Integrating morphology and kinematics in the scaling of hummingbird hovering metabolic rate and efficiency

Wing kinematics and morphology are influential upon the aerodynamics of flight. However, there is a lack of studies linking these variables to metabolic costs, particularly in the context of morphological adaptation to body size. Furthermore, the conversion efficiency from chemical energy into movement by the muscles (mechanochemical efficiency) scales with mass in terrestrial quadrupeds, but this scaling relationship has not been demonstrated within flying vertebrates. Positive scaling of efficiency with body size may reduce the metabolic costs of flight for relatively larger species. Here, we assembled a dataset of morphological, kinematic, and metabolic data on hovering hummingbirds to explore the influence of wing morphology, efficiency, and mass on hovering metabolic rate (HMR). We hypothesize that HMR would decline with increasing wing size, after accounting for mass. Furthermore, we hypothesize that efficiency will increase with mass, similarly to other forms of locomotion. We do not find a relationship between relative wing size and HMR, and instead find that the cost of each wingbeat increases hyperallometrically while wingbeat frequency declines with increasing mass. This suggests that increasing wing size is metabolically favourable over cycle frequency with increasing mass. Further benefits are offered to larger hummingbirds owing to the positive scaling of efficiency.

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Faculty Opinions recommendation of Metabolic rate and body size are linked with perception of temporal information.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.718136730.793485068 ◽

2013 ◽

Author(s):

Kevin Lafferty

Keyword(s):

Body Size ◽

Metabolic Rate ◽

Temporal Information

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Intraspecific Variation in Maximum Ingested Food Size and Body Mass in Varecia rubra and Propithecus coquereli

Anatomy Research International ◽

10.1155/2011/831943 ◽

2011 ◽

Vol 2011 ◽

pp. 1-8 ◽

Cited By ~ 9

Author(s):

Adam Hartstone-Rose ◽

Jonathan M. G. Perry

Keyword(s):

Body Size ◽

Body Mass ◽

Individual Variation ◽

Size Variation ◽

Maximum Size ◽

Least Squares Regression ◽

Scaling Relationship ◽

Varecia Rubra ◽

Food Size ◽

The Relationship

In a recent study, we quantified the scaling of ingested food size (Vb )—the maximum size at which an animal consistently ingests food whole—and found that Vb scaled isometrically between species of captive strepsirrhines. The current study examines the relationship between Vb and body size within species with a focus on the frugivorous Varecia rubra and the folivorous Propithecus coquereli. We found no overlap in Vb between the species (all V. rubra ingested larger pieces of food relative to those eaten by P. coquereli), and least-squares regression of Vb and three different measures of body mass showed no scaling relationship within each species. We believe that this lack of relationship results from the relatively narrow intraspecific body size variation and seemingly patternless individual variation in Vb within species and take this study as further evidence that general scaling questions are best examined interspecifically rather than intraspecifically.

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Changes in body temperature influence the scaling of and aerobic scope in mammals

Biology Letters ◽

10.1098/rsbl.2006.0576 ◽

2006 ◽

Vol 3 (1) ◽

pp. 100-103 ◽

Cited By ~ 21

Author(s):

James F Gillooly ◽

Andrew P Allen

Keyword(s):

Body Size ◽

Metabolic Rate ◽

Size Dependence ◽

Maximal Activity ◽

Scaling Exponent ◽

Temperature Influence ◽

Aerobic Scope ◽

Metabolic Scope ◽

Single Power ◽

Maximum Metabolic Rate

Debate on the mechanism(s) responsible for the scaling of metabolic rate with body size in mammals has focused on why the maximum metabolic rate ( ) appears to scale more steeply with body size than the basal metabolic rate (BMR). Consequently, metabolic scope, defined as /BMR, systematically increases with body size. These observations have led some to suggest that and BMR are controlled by fundamentally different processes, and to discount the generality of models that predict a single power-law scaling exponent for the size dependence of the metabolic rate. We present a model that predicts a steeper size dependence for than BMR based on the observation that changes in muscle temperature from rest to maximal activity are greater in larger mammals. Empirical data support the model's prediction. This model thus provides a potential theoretical and mechanistic link between BMR and .

