How the liver contributes to stomach warming in the endothermic white shark Carcharodon carcharias

Background

The Great White Shark (Carcharodon carcharias) is an ecological and physiological marvel. Although this incredible creature is, unfortunately, made famous by movies like Jaws, the apex Great White Shark is critical to marine ecosystems. Not only do they regulate healthy population sizes of animals throughout the marine trophic system, but they also are part of the ocean’s clean-up crew, clearing messes such as rotting whale carcasses. What’s more is that the Great White Shark is a feat among fishes, having overcome the limitation that just about all fish deal with: ectothermic physiology.

Fish are famously ectothermic, meaning they cannot regulate their body temperature. Ectotherms’ body temperature is determined by the ambient temperature of their environment. As a result, the vast majority of fish, including most sharks, are limited to habitats where the ambient temperature matches their optimal body temperature. However, few fish species, such as the Lamnidae family of sharks (also known as Mackerel Sharks or White Sharks), have adapted a specialized mechanism called the retia mirabilia, which is commonly referred to as the “rete”. The rete provides a way to regulate body temperature and allows Lamnidae sharks to function endothermically.

The rete is a concentrated network of arteries and veins located between the gills and red muscle. The red muscle is constantly active, particularly in sharks who must always be swimming in order to pass water over their gills and obtain oxygen from the water. Muscular activity produces heat, which is harnessed by the rete via countercurrent exchange. Gills are equipped with a vast capillary network to oxygenate the blood via diffusion-driven gas exchange with the water. This close contact with the water chills the blood to the ambient temperature. After oxygenation, blood circulates past the rete, which warms the blood using muscle-produced heat, sending warm blood to be circulated through the body. This method of endothermy allows the Great White Shark to maintain a body temperature of 18°C -21°C, which is ~12°C warmer than the surrounding water! Furthermore, the Great White Shark has been found to keep their stomach at an even higher temperature of 26°C.

It has long been assumed that the elevated stomach temperature is a side effect of digestion: a result of the heat released by catabolic reactions. Although, the authors of this preprint, Bernvi and Cliff from the University of KwaZulu-Natal in South Africa, pose that this is unlikely to be the case. The Great White Shark eats by biting and tearing their prey, swallowing mouthfuls at a time. With every bite, the shark swallows water, inevitably ingesting copious volumes of cold water over the course of a meal. The cold water flows through the digestive system and cools the stomach, effectively counteracting heat produced by digestive catabolism.

Recent research has discovered the existence of a vascular passage connecting the heart to the liver in the Great White Shark, and this passage flows through the rete. This allows blood to flow from the heart, become superheated by the rete, and enter the liver. Blood flow through this vascular passage appears to be under muscular control, where hepatic sphincter muscles can open to bring blood in, or shut, to cut off flow and store superheated blood. Bernvi and Cliff suggest this vascular passage may allow the liver to store and incubate superheated blood and act as a heater for the digestive system. It is also worth noting that sharks’ livers are massive, comprising up to 25% of their body mass, and they surround the digestive tract, potentially making them effective heaters for the digestive tract (including the stomach).

Key Findings

The research team started by examining liver morphology and abdominal morphometrics to estimate the heat insulation capacity of the liver, and of the thoracic body wall, in thirteen Great White Sharks. The team discovered novel morphological characteristics of the liver, which prime the organ to supply and insulate gastrointestinal heat.

The Liver Envelope

Like most sharks, the Great White Shark’s liver consists of two large lobes situated on either side of the body. Unlike most sharks, Bernvi and Cliff found that the lobes of the liver are interlocked underneath the stomach. This anatomical feature allows the liver to effectively, and closely, envelop the digestive tract between the liver and dorsal muscle.

The benefits of this liver envelope are two-fold. Firstly, it positions the liver to effectively buffer the digestive tract from the ventral abdomen. While the dorsal body wall has a ~10cm muscle layer that effectively buffers against heat loss, the ventral abdominal body wall is extremely thin (~1.2cm) as muscle is all but absent. Therefore, the ventral body wall is a considerable vulnerability for heat loss. By interlocking underneath, the liver protects the digestive system from losing heat across the ventral body wall (Figure 1).

