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PHYSIOLOGICAL ADAPTATIONS TO FREEDIVING IN MARINE MAMMALS

Alexandru RUSSU

Freedive Dahab, AIDA Instructor Course, September 2009

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Introduction In the Freediving community we’ve seen a certain fascination growing around the marine mammals: the dolphin is often recognised as a symbol of Freediving (e.g. Apnea Academy logo) and swimming techniques and materials (e.g. the monofin) are inspired from what we tend to see as a model – the marine mammals, the perfect freedivers. In our quest to understand why marine mammals are diving better than us, if they use different techniques and if they have the same physiological limitations, in the following pages we synthesised information from marine physiology experiments and publications and organized it under what we like to believe is a comprehensive structure. In a few words we found the marine mammals being better freedivers than humans because of:

1. More energetic resources 2. Better adaptation to pressure 3. Better dive response 4. Better breath hold control 5. More efficient recovery

These points will be developed in the following pages and we will mark the specific scientific findings for each one of them We will be closing with a separate chapter for the different diving behaviours encountered followed by the general conclusion.

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1. More energetic resources: Under point # 1 we grouped the adaptations susceptible to increase the energy resources during a breath hold dive

1.1 The aerobic system: The aerobic system is sustained by oxygen (O2) and any eventual reserves of O2 have a direct impact over the energetic potential of the body during apnoea

1.1.1 More oxygen stored in the muscles: Mioglobin is the primary oxygen carrier in the muscles and its values have been recorded as being much higher for the marine mammals.

Comparative mioglobin values for terrestrial and marine mammals:

Terrestrial mammals: 1g mioglobin / 100g muscle Marine mammals: 3-7g mioglobin / 100g muscles

1.1.2 More oxygen stored in the blood:

1.1.2.1 Higher blood volume The bellow study shows an O2 concentration of 20 ml/kg (body mass) in humans which goes up to values of around 60 ml/kg for some marine mammals

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Tests showed that blood volume is correlated with the dive time: a higher blood volume enables the individuals to have higher dive times. The results of the test are presented in the Annexe # 1

1.1.2.1.1: “Retia Mirabilia” is a group of blood vessels (tissues with twisted spirals of mainly arteries but also veins) located at the sternum level and functioning as a blood reservoir to increase O2 stores for the dive.

The sperm whale (the deepest mammal) has the most developed Retia Mirabilia The blood irrigation of the brain is not done by the carotids but directly by retia mirabilia. (http://cetoclub.unblog.fr/files/2009/02/pathomammar2008part8.ppt)

Retia Mirabilia is specific for marine mammals - it is not encountered in terrestrial mammals

1.1.2.1.2: Splenic O2 stores

During effort/dive for humans, as well as marine mammals, the spleen, by contracting, releases fresh blood with oxygenated red blood cells. The advantage for the marine mammals comes from the size of their spleen which is bigger than for the terrestrial mammals (the seals & sea lions spleen is 4.5% of their body weight and 3 times heavier than terrestrial mammals of same size) For the Weddell seal, the spleen gives 60 % increase in haemoglobin concentration in the first 10 min of the dive. For humans, the effects are much lower: the spleen is mainly contracting towards the end of the breath hold, long after the contraction started with an increase in haemoglobin of around 3% (tests done by the The Environmental Physiology Group from Mid Sweden University at the 2008 AIDA WC in Sharm El Sheik)

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1.1.2.1.2: The Aortic bulb For some marine mammals, aorta increases at the immediate exit from the heart by 30-40% and ramificates for all grate vessels (bronchiocephalic, left common carotid and left subclavian arteries) and decreases in diameter by 50% after this. “As consequences the bulb has a capacity for storage of the stroke work of more than two normal heart beats and a volume of more than three times normal stroke volume. The expanded aortic bulb functions through energy and volume storage actions and through uncoupling actions to maintain arterial pressures and stroke volume at near predive levels during a dive.” (American Journal of Physiology - Vol 251, Issue 1 174-R180)

It is common to all pinnipeds (sub-class of marine mammals) but the size of the bulb is bigger for the deep diving species

The aortic bulb

1.1.2.2 More red cells/haemoglobin In addition of having higher blood values, the marine mammals also have higher concentration of red cells (hematocrit) and consequently higher haemoglobin levels

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Seal blood consists of 60% haemoglobin vs. 35 to 40% in humans. (Julien Baudoin Gregory Zottos - Les limites physiologiques de l'apnée,.)

