Mar. Sci. 2023, 10, 1136138. [Google Scholar] [CrossRef]
- Otjacques, E.; Pissarra, V.; Bolstad, K.; Xavier, J.C.; McFall-Ngai, M.; Rosa, R. Bioluminescence in cephalopods: Biodiversity, biogeography and research trends. Front. Mar. Sci. 2023, 10, 1161049. [Google Scholar] [CrossRef]
- Bessho-Uehara, M.; Mallefet, J.; Haddock, S.H. Glowing sea cucumbers: Bioluminescence in the Holothuroidea. In The World of Sea Cucumbers, 1st ed.; Mercier, A., Hamel, J.F., Suhrbier, A., Pearce, C., Eds.; Academic Press: Cambridge, MA, USA, 2024; pp. 361–375. [Google Scholar]
- Costello, M.J.; Bouchet, P.; Boxshall, G.; Fauchald, K.; Gordon, D.; Hoeksema, B.W.; Poore, G.C.B.; van Soest, R.W.M.; Sabine Stöhr, S.; Walter, T.C.; et al. Global coordination and standardisation in marine biodiversity through the World Register of Marine Species (WoRMS) and related databases. PLoS ONE 2013, 8, e51629. [Google Scholar] [CrossRef]
- Bouchet, P.; Decock, W.; Lonneville, B.; Vanhoorne, B.; Vandepitte, L. Marine biodiversity discovery: The metrics of new species descriptions. Front. Mar. Sci. 2023, 10, 929989. [Google Scholar] [CrossRef]
- World Register of Marine Species (WoRMS). Available online: https://www.marinespecies.org/ (accessed on 15 January 2024).
- Lau, E.S.; Oakley, T.H. Multi-level convergence of complex traits and the evolution of bioluminescence. Biol. Rev. 2021, 96, 673–691. [Google Scholar] [CrossRef]
- Schultz, D.T.; Haddock, S.H.; Bredeson, J.V.; Green, R.E.; Simakov, O.; Rokhsar, D.S. Ancient gene linkages support ctenophores as sister to other animals. Nature 2023, 618, 110–117. [Google Scholar] [CrossRef]
- Martini, S.; Schultz, D.T.; Lundsten, L.; Haddock, S.H. Bioluminescence in an undescribed species of carnivorous sponge (Cladorhizidae) from the deep sea. Front. Mar. Sci. 2020, 7, 576476. [Google Scholar] [CrossRef]
- Harvey, E.N. Bioluminescence, 1st ed.; Academic Press, Inc.: New York, NY, USA, 1952; 649p. [Google Scholar]
- Herring, P.J. Bioluminescence in Action, 1st ed.; Academic Press: London, UK, 1978; 570p. [Google Scholar]
- Bessho-Uehara, M.; Francis, W.R.; Haddock, S.H. Biochemical characterization of diverse deep-sea anthozoan bioluminescence systems. Mar. Biol. 2020, 167, 114. [Google Scholar] [CrossRef]
- Verdes, A.; Gruber, D.F. Glowing worms: Biological, chemical, and functional diversity of bioluminescent annelids. Int. Comp. Biol. 2017, 57, 18–32. [Google Scholar] [CrossRef] [PubMed]
- Herring, P.J. Bioluminescence in decapod Crustacea. J. Mar. Biol. Assoc. UK 1976, 56, 1029–1047. [Google Scholar] [CrossRef]
- Herring, P.J. Bioluminescence in the Crustacea. J. Crustac. Biol. 1985, 5, 557–573. [Google Scholar] [CrossRef]
- Herring, P.J. Copepod luminescence. Hydrobiologia 1988, 167, 183–195. [Google Scholar] [CrossRef]
- Vereshchaka, A.L.; Kulagin, D.N.; Lunina, A.A. A phylogenetic study of krill (Crustacea: Euphausiacea) reveals new taxa and co-evolution of morphological characters. Cladistics 2019, 35, 150–172. [Google Scholar] [CrossRef]
- Chavtur, V.G.; Bashmanov, A.G. Pelagic ostracods of the new subtribe Conchoeciina (Ostracoda, Crustacea) from the North Pacific. Zootaxa 2018, 4516, 1–127. [Google Scholar] [CrossRef]
