Humpback Whale’s Physiology and Diving Mechanics
Instructor course handout
Valentino Rinaldi
Abstract
Humans diving below the water surface must tolerate low oxygen, high carbon dioxide, and an increase in water pressure. In 1929, August Krogh, Nobel laureate and grandfather of comparative physiology, postulated the Krogh principle, stating that «for every defined physiological problem, there is an optimally suited animal that would most efficiently yield an answer». This review demonstrates how humpback whales have diverse adaptations in physiology and mechanics that apply for an array of diving behaviors. Humpback whales diving characteristics range within the same order of magnitude of humans, which gives to this study a significant value. Some of these adaptations are still not completely understood. Research is not complete, and sometimes limited to dated investigations on dead samples. Broader studies on cetaceans will be mentioned when necessary, leaving the reader with the right to note possible differences. This study highlights the adaptations that make humpback whales better divers compared to average humans. The objective is to provide the freediving community with awareness for the importance of certain anatomy parts and processes when diving, and possibly developing training concepts and more efficient equipment.
Introduction
Northern Hemisphere fully grown humpback whales reach an average length of 15-16 m. Southern humpbacks reach 18 m. Females are generally slightly larger than the males. Newborn calves are roughly the length of their mother’s head, which is about 30% of the overall length. At birth, they measure 4.5 to 6 m. Body mass typically is in the range of 25–35 metric tons, with large specimens weighing over 40 metric tons. Calf average weight at birth is 900kg. The lifespan is believed to be between 50 and 100 years. The diving capabilities of marine mammals vary immensely. On average, a humpback whale can hold its breath up to 45 minutes. New born calves can hold their breath for 5 minutes. Sonar systems can be used to track whales underwater. Non-calf humpback whales in Alaska appeared to restrict their dives to 150m and rarely exceeded depths of 120m. One humpback whale has been recorded diving to 240 m. A study in the coast of Norway showed that over 70% of the dives performed by the whales were shallower than 50 m, a median depth of less than 30 m, and lasted for less than 3 min. The longest dive lasted for 21.05 min and the deepest dive was recorded at 265.5 m. Dolphin (1987) postulated that dives to depths of 40–60 m and 4–6 minutes in duration likely represented the highest distribution, because the percentage of time spent at the surface increased progressively for dives greater than 60 m, while was constant under 60 m.
Fig.1 – Frequency distributions for diving parameters (K.O.Zubiri, 2017).
Evolution
Humpback whales are cetacean baleen whale marine mammals part of the rorquals Balaenopteridae family. Hippos are the closest living relatives of whales, but they are not the ancestors of whales. The first whales evolved over 50 million years ago, (40 million years before humans), and the ancestor of this group was terrestrial. These animals evolved nostrils positioned further and further back along the snout. This trend has continued into living whales, which have a «blowhole» (nostrils) located on top of the head above the eyes. When humpback whales swim, they move their tails up and down. This is because whales evolved from walking land mammals whose backbones did not naturally bend side to side, but up and down. This can easily be seen watching a dog running. As whales began to swim by undulating the whole body, other changes in the skeleton allowed their limbs to be used more for steering than for paddling. In general, cetaceans possess many of the same physiological systems such as circulatory, digestive, respiratory, and nervous systems as the land mammals from which they evolved.
Fig.2 – Baleen whales evolution diagram (The evolution of whales,)
Respiratory adaptations
It is easy to assume that whales must have big lungs. But in fact, human lungs take up 7% of the internal body cavity while a whale’s lungs only take up 3%. If the lungs were really large, more nitrogen would be able to be contained and then absorbed, which would create toxicity in the body and decompression illness. Therefore, the lungs are fairly small and the animal has adapted so that it can retain as much oxygen as possible while diving. The traditional approach to represent a whale’s respiratory system is the model of lung/alveolar collapse, developed by Scholander, in 1940. Scholander assumed that the trachea behaved like an idealized non-compressible pipe connected to a very compliant lung/alveolar space (balloon-pipe model; Bostrom et al., 2008), allowing the alveolar collapse depth to be estimated from Boyle’s law (Scholander, 1940; Bostrom et al., 2008). Scholander proposed that the cartilaginous reinforcement prevents the compression of the airway, facilitating alveolar collapse and cessation of gas exchange. Collapsing the lungs prevents barotrauma. The collapse forces the air away from the alveoli stopping the gas exchange. This also prevents a high nitrogen blood level to occur. Depth of lung collapse is dependent on diving lung volume, which can