Secondly, Great White Sharks tend to eat large volumes of prey infrequently. A massive meal, consumed rapidly, can sustain a shark for weeks at a time. Such eating habits elicit dramatic changes in stomach volume throughout the digestion process, increasing the stomach size up to 75 times in the Great White Shark! Interlocked liver lobes allow the liver to remain effectively positioned underneath the stomach (at any and every stomach size) throughout digestion, thereby always providing an effective heat envelope.

Liver Heat via Incubated “Rete-Heat”

A shark’s liver accounts for up to 25% of their body mass, and naturally serves as a very large reservoir of blood. The liver’s high capacity for storing blood, combined with the Great White Shark’s liver envelope and vascular passage to supply the liver with rete-heated blood, gives the liver excellent potential to heat the stomach. Bernvi and Cliff examined liver vascularization to assess the likelihood of its function as an incubator of the digestive tract by retention of rete-heated blood. They found that the liver lacks any blood vessels on the outer surface, but on the inner surface, which is in direct contact with the digestive system, blood vessels were abundant, closely spaced, and large and flattened. Both this vascular distribution pattern and blood vessel morphology are incredible novel findings. Concentrated presence of blood vessels on the liver’s inner surface, and complete absence of vascularization on the outer surface, strongly suggests a role for vascular contact with the digestive system. Furthermore, blood vessels’ large, flattened morphology increases the surface area in contact with the digestive system, thereby allowing them to be more effective heat radiators. Additionally, blood flow through the vascular passage, and blood retention within the liver, are under the control of hepatic sphincter muscles, which are regulated by acetylcholine. Increased acetylcholine levels trigger the sphincter muscles to open, causing blood to enter the liver. Naturally, this would cause superheated blood to fill the liver following a meal, allowing the liver to heat the stomach during digestion, increasing the rate at which food is catabolized.

Bernvi and Cliff also examined the livers of two other species that are closely related to the Great White Shark: the Shortfin Mako Shark and Porbeagle Shark. These sharks showed the same vascularization pattern, where blood vessels were absent from the liver’s outer surface and were concentrated on the inner surface, and the same interlocking liver-lobe anatomy, which envelops the digestive tract. Regulating an optimal stomach temperature allows these sharks to maintain a higher metabolic rate, which is beneficial as it facilitates efficient digestion and a rate of energy production that maintains muscle function for effective “rete-heating”.

Why I Like This Preprint!

This study discovered what I consider to be a fascinating and incredible physiological feat in the (already astounding) Great White Shark! The endothermic capacity, made possible by the retia mirabilia utilizing heat produced by aerobic muscle activity to heat the blood, is a remarkable adaptation. To discover that the Great White Shark possesses even more sophisticated endothermic capabilities than we previously realized is extraordinary. Furthermore, I find the shark liver increasingly intriguing. In addition to carrying out their critical metabolic role, sharks’ livers are also responsible for preventing them from sinking! The shark’s liver has a very high lipid composition that can compensate for the animal’s body mass and maintain neutral buoyancy in the water column. Now add internal heater to the organ’s list of functions! This organ is truly astounding.

Questions for the Authors:

1. Might the effect of liver incubation reach further than the digestive tract? If the liver works as general insulation against heat loss over the ventral abdomen, then it might be beneficial, for instance, to incubate females’ uterus, particularly during mating season and when gestating embryos?
2. I find it very interesting that blood flow, through the vascular passage, into the liver is controlled by a hepatic muscle shunt. You theorize that this mechanism is regulated by acetylcholine, which increases following meals, allowing the stomach to be heated for the purpose of increasing the digestion rate. Might there be other chemicals that trigger the shunt? And/ or other biological reasons to heat the liver, for example, gestation of offspring or to raise the general internal temperature if the body temperature were to drop?
3. The insulating capacity of the liver allows the Great White Shark to maintain an elevated stomach temperature and, therefore, enhance the rate of digestion. For a roaming, generally slow-moving, apex predator such as this, why do you think it’s beneficial for the shark to digest rapidly as opposed to slowing their pace of life to digest slower, allowing each meal to sustain them longer?

Tags: physiology, poikilotherm, thermal biology, tolerance

doi: https://doi.org/10.1242/prelights.37176

Read preprint (1 votes)