The megamouth shark, Megachasma pelagios, is not a luminous species

Abstract

Despite its five meters length, the megamouth shark (Megachasma pelagios Taylor, Compagno & Struhsaker, 1983) is one of the rarest big sharks known in the world (117 specimens observed and documented so far). This filter-feeding shark has been assumed to be a luminous species, using its species-specific white band to produce bioluminescence as a lure trap. Another hypothesis was the use of the white band reflectivity to attract prey or for social recognition purposes. However, no histological study has ever been performed to confirm these assumptions so far. Two hypotheses about the megamouth shark's luminescence arose: firstly, the light emission may be intrinsically or extrinsically produced by specific light organs (photophores) located either on the upper jaw white band or inside the mouth; secondly, the luminous appearance might be a consequence of the reflection of prey luminescence on the white band during feeding events. Aims of the study were to test these hypotheses by highlighting the potential presence of specific photophores responsible for bioluminescence and to reveal and analyze the presence of specialized light-reflective structures in and around the mouth of the shark. By using different histological approaches (histological sections, fluorescent in situ hybridization, scanning electron microscopy) and spectrophotometry, this study allows to unravel these hypotheses and strongly supports that the megamouth shark does not emit bioluminescence, but might rather reflect the light produced by bioluminescent planktonic preys, thanks to the denticles of the white band.

Leaving the Dark Side? Insights Into the Evolution of Luciferases

“…Symbiotic associations with luminescent bacteria have also been described in teleost fish and squids (Dunlap and Kita-Tsukamoto, 2006) and suggested in other organisms (e.g., Taylor et al, 1983;Mackie and Bone, 1978). These last hypotheses (i.e., luminescence produced by symbiotic bacteria) were recently challenged in sharks (Duchatelet et al, 2020) and urochordates (Tessler et al, 2020). Multiple bacteria species have been identified in bioluminescent symbiotic associations: Aliivibrio fischeri, A. logei, Photobacterium leiognathi, P. phosphoreum, P. kishitanii, P. mandapamemsis, Candidatus Enterovibrio luxaltus, Candidatus E. escacola, Candidatus Photodesmus katoptron, Candidatus P. blepharon… (Boettcher and Ruby, 1990;Dunlap and Kita-Tsukamoto, 2006;Ast et al, 2007;Dunlap et al, 2007;Kaeding et al, 2007;Hendry et al, 2014Hendry et al, , 2018Freed et al, 2019) and some studies suggested that unidentified species could also be involved (Haygood and Distel, 1993).…”

“…Therefore, efforts are still needed to discover hitherto unknown bioluminescent systems. For instance, lanternfish, dragonfish and viperfish luminous systems were demonstrated to use coelenterazine as luciferin, but no luciferase/photoprotein has been identified to date (Tsuji and Haneda, 1971;Mallefet and Shimomura, 1995;Duchatelet et al, 2019). Similarly, shark bioluminescence systems -while these organisms have been extensively studied these last years (e.g., Mallefet et al, 2021;Claes et al, 2020) -remain totally enigmatic, even though attempts were made to decipher the bioluminescent compound in the lanternshark Etmopterus spinax (Renwart and Mallefet, 2013).…”

“…Coelenterazine is detected not only in luminescent organs but is also found in the digestive tract and hepatopancreas of several luminous and non-luminous decapods, cephalopods and fishes (Shimomura, 1987;Mallefet and Shimomura, 1995;Thomson et al, 1997;Rees et al, 1998;Duchatelet et al, 2019). These observations support an anti-oxidative function of this kind of compound and luciferins might then be antioxidant molecules emitting light as a by-product of their "reactive oxygen scavenging chemical activity" (Rees et al, 1998;Haddock et al, 2010).…”

Leaving the Dark Side? Insights Into the Evolution of Luciferases

“…Symbiotic associations with luminescent bacteria have also been described in teleost fish and squids (Dunlap and Kita-Tsukamoto, 2006) and suggested as hypotheses, in other organisms (e.g., Mackie and Bone, 1978;Taylor et al, 1983). These last hypotheses (i.e., luminescence produced by symbiotic bacteria) were recently challenged in sharks (Duchatelet et al, 2020) and urochordates (Tessler et al, 2020). Multiple bacteria species have been identified in bioluminescent symbiotic associations: Aliivibrio fischeri, Aliivibrio logei, Photobacterium leiognathi, Photobacterium phosphoreum, Photobacterium kishitanii, Photobacterium mandapamemsis, Candidatus Enterovibrio luxaltus, Candidatus Enterovibrio escacola, Candidatus Photodesmus katoptron, Candidatus Photodesmus blepharon, etc.…”

Spatial–Temporal Distribution of Megamouth Shark, Megachasma pelagios, Inferred from over 250 Individuals Recorded in the Three Oceans

“…Afterward, the Taiwan Fisheries Agency announced a ban fishing management measure on M. pelagios on 10 November 2020 for conservation purposes (the catching is forbidden; fisherman have to release the shark whether it is dead or alive); however, further effectiveness and study remain to be elucidated. Studies to date have included its morphology, movement, molecular biology, physiology, and chemical analysis [17][18][19][20][21][22][23][24][25].…”