Control of luminescence from pygmy shark (Squaliolus aliae) photophores

Abstract

SUMMARYThe smalleye pygmy shark (Squaliolus aliae) is a dwarf pelagic shark from the Dalatiidae family that harbours thousands of tiny photophores. In this work, we studied the organisation and physiological control of these photogenic organs. Results show that they are mainly situated on the ventral side of the shark, forming a homogeneous ventral photogenic area that appears well suited for counterillumination, a well-known camouflage technique of pelagic organisms. Isolated ventral skin patches containing photophores did not respond to classical neurotransmitters and nitric oxide but produced light after melatonin (MT) application. Prolactin and a-melanocyte-stimulating hormone inhibited this hormonally induced luminescence as well as the spontaneous luminescence from the photogenic tissue. The action of MT seems to be mediated by binding to the MT 2 receptor subtype, as the MT 2 receptor agonist 4P-PDOT inhibited the luminescence induced by this hormone. Binding to this receptor probably decreases the intracellular cAMP concentration because forskolin inhibited spontaneous and MT-induced luminescence. In addition, a GABA inhibitory tonus seems to be present in the photogenic tissue as well, as GABA inhibited MT-induced luminescence and the application of bicuculline provoked luminescence from S. aliae photophores. Similarly to what has been found in Etmopteridae, the other luminous shark family, the main target of the luminescence control appears to be the melanophores covering the photocytes. Results suggest that bioluminescence first appeared in Dalatiidae when they adopted a pelagic style at the Cretaceous/Tertiary boundary, and was modified by Etmopteridae when they started to colonize deep-water niches and rely on this light for intraspecific behaviours.

Iso-luminance counterillumination drove bioluminescent shark radiation

“…Although these small deep-sea sharks encompass ~12% of current shark diversity, with > 50 described species, their luminescence is rarely observed. Moreover, contrary to the condition in other bioluminescent animals, their tiny light producing organs (photophores) are primarily controlled by hormones rather than by nerves4567 and are found in very large numbers to form a diversity of patterns whose adaptive benefit is unclear18910111213. Indeed, since these organs are mostly situated on the ventral side (Fig.…”

Photon Hunting in the Twilight Zone: Visual Features of Mesopelagic Bioluminescent Sharks

“…the lanternfish Triphoturus mexicanus , the ambient light intensity is monitored by photoreceptors protruding into the lumen of the pineal vesicle [47]. Such mechanisms have not yet been discovered in bioluminescent sharks, although the presence of a clear pineal window and the use of melatonin to control photophore emission by all species investigated in this group [31], [32], [33], [48] clearly suggest the involvement of the pineal vesicle in the luminescence control mechanism.…”

“…Squaliolus aliae and E. splendidus , which both possess small fusiform bodies, clearly have a pelagic habit [33], [56], [60], while E. spinax , E. lucifer and T. kabeyai are larger benthopelagic sharks [27], [60]. Observation and capture data indicate that at least some of these species undergo diel vertical migrations, probably to follow their prey [38], [56], [61], [62].…”

“…Observation and capture data indicate that at least some of these species undergo diel vertical migrations, probably to follow their prey [38], [56], [61], [62]. All species share a similar diet, which consists mainly of small mesopelagic fishes (mainly myctophids), crustaceans and cephalopods [27], [33], [63] although E. spinax is also known to feed on benthic and dead animals [64]. However, their teeth and jaw morphology display striking dissimilarities.…”

“…Although they represent ∼12% of currently known shark species and are key predators of many oceanic communities, their biology and ecology is poorly known [27]. It is assumed that most of them perform vertical migrations and use their hormonally-controlled photogenic organs (photophores), whose intrinsic chemistry remains mysterious [28], to disguise their silhouette in the water column when viewed from below, a common pelagic camouflage tactic called counterillumination and used by many species [29], [30], [31], [32], [33]. Many lanternsharks are also thought to use their photophores for bioluminescent signalling, either to facilitate intraspecific behaviours [34], [35], [36], via clade-specific lateral markings, or to highlight the presence of their defensive finspines (an interesting example of bioluminescent aposematism) [37].…”