A “walking shark”, or Epaulette shark, Missol, West Papau, Indonesia. Credit: Matthew Oldfield Photgraphy.
Figure 1. A “walking shark”, or Epaulette shark,  rests upon the benthos in Missol, West Papau, Indonesia. The species demonstrates remarkable talents in camouflage, a  consequence of it’s motley patterning. The elongated, eel-like body shape of the Epaulette shark enables the species to navigate through the labyrinth of passages within the coral reef structure. Credit: Matthew Oldfield Photgraphy.

The Epaulette shark, Hemiscyllium ocellatum, is a somewhat diminutive species with an elongated body shape resembling that of an eel. Named accordingly to the dark patch present behind the gill slits on either side of the shark, this motley patterned shark frequents shallow coral reefs and coastal waters ranging from Western Australia to New Guinea. The elongated body shape of the Epaulette shark enables the species to navigate and explore the confined, meandering passageways within the coral reef structure in order to avoid predation with larger shark species (Figure 1). Rather than dynamically swimming, the Epaulette shark often “walks”.

The following video demonstrates such movement in a captive specimen: the combination of a “wriggling” motion of the shark’s body and highly mobile paired pectoral and pelvic fins enable the shark to glide over the benthos. The fins themselves are paddle-like and broad, with an internal skeletal structure that promotes greater flexibility and dramatically increases range of motion. In this way, the paired fins of the Epaulette shark assist in propulsion and maneuverability.  Such adaptations resemble the prototype limb and movements used by the first tertrapods to colonise the land and may provide insight into the evolution of terrestrial locomotion.

Movement of the Epaulette shark’s highly mobile paired pectoral and pelvic fins, combined with a “wriggling” motion of the body trunk, propel the Epaulette shark forwards whilst swimming – with the shark appearing to almost glide over the benthos. Such movements enable to Epaulette shark to explore the coral matrix whilst also facilitating avoidance behaviour towards larger predatory species. Video credit: Meghan Wharton/Filmed at Chester Zoo Aquarium. 

Life in an ever-changing environment

Epaulette sharks inhabit a frequently changing environment in shallow intertidal and coastal waters. The Great Barrier Reef, for example, in North-eastern Australia experiences extreme tides and profound variances in temperature. The retreating tide creates a labyrinth of isolated rocky pools, exposing the top most branches of the coral formations, which forces larger shark species out into deeper waters. Here, the Epaulette’s small size and elongate body become an ecological advantage, allowing the shark to explore the rich feeding opportunities within the exposed tidal pools without disturbance.

Nevertheless, what happens if the retreating tide renders the shark beached on the reef, exposed to the sun and elements? Generally, most vertebrates cannot tolerate prolonged periods of oxygen deprivation, with severe hypoxia and even anoxia occurring within a few minutes. The Epaulette shark however, has evolved methods that enhance survival in this naturally cyclic hypoxic environment. Exposure to hypoxia primes the respiratory and metabolic responses in Epaulette sharks. Such conditioning  motivates the reduction of both respiratory and heart rates – subsequently causing the shark’s organs to be shut down one by one. All non-essential brain function is switched off in order to further reduce oxygen consumption and demands. And if this doesn’t work, the shark switches to a second plan of action – the Epaulette shark is the only species that can literally walk its way out of trouble.

The walking shark – The Epaulette shark remains on the reef irrespective of the retreating tide. It lingers in tidal pools where conditions become increasingly hypoxic, i.e. where dissolved oxygen concentration is low. A reduction in brain activity, resulting from chemical changes within the brain, lowers the Epaulette’s metabolies. Additionally, “walking”enables the Epaulette shark to move between the tidal pools formed by the retreating tide. It may be slow going, but here the shark can exploit rich resources that few organisms can access let alone utilise. Video credit: BBC One’s Great Barrier Reef with David Attenborough/ YouTube (channel)

The “walking” shark: ecological advantages

It may be slow going but the somewhat clumsy gait of the Epaulette shark enables it to, in effect, “walk” between the shallow pools formed by the receding tide. Movement, resulting from a wriggling motion and its mobile pectoral and pelvic fins, enable the shark to clamber between rocky pools and exploit the rich feeding opportunities that few other organisms can utilise. Epaulette sharks are opportunistic feeders that undergo a transition in diet following maturation. Juveniles typically feed upon a range of prey items (e.g. worms, amphipods, and small teleost fish). Whereas the diet of mature sharks is focused primarily upon crustaceans. Within the tidal pools themselves, Epaulette sharks excavate hidden and buried prey by flipping over debris or probing sandy patches using a “suction-type” action produced using the shark’s mouth and gill musculature. Such behaviour is suggestive of a niche similar to that of eels rather than a shark.

Field observations also indicate that the Epaulette shark sometimes chews its food. Chewing would reduce stress upon the shark’s oesophagus by breaking down the calcite exoskeletons of crustacean prey, whilst also enhancing metabolies within the stomach, further increasing absorption of nutrients. The ecological advances of the Epaulette shark’s walking abilities are great; enabling a functionally marine organism to exploit the terrestrial environment, moving between oxygen deprived pools which few other organism can utilise. But what internal mechanisms enable the Epaulette shark to survive in such hypoxic conditions, both in the terrestrial environment and within intertidal rocky pools?