The different sources of information (mass media) are not consequent on the levels of haemoglobin recorded, but all the cases show human haemoglobin values much below those of marine mammals

Shallow diving mammals (including humans):

14-17g haemoglobin / 100 ml blood

Deep diving mammals 21-25g haemoglobin / 100 ml blood

1.1.3 More oxygen stored in the brain:

1.1.3.1 Higher concentration of globins Certain marine mammals are protected by elevated levels of complex oxygen-carrying proteins--called globins--, in the cerebral cortex. These species have evolved the capacity to protect their brains from conditions of low oxygen. According to a study by researchers at the University of California, Santa Cruz, led by Terrie Williams, some animals had three to ten times more neuroprotecting type globins than others. Weddell seals, animals that dive and hunt under the Antarctic sea ice hold their breath for as long as 90 minutes, and remain active and mentally alert the whole time. The seals aren't fazed at all by low levels of oxygen that would cause humans to black out. We did not found info about the presence of globins in the human brain.

1.2 The anaerobic system:

1.2.1 More glycogen stored in the muscles: According to Annalisa Berta & others (Marine mammals: evolutionary biology ) “the heart of harp seals has enlarged stores of glycogen” which means that cardiac tissues have a bigger anaerobic capacity.

The healthy human heart does not contain glycogen (only pathologic cases which have a negative impact on the contraction capacity of the heart by interrupting the electric impulse on the areas where they are located)

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1.2.2 Delayed effects of the Lactic Acid: The lactic acid is blocked by the vasoconstriction and its effects are delayed until the animal arrives at the surface. The main effect of the lactic acid over the body is the increase of the blood acidity which is controlled by the buffer of CO2. Practically when the lactic acid is released in the blood circulation, the CO2 levels increases commanding a stronger breathing reflex. As consequence the breath hold is harder to maintain. With the vasoconstriction, the lactic acid remains at the muscular level where it is produced without having the possibility to be released in the main circulation. The muscular pain (heavy legs) that human freedivers fill during long dives is the result of the existence in the human body of specialised sensors (chemoreceptor) sensitive to acidity. The pain is relative to these sensors and does not exist independently (in their absence, the muscles would function normally until the total exhaustion of energetic resources). We found no info about the existence of these sensors in the body of marine mammals

Assembling the elements of our chapter concerning the energetic resources and looking at the big picture we would say that the level of effort has an effect on the O2 consumption for both terrestrial and marine mammals but the loading time is different. The effort and O2 loading is:

- simultaneously for terrestrial mammals - temporally delayed for the marine mammals (the effects comes post dive during the

recovery period ).

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2. Better adaptation to pressure Under point #2 we grouped the adaptations susceptible to minimise the negative impact of the (hydrostatic) pressure during the deep dives

2.1 Allocation of O2 stores away from the lungs Man rely mainly on lungs to store oxygen but for the marine mammals, the percentage of O2 contained in the lungs is minimal, the blood and the muscles being the main carriers in their case. Only 5% of the oxygen stores are kept in the lungs in the case of the focid seals vs. 51% in humans. Picture from “Les Mammifères marins” - Emmanuel Bernier For more info on oxygen allocation see a different test in Annexe # 2 With collapsible lungs, air goes in the superior airways where it’s no more in contact with the blood. This avoids gas exchanges and N2 problems.

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2.2 Flexible chest walls The chest of marine mammals can squeeze to let the lungs virtually airless. Human freedivers can improve the chest flexibility (through stretching) but not at that extent.

