Scaling of morphology and ultrastructure of hearts among wild African antelope

Author:

Snelling Edward P.1ORCID,Maloney Shane K.12ORCID,Farrell Anthony P.34,Meyer Leith C. R.15ORCID,Izwan Adian2,Fuller Andrea15ORCID,Mitchell Duncan12ORCID,Haw Anna1,Costello Mary-Ann6,Seymour Roger S.7ORCID

Affiliation:

1. Brain Function Research Group, School of Physiology, University of the Witwatersrand, Johannesburg, South Africa

2. School of Human Sciences, University of Western Australia, Crawley, Western Australia, Australia

3. Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada

4. Faculty of Land and Food Systems, University of British Columbia, Vancouver, British Columbia, Canada

5. Department of Paraclinical Sciences, University of Pretoria, Pretoria, South Africa

6. Central Animal Service, University of the Witwatersrand, Johannesburg, South Africa

7. School of Biological Sciences, University of Adelaide, Adelaide, South Australia, Australia

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 still is 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−1 body mass) decreases with body mass according to a power equation with an exponent of –0.12±0.07 (± 95% CI) (P=0.0027). Likewise, capillary length density (km cm−3 of cardiomyocyte), mitochondrial volume density (fraction of cardiomyocyte), and mitochondrial inner membrane surface density (m2 cm−3 of mitochondria) also decrease with body mass with exponents of –0.17±0.16 (P=0.039), –0.06±0.05 (P=0.018), and –0.07±0.05 (P=0.015), respectively, trends likely to be associated with the greater mass-specific mechanical work rates of the hearts 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.

Funder

Australian Research Council

Claude Leon Foundation

Natural Sciences and Engineering Research Council of Canada

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

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