Julien M. Claes

Is Extreme Bite Performance Associated with Extreme Morphologies in Sharks

As top predators in many oceanic communities, sharks are known to eat large prey and are supposedly able to generate high bite forces. This notion has, however, largely gone untested due to the experimental intractability of these animals. For those species that have been investigated, it remains unclear whether their high bite forces are simply a consequence of their large body size or the result of diet‐related adaptation. As aquatic poikilotherms, sharks can grow very large, making them ideal subjects with which to investigate the effects of body size on bite force. Relative bite‐force capacity is often associated with changes in head shape because taller or wider heads can, for example, accommodate larger jaw muscles. Constraints on bite force in general may also be released by changes in tooth shape. For example, more pointed teeth may allow a predator to penetrate prey more effectively than blunt, pavementlike teeth. Our analyses show that large sharks do not bite hard for their body size, but they generally have larger heads. Head width is the best predictor of bite force across the species included in our study as indicated by a multiple regression model. Contrary to our predictions, sharks with relatively high bite forces for their body size also have relatively more pointed teeth at the front of the tooth row. Moreover, species including hard prey in their diet are characterized by high bite forces and narrow and pointed teeth at the jaw symphysis.

Hormonal control of luminescence from lantern shark (Etmopterus spinax) photophores

SUMMARY The velvet belly lantern shark (Etmopterus spinax) emits a blue luminescence from thousands of tiny photophores. In this work, we performed a pharmacological study to determine the physiological control of luminescence from these luminous organs. Isolated photophore-filled skin patches produced light under melatonin (MT) and prolactin (PRL) stimulation in a dose-dependent manner but did not react to classical neurotransmitters. Theα -melanocyte-stimulating hormone (α-MSH) had an inhibitory effect on hormonal-induced luminescence. Because luzindole and 4P-PDOT inhibited MT-induced luminescence, the action of this hormone is likely to be mediated through binding to the MT2 receptor subtype, which probably decreases the intracellular concentration of cyclic AMP (cAMP) because forskolin (a cAMP donor) strongly inhibits the light response to MT. However, PRL seems to achieve its effects via janus kinase 2 (JAK2) after binding to its receptor because a specific JAK2 inhibitor inhibits PRL-induced luminescence. The two stimulating hormones showed different kinetics as well as a seasonal variation of light intensity, which was higher in summer (April) than in winter (December and February). All of these results strongly suggest that, contrary to self-luminescent bony fishes, which harbour a nervous control mechanism of their photophore luminescence, the light emission is under hormonal control in the cartilaginous E. spinax. This clearly highlights the diversity of fish luminescence and confirms its multiple independent apparitions during the course of evolution.

Control of luminescence from pygmy shark (Squaliolus aliae) photophores.

SUMMARY The 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 α-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 MT2 receptor subtype, as the MT2 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.

Functional physiology of lantern shark (Etmopterus spinax) luminescent pattern: differential hormonal regulation of luminous zones.

SUMMARY Lantern sharks are small deep-sea sharks that harbour complex species-specific luminescent photophore patterns. The luminescent pattern of one of these sharks, Etmopterus spinax, is made up of nine luminous zones. Previous experiments revealed that in the largest of these zones (ventral zone), photophores are under hormonal control, light being triggered by both melatonin (MT) and prolactin (PRL). In this study, we analysed the luminescent responses to MT and PRL in five other luminous zones from 12 female and eight male E. spinax specimens. The results showed that all luminous zones respond to both hormones, with each zone having its own kinetic parameters (maximum light intensity, Lmax; total light emitted, Ltot; time from stimulation to Lmax, TLmax), which confirms the multifunctional character of this sharks luminescence. Ltot and Lmax were found to be directly dependent on the photophore density (PD) of the luminous zone, while TLmax varied independently from PD. In addition, we demonstrate a sexual dimorphism in the luminescent response to PRL, with male specimens having smaller Ltot and TLmax in the luminous zones from the pelvic region. As this region also harbours the sexual organs of this species, this strongly suggests a role for the luminescence from these zones in reproduction.

The lantern shark's light switch: turning shallow water crypsis into midwater camouflage.

Bioluminescence is a common feature in the permanent darkness of the deep-sea. In fishes, light is emitted by organs containing either photogenic cells (intrinsic photophores), which are under direct nervous control, or symbiotic luminous bacteria (symbiotic photophores), whose light is controlled by secondary means such as mechanical occlusion or physiological suppression. The intrinsic photophores of the lantern shark Etmopterus spinax were recently shown as an exception to this rule since they appear to be under hormonal control. Here, we show that hormones operate what amounts to a unique light switch, by acting on a chromatophore iris, which regulates light emission by pigment translocation. This result strongly suggests that this sharks luminescence control originates from the mechanism for physiological colour change found in shallow water sharks that also involves hormonally controlled chromatophores: the lantern shark would have turned the initial shallow water crypsis mechanism into a midwater luminous camouflage, more efficient in the deep-sea environment.

