On the bioluminescence of Echinodermata in the south-eastern Australian deep-sea: New insights into sacculi and light emission in Comatulida (Crinoidea)

Bioluminescence is an organism’s capacity of emitting cold, visible light thanks to a chemical reaction. It is a very widespread phenomenon specially in marine environments. Utilities vary from luring prey to intraspecific communication. In the phylum Echinodermata bioluminescence seems to be used mainly as a defence mechanism. The capacity of echinoderms to emit light has been known for over a century, yet, research on the topic is limited for echinoderms other than brittle stars. In this work, we used data collected by Pr. Jérôme Mallefet on board of the RV Investigator during the Sampling the Abyss cruise in 2017. Luminometry measurements were done on board. We note 26 new bioluminescent species with new records in all 4 luminescent classes and even the first record for the order Molpadida (Holothuroidea). We calculated the proportions of samples from bioluminescent genera for two latitudinal (tropical and temperate) and three depth categories (upper bathyal, lower bathyal and abyssal) as well as between the four bioluminescent echinoderm classes. We used this information to compare to current knowledge of general bioluminescence distribution and found that our data differs in that the proportion of bioluminescent echinoderm genera significantly decreases in temperate waters and significantly increases in abyssal depths. Furthermore, we find that Ophiuroidea and Holothuroidea have a smaller proportion of bioluminescent than non-luminescent genera. Also, the ratio of green to blue emitters seems to decrease with depth. Using environmental data from O’Hara et al., 2019, we fitted proportion, species richness and Shannon diversity of bioluminescent genera to carbon flux, oxygen and temperature. Here we find that proportion is explained by an increased oxygen concentration, Shannon diversity by an increase in carbon and species richness increases with carbon but decreases with oxygen. Using a SIMPROF we determine that the Central-eastern bioregion is probably a transition zone for echinoderm communities from tropical and temperate waters. We present some of the luminometry measurements with the highest emission intensities for all four classes as well as data showing that the bioluminescence in Ophioplinthaca rudis is probably under cholinergic control and that the bioluminescence of the thalassometrid 69_148 tends to increase along with the added adrenaline concentration. Arm tissue from two crinoid species, Monachocrinus cf. aotearoa and the thalassometrid 80_120, and caudal skin tissue from holothuroid, Psychropotes longicauda, were sectioned and observed under blue light stimulation Observations suggest that the sacculi might be the luminescent organ in some crinoids at least. In the holothuroid we observed epifluorescence of a similar type of granular cells than Herring, 1974. However, in both cases, we are unable to make any conclusion with certainty. Eventually, luciferin and luciferase assays were performed on the thalassometrid 69_148. The results show that it is a coelenterazine-luciferase system. Coelenterazine content and luciferin activity resemble that of Amphiura filiformis.