Heart mass and the maximum cardiac output of birds and mammals: implications for estimating the maximum aerobic power input of flying animals

“High athletic performance typically requires increased skeletal muscle mass (Weibel et al. 2004), heart size (Bishop 1997) and respiratory surface area (Muir & Hughes 1969), all of which may contribute to increased costs in animals while at rest due to the increased ATP expenditure required for…”

“By contrast, the relative mechanical and metabolic capacities of flying animals tend to decline with increasing size (Norberg, 1990; Bishop, 1997, 1999; Dudley, 2000).”

“Examples of adaptive responses to pressure loading include a comparison of mammals and birds, the latter having higher prevailing arterial blood pressures and larger hearts (Grubb 1983; Bishop 1997).”

“Although the flight muscles and heart generate and supply power for a substantial portion of locomotory and thermogenic activity [20–23], species variation in relative flight muscle size and heart index indicates the degree of importance of burst power [24] and endurance flight performance [17], respectively.”

“…of aerobic costs during extensive locomotion (Bishop 1997; Klaassen 1996), which is supported by species with energetically expensive flight mode possessing larger relative flight muscle and heart weight in order to produce more power and to meet the aerobic scope (Bishop 1997; Norberg 1990).”

“Everything else being equal, size alone should be a significant predictor of the heart's pumping capacity, as has been shown for heart mass and stroke volume or cardiac output (1, 17).”

“5·W; Westerterp and Drent, 1985) and those predicted from modelling cardiac output (11–12·W; Bishop 1997).”

“…extended submaximal exercise without oxygen debt and the daily energy expenditure (Clark 1927; Garland 1984; Walsberg et al. 1986; Daan et al. 1990; Weibel et al. 1991; Bishop & Butler 1995; Bishop 1997; Hammond & Diamond 1997; Meerlo et al. 1997; Hoppeler & Weibel 1998; Machida & Aohagi 2001).”

“Our resting and near-maximal values of cardiac output are close to those predicted for guinea fowl based on the equations of Grubb (1983) and Bishop (1997).”

“For each dependent variable, the best model was selected from a range of one to five parameter models (Table S2 cold, hypoxic environment (Tucker 1968; Bishop 1997).”

“Because maximal heart rates decrease with increasing body mass in endotherms and ectotherms (Lillywhite et al., 1999; Bishop, 1997), it is necessary to normalize the data to equivalent body mass.”

“…the model has subsequently been used to generate detailed quantitative predictions that address the dynamics of muscle function, the flight performance of birds, and a proposed functional equivalency between the mammalian and avian respiratory systems (Bishop, 1997; Bishop, 1999; Bishop, 2005).”

“However, some small phasianids, for example, Coturnix coturnix, are migratory and might be expected to have higher aerobic scopes during flight than running due to the high cost of flight (Bishop 1997).”

“Allometric equations for estimating cardiac variables are derived from 36 species of mammals and birds (Seymour & Blaylock 2000), but they are similar to equations in earlier studies (Bishop 1997; Gu« nther 1975; Holt et al. 1968; Stahl 1967).”

“Bishop (1997) presented two different methods for predicting a flying bird’s VO∑max.”

“An extension of the earlier work is also required in view of the increased understanding of the exercise state of mammals provided by the works of Baudinette (1978), Taylor et al. (1981), Weibel et al. (1991), Bishop (1997, 1999) and Darveau et al. (2002), among others.”

“One method proposed by Bishop (1997) allows the use of HR to estimate the rate of oxygen consumption ð _VO2Þ during flight from measured HR and estimates of stroke volume (V2) and oxygen extraction from the blood ðCaO2KC VO2Þ, where CaO2 is oxygen concentration in the arterial blood and C VO2is…”

“…tunnel were similar when using three different techniques (doubly-labelled water, mask respirometry and heat transfer modelling) and that they were also similar to measurements made on free-living starlings (Westerterp and Drent, 1985) and those predicted from the cardiac model of Bishop (1997).”

“…study (cetacean: 1.00) scale similarly, with those reported in both terrestrial and marine mammals (marine mammal: 0.97; terrestrial: 1.04) (Stahl, 1967; Bishop, 1997; Fahlman et al., 2019c) but the gain appears to be different, possibly reflecting the different challenges with an aquatic life.”

“The product of V s and extraction is V O 2 (22).”

“1 g; Bishop et al., 1998) is 30% heavier than that of the captive geese (17 g) flying in the WT (S. Ward, C.M. Bishop, A.J. Woakes and P.J. Butler, unpublished data). Bishop and Butler (1995) and Bishop (1997) used the Fick relationship in Eq.”

“All else being equal, mice with larger cardiopulmonary organs and higher hematocrits should have a higher aerobic performance (Bishop, 1997; Rezende et al., 2006).”

“This is now known not to be the case, as a result of work by Baudinette (1978), Taylor et al. (1981), Weibel et al. (1991) and Bishop (1997, 1999), among others.”

“Using the second model of Bishop (1997), Pelletier et al. (2008) estimated mass-specific flight costs of flight to be 79Æ5 W kg)1 and this estimate was used in the present study.”

“4; Bishop, 1997; Seymour and Blaylock, 2000; Stahl, 1967).”

“…for large cardiac output, short circulatory turnover, blood with high oxygen carrying capacity, high capillary surface area, and highly refined pulmonary structural components (Bishop, 1997; Johansen et al., 1987; Maina, 2000; Suarez et al., Jo u rn al o f Ex p er im en ta lB io lo g y 1991).”

“Our average SV, fH and CO for an average 175 kg dolphin were also lower than those estimated from allometric relationships in terrestrial mammals ranging in size from 0.333 to 446 kg (Bishop, 1997; SV=389 ml beat−1, fH=66 beats min −1, CO=21,856 ml min−1).”

