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Extreme Environments: Lessons from Ocean Depths

Adaptations of the Heart: Comparative Responses to Diving and Hypoxia Across Species…

Artwork by Alice Bongers
Artwork by Alice Bongers

Many physiological mechanisms have evolved in living organisms to cope with extreme environments, including high altitudes or deep ocean depths. These include changes in oxygen transport and utilization, metabolic adjustments, strategies to retain heat in cold conditions, adaptations to withstand high pressure, mechanisms for surviving in darkness, and efficient energy use to cope with limited food availability. At high altitudes, the reduction in oxygen pressure leads to a hypoxic condition. In response to acute high-altitude exposure, the body initiates systemic physiological responses that, over time, result in acclimatization. This acclimatization increases tolerance to hypoxia, leading to improved arterial oxygen content, enhanced oxygen delivery, and better aerobic exercise performance (Mallet et al., 2023). These biological adaptations result in high performance levels among indigenous high-altitude populations (Beall, 2003). These physiological changes can be categorized based on the duration of exposure: acclimatization, which involves short-term and temporary changes; phenotypic plasticity, which refers to flexible traits that develop within an organism's lifetime; and biological adaptation, which consists of permanent, inherited traits that evolve over multiple generations.


The ocean depths represent another extreme environment where human populations, such as the Sea Nomads (the Bajau), have developed significant physiological adaptations due to long-term exposure to acute hypoxia. The Bajau are known for their remarkable ability to perform long breath-hold dives. This ability appears to result partly from natural selection, which has led to various physiological adaptations, including an increased spleen size. A larger spleen provides a greater reservoir of oxygenated red blood cells, allowing more oxygen to be released during dives. Additionally, changes in the human diving reflex, such as increased peripheral vasoconstriction, help to preferentially oxygenate critical tissues like the brain, heart, and lungs, potentially extending dive duration (Ilardo et al., 2018).



Figure 1. A Bajau fisherman engaged in traditional fishing. Image courtesy of National Geographic.
Figure 1. A Bajau fisherman engaged in traditional fishing. Image courtesy of National Geographic.

Interestingly, similar physiological adaptations can occur in individuals from different ethnicities who engage in breath-hold diving (apnea) as a sport. This activity involves highly integrative physiological responses to both exercise and asphyxia as divers descend to progressively greater depths. Even before submersion, physiological changes occur during partial immersion, such as regional blood flow restrictions. During the final inspiration before immersion, lung volume increases by 11-26% (Patrician et al., 2021). The heart plays a crucial role in transporting oxygen, bound to hemoglobin, to tissues throughout the body, enabling them to function optimally. Heart rate, the number of beats per minute, adjusts to the body's varying oxygen demands in different situations. A particularly fascinating mechanism observed in breath-hold diving is the mammalian diving response. This response includes a reduction in heart rate (bradycardia) and vasoconstriction of peripheral blood vessels, which decreases blood flow to non-essential organs. These physiological changes, triggered by facial immersion, work together to reduce oxygen consumption, leading to heart rates as low as 20-30 beats per minute during dives (Patrician et al., 2021). It is important to note that bradycardia, characterized by a heart rate of fewer than 60 beats per minute, can be a risk factor for future cardiovascular events (Makita et al., 2014). However, the bradycardia observed during the mammalian diving response is a temporary adaptation initiated by increased parasympathetic nerve activity, which slows the heart rate (Patrician et al., 2021). The parasympathetic and sympathetic nerves, components of the autonomic nervous system, regulate involuntary body functions such as heart rate, with the parasympathetic nerve promoting relaxation.


An intriguing aspect of the diving response is that the physiological adaptations observed in humans during acute immersions are also found in other aquatic mammals, supporting the evolutionary conservation of these mechanisms. Recently, a noninvasive tag equipped with surface electrodes has been developed to assess heart rate in marine mammals during deep foraging dives and at the sea surface (Goldbogen et al., 2019). This technology has provided valuable insights into the physiological strategies employed by these animals. The blue whale, in particular, offers a unique perspective on how extreme body size and deep-sea living affect fundamental biological processes such as respiration, circulation, and energy management. The whale's massive size presents distinct challenges for its circulatory and respiratory systems, making it an excellent model for studying how large animals efficiently transport oxygen and nutrients throughout their bodies (Goldbogen and Madsen, 2021)


Figure 2. Suction-cup tag apparatus on a blue whale, designed for in vivo heart rate monitoring in the open ocean. Video by Kurt Hickman, Stanford Report.