2.3 Cartilaginous rings reinforcing the airways Shallow diving mammals have partially calcified rings on the airways maintaining them open deeper than the human airways could support, but prohibiting diving to the extreme depths reached by the species presenting collapsible airways system. Deep diving mammals have low calcification of trachea rings which can bent without breaking at extreme depths.

2.4 Sphincter muscles in the smaller airways Marine mammals have very muscular bronchioles able to close the air passages

This allows progressive collapse of lung structures at pressure with initial collapse of the alveoli, followed by small and then large airways. This pattern works in reverse during ascent and the lungs are able to re-inflate in a progressive manner. The lung collapse is blocking the gas exchange minimising the risks related to excessive N2 build-up (DCS & narcosis)

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2.5 Control of body floatability (density) The dugong uses the sphincter muscles of the bronchioles to compress the density of air in the lungs and change floatability without expelling air or using flippers. Since cartilages occur throughout the length of air passages, this keeps the air volume compressed when needed. Another case of floatability control is encountered at the sperm whale (cachalot) Spermaceti (from Greek sperma, seed, and cetus, whale) is an organ regulating the corporal density of the sperm whale , with similar benefits as the BCD of a scuba diver The spermaceti weights a few tones and is positioned in the head of the animal (see below picture) – ideal positioning for a “variable weight” dive At 37 °C, body temperature of the animal on surface, spermaceti lipids are liquefied. When diving, the cachalot inhale cold water through the left nostril (évent - in the above picture), and circulates it to cool down his spermaceti; the temperature going down crystallises the spermaceti (lipids). As consequence, the density of the spermaceti increases and its volume reduces bringing negative floatability. To come up, the sperm whale is heating the spermaceti with an influx of warm blood; the process is reversing bringing positive buoyancy this time. This way, the cachalot is diving with a minimum of energy expenditure and this body density control system also explains the fact that sperm whales when diving deep they come up almost in the same place (like on a « no limit » dive the propulsion force is only down and up).

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Reaching the end of the point #3 , the collapsible airway seems for us to be the most important adaptation (marine mammals have) to pressure because it is very effective against N2 build-up and the related problems (DCS & narcoses). A couple other physiological adaptations helping marine mammals to deal with the N2 are presented in Annexe #4

However, a 2004 study on sperm whales showed that, they are also prone to accidents of decompression. The whales suffer DCS. This is caused by the formation of nitrogen bubbles in the joints which, over the long term, will cause necrosis and bone deformities. These effects were observed in individuals showing the presence of osteonecrosis increased with age, so with the diving experience of animals. It seems that sperm whale naturally follows a decompression protocol (slow ascent and "deco stop" before surfacing. (Respirer de l'air… et vivre dans l'eau - François Rebufat , 2006)

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3. Better diving response The “mammalian dive response” is a set of physiological adaptations which, as it’s name says it, it’s common to all mammals, but the marine mammals seems to have again certain advantages

3.1 Bradicardia Heart rate of marine mammals can go bellow 5% of predive period vs. 70% for humans Rus Hoelzel in “Marine Mammal Biology” is mentioning a 200kg focid seal having 119 bpm on surface and 4 bpm during the dive. More recorded values of bradicardia are available in Annex # 3 (for the Bottlenose dolphin) Voluntary control of cardio-vascular system: The heart rate of marine mammals at the start of the dive is correlated with the duration of the dive they prepare for a dive of a certain time (if they go for a longer dive they start with a lower heart rate).

