Blood flow for bone remodelling correlates with locomotion in living and extinct birds

Allan, Georgina H.; Cassey, Phillip; Snelling, Edward P.; Maloney, Shane K.; Seymour, Roger S.

doi:10.1242/jeb.102889

Cited by 17 publications

(48 citation statements)

References 53 publications

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“…During bone remodelling, bone matrices are dissolved by osteoclasts and then renewed by osteoblasts associated with capillary loops in the secondary osteons of Haversian bone (Rucci, 2008). An index of blood flow rate (Q i ), based on the size of the femoral nutrient foramina of adult mammals, reptiles and birds, appears to be proportional to locomotor activity levels and can be used as an indicator of general locomotion intensity in living and extinct species (Seymour et al, 2012;Allan et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…Although it has been suggested that the rate of blood flow through the femoral nutrient artery corresponds with the locomotor activity levels of terrestrial vertebrates, previous femoral bone blood flow studies using Q i have considered only the adults of several species (Seymour et al, 2012;Allan et al, 2014). There have been no studies of femoral bone blood flow rate across ontogeny.…”

Section: Introductionmentioning

confidence: 99%

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Femoral bone perfusion through the nutrient foramen during growth and locomotor development of western grey kangaroos Macropus fuliginosus

Nelson

Snelling

et al. 2017

Journal of Experimental Biology

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The nutrient artery passes through the nutrient foramen on the shaft of the femur and supplies more than half of the total blood flow to the bone. Assuming that the size of the nutrient foramen correlates with the size of the nutrient artery, an index of blood flow rate () can be calculated from nutrient foramen dimensions. Interspecific is proportional to locomotor activity levels in adult mammals, birds and reptiles. However, no studies have yet estimated intraspecific to test for the effects of growth and locomotor development on bone blood flow requirements. In this study, we used micro-CT and medical CT scanning to measure femoral dimensions and foramen radius to calculate femoral during the in-pouch and post-pouch life stages of western grey kangaroos () weighing 5.7 g to 70.5 kg and representing a 12,350-fold range in body mass. A biphasic scaling relationship between and body mass was observed (breakpoint at ca. 1-5 kg body mass right before permanent pouch exit), with a steep exponent of 0.96±0.09 (95% CI) during the in-pouch life stage and a statistically independent exponent of -0.59±0.90 during the post-pouch life stage. In-pouch joeys showed values that were 50-100 times higher than those of adult diprotodont marsupials of the same body mass, but gradually converged with them as post-pouch adults. Bone modelling during growth appears to be the main determinant of femoral bone blood flow during in-pouch development, whereas bone remodelling for micro-fracture repair due to locomotion gradually becomes the main determinant when kangaroos leave the pouch and become more active.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Femoral bone perfusion through the nutrient foramen during growth and locomotor development of western grey kangaroos Macropus fuliginosus

Nelson

Snelling

et al. 2017

Journal of Experimental Biology

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“…; Allan et al. ), there are currently no precedents for modeling and quantifying the major vessels supplying blood to the skeleton, and very little is known about the morphology of, and potential variation in, the shapes of the canals themselves. A primary objective of this study was to develop a method to quantify accurately the morphology of nutrient canals, in particular their cross‐sectional areas.…”

Section: Discussionmentioning

confidence: 99%

Effects of selective breeding for high voluntary wheel‐running behavior on femoral nutrient canal size and abundance in house mice