The blue whale, the largest living animal on the planet, measuring up to 30 meters in length and weighing as much as 160 tons, performs dives as deep as 184 meters and lasting up to 16.5 minutes. During these dives, the whale's heart rate decreases to around 2 beats per minute (bpm), similar to the decrease observed in humans during diving. After surfacing, the heart rate increases to 25-37 bpm to facilitate rapid gas exchange during brief ventilation bouts. This slow heart rate during dives is explained by the whale's large-diameter, elastic aortic arch, which allows the aorta to accommodate the blood ejected by the heart and maintain blood flow during the prolonged and variable pauses between heartbeats (Goldbogen et al., 2019). The primary purpose of a slower heart rate during dives is to slow the overall depletion of blood oxygen stores while also reducing the oxygen consumption of the heart itself. An increase in heart rate, and consequently in blood oxygen delivery to tissues, would lead to a faster depletion of these oxygen stores. Maintaining a low heart rate not only prolongs dive times but also helps mitigate the risk of decompression sickness (Goldbogen and Madsen, 2021). Like humans, blue whales exhibit a dive response characterized by peripheral vasoconstriction. Along with bradycardia, this response limits blood perfusion to most organs except the brain and heart, ensuring that these critical tissues receive sufficient oxygen during extended dives (Goldbogen and Madsen, 2021).


Physiological adaptations observed during breath-holding and deep diving, such as reduced heart rates and vasoconstriction, are not unique to blue whales but are also found in other marine mammals, including dolphins, Weddell seals, and sea lions (Williams et al., 2015) (Ponganis et al., 2017).


Understanding the physiological mechanisms underlying adaptations to extreme conditions on Earth could have significant biomedical applications. For example, chronic hypoxic exposure at high altitudes has been associated with reduced cancer mortality, likely due to physiological adaptive processes related to this exposure (Thiersch and Swenson, 2018). Additionally, a better comprehension of the mechanisms and consequences of the low heart rates observed in marine mammals during diving, as well as the modulation of their vascular structure, could enhance our understanding of the origin, causes, development, and impact of arrhythmias in human health.


 

References


  1. Beall, C. M. (2003) “High-altitude adaptations,” Lancet. Elsevier BV, 362, pp. s14–s15. doi: 10.1016/s0140-6736(03)15058-1.

  2. Goldbogen, J. A. et al. (2019) “Extreme bradycardia and tachycardia in the world’s largest animal,” Proceedings of the National Academy of Sciences of the United States of America. Proceedings of the National Academy of Sciences, 116(50), pp. 25329–25332. doi: 10.1073/pnas.1914273116.

  3. Goldbogen, J. A. and Madsen, P. T. (2021) “The largest of August Krogh animals: Physiology and biomechanics of the blue whale revisited,” Comparative biochemistry and physiology. Part A, Molecular & integrative physiology. Elsevier BV, 254(110894), p. 110894. doi: 10.1016/j.cbpa.2020.110894.

  4. Ilardo, M. A. et al. (2018) “Physiological and genetic adaptations to diving in sea nomads,” Cell. Elsevier BV, 173(3), pp. 569-580.e15. doi: 10.1016/j.cell.2018.03.054.

  5. Makita, S. et al. (2014) “Bradycardia is associated with future cardiovascular diseases and death in men from the general population,” Atherosclerosis. Elsevier BV, 236(1), pp. 116–120. doi: 10.1016/j.atherosclerosis.2014.06.024.

  6. Mallet, R. T. et al. (2023) “Molecular mechanisms of high-altitude acclimatization,” International journal of molecular sciences. MDPI AG, 24(2), p. 1698. doi: 10.3390/ijms24021698.

  7. Patrician, A. et al. (2021) “Breath-hold diving - the physiology of diving deep and returning,” Frontiers in physiology. Frontiers Media SA, 12, p. 639377. doi: 10.3389/fphys.2021.639377.

  8. Ponganis, P. J. et al. (2017) “Heart rate regulation in diving sea lions: the vagus nerve rules,” The journal of experimental biology. The Company of Biologists, 220(8), pp. 1372–1381. doi: 10.1242/jeb.146779.

  9. Thiersch, M. and Swenson, E. R. (2018) “High altitude and cancer mortality,” High altitude medicine & biology. Mary Ann Liebert Inc, 19(2), pp. 116–123. doi: 10.1089/ham.2017.0061.

  10. Williams, T. M. et al. (2015) “Exercise at depth alters bradycardia and incidence of cardiac anomalies in deep-diving marine mammals,” Nature communications. Springer Science and Business Media LLC, 6(1), p. 6055. doi: 10.1038/ncomms7055.


This article was copy edited by Etienne Patin.


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