be altered, based on the expecting dive depth. After alveoli collapse surfactant is required for re-inflation. In marine mammals, surfactants have the role of reducing alveolar surface tension. Surfactant production can be regulated hormonally. (Miller et al., 2004a; Hammond et al., 2005). In terrestrial mammals production can be augmented through hyperventilation (Hammond et al., 2005). The functional residual capacity (FRC) and residual volumes (RV) are, respectively, the amounts of air that remain in the lung following a passive and maximal exhalation. In the human lung, FRC and RV are approximately 40% and 22% of total lung capacity (TLC), respectively (Berend et al., 1980; Crapo et al., 1981). In whale species, relaxed FRC is close to or equal to RV. The lung of a terrestrial mammal retains a certain amount of air whereas the pulmonary architecture in marine mammals allows for near-complete alveolar emptying (Denison et al., 1971; Kooyman and Sinnett, 1979; Piscitelli et al., 2010; Fahlman et al., 2011). Consequently, residual air in the lungs of marine mammals following a maximal exhalation is minimal, and the maximal volume that can be exchanged during a breath, the VC (vital capacity) is close to TLC. Terrestrial mammals have stiff chest walls, resulting in a relatively large FRC. The terrestrial thorax resists compression as external hydrostatic pressure increases, which causes negative pressures to develop inside the chest (i.e. lung squeeze) (Lundgren and Miller, 1999). In humans, these negative pressures cause blood to be drawn into the thoracic cavity (thoracic blood pooling), by as much as 1 L (Schaefer et al., 1968; Leith, 1989). The structural properties of the cetacean thorax allow pressure to compress the chest and lung to very low volumes, thereby preventing pulmonary barotrauma (lung squeeze). The shape of the cetacean thorax may be altered actively by ventilatory muscles (Cotten et al., 2008) and passively by ambient pressures (Kooyman and Andersen, 1969). In newborn human infants, with a highly compliant chest wall, the aquatic respiratory pattern is present for a few hours following birth (Fisher et al., 1982).
Breathing
A complete breathing cycle for a whale consists of a very rapid exhale, immediately followed by a slightly longer and much less strong inhale. The process can be repeated several times before an extended period of apnea. Cetaceans can remove nearly 90% of the oxygen available in each breath (Ridgway et al., 1969). In comparison, humans and most other terrestrial mammals only 75%. The diving lung volume can be adjusted before the dive or by exhaling while submerged. Whales are voluntary breathers, as they have to think about every breath they take. Respiratory frequency is significantly lower in an aquatic mammal as compared with a terrestrial one. Marine mammals, and in particular cetaceans, are able to generate high expiratory flow. In humans, peak expiratory flow is achieved at 80% TLC, but flow declines rapidly to zero once volume reaches 20% due to terminal airway compression (Kooyman and Sinnett, 1979). In whales, high flow rates can continue even with a TV of only 15% TLC (Denison et al., 1971; Kooyman, 1973), at average frequency of 20 L/s.
Cardiovascular adaptations
The structure of the heart of cetaceans closely resembles that of other mammals. In terms of relative size, the heart is about 1% of the animal’s body size, which is not dissimilar to the equivalent size in humans. However, it has been observed that they possess enlarged stores of glycogen, which strongly suggests that the cardiac tissues of theses animals are capable of a greater anaerobic capacity than those of terrestrial mammals (Pfeiffer, 1990; Pfeiffer and Viers, 1995). The circulatory systems of marine mammals are characterized by groups of blood vessels (retia mirabilia). Retia mirabilia are tissue masses containing extensive contorted spirals of blood vessels, mainly arteries but with thin-walled veins among them. These structures serve as blood reservoirs to increase oxygen stores for use during diving (e.g., Pfeiffer and Kinkead, 1990). Maximum heart rate measured to date for humpback whales is approximately 40 bpm. In general, the larger the animal, the slower the heart beat.
Oxygen store
Oxygen is stored and transported around human body through red blood cells by means of a protein called hemoglobin. The red blood cell size of terrestrial and marine mammals are similar. However, human blood is 30% hemoglobin, while a whale’s blood is 60% hemoglobin. In addition to more hemoglobin, whales have a higher percentage of blood. Blood takes up 10-20% of a whale’s body volume, while human blood volume to body ratio is only around 7%. Oxygen is also stored in muscle tissue through a protein called myoglobin. Whales’ myoglobin concentrations in their muscle are up to 30% higher than their terrestrial relatives. This molecule is distributed throughout the muscles in the body and holds up to 35% of whales’ oxygen stores. This is crucial as it is important for oxygen to not only last as long as possible, but also be constantly supplied to the brain while they are under water. Finally, a team of scientists in Brazil registered 13 spleens in humpback whales. The additional spleens contract during a dive to release fresh blood with oxygenated red blood cells.