- Herring, P.J. Bioluminescent echinoderms: Unity of function in diversity of expression. In Echinoderm Research, 1st ed.; Emson, R.H., Smith, A.B., Campbell, A.C., Eds.; A.A. Balkema: Rotterdam, The Netherlands, 1995; pp. 1–9. [Google Scholar]
- Galt, C.P.; Grober, M.S.; Sykes, P.F. Taxonomic correlates of bioluminescence among appendicularians (Urochordata: Larvacea). Biol. Bull. 1985, 168, 125–134. [Google Scholar] [CrossRef]
- Rodionova, N.S.; Rota, E.; Tsarkova, A.S.; Petushkov, V.N. Progress in the study of bioluminescent earthworms. Photochem. Photobiol. 2017, 93, 416–428. [Google Scholar] [CrossRef]
- Rodionova, N.S.; Petushkov, V.N. Comparison of earthworm bioluminescent systems. Dokl. Biochem. Biophys. 2019, 485, 157–161. [Google Scholar] [CrossRef] [PubMed]
- Pholyotha, A.; Yano, D.; Mizuno, G.; Sutcharit, C.; Tongkerd, P.; Oba, Y.; Panha, S. A new discovery of the bioluminescent terrestrial snail genus Phuphania (Gastropoda: Dyakiidae). Sci. Rep. 2023, 13, 15137. [Google Scholar] [CrossRef] [PubMed]
- Rosenberg, J.; Meyer-Rochow, V.B. Luminescent myriapoda: A brief review. In Bioluminescence in Focus—A Collection of Illuminating Essays; Meyer Rochow, V.B., Ed.; Research Signpost: Trivandrum, India, 2009; pp. 139–146. [Google Scholar]
- Oba, Y.; Branham, M.A.; Fukatsu, T. The terrestrial bioluminescent animals of Japan. Zool. Sci. 2011, 28, 771–789. [Google Scholar] [CrossRef] [PubMed]
- Rosa, S.P.; Costa, C. Metapyrophorus pharolim a new genus and species of Pyrophorini (Coleoptera, Elateridae, Agrypninae). Rev. Bras. Entomol. 2009, 53, 45–48. [Google Scholar] [CrossRef]
- Oba, Y.; Hoffmann, K.H. Insect bioluminescence in the post-molecular biology era. Insect Mol. Biol. 2014, 94, 120. [Google Scholar]
- Bi, W.X.; He, J.W.; Chen, C.C.; Kundrata, R.; Li, X.Y. Sinopyrophorinae, a new subfamily of Elateridae (Coleoptera, Elateroidea) with the first record of a luminous click beetle in Asia and evidence for multiple origins of bioluminescence in Elateridae. ZooKeys 2019, 864, 79–97. [Google Scholar] [CrossRef] [PubMed]
- Falaschi, R.L.; Amaral, D.T.; Santos, I.; Domingos, A.H.; Johnson, G.A.; Martins, A.G.; Viroomal, I.B.; Pompéia, S.L.; Mirza, J.D.; Oliveira, A.G.; et al. Neoceroplatus betaryiensis nov. sp. (Diptera: Keroplatidae) is the first record of a bioluminescent fungus-gnat in South America. Sci. Rep. 2019, 9, 11291. [Google Scholar] [CrossRef] [PubMed]
- Sano, T.; Kobayashi, Y.; Sakai, I.; Ogoh, K.; Suzuki, H. Ecological and histological notes on the luminous springtail, Lobella sp. (Collembola: Neanuridae), discovered in Tokyo, Japan. In Bioluminescence-Analytical Applications and Basic Biology; Suzuki, H., Ed.; IntechOpen: London, UK, 2019; pp. 63–74. [Google Scholar] [CrossRef]
- Vega-Badillo, V.; Zaragoza-Caballero, S.; Ivie, M.A. A new genus of Phengodidae (Coleoptera) from the Neotropical Region. Pap. Avulsos Zool. 2020, 60, e202060-si. [Google Scholar] [CrossRef]
- Catalogue of Life (COL). Available online: https://www.catalogueoflife.org/ (accessed on 15 January 2024).
