This meta-study uses phylogenetic scaling models across more than 30 species, spanning five orders of magnitude in body mass, to show that cardiac capillary numerical density and mitochondrial volume density decrease with body mass raised to the –0.07 ± 0.03 and –0.04 ± 0.01 exponents, respectively. Thus, while an average 10 g mammal has a cardiac capillary density of approximately 4150 mm −2 and a mitochondrial density of 33%, a 1 t mammal has considerably lower corresponding values of 1850 mm −2 and 21%. These similar scaling trajectories suggest quantitative matching for the primary oxygen supply and oxygen consuming structures of the heart, supporting economic design at the cellular level of the oxygen cascade in this aerobic organ. These scaling trajectories are nonetheless somewhat shallower than the exponent of –0.11 calculated for the maximum external mechanical power of the cardiac tissue, under conditions of heavy exercise, when oxygen flow between capillaries and mitochondria is probably fully exploited. This mismatch, if substantiated, implies a declining external mechanical efficiency of the heart with increasing body mass, whereby larger individuals put more energy in but get less energy out, a scenario with implications for cardiovascular design, aerobic capacity and limits of body size.
There was an error published in J. Exp. Biol. (2018) 221, jeb168625 (doi: 10.1242/jeb.168625).In Figs 2 and 3, the numbers on the x-axis for body mass were incorrect. The corrected figures are shown below. We apologise to the authors and readers for any inconvenience this may have caused.
Abstract Scaling of the heart across development can reveal the degree to which variation in cardiac morphology depends on body mass. In this study, we assessed the scaling of heart mass, left and right ventricular masses, and ventricular mass ratio, as a function of eviscerated body mass across fetal and postnatal development in Horro sheep Ovis aries (~50‐fold body mass range; N = 21). Whole hearts were extracted from carcasses, cleaned, dissected into chambers and weighed. We found a biphasic relationship when heart mass was scaled against body mass, with a conspicuous ‘breakpoint’ around the time of birth, manifest not by a change in the scaling exponent (slope), but rather a jump in the elevation. Fetal heart mass (g) increased with eviscerated body mass ( M b , kg) according to the power equation 4.90 M b 0.88 ± 0.26 (± 95% CI ) , whereas postnatal heart mass increased according to 10.0 M b 0.88 ± 0.10 . While the fetal and postnatal scaling exponents are identical (0.88) and reveal a clear dependence of heart mass on body mass, only the postnatal exponent is significantly less than 1.0, indicating the postnatal heart becomes a smaller component of body mass as the body grows, which is a pattern found frequently with postnatal cardiac development among mammals. The rapid doubling in heart mass around the time of birth is independent of any increase in body mass and is consistent with the normalization of wall stress in response to abrupt changes in volume loading and pressure loading at parturition. We discuss variation in scaling patterns of heart mass across development among mammals, and suggest that the variation results from a complex interplay between hard‐wired genetics and epigenetic influences.
The heart and left ventricle of the marsupial western grey kangaroo Macropus fuliginosus exhibit biphasic allometric growth, whereby a negative shift in the trajectory of cardiac growth occurs at pouch exit. In this study, we use transmission electron microscopy to examine the scaling of left ventricle cardiomyocyte ultrastructure across development in the western grey kangaroo over a 190-fold body mass range (0.355−67.5 kg). The volume-density (%) of myofibrils, mitochondria, sarcoplasmic reticuli and t-tubules increase significantly during in-pouch growth, such that the absolute volume (mL) of these organelles scale with body mass (Mb; kg) with steep hyperallometry, 1.41Mb1.38, 0.64Mb1.29, 0.066Mb1.45, and 0.035Mb1.87, respectively. Maturation of the left ventricle ultrastructure coincides with pouch vacation, as organelle volume-densities scale independent of body mass across postpouch development, such that absolute organelle volumes scale in parallel and with relatively shallow hypoallometry, 4.65Mb0.79, 1.75Mb0.77, 0.21Mb0.79, and 0.35Mb0.79, respectively. The steep hyperallometry of organelle volumes and volume-densities across in-pouch growth is consistent with the improved contractile performance of isolated cardiac muscle during foetal development in placental mammals, and is likely critical in augmenting cardiac output to levels necessary for endothermy and independent locomotion in the young kangaroo as it prepares for pouch exit. The shallow hypoallometry of organelle volumes during postpouch growth suggests a decrease in relative cardiac requirements as body mass increases in free-roaming kangaroos, which is possibly because the energy required for hopping is independent of speed, and the capacity for energy storage during hopping could increase as the kangaroo grows.
