Epaulette Shark Hemiscyllium Ocellatum Research Articles

The complete mitochondrial genome of the Epaulette Shark, Hemiscyllium ocellatum (Bonnaterre, 1788)

We present the complete mitochondrial genome of the Epaulette Shark Hemiscyllium ocellatum, sequenced with 24 primer sets. The 16,728 bp long circular genome consisted of 13 protein-coding genes, 22 tRNA genes, 2 rRNA genes, and a non-coding control region. Several protein-coding genes ended with incomplete stop codons (TA- or T–). Phylogenetic analysis indicated that H. ocellatum clusters within the Hemiscylliidae clade but separately from members of its sister genus Chiloscyllium. Utilization of the genome and primer sets presented here will be beneficial to future molecular studies involving H. ocellatum and other members of the Orectolobiformes.

Foraging behaviour of the epaulette shark Hemiscyllium ocellatum is not affected by elevated CO2

Abstract Increased oceanic uptake of atmospheric carbon dioxide (CO2) is a threat to marine organisms and ecosystems. Among the most dramatic consequences predicted to date are behavioural impairments in marine fish which appear to be caused by the interference of elevated CO2 with a key neurotransmitter receptor in the brain. In this study, we tested the effects of elevated CO2 on the foraging and shelter-seeking behaviours of the reef-dwelling epaulette shark, Hemiscyllium ocellatum. Juvenile sharks were exposed for 30 d to control CO2 (400 µatm) and two elevated CO2 treatments (615 and 910 µatm), consistent with medium- and high-end projections for ocean pCO2 by 2100. Contrary to the effects observed in teleosts and in some other sharks, behaviour of the epaulette shark was unaffected by elevated CO2. A potential explanation is the remarkable adaptation of H. ocellatum to low environmental oxygen conditions (hypoxia) and diel fluctuations in CO2 encountered in their shallow reef habitat. This ability translates into behavioural tolerance of near-future ocean acidification, suggesting that behavioural tolerance and subsequent adaptation to projected future CO2 levels might be possible in some other fish, if adaptation can keep pace with the rate of rising CO2 levels.

Comparative retinal anatomy in four species of elasmobranch

Using both light and transmission electron microscopy, we examined the retinal anatomy of four elasmobranch species with differing ecologies: the bull shark Carcharhinus leucas, Port Jackson shark Heterodontus portusjacksoni, epaulette shark Hemiscyllium ocellatum and pink whipray Himantura fai. Their retinas are typical of other vertebrates, having three nuclear and two synaptic layers, but are characterised by very large horizontal cells, low densities of ganglion cells (many of which are displaced to the inner nuclear and inner plexiform layers) and the presence of numerous myelinated axons within the nerve fibre layer. Carcharhinus leucas, H. fai and H. ocellatum have duplex retinas containing both rods and single cones. The peak ratio of rods to cones is much lower in C. leucas (4:1) and H. fai (3:1) compared to H. ocellatum (19:1), reflecting differences in diel activity patterns. No cones were observed in the retina of H. portusjacksoni, which is strongly nocturnal. The cones of H. fai lack a distinct myoid and their nuclei are located in a discrete layer sclerad to the external limiting membrane (ELM), whereas those of C. leucas and H. ocellatum have an obvious myoid, and their nuclei are located vitread to the ELM. No double/twin cones were observed in any species. Incorporating data from other studies, there is a clear correlation between rod outer segment volume and visual ecology in elasmobranchs, with smaller volumes found in partly diurnal pelagic species and larger volumes in benthic nocturnal species. This trend may reflect fundamental differences in visual temporal resolution between active and more sedentary species.