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Speed, stride frequency and energy cost per stride: how do they change with body size and gait?

Journal of Experimental Biology ◽

10.1242/jeb.138.1.301 ◽

1988 ◽

Vol 138 (1) ◽

pp. 301-318 ◽

Cited By ~ 47

Author(s):

N. C. Heglund ◽

C. R. Taylor

Keyword(s):

Body Size ◽

Body Mass ◽

Energy Cost ◽

Reaction Force ◽

Stride Frequency ◽

Energetic Cost ◽

Published Data ◽

Frequency Change ◽

Cost Of Locomotion ◽

The Cost

In this study we investigate how speed and stride frequency change with body size. We use this information to define ‘equivalent speeds’ for animals of different size and to explore the factors underlying the six-fold difference in mass-specific energy cost of locomotion between mouse- and horse-sized animals at these speeds. Speeds and stride frequencies within a trot and a gallop were measured on a treadmill in 16 species of wild and domestic quadrupeds, ranging in body size from 30 g mice to 200 kg horses. We found that the minimum, preferred and maximum sustained speeds within a trot and a gallop all change in the same rather dramatic manner with body size, differing by nine-fold between mice and horses (i.e. all three speeds scale with about the 0.2 power of body mass). Although the absolute speeds differ greatly, the maximum sustainable speed was about 2.6-fold greater than the minimum within a trot, and 2.1-fold greater within a gallop. The frequencies used to sustain the equivalent speeds (with the exception of the minimum trotting speed) scale with about the same factor, the −0.15 power of body mass. Combining this speed and frequency data with previously published data on the energetic cost of locomotion, we find that the mass-specific energetic cost of locomotion is almost directly proportional to the stride frequency used to sustain a constant speed at all the equivalent speeds within a trot and a gallop, except for the minimum trotting speed (where it changes by a factor of two over the size range of animals studied). Thus the energy cost per kilogram per stride at five of the six equivalent speeds is about the same for all animals, independent of body size, but increases with speed: 5.0 J kg-1 stride-1 at the preferred trotting speed; 5.3 J kg-1 stride-1 at the trot-gallop transition speed; 7.5 J kg-1 stride-1 at the preferred galloping speed; and 9.4 J kg-1 stride-1 at the maximum sustained galloping speed. The cost of locomotion is determined primarily by the cost of activating muscles and of generating a unit of force for a unit of time. Our data show that both these costs increase directly with the stride frequency used at equivalent speeds by different-sized animals. The increase in cost per stride with muscles (necessitating higher muscle forces for the same ground reaction force) as stride length increases both in the trot and in the gallop.

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Respiratory Exchange and Body Size in the Aldabra Giant Tortoise

Journal of Experimental Biology ◽

10.1242/jeb.55.3.651 ◽

1971 ◽

Vol 55 (3) ◽

pp. 651-665 ◽

Cited By ~ 1

Author(s):

G. M. HUGHES ◽

R. GAYMER ◽

MARGARET MOORE ◽

A. J. WOAKES

Keyword(s):

