The first evidence of intrinsic epidermal bioluminescence within ray-finned fishes in the linebelly swallower Pseudoscopelus sagamianus (Chiasmodontidae)

External and histological examination of the photophores of the linebelly swallower Pseudoscopelus sagamianus reveal three epidermal layers of cells that form the light-producing and light-transmitting components of the photophores. Photophores among the examined photophore tracts are not significantly different in structure but the presence of mucous cells in the superficial layers of the photophore suggest continued function of the epidermal photophore in contributing to the mucous coat. This is the first evidence of intrinsic bioluminescence in primarily epidermal photophores reported in ray-finned fishes.     

The photophore morphology of Selenoteuthis scintillans Voss and other lycoteuthids (Cephalopoda: Lycoteuthidae)

Females and juveniles of Selenoteuthis scintillans have photophores of several structural types, distributed on the tentacles and eyeballs, and within the mantle cavity and tail. Three distinct photophore types can be recognized on the basis of their accessory structures, though their photocytes are identical. The tail and some tentacular photophores (Type 1) lack any accessory optical structures; other tentacular and abdominal photophores (Type 2) have collagenous diffusing fibres; the anal and ocular photophores (Type 3) have a variety of iridosomes but no collagen. The distal tentacular organ is a double structure composed of a unit each of Type 1 and Type 2. Ocular photophores 1 and 5 are also double structures, composed of two Type 3 units. The photophores closely resemble in structure those of Lycoteuthis diadema. The photocytes have a marked fluorescence and luminesce on treatment with dilute hydrogen peroxide. The bio-luminescence intensity of the tail organ may be modified by chromatophore movements and has a blue-green spectral emission.
The photophores of juvenile Lampadioteuthis megaleia are similar in structure to those of Selenoteuthis but somewhat less complex. A comparison between the morphology of the photophores of lycoteuthid and enoploteuthid squids emphasizes the close similarity between the two families. At the ultrastructural level, certain photophores of both families have very characteristic microvillous blood vessels associated with the photocytes.     

Putatively luminous tissue in the abdominal pouch of a male dalatiine shark, Euprotomicroides zantedeschia Hulley & Penrith, 1966

The putatively luminous villous tissue in an abdominal pouch of a male specimen of the oceanic midwater shark Euprotomicroides zantedeschia is described. The epithelium within the pouch is probably stratified. The most conspicuous cell type is tall columnar cells, typically containing small cytoplasmic granules and a large inclusion. Cells with similar cytoplasmic characteristics, thought to be photogenic cells, are present in the epidermal skin photophores in other selachians which are known to be luminous.     

The comparative morphology of the photophores of the squid Pyroteuthis margaritifera (Cephalopoda: Enoploteuthidae)

Pyroteuthis margaritifera has morphologically distinctive photophores on the tentacles, eyeball and in the mantle cavity. The photogenic tissue in each photophore is identical, has a blue-green fluorescence and luminesces on treatment with dilute hydrogen peroxide. The photocytes frequently contain organized fibrillar material akin to that in the photocytes of certain other cephalopods. Several different types of blood vessel are present among the photocytes, including some, apparently restricted to the photophores, with a microvillous endothelium. Haemocyanin is present not only within identifiable blood vessels but also in some intercellular spaces.
On the basis of their characteristic optical systems the photophores can be separated into three types: (1) tentacular; (2) ocular and anal; (3) branchial and median abdominal. The tentacular photophores have collagenous reflector and light guide systems and the median ones are double organs. The ocular and anal organs do not have collagenous optical structures but an elaborate variety of reflective iridosomes. Those in the aperture of the photophores appear to act as interference filters. The branchial and abdominal organs have iridosomes as the major reflective tissue but collagenous fibrils function as light guides in the aperture of these organs and their emission is diffuse rather than collimated.     