Despite resembling a “death-like” state, the Epaulette shark is still able to hunt, feed, and traverse between tidal pools. Adenosine secretions in the brain act as an endrogenous neural depressant, enabling the shark to reduce ATP consumption whilst maintaining brain fucnction. Credit: BBC/Rachel Hunter.
Figure 2. Adenosine secretions in the brain act as an endrogenous neural depressant, enabling the shark to reduce ATP consumption whilst maintaining brain function. Despite resembling a “death-like state”, the Epaulette shark is still able to hunt, feed, and traverse between intertidal rocky pools. Credit: BBC One/Shark – The Epaulette shark/Rachel Hunter

Adaptive mechanisms: chemical control in the brain

The Epaulette shark is one of the few vertebrates that are capable of tolerating prolonged extreme hypoxia. In a recent study, anoxia was found to affect the shark’s rate of responsiveness and the concentration of ATP and adenosine in the brain. Brain ATP and adenosine act as an endogenous neural depressant, enabling the shark’s nerves to function under low concentrations of oxygen (figure 2).  Anoxia resulted in a 3.5-fold increase in the secretion of adenosine in the brain, resulting in metabolic depression. Alternatively, when test subjects were exposed to an adenosine receptor antagonist (aminophylline), the shark’s level of responsiveness to touch, orientation in the water column, and the frequency of ventilatory movements increased by 46%. Furthermore, adenosine receptor activation in Epaulette sharks serves to initiate metabolic depression whilst reducing ATP consumption, thus maintaining brain function.

 

An Epaulette shark exploring the reef top at low tide. Such behaviour offers an ecological advantage in exploiting an environment that few other organisms can inhabit, let alone utilise for its resources.  Credit: BBC/Rachel Hunter.
Figure 3. An Epaulette shark exploring the reef top at low tide. Such behaviour is maintained by neurological responses in the brain – the concentration of an inhibitory neurotransmitter GABA changes regionally within the Epaulette shark’s brain. Concentrations are only elevated within key areas of the brainstem. Thus vital areas of the brain and organs are protected from neuronal damage.  Credit: BBC One/Earth – Revealing the secret lives of sharks/Rachel Hunter.

Elevated secretions of the inhibatory neurotransmitter GABA (Gamma-Amino Butyric acid) in the brain have also been observed to facilitate neural depression and a reduction in ATP consumption. Such a protective mechanism would enable hypoxia/anoxia tolerant animals to withstand the damaging effects of oxygen deprivation. However in regards to the Epaulette shark, the inhibitory neurotransmitter GABA is not elevated during neuroprotective neuronal depression. Research has indicated that the overall mean concentration of GABA in the brain doesn’t increase in response to a decrease in environmental oxygen concentration.  Instead GABA concentration changes regionally, with a significant increase in key areas of the brainstem in response to hypoxic conditions (Figure 3). Such mechanisms are likely to be multifactorial; however adenosine secretions increase 3.5-fold (as previously presented) in response to anoxic conditions – once again suggestive that adenosine secretions in the brain correspond with depression of metabolies and subsequent neuroprotective responses in the Epaulette shark.

 

The scientific outlook

Past studies regarding vertebrates, such as freshwater turtles and Crucian carp, provide an understanding of their ability to combat anoxia in a cold environment. The Epaulette shark however is capable of similar abilities but whilst frequenting a much warmer environment, similar to that of human body temperature. Understanding such successful mechanisms in the Epaulette shark will provide a greater understanding of organism ecophysiology in extreme environments. Furthermore, it may also lead to advances in neuroscience and facilitate the development of medicinal strategies in the treatment of stroke and heart attack patients, birth hypoxia, brain injuries, and potentially preoperative preconditioning in patients about to undergo cardiac or cerebrovascular surgery – all of which are conditions that experience an extreme deprivation of oxygen.  An understanding of such mechanisms may reduce morbidity and mortality in patients with conditions associated with hypoxia.

Strike sites in the brain, indicated by the red outline of the CT scan. Understanding the tolerance mechanims regarding aoxia in the Epaulette shark could give rise to neuro-medicinal interventions that may reduce the extent of damage arising from insufficient oxygen concentrations, for example, such deprivations ofoxygen that occur in stroke patients. Credit: Naccarato et al., Lipids in Health and Disease 2010.
Figure 4. Stroke sites in the brain, indicated by the red outline of the CT scan. Understanding the tolerance mechanisms regarding anoxia in the Epaulette shark could give rise to neuro-medicinal interventions. Such interventions have the potential to reduce the extent of damage that can arise from insufficient oxygen concentrations, for example, stroke pateinst experience severe oxygen deprivation following blood restriction to parts of the brain. Credit: Naccarato et al., Lipids in Health and Disease 2010.

Epaulette sharks are considered to be remnants of the past; organisms which were present when the oceans were in a hypoxic state. In regards to conservation efforts, the Epaulette shark may hold the key to survival for aquatic species as today’s oceanic world becomes increasingly oxygen deprived. That being said, just how the Epaulette shark detects the initial drop in oxygen is still a mystery to science. Time and further studies into this diminutive shark species, especially with regards to the mechanisms underpinning hypoxia tolerance, may prove vital to both medical breakthroughs and the capability of other species to survive in an increasingly hypoxic environment.

 

 

 

 

 

 

 

 

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