Iso-luminance counterillumination drove bioluminescent shark radiation

Counterilluminating animals use ventral photogenic organs (photophores) to mimic the residual downwelling light and cloak their silhouette from upward-looking predators. To cope with variable conditions of pelagic light environments they typically adjust their luminescence intensity. Here, we found evidence that bioluminescent sharks instead emit a constant light output and move up and down in the water column to remain cryptic at iso-luminance depth. We observed, across 21 globally distributed shark species, a correlation between capture depth and the proportion of a ventral area occupied by photophores. This information further allowed us, using visual modelling, to provide an adaptive explanation for shark photophore pattern diversity: in species facing moderate predation risk from below, counterilluminating photophores were partially co-opted for bioluminescent signalling, leading to complex patterns. In addition to increase our understanding of pelagic ecosystems our study emphasizes the importance of bioluminescence as a speciation driver.

Nitric oxide in the control of luminescence from lantern shark (Etmopterus spinax) photophores.

SUMMARY Photophores (photogenic organs) of the lantern shark Etmopterus spinax are under hormonal control, with prolactin (PRL) and melatonin (MT) triggering the light emission. Differential sensitivity to these hormones in adult individuals suggests, however, that the luminescence of this shark is controlled by an additional mechanism. In this study, different techniques were used to investigate a potential modulator of E. spinax luminescence – nitric oxide (NO). NO synthase (NOS)-like immunoreactivity (IR) was found in the photocytes (photogenic cells) of the photophores. In addition, acetylated tubulin IR also supported the presence of nerves running through the photogenic tissue and innervating different structural elements of the photophores: photocytes, pigmented cells from the iris-like structure and lens cells. Pharmacological experiments confirmed a modulatory action of NO on the hormonally induced luminescence: NO donors sodium nitroprusside (SNP) and hydroxylamine decreased the time to reach the maximum amplitude (TLmax) of MT-induced luminescence while these substances decreased the maximum amplitude of PRL-induced luminescence (and also the TLmax in the case of SNP). The small impact of the NOS inhibitor l-NAME on hormonally induced luminescence suggests that NO is only produced on demand. The cGMP analogue 8BrcGMP mimicked the effects of NO donors suggesting that the effects of NO are mediated by cGMP.

Control of luminescence from lantern shark (Etmopterus spinax) photophores

The velvet belly lantern shark (Etmopterus spinax) is a common deep-sea shark that has been used, in the recent years, as a model for experimental studies on physiological control of shark luminescence. These studies demonstrated that, unlike any other luminous organism, the luminescence of this shark was under a dual control of hormones and neurotransmitters (or neuromodulators). The present paper, by making a short review of histological and pharmacological results from these studies, aims to propose a first model of luminescence control in E. spinax.

Cytological changes during luminescence production in lanternshark (Etmopterus spinax Linnaeus, 1758) photophores

Studying an organism’s photogenic structures at the ultrastructural level is a key step in the understanding of its light-emission process. Recently, the photophore ultrastructure of the deep-sea lanternshark Etmopterus spinax Linnaeus, 1758 was described. The photocytes appeared to be divided into three areas including an apical granular area, which contains inclusions and was hypothesized to be the light-producing reaction site. In this study, we investigated the morphological changes occurring within the granular area during the bioluminescent emissions induced by two hormones: prolactin and melatonin. Prolactin provoked the formation of new structures in the granular area, the “grey particles”, whose number was proportional to the amount of light produced by the reaction. An increase in the number of granular inclusions was also detected at the end of the prolactin-induced light emission. Conversely, melatonin induced a decrease in the number of granular inclusions and an increase in their diameter. An effect of hormones was also observed on the iris-like structure where they triggered pigment retraction and hence an increase in the iris aperture diameter. This is consistent with previous findings and is shown for the first time at the cellular level. The possible role of grey particles in E. spinax light-emission mechanism is discussed, while granular inclusion is considered to be E. spinax’s intracellular luminescence site. Regarding typical shark long-lasting glows, a new term (“glowon”) is proposed to characterize this novel membrane-free microsource.

Ultrastructural organization of lantern shark ( Etmopterus spinax Linnaeus, 1758) photophores

Etmopterus spinax Linnaeus, 1758 is a deep-sea lantern shark that emits blue light thanks to thousands of tiny cup-shaped organs made of a pigmented sheath enclosing light-emitting cells topped by an iris-like structure and a lens. In this study, we investigate the ultrastructure of these photophores in order to improve our understanding of the light emission process. The presence of a novel layer, a putative reflector upholstering the pigmented sheath, is highlighted. The intracellular organization of the photocytes is addressed. They appear as regionalized cells: their basal area is occupied by an ovoid nucleus, their medial area is highly vesiculated and their apical area, oriented toward the photophore center, displays small granular inclusions. We hypothesize this granular area to be the intracellular site of photogenesis in E. spinax, as it is also the most fluorescent part of the photocyte.