“Bishop, R.J. Spivey / Journal of Theoretical Biology 323 (2013) 11–19 12”

“birds (7, 34), in hypertensive giraffes (68), and even among mammals of different sizes (99).”

“Under the assumption that SV increases to its maximum capacity (∼0.03 ml min−1, calculated using eqn 7 of Bishop, 1997; using the heart mass reported for C. gouldii from Bullen et al., 2009), we calculate that arteriovenous difference must increase to a maximum of 26.23 ml O2 dl −1 blood at −2°C.”

“heart mass is a good indicator of adaptive specialization for prolonged locomotor activities in birds and mammals (48).”

“…to body mass across species (phylogenetic) based on a number of influential allometric analyses that arrive at an exponent of bp 0.96–1.06 (Brody 1945; Stahl 1965; Holt et al. 1968; Prothero 1979; Hoppeler et al. 1984; Bishop 1997; Seymour and Blaylock 2000; Lindstedt and Schaeffer 2002).”

“Ward, S., Bishop, C. M., Woakes, A. J. and Butler, P. J. (2002).”

“Using the second model of Bishop (Bishop, 1997), Pelletier et al. (Pelletier et al., 2008) estimated massspecific flight costs of flight to be 79.5Wkg–1, and this estimate was used in the present study.”

“The results were striking: during displays, the heart rate of a male Golden-collared Manakin can rise above 1,200 beats per minute (Barske et al. 2011), a rate that has been previously recorded only in small hummingbirds during flight (Bishop 1997).”

“Indeed, internal organs potentially scale geometrically with mb, for example, heart mass scales almost with geometric similarity (0.93) against mb (Bishop, 1997).”

“Thus, within the two vertebrate groups demonstrating whole body endothermy, on average the bird heart is capable of equal or greater output than the mammalian heart, a feature which may be necessary to support their elevated body temperature (average bird 41°C, average placental mammal 37°C [22]) and the energetic cos…”

“…birds (Nespolo et al., 2018) and, for example, Golden-collared manakins have some 20% greater cardiac mass and left ventricular wall thickness than similar-sized zebra finches (Barske et al., 2019) mammals also have a substantially varied, heart weight (Bishop, 1997; Seymour & Blaylock, 2000).”

“Heart size/mass has often been used as a predictor of cardiac output and ultimately VO2,max (Bishop, 1997; Richardson et al., 1999a; Chen et al., 2001; Hussain et al., 2001).”

“Differences in heart size between strategies (which would result in difference in stroke volume 33,34 and haematocrit values 35 ) could, in principle, increase during the pre-migration phase, potentially decoupling f H from oxygen consumption and, thus, energy expenditure.”

“…mammalian species shows that heart mass increases with body mass more-or-less isometrically, with an exponent (b) between 0.96 and 1.06 (Bishop, 1997; Brody, 1945; Holt et al., 1968; Hoppeler et al., 1984; Lindstedt and Schaeffer, 2002; Prothero, 1979; Seymour and Blaylock, 2000;…”

“Cardiac output is a function of both heart rate and stroke volume, but it is known to increase with both temperature and activity level (Bishop, 1997; Farrell, 1991; Vinogradov & Anatskaya, 2006; Hillman, Hancock & Hedrick, 2013).”

“The relationship between RMR and flight MR, however, has not been extensively examined in birds, with the exception of some attempts to estimate the relationship [40,41].”

“To support an energetic lifestyle, large hearts (Hartman, 1955) with large cardiac outputs (Grubb, 1983; Bishop, 1997; Seymour and Blaylock, 2000) supply tissues with oxygen.”

“Additionally, the hearts of hummingbirds are larger, relative to their body size, than other birds and can pump at a rate of more than 1000 beats per minute (9).”

“…transport cascade (Butler, 2010; Scott et al. , 2015; Hawkes et al. , 2017), but because flight costs scale following a power law with body mass (Bishop, 1997), it is likely that smaller species (e.g. alpine chough Pyrrhocorax graculus digitatus , or other smaller passerine species) may have…”

“This finding is at odds with the isometric scaling of heart mass on body mass reported from broad interspecific analyses of mammals (Bishop, 1997; Brody, 1945; Prothero, 1979; Stahl, 1965), as well as narrower analyses of some phylogenetic groups (Davis, 1962; Prothero, 1979; Stahl, 1965).”

“7(4) Time to half twitch relaxation, ms 37.”

“Unlike goshawks and buzzards, they might rely on their metatarsal fat pad to distribute pressure, but, compared to falcons, their degree of “adaptive specialization for prolonged locomotor activity” appears to be lower, as indicated by a smaller heart muscle mass [62].”

“Birds are known to have higher blood pressure in comparison to mammals [26], and it was found that blood pressure is not related to body mass [25].”

“rates to maintain adequate cardiac output.(19) It is, therefore, reasonable to assume that bradycardia may be exceptionally harmful for this avian species and that the cardiac-depressant effects of the anesthetic drugs, together with the peculiar cardiovascular physiology of tinamous, may have created the potential fo…”

“Additional references Bishop, C. M. (1997). Heart mass and the maximum cardiac output of birds and mammals: implications for estimating the maximum aerobic power input of flying animals. Philos. Trans. R. S. Lond. B. 352, 447–456. Bullen, R. D., McKenzie, N. L. and Cruz-Neto, A. P. (2014). Aerodynamic power and mechan…”

“…elevated aerobic capacity, the juvenile pterosaur exhibits lower mass-specific power output for sustained vertical takeoff when compared to similarly sized migratory phasianids, such as Coturnix coturnix and Coturnix chinensis ( Bishop, 1997 ; Askew & Marsh, 2001 ; Henry, Ellerby & Marsh, 2005 ).”