3.2 Metabolic inhibition with reduction in temperature Marine mammals adjust swimming speeds and metabolic rates to sustain all dives aerobically (the prove are the continuous dives with only few minutes recovery)

3.3 Selective ischemia During the dive, the marine mammals present selective ischemia which is similar with the peripheral vasoconstriction encountered in humans. We use to know this set of physiological adaptation under the name of “mammalian dive reflex” and this is also what the scientific community was using up to the point when voluntary bradicardia has been discovered – since then, the terminology changed to “mammalian dive response”

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4. Better breath hold control

For humans, the breath hold control is closely related to the inspiratory reflex manifested as diaphragmatic contractions which seams to be missing in the case of marine mammals

4.1 No diaphragmatic contractions (low sensitivity to hypercapnia) The CO2 levels in the blood, triggers the inspiratory reflex, but in marine mammals “this reflex seems very diminished, allowing them to remain under water until the total exhaustion of available oxygen” (Annalisa Berta, Marine mammals: evolutionary biology) Measurements mentioned by Cetoclub shows values of 10% CO2 (man would black-out at 6%) and less than 2% O2 on exhaled gases after deep diving. Further evidence is provided by the analysis of intratissualires diatoms (plankton): “ In human forensics, one of the element that confirm a diagnosis of drowning is based on the research of diatoms in the body of the victim. The unicellular algae are composed of silica plates present in all waters. At the break of apnea, there are violent inspirations of water containing diatoms. They pass the alveolar-capillary barrier, go into the circulation and be distributed in some organs (kidney, heart, ...) due to the last heart contractions. No diatom has ever been found in the bodies of marine mammals found dead in fishing nets, suggesting that they die not drowned, but suffocated”. http://cetoclub.unblog.fr/files/2009/02/pathomammar2008part8.ppt The missing diatoms in the body of the marine mammal found death in the fishing nets are also evidence that they do not suffer “black-outs”

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5. More efficient recovery

Even for long sessions of long and deep dives marine mammals only needs to breath for a few minutes on the surface and they are completely recovered. The bellow table shows surface intervals of mainly 3-4 minutes in between dives of mainly 20 minutes to depths of 400 m. During rest or sleep they perform series of breath holds with brief & fast recovery For the marine mammals, during inspiration, extensive elastic tissue in the lungs and diaphragm is stretch by diaphragm and intercostals muscles. These fibres recoil during expiration to rapidly and near completely empty the lungs. The air is moved in contact with the walls of the alveoli by the action of small myoelastic bundles scattered throughout the lungs. In some species, the alveoli are highly vascularised to promote rapid uptake of oxygen. This allows marine mammals to remove almost 90% of the O2 available in each breath in comparison with humans which are only able to remove 20% . The very short recovery times during long and difficult diving sessions may be an indication that marine mammals support the entire dives aerobically (the anaerobic system – glycogen- would take much longer to regenerate)

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6. Diving behaviour:

6.1 Empty lungs The Phocids exhale at the initiation of the dive - they have a collapsible airway system (Annalisa Berta, Marine mammals: evolutionary biology) The seal, depending on whether or not he dives deep, adjusts his breathing to his diving. So when he goes deep, it expires before diving to not take too much nitrogen in his lungs. (Les limites physiologiques de l'apnée. Julien Baudoin Gregory Zottos)

6.2 Full lungs Otariids inhale before the dive and their airway system does not completely colapse (Annalisa Berta, Marine mammals: evolutionary biology)

6.3 Exhale on descent Throughout its descent, the seal let escape from his rib cage, the air pushed by the pressure. (Les limites physiologiques de l'apnée. Julien Baudoin Gregory Zottos)

6.4 Exhale on ascent Antarctic fur seals dive with full lungs and exhale on the last part of the ascent ( Annalisa Berta, “Marine mammals: evolutionary biology”)

6.5 Worm-up Freedivers are not the only ones doing shallow worm-up dives to prepare for the deep dives: Beaked whales are feeding close to 2000m deep (wikipidia) and it looks like even they need to prepare for such a dive. Beaked whales have been observed doing a succession of shallow dives (without eating behaviour, 90 min) and just after going for the deep dives (with eating behaviour ) (http://cetoclub.unblog.fr/files/2009/02/pathomammar2008part8.ppt)

6.6 Deco. stops As mentioned before when speaking about the pressure adaptations and DCS, the sperm whale is exposed to the “bends” and he naturally follows a decompression protocol: slow ascent and "deco stop" before surfacing. (Respirer de l'air… et vivre dans l'eau - François Rebufat , 2006)