Ecophysiology of neuronal metabolism in transiently oxygen-depleted environments: Evidence that GABA is accumulated pre-synaptically in the cerebellum

Interactions between coral reef topography, tide cycles, and photoperiod provided selection pressure for adaptive physiological changes in sheltered hypoxic niches to be exploited by specialized tropical reef fish. The epaulette shark Hemiscyllium ocellatum withstands cyclic hypoxia in its natural environment, many hours of experimental hypoxia, and anoxia for up to 5 h. It shows neuronal hypometabolism in response to 5% oxygen saturation. Northern-hemisphere hypoxia- and anoxia-tolerant vertebrates that over-winter under ice alter their inhibitory to excitatory neurotransmitter balance to forestall brain ATP depletion in the absence of oxidative phosphorylation. GABA immunochemistry, HPLC analysis and receptor binding studies in H. ocellatum cerebellum revealed a heterogeneous regional accumulation of neuronal GABA despite no change in its overall concentration, and a significant increase in GABA A receptor density without altered binding affinity. Increased GABA A receptor density would protect the cerebellum during reoxygenation when transmitter release resumes. While all hypoxia- and anoxia-tolerant teleosts examined to date respond to low oxygen levels by elevating brain GABA, the phylogenetically older epaulette shark did not, suggesting that it uses an alternative neuroprotective mechanism for energy conservation. This may reflect an inherent phylogenetic difference, or represent a novel ecophysiological adaptation to cyclic variations in the availability of oxygen.

Reproductive and feeding ecology of parasitic gnathiid isopods of epaulette sharks ( Hemiscyllium ocellatum) with consideration of their role in the transmission of a haemogregarine

Epaulette sharks Hemiscyllium ocellatum were surveyed on Heron Island, Great Barrier Reef, Australia for gnathiid isopods and protozoan (haemogregarine) parasites to determine the prevalence and intensity of infection and to investigate the potential role of gnathiids as vectors of these haemogregarines, the first such study carried out on elasmobranchs. Juvenile gnathiids were collected and quantified using a novel non-invasive and chemical-free technique and gnathiid squashes were examined for haemogregarine developmental stages. The feeding and reproductive ecology of the Gnathia spp. was investigated to better understand the relationship between gnathiids and haemogregarines. Gnathiids were found on all sharks and intensities ranged between two and 66. Only third-stage gnathiid juveniles were found, which fell into two size groups (A and B). These juveniles remained attached to H. ocellatum for up to 17 days, the longest period of attachment yet recorded for gnathiids. Group A female gnathiids produced broods of 45–187 (median =120) first stage juveniles from between 54 and 82 days (median=63 days) after detachment. First stage juveniles survived for an average of 15.8±0.1 (SEM) days without feeding. The prevalence (6.7%) and parasitaemia (usually <0.1% infected erythrocytes) of infections of the haemogregarine Haemogregarina hemiscyllii were relatively low and most stages were immature gamonts. Two undescribed Gnathia spp. were identified by examining adult male gnathiids that metamorphosed from juveniles from each of the two size groups. Our hypothesis that Gnathia spp. transmit H. hemiscyllii is neither supported or refuted, as although intact H. hemiscyllii gamonts were detected in squashes of gnathiids that had engorged on haemogregarine-positive H. ocellatum 24–57 days previously, no further developmental stages were detected.

The behavioural role of pit organs in the epaulette shark

Epaulette sharks Hemiscyllium ocellatum in three treatments, pit organs (free neuromasts) ablated, sham‐operated and normal (n = 8 for each treatment), showed a significant preference for facing upstream in a flume (P &lt; 0·05). There were no significant differences in the mean angles or angular variances among treatments. Individuals with ablated pit organs, however, spent significantly less time moving around than controls (P &lt; 0·05), suggesting that pit organs contributed to motivation for activity. Pit organs do not appear to make an important contribution to rheotaxis in H. ocellatum. It is suggested that this may be due to structural differences in the pit organs of H. ocellatum compared with other species.

Brain blood flow and blood pressure during hypoxia in the epaulette shark Hemiscyllium ocellatum, a hypoxia-tolerant elasmobranch.