Body Weight ◽

Body Size ◽

Metabolic Rate ◽

Relative Proportion ◽

The Body ◽

O2 Consumption ◽

Weight Range ◽

Testudo Hermanni ◽

The Mean ◽

Good Agreement

1. The O2 consumption and CO2 release of nine giant tortoises Testudo gigantea (weight range 118 g-35·5 kg) were measured at a temperature of about 25·5°C. Four European tortoises Testudo hermanni (weight range 640 g-2·16 kg) were also used. The mean RQ values obtained were 1·01 for T. gigantea and 0·97 for T. hermanni. These values were not influenced by activity or size. 2. The data was analysed by plotting log/log regression lines relating body weight to O2 consumption. Both maximum and minimum metabolic rates recorded for each individual T. gigantea showed a negative correlation with body weight. For active rates the relation was O2 consumption = 140·8W0·97, whereas for inactive animals O2 consumption = 45·47W0·82. 3. The maximum rates were obtained from animals that were observed to be active in the respirometer and the minimum rates from animals that remained quiet throughout. The scope for activity increased with body size, being 82 ml/kg/h for animals of 100 g and 103 ml/kg/h for 100 kg animals. The corresponding ratio between maximum and minimum rates increases from about 2 to 6 for the same weight range. 4. Values for metabolic rate in T. hermanni seem to be rather lower than in T. gigantea. Analysis of the relative proportion of the shell and other organs indicates that the shell forms about 31% of the body weight in adult T. hermanni but only about 18% in T. gigantea of similar size. The shell is not appreciably heavier in adult T. gigantea (about 20%). 5. Data obtained for inactive animals is in good agreement with results of other workers using lizards and snakes. Previous evidence suggesting that chelonians show no reduction in metabolic rate with increasing size is not considered to conflict with data obtained in the present work.

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Relation between Metabolic Rate and Body Size in the Ovine Fetus

Journal of Nutrition ◽

10.1093/jn/117.6.1181 ◽

1987 ◽

Vol 117 (6) ◽

pp. 1181-1186 ◽

Cited By ~ 23

Author(s):

Alan W. Bell ◽

Frederick C. Battaglia ◽

Giacomo Meschia

Keyword(s):

Body Size ◽

Metabolic Rate ◽

Ovine Fetus

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Field Metabolic Rate and the Cost of Ranging of the Red-Tailed Sportive Lemur (Lepilemur Ruficaudatus)

New Directions in Lemur Studies ◽

10.1007/978-1-4615-4705-1_5 ◽

1999 ◽

pp. 83-91 ◽

Cited By ~ 13

Author(s):

Sonja Drack ◽

Sylvia Ortmann ◽

Nathalie Bührmann ◽

Jutta Schmid ◽

Ruth D. Heldmaier ◽

...

Keyword(s):

Metabolic Rate ◽

Field Metabolic Rate ◽

The Cost ◽

Sportive Lemur ◽

Lepilemur Ruficaudatus

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Changing the relative size of the body parts of Drosophila by selection

Genetics Research ◽

10.1017/s0016672300034972 ◽

1962 ◽

Vol 3 (2) ◽

pp. 169-180 ◽

Cited By ~ 36

Author(s):

Forbes W. Robertson

Keyword(s):

Body Size ◽

Relative Size ◽

Cell Number ◽

High Ratio ◽

Growth Patterns ◽

The Body ◽

Mass Selection ◽

Body Parts ◽

Wing Size ◽

Thorax Length

1. Mass selection for both high- and low-ratio of wing to thorax length has been carried out on a population of Drosophila melanogaster. The response to selection was immediate and sustained. When the experiment was stopped after ten generations, the wing area in the two selected lines differed by about 30%. The heritability estimate worked out at 0·56 ± 0·08.2. Thorax length remained comparatively unchanged during selection nor was there any change in wing shape. There was some evidence of assymetry of response since there was a relatively greater change in favour of smaller rather than larger size.3. The tibia length of all pairs of legs showed correlated changes so that the lines with larger or smaller wing sizes had also larger and smaller legs.4. The normal allometric relation between wing and thorax length, associated with variation in body-size, apparently also changed, so that for a given change in thorax length there was a greater or smaller proportional change in wing size in the high- or low-ratio lines.5. The changes in relative wing size are due to changes in cell number.6. It is suggested that the genetic changes due to selection act in the early pupal period when the imaginal discs are undergoing differentiation and proliferation to form imaginal hypoderm and appendages.7. Tests of genetic behaviour failed to show any departure from additivity in crosses which involved the unselected population and the high-ratio line. But highly significant departures existed in the cross to the low-ratio line. Relatively smaller wing size behaves as largely recessive. Stability of the normal wing/thorax ratio involves dominance and probably also epistasis. The genetic properties of the relative size of the appendage are apparently similar to those which characterize body-size as a whole.8. It is suggested that selection provides a valuable tool for studying the constancy or lability of the growth patterns which determine morphology.

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