Overwintering Turtles and the Implications for Humans Avoiding Anoxia
Oxygen is necessary for animal life, a truism that is so ingrained in experience and knowledge that few people stop to consider that many animals can go for significantly long periods of time without taking in oxygen. The freshwater turtle is a wonderful example of this adaptive physiology; it overwinters at the bottoms of lakes, and, to do so goes into a state of hibernation that allows it to live at the bottom of the lake without taking in additional oxygen for long periods of time. Scientists believe that two main physiological adaptations enable the turtles to engage in this behavior. First, the turtles' bodies depress their metabolic and cellular processes, which reduces their need for oxygen consumption. However, dealing with the need for oxygen only solves half of the hibernation dilemma; animals also build up lactic acid and this build up can be fatal. Therefore, it is important to understand how . Second, both the turtle's shell and its skeleton function as lactic-acid neutralizes. Between these two processes, turtles can overwinter underwater at just over freezing temperatures, with no oxygen, and extremely high circulating lactate levels for periods of up to four months (Jackson).
It was once common for scientists to believe that turtles, particularly hatchling turtles, were somehow freeze-proof and that their resistance to freezing had something to do with their ability to overwinter underwater. However, more recent evidence suggests that turtles are no more freeze-tolerant than other vertebrates. "Indeed, the weight of current evidence indicates that hatchlings overwintering in the field typically withstand exposure to ice and cold by avoiding freezing altogether and that they do so without benefit of an antifreeze to depress the equilibrium freezing point for bodily fluids" (Packard and Packard). They do not have antifreeze in their systems, but they do engage in a process whereby they remove more freeze-prone elements from their body prior to hibernation. "As autumn turns to winter, turtles remove active nucleating agents from bodily fluids (including bladder and gut), and their integument becomes a highly efficient barrier to the penetration of ice into body compartments from frozen soil. In the absence of a nucleating agent or a crystal of ice to 'catalyze' the transformation of water from liquid to solid, the bodily fluids remain in a supercooled, liquid state" (Packard and Packard). This speculation is backed up by the fact that hatchling turtles frequently spontaneously freeze at much higher temperatures than older turtles and that hatchlings frequently ingest materials from their nests, so that they do not complete the gut-emptying function that adult turtles complete as they prepare for hibernation (Costanzo et al.). Therefore, by ridding their bodies of things that could freeze, turtles are able to withstand extremely cold temperatures with a reduced risk of freeze, but this is not due to any anti-freeze production in their bodies.
Furthermore, although turtles can survive extended anoxic periods it would be both overly simplistic and simply incorrect to suggest that turtles can live without oxygen. Just like other higher-order animals, turtles require oxygen to survive. Oxygen is necessary for the production of adenosine triphosphate (ATP), which bodies need in order to maintain cellular functioning. "Anaerobic energy sources can only temporarily supply the requisite ATP and maintain cellular function before substrate depletion, energy shortfall, or endproduct poisoning threaten survival" (Jackson). However, turtles are able to withstand much longer periods of anoxia than most other animals, which makes their physiology fascinating and inspirational. When they are hibernating their bodies do not actually shut down; instead, the turtles rely on anaerobic glycolysis for energy during periods of hibernation (Jackson). Of course, human beings have looked to nature for inspiration for adaptations in the past, and many people believe that by examining how turtle physiology enables anoxia, that researchers will begin to understand and apply technologies that permit humans to go for extended oxygen-free periods.
This long-term underwater hibernation would be impossible without the turtles being able to achieve an extremely low metabolic rate. Hibernation is a complex state; the animal must be able to dramatically reduce its utilization of stored substrate and slow the build-up of endproducts, yet still be able to maintain baseline living conditions. Hibernating turtles are not in a coma or similar non-conscious state, though they do not maintain normal physical activity levels during anoxic periods like the Crucian carp (Overgaard et al.). Instead, "the turtles become lethargic and are in a near-comatose state where energy expenditure on many physiological functions is greatly reduced. Turtles reduce their metabolic rate tenfold during anoxia and a similar anoxic depression of metabolism has also been characterised in isolated hepatocytes" (Overgaard et al.) Furthermore, the heart continues to function normally, in that the circulatory systems still transports nutrients, hormones, and waste products throughout the body, albeit at greatly reduced rates (Overgaard et al.). Therefore, instead of being comatose or near-comatose, "the animals are responsive to stimuli and periodically move about but are generally extremely sluggish" (Jackson). Their blood pressure and heart rate slow dramatically during this time. Therefore, while they remain capable of movement and response, they are dramatically slower than when in a non-hibernation state.
