Coupling the mechanics and energetics of bird and insect flight

Humanity has long been fascinated by the mysteries of bird and insect flight, but only recently have we developed the technologies required to understand the complex mechanisms at work. These mechanisms range from molecular interactions to the interactions between whole organisms, encompassing a great number of mechanical and energetic processes. Research into animal flight has made great progress over the past half-century thanks to developments in technology and methodology, allowing for greater insights into the metabolic, mechanical and aerodynamic processes central to animal flight. Currently, there is a good understanding of several of these components but the topic of animal flight has been explored with a rather piecemeal approach and a more integrative understanding of the mechanics and energetics of animal flight is required. The research presented in this thesis aims to bridge our understanding of the often separately analysed mechanical and energetic aspects of animal flight and address key gaps in the existing knowledge.
Many volant bird species exhibit asymmetrical wingbeat cycles such that the flight muscles spend relatively more time shortening than lengthening. Through the simultaneous determination of mechanical work generation and energy consumption in the mouse soleus during in vitro contraction cycles with asymmetrical length trajectories, we reveal that mechanical power production can be increased by increasing the proportion of the cycle spent shortening without sacrificing net muscle efficiency. These experiments also served to validate a methodology for estimating the net muscle efficiency of the avian pectoralis muscle.
The following experiments determined the mechanical power generation, muscular costs of contraction and muscle efficiency of the budgerigar pectoralis during a range of simulated flight speeds. The efficiency of avian flight muscle was previously unknown and unsubstantiated values had been used in common predictive models of flight energetics. It was found that avian flight muscle efficiency is approximately 21% during the downstroke and remains constant with flight speed, with muscular energy consumption and power generation sharing characteristics with whole-animal metabolic and mechanical power-speed relationships. The consequences of these findings for the estimation of energetic flight costs are discussed.
While respirometry serves as the gold standard for measuring metabolic expenditure during activity, accelerometry affords the potential for estimating the energetic costs of flight in birds in the field. However, there has been no calibration of the relationship between body acceleration and energy expenditure. By measuring energy consumption via respirometry and dynamic body acceleration in masked lovebirds during wind tunnel flights at a range of speeds, we determine the metabolic requirements of flight for a new avian species and validate the use of accelerometry for estimating energy expenditure and flight kinematics.
Finally, we examined the previously unexplored relationship between myoplasmic calcium ion concentration, contraction frequency, mechanical power and myofibrillar efficiency in asynchronous insect flight muscles. There is increasing evidence to suggest that calcium plays an important role in the modulation of mechanical power during flight in insects with asynchronous flight muscles. By simultaneously measuring mechanical power generation and ATPase activity of flight muscles from giant waterbugs (Lethocerus), we reveal a positively shifting relationship between increasing calcium concentrations and optimal frequency for generating power, but with no evidence of a shift in optimal frequency for muscle efficiency.
This research demonstrates scientific impact by improving our understanding of the factors that affect muscle efficiency, refining the models used to predict wild animal metabolism during flight, developing and validating existing experimental techniques for determining the costs of flight, and improving our understanding of how both mechanical and physiological factors can affect the mechanical and energetic performance of bird and insect flight muscles.