- Kundrata, R.; Hoffmannova, J.; Hinson, K.R.; Keller, O.; Packova, G. Rhagophthalmidae Olivier, 1907 (Coleoptera, Elateroidea): Described genera and species, current problems, and prospects for the bioluminescent and paedomorphic beetle lineage. ZooKeys 2022, 1126, 55–130. [Google Scholar] [CrossRef] [PubMed]
- Oba, Y.; Schultz, D.T. Firefly genomes illuminate the evolution of beetle bioluminescent systems. Curr. Opin. Insect Sci. 2022, 50, 100879. [Google Scholar] [CrossRef] [PubMed]
- Desjardin, D.E.; Oliveira, A.G.; Stevani, C.V. Fungi bioluminescence revisited. Photochem. Photobiol. Sci. 2008, 7, 170–182. [Google Scholar] [CrossRef]
- Ke, H.M.; Lu, M.R.; Chang, C.C.; Hsiao, C.; Ou, J.H.; Taneyama, Y.; Tsai, I.J. Evolution and Diversity of Bioluminescent Fungi. In Evolution of Fungi and Fungal-like Organisms; Pöggeler, S., James, T., Eds.; Springer International Publishing: Cham, Switzerland, 2023; pp. 275–294. [Google Scholar] [CrossRef]
- Oba, Y.; Hosaka, K. The Luminous Fungi of Japan. J. Fungi 2023, 9, 615. [Google Scholar] [CrossRef]
- Park, S.A.; Jeong, H.J.; Ok, J.H.; Kang, H.C.; You, J.H.; Eom, S.H.; Yeong, D.Y.; Lee, M.J. Bioluminescence capability and intensity in the dinoflagellate Alexandrium species. Algae 2021, 36, 299–314. [Google Scholar] [CrossRef]
- Dunlap, P. Biochemistry and genetics of bacterial bioluminescence. In Bioluminescence: Fundamentals and Applications in Biotechnology; Thouand, G., Marks, R., Eds.; Springer: Berlin, Germany, 2014; Volume 1, pp. 37–64. [Google Scholar] [CrossRef]
- Machado, R.A.; Wüthrich, D.; Kuhnert, P.; Arce, C.C.; Thönen, L.; Ruiz, C.; Zhang, X.; Robert, C.A.M.; Karimi, J.; Kamali, S.; et al. Whole-genome-based revisit of Photorhabdus phylogeny: Proposal for the elevation of most Photorhabdus subspecies to the species level and description of one novel species Photorhabdus bodei sp. nov., and one novel subspecies Photorhabdus laumondii subsp. clarkei subsp. nov. Int. J. Syst. Evol. Microbiol. 2018, 68, 2664–2681. [Google Scholar] [CrossRef]
- Burtseva, O.; Kublanovskaya, A.; Baulina, O.; Fedorenko, T.; Lobakova, E.; Chekanov, K. The strains of bioluminescent bacteria isolated from the White Sea finfishes: Genera Photobacterium, Aliivibrio, Vibrio, Shewanella, and first luminous Kosakonia. J. Photochem. Photobiol. B Biol. 2020, 208, 111895. [Google Scholar] [CrossRef]
- Machado, R.A.; Muller, A.; Ghazal, S.M.; Thanwisai, A.; Pagès, S.; Bode, H.B.; Hussein, M.A.; Khalil, K.M.; Tisa, L.S. Photorhabdus heterorhabditis subsp. aluminescens subsp. nov., Photorhabdus heterorhabditis subsp. heterorhabditis subsp. nov., Photorhabdus australis subsp. thailandensis subsp. nov., Photorhabdus australis subsp. australis subsp. nov., and Photorhabdus aegyptia sp. nov. isolated from Heterorhabditis entomopathogenic nematodes. Int. J. Syst. Evol. Microbiol. 2021, 71, 004610. [Google Scholar] [CrossRef]
- Haddock, S.H.; Christianson, L.M.; Francis, W.R.; Martini, S.; Dunn, C.W.; Pugh, P.R.; Mills, C.E.; Osborn, K.J.; Seibel, B.A.; Choy, C.A.; et al. Insights Into the Biodiversity, Behavior, and Bioluminescence of Deep-Sea Organisms: Using Molecular and Maritime Technology. Oceanography 2017, 30, 38–47. [Google Scholar] [CrossRef]
- Robinson, N.J.; Johnsen, S.; Brooks, A.; Frey, L.; Judkins, H.; Vecchione, M.; Widder, E. Studying the swift, smart, and shy: Unobtrusive camera-platforms for observing large deep-sea squid. Deep-Sea Res. I Oceanogr. Res. Pap. 2021, 172, 103538. [Google Scholar] [CrossRef]
- Bell, K.L.; Chow, J.S.; Hope, A.; Quinzin, M.C.; Cantner, K.A.; Amon, D.J.; Cramp, J.E.; Rotjan, R.D.; Kamalu, L.; de Vos, A.; et al. Low-cost, deep-sea imaging and analysis tools for deep-sea exploration: A collaborative design study. Front. Mar. Sci. 2022, 9, 873700. [Google Scholar] [CrossRef]