Different types of photophore in the oceanic squids Octopoteuthis and Taningia (Cephalopoda: Octopoteuthidae)

The oceanic squid Octopoteuthis danue Joubin has one type of photophore on the head, body and arms, but another type on the eight arm tips. The first type has acomplexcapillary network, with elastic walls and a thick reflector. The arm tip organs have no such capillary core but a dense matrix containing paracrystalline assemblies.
Taningia danae Joubin (the only other genus in the family Octopoteuthidae) has only two large arm tip photophores. These are similar in their general organization to the arm tip photophores of Octopoteuthis , but their detailed structure is quite different.
There has evidently been independent evolution of photophores in this family of squids.     

Pharmacomorphological study of denervation induced by 6-hydroxydopamine in Porichthys photophores

The effects of 6-hydroxydopamine (6-OHDA) on the bioluminescent response of Porichthys photophores were investigated as part of a pharmacological study of the neural control of luminescence in this fish. Subcutaneous injections of 6-OHDA induce a luminescent response similar to that of norepinephrine (NE), suggesting a sympathomimetic action. The luminescent response to electrical stimulation is almost completely and irreversibly abolished within 24 hours following low-dose treatment of the photophores with 6-OHDA, while the sensitivity of these organs to exogenous NE is increased significantly over the few days post-treatment. During this period the photophores continuously emitted a steady low-level glow. Electronmicroscopic studies of such photophores revealed progressive destruction of the nerve endings. Photophore luminescent sensitivity to NE subsequently became sub-normal, and at this stage electron microscopy revealed an increasingly larger number of damaged photocytes, supportive cells and, in one case, lens cells. From these results it is suggested that 6-OHDA initially impairs neuro-photocyte transmission by destroying catecholaminergic nerve endings. In turn, the transmitter reuptake mechanism is also impaired, thus accounting for development of supersensitive responses to exogenous NE. Subnormal luminescent responses to NE appear as a result of loss of photocyte competence due to structural deterioration. The latter are interpreted as the consequence of removal of trophic factors supplied by the photophore adrenergic innervation.Suppression of luminescent response to both electrical stimulation and exogenous NE in photophores treated with higher doses of 6-OHDA, may be due to a direct effect of this drug on the receptor sites of the photocytes.     

Determination by HPLC of adrenalin (E) and of noradrenalin (NE) in certain species of mesopelagic fish in the Strait of Messina

The presence of adrenalin (E) and noradrenalin (NE) was found by HPLC both in the photophores and at other tissue levels of numerous species of mesopelagic fish in The Strait of Messina, with the aim of determining the incidence of these catecholamines in photophores, in light transmission and the eventual presence at other tissue levels. © 1998 John Wiley & Sons, Ltd.     

Adrenergic control of luminescence and cellular metabolism in Porichthys isolated luminous organs

1. Isolated photophores from the luminous fish Porichthys produce light in response to adrenaline and the metabolic inhibitors iodoacetic acid (IAA) or potassium cyanide (KCN).2. We attempted to analyse the interactions of cellular metabolism and adrenergic stimulation of the photogenic cells.3. Photophores were treated with IAA in the presence of pyruvate. In these conditions, IAA does inhibit glycolysis without inducing any luminescent activity of the cells.4. Similarly, other photophores were incubated with KCN in the presence of glucose, in order to inhibit cellular respiration while keeping the luminous system inactive.5. We observed that adrenergic stimulation of these photophores remained effective and induced a light emission, demonstrating that glycolytic and oxidative metabolism are not absolutely essential to the mechanism underlying adrenergic activation of the luminous system.6. The comparison of these luminescences with adrenergic responses of control photophores showed that the light emission to adrenaline was markedly inhibited by glycolysis blockade but potentiated by an inhibition of cellular respiration.7. As the inhibitory effect of IAA does not result from a direct action of IAA on the luminous system, these results suggest that adrenaline activation of adrenergic receptors might interact with glycolysis in photogenic cells.8. Glyceraldehyde 3-phosphate, or some derivatives, could be implicated in the glycolytic control of luminescence in the photophores.     

