Year

1984

Degree Name

Doctor of Philosophy

Department

Department of Biology

Abstract

In a comparison of a single mammalian (R. norvegicus) and reptilian species (A. vitticeps) of the same body weight and "preferred" body temperature,the metabolic capacity for energy production was assessed in liver, heart, brain, kidney, lung and skeletal muscle tissues by two methods: measurement of mitochondrial enzyme activity (cytochrome oxidase) and measurement of mitochondrial volume and membrane surface area densities. Both methods showed the mammal to possess an average 2-3 fold greater metabolic capacity per gram of tissue. When the larger relative tissue sizes of the mammal were included into the comparison the differences were increased to approximately 5 fold.

When the mitochondrial enzyme activities of the six mammalian and reptilian tissues were expressed per gram of tissue protein the differences were reduced. This was because all the reptilian tissues measured had significantly less protein per gram of tissue than the mammalian tissues. Isolated mitochondria from the same six tissues showed the mammalian mitochondria in general to have more protein and less lipid than the reptilian mitochondria and similar oxygen consumptions (measured using cytochrome oxidase) per mg of protein for liver, brain and kidney mitochondria. Isolated mammalian lung, heart and skeletal muscle mitochondria however, consumed twice the amount of oxygen consumed by the same reptilian mitochondria per gram of mitochondrial protein.

To assess the use of energy by the same mammalian and reptilian species the "in vitro" oxygen consumption of liver, kidney and brain tissues were measured. "Sodium dependent" metabolism (i.e., the amount of energy used on pumping Na+ out and K+ into the cells of tissues) was also measured in these tissues. The mammal had "in vitro" tissue metabolisms generally 4 times greater and spent 4 times more energy on Na+ pumping than did the same reptilian tissues. In the liver particularly this difference was 5 fold.

To examine the reasons for this difference in "sodium dependent" metabolism between the mammal and reptile, the liver cell membrane Na+ permeabilities of the mammal and reptile plus an amphibian, B. marinus were examined using primary monolayer liver cell culture. The mammalian liver cells were found to be 5 times more permeable to Na+ than either the reptilian or amphibian liver cells. This increased permeability of the endothermic liver cells probably accounts for the large differences in the amounts of energy used by the mammal and ectotherms on Na+ and K+ pumping. This inefficiency in terms of relative energy use of the mammalian cells compared to the ectothermic cells is postulated as having evolved as a means of increasing heat production.

The effects of body size and phylogeny on metabolic capacities were examined by comparing the mitochondrial capacities of 6 mammalian and 4 reptilian species representing 100 fold body weight ranges. The mammals examined included 3 eutherian, 2 marsupial and a monotreme and the reptiles 2 saurian, 1 crocodilian and 1 testudine species. The tissues examined were the same six tissues previously mentioned. Allometric equations were derived for tissue weights, mitochondrial volume densities, internal mitochondrial membrane surface area densities, tissue mitochondrial membrane surface areas both per gram and per total tissue and summated tissue mitochondrial membrane surface areas.

For the mammals and reptiles studied a 100% increase in body size results in average increases of 68% in internal organ size and 107% in skeletal muscle mass. Similarly, total organ mitochondrial membrane surface areas increase in mammals and reptiles by an average 54% and for skeletal muscle by an average 96%. These values are similar to increases in standard (54 and 71%) and maximum (73 and 77%) organismal metabolism values found by other authors for mammals and reptiles respectively.

Although the allometric exponents or rates of change with increasing body size of the mitochondrial parameters in mammals and reptiles are statistically the same in general the total amount of mitochondrial membrane surface area in the mammalian tissues are four times greater than found in the reptilian tissues. These differences were not the result of any single "guantum" factor but are the result of the mammals having relatively larger tissues with a greater proportion of their volume occupied by mitochondria. Mitochondrial volume density from this present study would appear to be the major factor involved in changing weight specific metabolism of tissues both as a result of changes in body size and in the evolution of endothermy in mammals from reptiles.

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