et al. 2018

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Bone modeling and remodeling are aerobic processes that entail relatively high oxygen demands. Long bones receive oxygenated blood from nutrient arteries, epiphyseal-metaphyseal arteries, and periosteal arteries, with the nutrient artery supplying the bulk of total blood volume in mammals (~ 50-70%). Estimates of blood flow into these bones can be made from the dimensions of the nutrient canal, through which nutrient arteries pass. Unfortunately, measuring these canal dimensions non-invasively (i.e. without physical sectioning) is difficult, and thus researchers have relied on more readily visible skeletal proxies. Specifically, the size of the nutrient artery has been estimated from dimensions (e.g. minimum diameters) of the periosteal (external) opening of the nutrient canal. This approach has also been utilized by some comparative morphologists and paleontologists, as the opening of a nutrient canal is present long after the vascular soft tissue has degenerated. The literature on nutrient arteries and canals is sparse, with most studies consisting of anatomical descriptions from surgical proceedings, and only a few investigating the links between nutrient canal morphology and physiology or behavior. The primary objective of this study was to evaluate femur nutrient canal morphology in mice with known physiological and behavioral differences; specifically, mice from an artificial selection experiment for high voluntary wheel-running behavior. Mice from four replicate high runner (HR) lines are known to differ from four non-selected control (C) lines in both locomotor and metabolic activity, with HR mice having increased voluntary wheel-running behavior and maximal aerobic capacity (VO max) during forced treadmill exercise. Femora from adult mice (average age 7.5 months) of the 11th generation of this selection experiment were μCT-scanned and three-dimensional virtual reconstructions of nutrient canals were measured for minimum cross-sectional area as a skeletal proxy of blood flow. Gross observations revealed that nutrient canals varied far more in number and shape than prior descriptions would indicate, regardless of sex or genetic background (i.e. HR vs. C lines). Canals adopted non-linear shapes and paths as they traversed from the periosteal to endosteal borders through the cortex, occasionally even branching within the cortical bone. Additionally, mice from both HR and C lines averaged more than four nutrient canals per femur, in contrast to the one to two nutrient canals described for femora from rats, pigs, and humans in prior literature. Mice from HR lines had significantly larger total nutrient canal area than C lines, which was the result not of an increase in the number of nutrient canals, but rather an increase in their average cross-section size. This study demonstrates that mice with an evolutionary history of increased locomotor activity and maximal aerobic metabolic rate have a concomitant increase in the size of their femoral nutrient canals. Although the primary determinant of nutrient canal s...

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“…Therefore, measurements of external arterial dimensions can indicate the rate of blood flow within them. Where an artery passes through a foramen in a bone, the foramen size can be a gauge of arterial size, which is the key innovation that has allowed estimates of bone perfusion in living and extinct vertebrates (Allan et al, 2014;Seymour et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Scaling of cerebral blood perfusion in primates and marsupials

Seymour

Angove

Snelling

et al. 2015

Journal of Experimental Biology

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The evolution of primates involved increasing body size, brain size and presumably cognitive ability. Cognition is related to neural activity, metabolic rate and rate of blood flow to the cerebral cortex. These parameters are difficult to quantify in living animals. This study shows that it is possible to determine the rate of cortical brain perfusion from the size of the internal carotid artery foramina in skulls of certain mammals, including haplorrhine primates and diprotodont marsupials. We quantify combined blood flow rate in both internal carotid arteries as a proxy of brain metabolism in 34 species of haplorrhine primates (0.116-145 kg body mass) and compare it to the same analysis for 19 species of diprotodont marsupials (0.014-46 kg). Brain volume is related to body mass by essentially the same exponent of 0.70 in both groups. Flow rate increases with haplorrhine brain volume to the 0.95 power, which is significantly higher than the exponent (0.75) expected for most organs according to 'Kleiber's Law'. By comparison, the exponent is 0.73 in marsupials. Thus, the brain perfusion rate increases with body size and brain size much faster in primates than in marsupials. The trajectory of cerebral perfusion in primates is set by the phylogenetically older groups (New and Old World monkeys, lesser apes) and the phylogenetically younger groups (great apes, including humans) fall near the line, with the highest perfusion. This may be associated with disproportionate increases in cortical surface area and mental capacity in the highly social, larger primates.

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Blood flow for bone remodelling correlates with locomotion in living and extinct birds

Cited by 17 publications

References 53 publications

Femoral bone perfusion through the nutrient foramen during growth and locomotor development of western grey kangaroos Macropus fuliginosus

Femoral bone perfusion through the nutrient foramen during growth and locomotor development of western grey kangaroos Macropus fuliginosus

Effects of selective breeding for high voluntary wheel‐running behavior on femoral nutrient canal size and abundance in house mice

Scaling of cerebral blood perfusion in primates and marsupials

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