- Feng, J.C.; Liang, J.; Cai, Y.; Zhang, S.; Xue, J.; Yang, Z. Deep-sea organisms research oriented by deep-sea technologies development. Sci. Bull. 2022, 67, 1802–1816. [Google Scholar] [CrossRef]
- Davis, M.P.; Holcroft, N.I.; Wiley, E.O.; Sparks, J.S.; Leo Smith, W. Species-specific bioluminescence facilitates speciation in the deep sea. Mar. Biol. 2014, 161, 1139–1148. [Google Scholar] [CrossRef] [PubMed]
- Claes, J.M.; Nilsson, D.E.; Mallefet, J.; Straube, N. The presence of lateral photophores correlates with increased speciation in deep-sea bioluminescent sharks. R. Soc. Open Sci. 2015, 2, 150219. [Google Scholar] [CrossRef]
- Ellis, E.A.; Oakley, T.H. High rates of species accumulation in animals with bioluminescent courtship displays. Curr. Biol. 2016, 26, 1916–1921. [Google Scholar] [CrossRef]
- Matsui, T.; Rosenblatt, R.H. Review of the deep-sea fish family Platytroctidae (Pisces: Salmoniformes). Bull. Scripps. Inst. Oceanogr. Univ. Calif. 1984, 26, 1–59. [Google Scholar]
- Claes, J.M.; Nilsson, D.E.; Straube, N.; Collin, S.P.; Mallefet, J. Iso-luminance counterillumination drove bioluminescent shark radiation. Sci. Rep. 2014, 4, 4328. [Google Scholar] [CrossRef]
- Davis, A.L.; Sutton, T.T.; Kier, W.M.; Johnsen, S. Evidence that eye-facing photophores serve as a reference for counterillumination in an order of deep-sea fishes. Proc. R. Soc. B 2020, 287, 20192918. [Google Scholar] [CrossRef]
- Denton, E.J.; Gilpin-Brown, J.B.; Wright, P.G. The angular distribution of the light produced by some mesopelagic fish in relation to their camouflage. Proc. R. Soc. B 1972, 182, 145–158. [Google Scholar] [CrossRef]
- Young, R.E.; Kampa, E.M.; Maynard, S.D.; Mencher, F.M.; Roper, C.F. Counterillumination and the upper depth limits of midwater animals. Deep Sea Res. Part I Oceanogr. 1980, 27, 671–691. [Google Scholar] [CrossRef]
- Herring, P.J.; Widder, E.A. Bioluminescence of deep-sea coronate medusae (Cnidaria: Scyphozoa). Mar. Biol. 2004, 146, 39–51. [Google Scholar] [CrossRef]
- Plyuscheva, M.; Martin, D. On the morphology of elytra as luminescent organs in scale-worms (Polychaeta, Polynoidae). Zoosymposia 2009, 2, 379–389. [Google Scholar] [CrossRef]
- Deheyn, D.D.; Wilson, N.G. Bioluminescent signals spatially amplified by wavelength-specific diffusion through the shell of a marine snail. Proc. R. Soc. B 2011, 278, 2112–2121. [Google Scholar] [CrossRef] [PubMed]
- Jones, A.; Mallefet, J. Why do brittle stars emit light? Behavioural and evolutionary approaches of bioluminescence. Cah. Biol. Mar. 2013, 54, 729–734. [Google Scholar]
- Gouveneaux, A.; Gielen, M.C.; Mallefet, J. Behavioural responses of the yellow emitting annelid Tomopteris helgolandica to photic stimuli. Luminescence 2018, 33, 511–520. [Google Scholar] [CrossRef] [PubMed]
- Livermore, J.; Perreault, T.; Rivers, T. Luminescent defensive behaviors of polynoid polychaete worms to natural predators. Mar. Biol. 2018, 165, 149. [Google Scholar] [CrossRef]
- Johnsen, S.; Frank, T.M.; Haddock, S.H.; Widder, E.A.; Messing, C.G. Light and vision in the deep-sea benthos: I. Bioluminescence at 500–1000 m depth in the Bahamian Islands. J. Exp. Biol. 2012, 215, 3335–3343. [Google Scholar] [CrossRef]
- Mallefet, J. New lights on echinoderm’s bioluminescence. In Proceedings of the 21st International Symposium on Bioluminescence & Chemiluminescence, Gijon, Spain, 31 May 2022. [Google Scholar]
- DeLeo, D.; Bessho-Uehara, M.; McFadden, C.; Haddock, S.H.D.; Quattrini, A. Evolution of bioluminescence in Anthozoa with emphasis on Octocorallia. Proc. R. Soc. B 2024, in press. [Google Scholar]