Abstract We used a high‐precision weighing system and flow‐through respirometry to quantify cutaneous evaporative water loss rates in woolly sheep (wool thickness, ca. 6.5 cm) and haired goats (coat thickness, ca. 2.5 cm), while simultaneously recording parallel data obtained from (1) a flow‐through ventilated capsule, (2) a closed hand‐held electronic evaporimeter chamber, and (3) a closed colorimetric paper disc chamber. In comparison to the weighing system and respirometry, used here as a “gold standard” measure of cutaneous evaporative water loss rate, we found relatively good agreement with data obtained from the flow‐through ventilated capsules. However, we found poor agreement with data obtained from the closed electronic evaporimeter chambers (underestimated by 60%, on average) and the closed colorimetric paper disc chambers (overestimated by 52%, on average). This deviation was likely associated with a requirement for shaved skin in the closed chamber methods. Our results therefore cast doubt on the validity of the closed chamber methods for measurement of cutaneous evaporative water loss rates in furred and fleeced mammals, and instead show that more accurate values can be obtained using flow‐through ventilated capsules.
Bipedal hopping is used by macropods, including rat-kangaroos, wallabies and kangaroos (superfamily Macropodoidea). Interspecific scaling of the ankle extensor muscle-tendon units in the lower hindlimbs of these hopping bipeds shows that peak tendon stress increases disproportionately with body size. Consequently, large kangaroos store and recover more strain energy in their tendons, making hopping more efficient, but their tendons are at greater risk of rupture. This is the first intraspecific scaling analysis on the functional morphology of the ankle extensor muscle-tendon units (gastrocnemius, plantaris and flexor digitorum longus) in one of the largest extant species of hopping mammal, the western grey kangaroo Macropus fuliginosus (5.8-70.5 kg post-pouch body mass). The effective mechanical advantage of the ankle extensors does not vary with post-pouch body mass, scaling with an exponent not significantly different from 0.0. Therefore, larger kangaroos balance rotational moments around the ankle by generating muscle forces proportional to weight-related gravitational forces. Maximum force is dependent upon the physiological cross-sectional area of the muscle, which we found scales geometrically with a mean exponent of only 0.67, rather than 1.0. Therefore, larger kangaroos are limited in their capacity to oppose large external forces around the ankle, potentially compromising fast or accelerative hopping. The strain energy return capacity of the ankle extensor tendons increases with a mean exponent of ~1.0, which is much shallower than the exponent derived from interspecific analyses of hopping mammals (~1.4-1.9). Tendon safety factor (ratio of rupture stress to estimated peak hopping stress) is lowest in the gastrocnemius (< 2), and it decreases with body mass with an exponent of -0.15, extrapolating to a predicted rupture at 160 kg. Extinct giant kangaroos weighing 250 kg could therefore not have engaged in fast hopping using 'scaled-up' lower hindlimb morphology of extant western grey kangaroos.
Summary Weibel and Taylor's theory of symmorphosis predicts that the structural components of the respiratory system are quantitatively adjusted to satisfy, but not exceed, an animal's maximum requirement for oxygen. We test this in the respiratory system of the adult migratory locust Locusta migratoria by comparing the aerobic capacity of hopping and flight muscle with the morphology of the oxygen cascade. Maximum oxygen uptake by flight muscle during tethered-flight is 967 ± 76 μmol h-1 g-1 (body mass-specific, ± 95% CI), whereas the hopping muscles consume a maximum of 158 ± 8 during jumping. The 6.1-fold difference in aerobic capacity between the two muscles is matched by a 6.4-fold difference in tracheole lumen volume, which is 3.5×108 ± 1.2×108 μm3 g-1 in flight muscle and 5.5×107 ± 1.8×107 in the hopping muscles, a 6.4-fold difference in tracheole inner cuticle surface area, which is 3.2×109 ± 1.1×109 μm2 g-1 in flight muscle and 5.0×108 ± 1.7×108 in the hopping muscles, and a 6.8-fold difference in tracheole radial diffusing capacity, which is 113 ± 47 μmol kPa-1 h-1 g-1 in flight muscle and 16.7 ± 6.5 in the hopping muscles. However, there is little congruence between the 6.1-fold difference in aerobic capacity and the 19.8-fold difference in mitochondrial volume, which is 3.2×1010 ± 3.9×109 μm3 g-1 in flight muscle and only 1.6×109 ± 1.4×108 in the hopping muscles. Therefore, symmorphosis is upheld in the design of the tracheal system, but not in relation to the amount of mitochondria, which might be due to other factors operating on the molecular level.
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