Diving reflex
During a dive, there is a decline in the amount of available oxygen (hypoxia) and an increase in carbon dioxide (hypercapnia). When the dive continues beyond a time that can be serviced by aerobic metabolism, byproducts of anaerobic metabolism such as lactic acid and hydrogen ions begin to accumulate. Marine mammals have a complex array of physiological responses known as diving reflex. These responses include decline in heart rate (bradycardia), regional vasoconstriction (selective ischemia) that entails a preferential distribution of circulating blood to oxygen-sensitive organs, drop in core body temperature, hypo-metabolism, tolerance to low oxygen and high CO2 concentrations. Irving was the pioneer (Irving et al., 1935; Irving, 1939) who provided evidence of diving reflex for marine mammals. Whales are likely to have a remarkable level of voluntary control over the cardiovascular system. Tissues such as those in the liver and kidney that regularly experience drastic reductions in blood flow during diving show extreme tolerance of these conditions. Additionally, deprivation of arterial blood flow to selected organs produces a gradual reduction in body temperature (Scholander et al., 1942b;Hammel et al., 1977; Hill et al., 1987; Andrews et al., 1995). There is evidence that even normally sensitive tissues such as the brain and heart are adapted to dealing with low oxygen (Ridgway et al., 1969; Kjukshus et al., 1982; Elsner and Gooden, 1983; White et al., 1990). A mechanism that might result in metabolic inhibition during diving is increasing tissue acidity (Harken, 1976). It is established that marine mammals can tolerate anaerobic cellular conditions with elevated lactic acid and declining pH that terrestrial mammals would find disruptive or even lethal (e.g., Elsner, 1987; Ponganis et al., 1990; Williams et al., 1991, 1993).
Equalization
Humpback whales have an external opening on either side of the head, known as the ear opening. This leads to an auditory canal. The ear bones are extremely hard and dense to resist pressure. To protect the canal from being damaged by sea water, there is a waxy plug to block the water from entering. Ear equalization is solved by lining the middle ear cavity with flexible material (Venous Plexus). There are complexes of blood vessels in both the ear canal and the walls of the pterygoid sinuses that house the structures of the inner ear. When diving to depth sinuses flood with blood, which expands into the space in the inner ear, and drastically reduces the air space making equalization an easy task. To complete the work, whales have large Eustachian tubes. Air can be easily displaced from the mouth to the ear. Lastly, humans have relatively large frontal sinuses, but for many diving mammals, the frontal sinuses are drastically reduced, or absent, so that the pressure which the water exerts on them is much lower.
Diving mechanics
Humpback whales cruise at a speed of 3.8 to 14.3 km/h, although they can reach speeds of 27 km/h. K.O.Zubiri assessed that the ascent and descent rates averaged approximately 1 m/s, with occasional peaks at 4 m/s. Humpback whales have four fins: two pectoral fins (flippers), one dorsal fin, one caudal fin (fluke, tail). Caudal fin is used for propulsion, with up and down movements created by powerful muscles along the peduncle. The tail can be up to a third of body length and it is fully cartilaginous, with absence of bones. Pectoral fins serve as rudders and stabilizers. They measure approximately 1/3 of the body length, up to 6 m. The pectoral fins contain 5 large finger bones. They offer high maneuverability for a wide variety of conditions. Scientists were able to find that humpback whales occasionally flap their flippers, causing a short boost in acceleration. This movement likely requires a lot of energy, but can be very beneficial to the whale if it needs to travel short distances very quickly. The large dorsal fin is located at 2/3 of the length from the head. It enhances hydrodynamics and stabilizes rotations around the longitudinal axis. A West Chester University professor has developed a wind turbine that draws inspiration from the flippers of humpback whales. The bumps on the flippers cause water to flow over the fins more smoothly, channeling the flow and reducing turbulence. Researchers at the German Aerospace Center in Göttingen have analyzed humpback whales to find a solution to air flow disruption in helicopter rotor blades. Flow disruption occurs when a whale’s pectoral fin or a helicopter’s rotor blade is pitched too steeply. Researchers demonstrated the process with a whale fin model in a wind tunnel, reproducing the bumps on the back of a humpback whale. They found that whales perform much better. The experiment led to a new invention. The artificial bumps can be punched out of a rubber mat with adhesive film and then stuck to the front edge of wings, creating tiny vortices in the air that hold the flow, reducing disruption.
Fig.3 – Caudal and pectoral fin representation (J.Struthers Delt, Journal of anatomy and physics, 1888)
Conclusions
Whales evolved from terrestrial mammals millions of years ago. The nature of diving efforts to which they have been exposed have developed physiological adaptations. The diving mechanics is still not fully understood, but the efficiency has been proved to enhance performances when reproduced to engineering (wind turbines, airplanes, helicopters). Equipment manufacturers of wetsuits and fins are encouraged to investigate and imitate animal’s geometry, texture, even imperfections. Bio-inspired design often results in better performances. Humpback whale physiology is an ideal reference for freedivers. Although some adaptations take more than one life to be achieved, there are some aspects that can be altered by athletes. First, it is confirmed that performance at depth depends on thorax flexibility. Freedivers may benefit from chest stretching. Stamina repetitions, can lower the heart rate in the long term, contributing to a better cardiovascular efficiency and lower energy usage during the dive. Foods like dates, grapes, pears, potatoes, cucumber and carrots enhance the spleen activity, which is an important organ for freediving. A diet rich of iron and vitamins helps the production of red cells, which are found to not only transport, but also store oxygen. Finally, prolonged time in the water, relaxation, empty lungs dives are well known strategies so far to strengthen the diving reflex.
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