The key to surviving hypoxia is to protect the brain from energy depletion. The epaulette shark (Hemiscyllium ocellatum) is an elasmobranch able to resist energy depletion and to survive hypoxia. Using epi-illumination microscopy in vivo to observe cerebral blood flow velocity on the brain surface, we show that cerebral blood flow in the epaulette shark is unaffected by 2 h of severe hypoxia (0.35 mg O2 l-1 in the respiratory water, 24 C). Thus, the epaulette shark differs from other hypoxia- and anoxia-tolerant species studied: there is no adenosine-mediated increase in cerebral blood flow such as that occurring in freshwater turtles and cyprinid fish. However, blood pressure showed a 50 % decrease in the epaulette shark during hypoxia, indicating that a compensatory cerebral vasodilatation occurs to maintain cerebral blood flow. We observed an increase in cerebral blood flow velocity when superfusing the normoxic brain with adenosine (making sharks the oldest vertebrate group in which this mechanism has been found). The adenosine-induced increase in cerebral blood flow velocity was reduced by the adenosine receptor antagonist aminophylline. Aminophylline had no effect upon the maintenance of cerebral blood flow during hypoxia, however, indicating that adenosine is not involved in maintaining cerebral blood flow in the epaulette shark during hypoxic hypotension.

The occurrence, distribution and pathology associated with gnathiid isopod larvae infecting the epaulette shark, Hemiscyllium ocellatum

Gnathiid isopod praniza larvae were found to infect the epaulette shark Hemiscyllium ocellatum. All sharks carried larvae on their external body surface, with the preferred attachment site in both sexes around the cloaca ( P<0.05). The claspers were the second site of preference in male sharks. Within the buccal and branchial cavities, about 16% of larvae were attached to the roof and floor of the mouth and 84% attached to the gills. A significant positive correlation existed between larval number and fish size. Histological examination showed that larval attachment in the buccal cavity elicited variable responses, the most severe being a loss of epithelium and compression of underlying tissue. No host cellular response or tissue proliferation was observed. Praniza attached preferentially to the efferent side of gill filaments (relative to blood flow), and caused loss of epithelium, compression of tissue, and a small amount of connective tissue proliferation. Attachment to the gill septum or to the afferent side of the gill filament caused lamellar disruption, a cellular inflammatory response, and connective tissue proliferation. Scanning electron microscopy showed little obvious praniza-induced gill damage, other than localised tissue distortion to form pockets around larvae attached between filaments. The results suggest that praniza larvae do not cause sufficient tissue damage to adversely affect the health of this shark species.

Histology of dart tag insertion sites in the epaulette shark

Samples of dermal and epidermal tissues of epaulette sharks Hemiscyllium ocellatum were examined histologically to assess damage caused by tagging. Tissues from around tag sites were removed at time intervals ranging from 100 min to 284 days post‐tagging. These samples showed acute and chronic responses to tagging. Acute responses consisted of localized tissue breakdown and haemorrhaging, and occurred within the first few hours after tag insertion. At 10 h post‐tagging, an intermediate response was apparent. This phase was characterized by further haemorrhaging and red and white blood cell movement into the wound area. The chronic response observed in the 10–284‐day post‐tagging samples was characterized by fibrous tissue formation to sequester the tag. This tissue presumably protects the adjacent musculature from further trauma produced by movement of the tag and provides a continuous barrier between the internal and external milieu. Tissue repair appeared to progress consistently in all specimens and no secondary infections at the tag site were seen. Tagging produced only localized tissue disruption and did not appear to be detrimental to the long term health of individual sharks. Our findings show that spaghetti style dart tagging is an acceptable method for marking individuals (40–75+ cm total length) of this species.

Histology of dart tag insertion sites in the epaulette shark

Samples of dermal and epidermal tissues of epaulette sharks Hemiscyllium ocellatum were examined histologically to assess damage caused by tagging. Tissues from around tag sites were removed at time intervals ranging from 100 min to 284 days post-tagging. These samples showed acute and chronic responses to tagging. Acute responses consisted of localized tissue breakdown and haemorrhaging, and occurred within the first few hours after tag insertion. At 10 h post-tagging, an intermediate response was apparent. This phase was characterized by further haemorrhaging and red and white blood cell movement into the wound area. The chronic response observed in the 10–284-day post-tagging samples was characterized by fibrous tissue formation to sequester the tag. This tissue presumably protects the adjacent musculature from further trauma produced by movement of the tag and provides a continuous barrier between the internal and external milieu. Tissue repair appeared to progress consistently in all specimens and no secondary infections at the tag site were seen. Tagging produced only localized tissue disruption and did not appear to be detrimental to the long term health of individual sharks. Our findings show that spaghetti style dart tagging is an acceptable method for marking individuals (40–75+ cm total length) of this species.