- Haddock, S.H.; Case, J.F. A bioluminescent chaetognath. Nature 1994, 367, 225–226. [Google Scholar] [CrossRef]
- Thuesen, E.V.; Goetz, F.E.; Haddock, S.H. Bioluminescent organs of two deep-sea arrow worms, Eukrohnia fowleri and Caecosagitta macrocephala, with further observations on bioluminescence in chaetognaths. Biol. Bull. 2010, 219, 100–111. [Google Scholar] [CrossRef] [PubMed]
Score | Name | Description |
---|---|---|
1 | Uncertain luminescence | Report previously considered as dubious by a luminescence authority (e.g., Peter J. Herring), or to genera reported as luminescent but currently lacking a species-level report following the reallocation of luminescent species to other genera. |
2 | Putative photogenic structure | Report featuring an anatomical element considered as photogenic while not sharing similarities with structures confirmed as photogenic in species from the same order. |
3 | Potential photogenic structure | Report featuring an anatomical element sharing similarities (e.g., similar shape or fluorescence pattern) with structures confirmed as photogenic in species from the same order. |
4 | Photogenic structure | Report featuring an anatomical element displaying the typical morphology of structures confirmed as photogenic in species from the same family (e.g., counterilluminating photophores of crustaceans, cephalopods, and fishes). |
5 | Observed luminescence | Report featuring luminescence observations made in relevant conditions and reported by credible scientific authorities. |
6 | Substantiated luminescence | Report for which irrefutable scientific evidence (e.g., via luminometry, spectrophotometry, biochemistry, long exposure photography or light-intensified video recordings) of the luminescence competence of the species has been provided. |
Number of Species with Undetermined Status | |||
---|---|---|---|
Taxonomic Group | From Luminescent Genera | From Potentially Luminescent Genera | Proportion with Undetermined Status (% 1,2) |
CTENOPHORA * | 54 | 26 | 46.15–68.38 |
PORIFERA * | 0 | 118 | 0.00–97.52 |
CNIDARIA ** | 898 | 111 | 75.40–84.72 |
CHAETOGNATHA ** | 10 | 0 | 83.33 |
NEMERTEA ** | 24 | 0 | 96.00 |
ANNELIDA ** | 944 | 185 | 76.01–90.90 |
MOLLUSCA | |||
Bivalvia ** | 38 | 0 | 90.48 |
Gastropoda ** | 238 | 31 | 82.93–93.73 |
Octopodiformes | 1 | 0 | 7.69 |
Decapodiformes | 0 | 11 | 0.0–3.97 |
ARTHROPODA | |||
Pycnogonida ** | 334 | 0 | 98.82 |
Ostracoda ** | 139 | 1 | 56.28–56.68 |
Copepoda * | 200 | 414 | 27.82–85.40 |
Peracarida * | 58 | 178 | 21.16–81.91 |
Eucarida ** | 303 | 21 | 53.63–57.35 |
ECHINODERMATA ** | 1589 | 3 | 88.52–88.69 |
HEMICHORDATA ** | 36 | 0 | 83.33 |
CHORDATA | |||
Tunicata ** | 55 | 2 | 56.70–58.76 |
Selachii | 1 | 0 | 1.54 |
Basal Teleostei | 22 | 23 | 15.94–32.61 |
Stomiiformes | 0 | 0 | 0.00 |
Aulopiformes | 7 | 0 | 15.91 |
Myctophiformes | 0 | 0 | 0.00 |
Gadiformes | 11 | 1 | 3.02–3.30 |
Derived Teleostei | 88 | 211 | 13.25–45.03 |
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Claes, J.M.; Haddock, S.H.D.; Coubris, C.; Mallefet, J. Systematic Distribution of Bioluminescence in Marine Animals: A Species-Level Inventory. Life 2024, 14, 432. https://doi.org/10.3390/life14040432
Claes JM, Haddock SHD, Coubris C, Mallefet J. Systematic Distribution of Bioluminescence in Marine Animals: A Species-Level Inventory. Life. 2024; 14(4):432. https://doi.org/10.3390/life14040432
Chicago/Turabian StyleClaes, Julien M., Steven H. D. Haddock, Constance Coubris, and Jérôme Mallefet. 2024. "Systematic Distribution of Bioluminescence in Marine Animals: A Species-Level Inventory" Life 14, no. 4: 432. https://doi.org/10.3390/life14040432