174
Marine Mammal Physiology: Requisites for Ocean Living
death by starvation is linked to depletion of lean body mass; therefore, limiting protein
catabolism during the fast has a direct effect on survival (Øritsland 1990; Øritsland
and Markussen 1990). Protein catabolism also generates nitrogen end-products that
must be recycled or removed in urine. This is at odds with the strategy to minimize
urinary water loss observed in many animals without access to external water stores
(see Chapter 7).
However, protein stores do play an important role in providing glucose during a fast.
A constant supply of glucose is required by neurons and aspects of the central nervous
system (which lack enzymes to oxidize FFA, although they can use ketone bodies for a
portion of their energy requirements) and red blood cells (which lack mitochondria and
therefore, the enzymes for both FFA and ketone oxidation). Glycogen stores in the liver are
usually depleted within a few days of fasting. Fortunately, the liver and kidneys can then
produce glucose through the process of gluconeogenesis, which helps to maintain a reduced
but relatively constant blood glucose level throughout extended fasts. Gluconeogenesis
forms glucose from the non-carbohydrate precursors glycerol (from lipolysis of adipose
triacylglycerols), and amino acids (via proteolysis, the breakdown of proteins to individual
amino acids). Because most fatty acids cannot provide carbon for gluconeogenesis, only
the small glycerol portion of the vast store of food energy contained in adipose tissue triacylglycerols can enter the gluconeogenic pathway. Thus, some level of protein catabolism
is constantly required during fasting to provide the components to manufacture glucose
for these glucose-obligate systems.
These differences in the abundance, benefits, and consequences of fueling fasting
metabolism through different substrates results in many vertebrates, including marine
mammals, undergoing a predictable progression in fasting physiology. This series of
adaptive changes was formalized in the late 1980s and 1990s by scientists such as George
Cahill and Yves Cherel into three “classical phases of fasting” (Figure 3).
Phase I: Readily accessible but limited carbohydrates stores (such as glycogen) are used
to fuel the initial stages of fasting (Cherel et al. 1988). Animals also transition to a protein-sparing metabolism and increase mobilization of lipid resources. Despite energetic contributions from other tissue sources, carbohydrates are depleted in hours to
days.
Phase II: This period represents the most physiologically stable fasting state that can last
for weeks to months, where fasting marine mammals rely almost entirely on lipid
stores. Despite this strong metabolic preference, not all biochemical processes can be
met by lipid catabolism alone. Protein sources play a limited but vital role by supplying amino acids to replenish circulating glucose via gluconeogenesis. Animals able
to accumulate greater body fat reserves prior to fasting will sustain this physiology
longer; however, lipid stores are obviously finite.
Phase III: The blubber layer cannot be completely depleted without infringing on thermoregulatory capabilities, causing further energetic imbalances (Rosen et al. 2007).
At this point, marine mammals must end their protein-sparing strategy; however,
increased protein catabolism represents the “end-game” physiological state associated with impending exhaustion of fuel reserves. Although Phase III physiology can
be reversible upon re-feeding, at this point animals must quickly end their fast or
suffer severe physical consequences, including death. For this reason, reliance on
protein catabolism only lasts days to weeks, and fasting in most marine mammals
does not typically extend into Phase III.
Marine Mammal Physiology: Requisites for Ocean Living
death by starvation is linked to depletion of lean body mass; therefore, limiting protein
catabolism during the fast has a direct effect on survival (Øritsland 1990; Øritsland
and Markussen 1990). Protein catabolism also generates nitrogen end-products that
must be recycled or removed in urine. This is at odds with the strategy to minimize
urinary water loss observed in many animals without access to external water stores
(see Chapter 7).
However, protein stores do play an important role in providing glucose during a fast.
A constant supply of glucose is required by neurons and aspects of the central nervous
system (which lack enzymes to oxidize FFA, although they can use ketone bodies for a
portion of their energy requirements) and red blood cells (which lack mitochondria and
therefore, the enzymes for both FFA and ketone oxidation). Glycogen stores in the liver are
usually depleted within a few days of fasting. Fortunately, the liver and kidneys can then
produce glucose through the process of gluconeogenesis, which helps to maintain a reduced
but relatively constant blood glucose level throughout extended fasts. Gluconeogenesis
forms glucose from the non-carbohydrate precursors glycerol (from lipolysis of adipose
triacylglycerols), and amino acids (via proteolysis, the breakdown of proteins to individual
amino acids). Because most fatty acids cannot provide carbon for gluconeogenesis, only
the small glycerol portion of the vast store of food energy contained in adipose tissue triacylglycerols can enter the gluconeogenic pathway. Thus, some level of protein catabolism
is constantly required during fasting to provide the components to manufacture glucose
for these glucose-obligate systems.
These differences in the abundance, benefits, and consequences of fueling fasting
metabolism through different substrates results in many vertebrates, including marine
mammals, undergoing a predictable progression in fasting physiology. This series of
adaptive changes was formalized in the late 1980s and 1990s by scientists such as George
Cahill and Yves Cherel into three “classical phases of fasting” (Figure 3).
Phase I: Readily accessible but limited carbohydrates stores (such as glycogen) are used
to fuel the initial stages of fasting (Cherel et al. 1988). Animals also transition to a protein-sparing metabolism and increase mobilization of lipid resources. Despite energetic contributions from other tissue sources, carbohydrates are depleted in hours to
days.
Phase II: This period represents the most physiologically stable fasting state that can last
for weeks to months, where fasting marine mammals rely almost entirely on lipid
stores. Despite this strong metabolic preference, not all biochemical processes can be
met by lipid catabolism alone. Protein sources play a limited but vital role by supplying amino acids to replenish circulating glucose via gluconeogenesis. Animals able
to accumulate greater body fat reserves prior to fasting will sustain this physiology
longer; however, lipid stores are obviously finite.
Phase III: The blubber layer cannot be completely depleted without infringing on thermoregulatory capabilities, causing further energetic imbalances (Rosen et al. 2007).
At this point, marine mammals must end their protein-sparing strategy; however,
increased protein catabolism represents the “end-game” physiological state associated with impending exhaustion of fuel reserves. Although Phase III physiology can
be reversible upon re-feeding, at this point animals must quickly end their fast or
suffer severe physical consequences, including death. For this reason, reliance on
protein catabolism only lasts days to weeks, and fasting in most marine mammals
does not typically extend into Phase III.