The trigeminofacial innervation of the cephalic lateral line organs and photophores of the lantern fish Tarletonbeania crenularis (Myctophidae)

The trigeminofacial innervation of the cephalic photophores and lateral line organs of Tarletonbeania crenularis has been studied from gross dissections. The facial and trigeminal roots leave the brainstem separately, but later intermingle forming a trigemino‐facial complex. The seventh nerve gives rise to the hyomandibular trunk and sends a branch rostrad to join the trigeminal forming the supra‐ and infraorbital trunks. The supraorbital trunk innervates the Dn photophore, the snout, the iris, the supraorbital lateral line organs and part of the olfactory sacs. The infraorbital trunk supplies the infraorbital lateral line organs, the Vn photophore and the tissues surrounding the premaxillaries. The hyomandibular trunk passes to the opercular photophores and lateral line organs, and together with a branch from the infraorbital trunk supplies the branchiostegal photophores and lateral line organs of the mandible.     

Functions of Scales and Photophores in Mesopelagic Luminescent Sharks

In sharks bioluminescence is only known from the family Squalidae. It evolved independently in two out of six squalid subfamilies, Dalatiinae and Etmopterinae. The distribution of photophores was mapped in several species. It is suggested that in the Dalatiinae, which do not school, but migrate vertically, luminescence serves as ventral countershading. The Etmopterinae school and feed close to the bottom. Their luminescence is an aid in schooling. Four different placoid scale patterns are found in luminescent sharks and they allow to accommodation the photophores in the skin.     

Integumental organs of unknown function on chelipeds of deep-sea crabs,genus Hypsophrys

Homolid crabs (Hypsophrys) from water deeper than 700 m in the Straits of Florida and Arabian Sea have smooth darkened oval spots contrasting with the surrounding roughened integument on inner and outer surfaces of each pincer at the base of the fixed finger. Cuticle is thinner over these spots than over surrounaing tissues. Beneath each spot is an organ composed of two markedly contrasting layers of tissue: (1) an outer, densely staining layer of tightly packed tubules, relatively straight and perpendicular to the overlying surface proximally but progressively convoluted and narrowed distally, finally ending blindly in association with the overlying thinned cuticle; (2) an inner layer of relatively large, eosinophilic, irregular cells with dark nuclei also trending at a right angle to the integument and bulging into the hemal sinus of the hand but separated from it by an epidermal lining. Droplets secreted from the inner layer apparently move into and along the tubules. Similar organs are known in no other crabs. The function is unknown but the structure suggests that they may be photophores.     

Ultrastructural correlates of luminescence in Porichthys photophores. II. Effects of metabolic inhibitors.

Prolonged, bright luminescent glows in Porichthys photophores are elicited by administration of 2,4-dinitrophenol (DNP) and potassium cyanide (KCN). Ultrastructural alterations of varicose nerve endings precede photocyte changes during such luminescent activity. Common alterations of nerve profiles include mitochondrial disruptions, flattening and depletion of synaptic vesicles, formation of large vacuolar cisternae, and invaginations in the contour of axolemma. Protracted luminescent activity in response to DNP results in depletion of photocyte vesicle material while vesicle and ER membranes accumulate and coil inside coalesced vesicle pools, and photocyte microvilli disappear completely. Although similar photocyte alterations are initially observed in KCN treated luminescing photophores, the early extinction of the response to KCN is related to deleterious, irreversible effects of this chemical on photocytes. These observations, along with some pharmacological manipulations, indicate that at least DNP acts initially and primarily on neural structures, probably the mitochondria, to induced transmitter release and consequent photocyte activity. Based on this and earlier studies, a chain of subcellular events leading to light emission of Porichthys photophores is proposed and discussed.     

