Scaling of morphology and ultrastructure of hearts among wild African antelope

Abstract

The hearts of smaller mammals tend to operate at higher mass-specific mechanical work rates than those of larger mammals. The ultrastructural characteristics of the heart that allow for such variation in work rate are still largely unknown. We have used perfusion-fixation, transmission electron microscopy and stereology to assess the morphology and anatomical aerobic power density of the heart as a function of body mass across six species of wild African antelope differing by approximately 20-fold in body mass. The survival of wild antelope, as prey animals, depends on competent cardiovascular performance. We found that relative heart mass (g kg body mass) decreases with body mass according to a power equation with an exponent of -0.12±0.07 (±95% confidence interval). Likewise, capillary length density (km cm of cardiomyocyte), mitochondrial volume density (fraction of cardiomyocyte) and mitochondrial inner membrane surface density (m cm of mitochondria) also decrease with body mass with exponents of -0.17±0.16, -0.06±0.05 and -0.07±0.05, respectively, trends likely to be associated with the greater mass-specific mechanical work rate of the heart in smaller antelope. Finally, we found proportionality between quantitative characteristics of a structure responsible for the delivery of oxygen (total capillary length) and those of a structure that ultimately uses that oxygen (total mitochondrial inner membrane surface area), which provides support for the economic principle of symmorphosis at the cellular level of the oxygen cascade in an aerobic organ.

Relationship between capillaries, mitochondria and maximum power of the heart: a meta-study from shrew to elephant

“…That our capillary and mitochondrial density exponents are similar indicates parallel scaling of these two traits as a function of body mass across almost the full range for terrestrial mammals (figure 2). A parallel scaling between cardiac capillary supply and mitochondrial investments was previously shown across six species of different-sized adult wild African antelope where, relative to the cardiomyocyte reference space, the capillary numerical density matched the mitochondrial inner membrane surface density [1]. In this earlier study for a single family of mammals, the negative exponents were somewhat steeper ( ca –0.15) than in the present study assessing general mammalian trends, highlighting that patterns observed within phylogenetic groups do not necessarily translate across all mammals.…”

“…The evolution of heart size among mammals of increasing body mass is explained primarily by the large increase in volume loads that act upon the walls of the ventricles in larger species [1], and secondarily by the subtle increase in central arterial blood pressures in larger and taller terrestrial species [2–4]. According to the Principle of Laplace, the increase in volume and pressure loads necessitate an increase in cardiac wall thickness so that wall stress is conserved [5].…”

“…In recent years, phylogenetic information of species relatedness has been incorporated into these analyses to help satisfy statistical prerequisites pertaining to the independence of data points [9]. Using this approach, we recently showed proportionality between capillary supply and mitochondrial investments of the heart across six species of different-sized wild African antelope, evident by the similar scaling exponents derived for total capillary length and for total mitochondrial inner membrane surface area [1]. The only previous analysis, across 11 species of mammal, showed that mitochondrial volume density scales with body mass with an exponent significantly less than zero, thus decreasing appreciably from 36.1% in a 2.4 g shrew to 21.1% in a 920 kg cow [10].…”

Comparative omasum anatomy in ruminants: Relationships with natural diet, digestive physiology, and general considerations on allometric investigations

“…Ideally, comparative anatomical data should be generated by a team of investigators within a defined period of time, under standardized conditions (in the habitat considered the typical for the species, during a period of either optimal or limiting resource availability), on a consistent number of specimens of each species considered, recording not only body mass but less condition‐dependent proxies for body size. Such an approach is feasible for concise questions limited to species of a specific region (e.g., Snelling et al, ), but is much more difficult to achieve on a global level.…”