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Conclusion: Comparing the cardiovascular and respiratory system of marine mammals and humans we could see a series of physiological advantages explaining the biggest depths and dive times marine mammals are able to reach. The bellow table is a summary of the main elements we presented: more O2 in the muscles Retia mirabilia higher blood volume Splenic O2 stores Aortic bulb aerobic system more O2 in the blood more red cells more O2 in the brain more globins

1. More energetic resources

more glycogen anaerobic system Lactic acid delayed

2. Better adaptation to pressure

O2 repartition Flexible chest walls

cartilaginous rings sphincter muscles variable body density

3. Better dive response

bradicardia metabolic inhibition

selective ischemia

4. Better breath hold control

no contractions

5. More efficient recovery

From a physiological perspective marine mammals are better freedivers, however this is not the most relevant perspective in what human existence is concerned. The meaning of “freediving” for the marine mammals is: fish (physiological need) and security; and on the other side, for humans it’s meaning may be related with maximising efficiency, selfawarness and control, or many other values. These values, whatever they may be, they take us in a cultural dimension and mark the border with the physical dimension in which marine mammals dive to feed and stay alive. The cultural perspective being the most relevant for us we can say that the better freediver is the one who enjoys it more and makes the most out of it to enhance his life experience.

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Annexe #1

Annalisa Berta, James L. Sumich, Kit M. Kovacs , Marine mammals: evolutionary biology

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Annexe #2

Oxygen repartition in the body

O2 (ml/kg) % from total

HOMME (70kg) man

Poumons (4,5L) lungs 10,3 33,5

Sang (5L) blood 14,3 46,0

Muscles (16kg) muscles 3,4 11,5

Eau tissulaire (40L) tissues water 2,8 9,0

Total 30,8

PHOQUE (35kg) seal

Poumons (350mL) blood 1,8 3,5

Sang (4,5L) blood 37,5 72,5

Muscles (6kg) muscles 9,0 17,5

Eau tissulaire (20L) tissues water 3,3 6,5

Total 51,6 “Les Mammifères marins” - Emmanuel Bernier, www.club-aquabulles.fr/lecoindelabio/eb-mammiferes.ppt

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Annexe #3

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Annexe #4 In the case of the marine mammals a significant quantity of 'nitrogen dissolves in the fats. translation after: http://cetoclub.unblog.fr/files/2009/02/pathomammar2008part8.ppt The sperm whale are suspected of producing a lipid coating that lines the airways. This "oil" would serve to capture nitrogen from the air and prevent it from dissolving into the tissues of the animal, thus preserving the narcoses and the DCS.

translation after: François Rebufat, Respirer de l'air… et vivre dans l'eau, 2006

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Annexe #5

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Bibliography: Annalisa Berta, James L. Sumich, Kit M. Kovacs, “Marine mammals: evolutionary biology”, Academic Press, 2005, ISBN: 0120885522, 9780120885527

A. Rus Hoelzel, “Marine mammal biology: an evolutionary approach”, Wiley-Blackwell, 2002 ISBN: 0632052325, 9780632052325 American Journal of Physiology - Regulatory, Integrative and Comparative Physiology, Vol 251,

Issue 1 174-R180, ARTICLE: “Pressure-volume characteristics of aortas of harbor and Weddell seals” by E. A. Rhode, R. Elsner, T. M. Peterson, K. B. Campbell and W. Spangler

Les Mammifères marins ppt - Emmanuel Bernier, www.club-aquabulles.fr/lecoindelabio/eb-

mammiferes.ppt

Les limites physiologiques de l'apnée. Julien Baudoin Gregory Zottos, http://tecfa.unige.ch/perso/lombardf/calvin/TM/02/limites-apnee/baudoin-zottos.html

Respirer de l'air… et vivre dans l'eau - François Rebufat (2006), http://scaphinfo.free.fr/bio/apnee.html http://cetoclub.unblog.fr/files/2009/02/pathomammar2008part8.ppt http://www.medicalnewstoday.com/articles/92310.php