Reflector of the body photophore in lanternfish is mechanistically tuned to project the biochemical emission in photocytes for counterillumination

Lanternfish, a family Myctophidae, use ventro-lateral body photophores for camouflage of the ventral silhouette, a strategy called counterillumination. While other deep-sea fishes possess pigmented filters and silver reflectors to match sunlight filtering down through the depths, myctophids developed a blue-green reflector for this purpose. In this study, we showed in a lanternfish Diaphus watasei that the reflector comprised monolayered iridophores containing multilayered guanine crystals which enable high reflection with light interference colouration. Platelets shape in body photophores is an unique near-regular hexagonal, probably to allow the homogeneity of reflection angle of the luminescence from photocytes. Focus point of the parabola-like reflector is positioned on the photocytes that ensures the light produced from the photocytes is redirected to the ventral direction. In vitro luminescence reaction using purified luciferase and the substrate coelenterazine showed the light emission at λ_max 454 nm, while reflection spectra of the iridophores exhibit peaks at longer wavelength, which accomplish to alter the luminescence emitted from photocytes to longer wavelength to fit the mesopelagic light environment. Taken together, we revealed multiple mechanistic elaborations in myctophid body photophores to achieve effective control of biochemical luminescence for counterillumination.     

Uptake and release of [3H]-serotonin in photophores of the midshipman fish, Porichthys notatus

A kinetic analysis of [3H]-5-HT uptake in the photocytes of the photophores of Porichthys notatus revealed a high affinity (Km: 1.71 X 10(-7] and low affinity component (Km: 1.10 X 10(-5) M). The high affinity uptake was sodium- and potassium-dependent but largely insensitive to temperatures between 0 and 20 C. Ouabain (5 X 10(-3) M) and dinitrophenol (10(-3) M) reduced uptake significantly. DMI, imipramine and fluoxetine, in that order of potency, greatly inhibited [3H]-5-HT uptake. Noradrenaline and adrenaline reduced uptake in a non-competitive manner, while dopamine, tryptophan, 5-hydroxytryptophan and Cypridina luciferin had little or not effect on uptake. Non-facilitated luminescent responses to electrical stimulation were accompanied by release of [3H]-5-HT accumulated in the photocytes. Facilitatory luminescence excitation consistently failed to induce the release of [3H]-5-HT. Electrical and adrenaline (10(-5) M) stimulation of photophores after [3H]-5-HT release has occurred, failed to elicit any additional luminescent response. The photophores were responsive to KCN (10(-3) M) under these conditions. The results indicate that a specific carrier-mediated transport system is responsible for photocytic [3H]-5-HT uptake, and that release of photocytic [3H]-5-HT is stringently regulated and followed by inhibition of luminescence excitability.     

Propagation and perception of bioluminescence: factors affecting counterillumination as a cryptic strategy

Many deep-sea species, particularly crustaceans, cephalopods, and fish, use photophores to illuminate their ventral surfaces and thus disguise their silhouettes from predators viewing them from below. This strategy has several potential limitations, two of which are examined here. First, a predator with acute vision may be able to detect the individual photophores on the ventral surface. Second, a predator may be able to detect any mismatch between the spectrum of the bioluminescence and that of the background light. The first limitation was examined by modeling the perceived images of the counterillumination of the squid Abralia veranyi and the myctophid fish Ceratoscopelus maderensis as a function of the distance and visual acuity of the viewer. The second limitation was addressed by measuring downwelling irradiance under moonlight and starlight and then modeling underwater spectra. Four water types were examined: coastal water at a depth of 5 m and oceanic water at 5, 210, and 800 m. The appearance of the counterillumination was more affected by the visual acuity of the viewer than by the clarity of the water, even at relatively large distances. Species with high visual acuity (0.11 degrees resolution) were able to distinguish the individual photophores of some counterilluminating signals at distances of several meters, thus breaking the camouflage. Depth and the presence or absence of moonlight strongly affected the spectrum of the background light, particularly near the surface. The increased variability near the surface was partially offset by the higher contrast attenuation at shallow depths, which reduced the sighting distance of mismatches. This research has implications for the study of spatial resolution, contrast sensitivity, and color discrimination in deep-sea visual systems.     