First, it is important to understand that turtles already have low metabolic rates when compared to mammals because they are ectothermic reptiles; therefore, the turtle's "energy metabolism is only 10-20% that of a mammal of similar size even at the same body temperature" (Jackson). The exothermic quality makes an even greater difference as temperatures fall; "At lower temperatures, metabolism falls still further in the thermally conforming ectotherm, typically at a rate of 2- to 3- fold per 10 "C decrease in temperature" (Jackson). As temperatures approach freezing, the difference in metabolism becomes even more dramatic. "At 3 "C aerobic metabolism is depressed to about 0.1% of the euthermic mammalian level" (Jackson). Keeping in mind that those figures reflect an active, not a hibernating animal, it is clear that exothermic reptiles are able to be far more oxygen efficient than comparably-sized animals under all circumstances. Furthermore, when the turtle hibernates it enters an anoxic state, and its metabolism falls by about 90% from its normal metabolic rates, which make its metabolic rate at its normal hibernating temperature approximately 10, 0000 times lower than that of a similar-sized mammal (Jackson).
On a cellular level, hibernating turtles coordinate downregulation by two different means ATP utilization and ATP production. First, turtles' bodies use a process called channel arrest, which slows down the passive flux of ions through membrane channels (Jackson). Reptiles normally have lower metabolic rates than mammals, which is thought to be partially due to this channel arrest phenomenon. "Furthermore, when the reptile's temperature falls, so does its metabolic rate, but ion concentrations remain essentially unchanged. The interpretation is that membrane ion leakage through ion channels is less in the reptile, and that it falls further when the animal's temperature falls. Anoxia induces a further reduction in ion channel activity" (Jackson). There is some evidence that this reduced channel function specifically impacts particular ions in the turtle brain, including sodium (Na), potassium (K), and calcium (Ca) (Jackson). These ions are not reduced in direct relation to the drop in function, but there is some correlation. Scientists do not fully understand how this channel arrest works, but they believe that turtles do not have ATP-specific K. Or NA channels, so that it can reduce activity in other K. And Na channels and effectuate a reduction in ATP activity. In fact, studies have suggested that adenosine helps with downregulation by decreasing the open probability of Ca channels (Jackson). Those strategies are indicative of long-term coping mechanisms for anoxic states. In contrast, "The mammalian brain responds to anoxia and the attendant fall in ATP by opening ATP-sensitive K+ channels (KATP channels). The resultant hyperpolarization reduces electrical activity and serves as a short-term defence mechanism, but persistent anoxia leads in minutes to massive failure due to a rapid increase in extracellular K+, membrane depolarization, rapid influx of Ca2+ through voltage-dependent channels and Ca2+- induced cellular damage (Jackson). Furthermore, during anoxia turtles suppress utilization of ATP for protein synthesis in the hepatocytes and heart, though not all systems demonstrate reduced protein synthesis; it is actually increased in some systems (Jackson).
Reducing ATP utilization is not enough to permit turtles to survive extend periods of anoxia without also reducing ATP production because the ATP buildup would become toxic to the animal. During anoxia, ATP production is than it is during hypoxia. "During anoxia, ATP production occurs via glycolysis, and modulation of the flux rate is considered to be via control of key enzymes in this pathway (Jackson). This results in a low rate of ATP production. Generally, this form of ATP production would require a large glucose or glycogen supply, which creates a limiting function in many animals. However, hibernating turtles exhibit such low normal rates of glycolysis that their large stores of glycogen in their liver and muscles are adequate for the period of overwintering…