GABA inhibition of luminescence from lantern shark (Etmopterus spinax) photophores

Photogenic organs (photophores) of the velvet belly lantern shark (Etmopterus spinax) are under hormonal control, since melatonin (MT) and prolactin (PRL) trigger luminescence while α-melanocyte-stimulating hormone (α-MSH) prevents this light to be emitted. A recent study supported, however, the presence of numerous nerve fibres in the photogenic tissue of this shark. Immunohistochemical and pharmacological results collected in this work support these nerve fibres to be inhibitory GABAergic nerves since (i) GABA immunoreactivity was detected inside the photogenic tissue, where previous labelling detected the nerve fibre structures and (ii) GABA was able to inhibit MT and PRL-induced luminescence, which was on the other hand increased by the GABA(A) antagonist bicuculline (BICU). In addition, we also demonstrated that BICU can induce light per se by provoking pigment retraction in the pigmented cells composing the iris-like structure of the photophore, attaining, however, only about 10% of hormonally induced luminescence intensity at 10(-3)mol L(-1). This strongly supports that a GABA inhibitory tonus controls photophore "aperture" in the photogenic tissue of E. spinax but also that MT and PRL have more than one target cell type in the photophores.     

Photophores and Presumably Luminous Chin Barbel and Pectoral Fin Ray Filaments of Thysanactis dentex (Pisces: Stomiatoidea)

The photophores of the presumably mesopelagic deep-sea teleost Thysanactis dentex are described. The entire chin barbel and the isolated first pectoral fin ray and its filaments contain aggregations of photocytes of the same type as those present in the body-photophores and the limbus-photophores of the eyeball. The chin barbel and the first pectoral fin ray are consequently thought to be luminous.     

Comparative innervation of cephalic photophores of the loosejaw dragonfishes (Teleostei: Stomiiformes: Stomiidae): Evidence for parallel evolution of long‐wave bioluminescence

Four genera of the teleost family Stomiidae, the loosejaw dragonfishes, possess accessory cephalic photophores (AOs). Species of three genera, Aristostomias, Malacosteus, and Pachystomias, are capable of producing far‐red, long‐wave emissions (>650nm) from their AOs, a character unique among vertebrates. Aristostomias and Malacosteus posses a single far‐red AO, while Pachystomias possesses anterior and posterior far‐red AOs, each with smaller separate photophores positioned in their ventral margins. The purpose of this study was to establish the primary homology of the loosejaw AOs based on topological similarity of cranial nerve innervation, and subject these homology conjectures to tests of congruence under a phylogenetic hypothesis for the loosejaw dragonfishes. On the basis of whole‐mount, triple‐stained specimens, innervation of the loosejaw AOs is described. The AO of Aristostomias and the anterior AO of Pachystomias are innervated by the profundal ramus of the trigeminal (Tpr), while the far‐red AO of Malacosteus and a small ventral AO of Pachystomias are innervated by the maxillary ramus of the trigeminal (Tmx). The largest far‐red AO of Pachystomias, positioned directly below the orbit, and the short‐wave AO of Photostomias are innervated by a branch of the mandibular ramus of the trigeminal nerve. Conjectures of primary homology drawn from these neuroanatomical similarities were subjected to tests of congruence on a phylogeny of the loosejaws inferred from a reanalysis of a previously published morphological dataset. Optimized for accelerated transformation, the AO innervated by the Tpr appears as a single transformation on the new topology, thereby establishing secondary homology. The AOs innervated by the Tmd found in Pachystomias and Photostomias appear as two transformations in a reconstruction on the new topology, a result that rejects secondary homology of this structure. The secondary homology of AOs innervated by the Tmx found in Malacosteus and Pachystomias is rejected on the same grounds. Two short‐wave cephalic photophores present in all four genera, the suborbital (SO) and the postorbital (PO), positioned in the posteroventral margin of the orbit and directly posterior to the orbit, respectively, are innervated by separate divisions of the Tmd. The primary homologies of the loosejaw PO and SO across loosejaw taxa are proposed on the basis of similar innervation patterns. Because of dissimilar innervation of the loosejaw SO and SO of basal stomiiforms, primary homology of these photophores cannot be established. Because of similar function and position, the PO of all other stomiid taxa is likely homologous with the loosejaw PO. Nonhomology of loosejaw long‐wave photophores is corroborated by previously published histological evidence. The totality of evidence suggests that the only known far‐red bioluminescent system in vertebrates has evolved as many as three times in a closely related group of deep‐sea fishes. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.