Ecologists would love to know the metabolic energy requirements that dictate bird behaviours such as flight, but getting a handle on this is challenging. ‘Understanding what determines overall energy requirements is a theme of my lab,’ says Graham Askew from the University of Leeds, UK, and adds, ‘I am trying to get the link between what the muscles are doing and how much energy they use to get a global picture of animal locomotion.’ But very few studies into the energetics of bird fight had systematically scrutinised the problem from the perspective of the mechanical power through to the metabolic energy consumed. Teaming up with graduate student Charlotte Morris, Askew began methodically dissecting out the different components that power bird flight.
First the duo focused on how birds modulate the amount of mechanical power they produce during flight (p. 2770). Askew explains that if you plot the mechanical power that a bird produces against its flight speed, you get a U-shaped curve where the power is highest at low speeds (it takes a lot of energy to hover), drops to a minimum at intermediate cruising speeds and rises again at the highest speeds. Curious to know how birds modulate the power output by the main flight muscle, the pectoralis, at different speeds, Morris and Askew trained cockatiels to fly in a wind tunnel at speeds ranging from hovering at 0 m s−1 up to a speedy 16 m s−1. Once the birds had got the hang of flying in the wind tunnel, the duo inserted minute ultra-sonic crystals into the birds' pectoral muscles to measure how much the muscle length changed during each muscular contraction, placed hair-like electrodes adjacent to the sonomicrometry crystals to record the electrical impulses that triggered each contraction and filmed the birds with a high-speed digital camera as they flew.
Analysing the muscle's electrical activity, Morris and Askew could see that the birds primarily modulated their muscle activation to modulate their power output, increasing the electrical activity to recruit more muscle fibres at low and high speeds. The duo also noticed that at low speeds, the birds increased the amount of time spent shortening the muscle during each wing beat cycle from 50% to 60%. However, at the highest speeds, the birds increased their mechanical power output by increasing the muscle strain: that is, they increased the relative amount of slide between the actin and myosin filaments to increase the mechanical power output. And when they analysed the movies, Morris and Askew saw that the cockatiels alternated between flapping and gliding at low power intermediate speeds, and switched to flapping continuously when they needed most power at the lowest and highest speeds.
But how much power was the pectoral muscle actually producing as the bird flapped at different speeds? Askew decided to determine the muscle's power output by measuring the power of isolated bundles of muscle fibres (fascicles) while they contracted. Isolating individual fascicles from the cockatiels' pectoralis muscles, Morris and Askew stretched and released the muscle fibres in the same way that the muscle filaments had slid past each other as the bird flew while electrically activating the muscle fibres using the electrical impulse pattern that they had recorded during flight. Measuring the force produced by the stimulated muscle fibres, the duo were then able to calculate the power produced by the muscles at various speeds and found that it varied from approximately 120 W kg−1 at the high speeds to a minimum of approximately 40 W kg−1 at intermediate speeds.
But how did the power estimates based on an aerodynamic model of flight compare with the powers measured from the muscle fascicles (p. 2781)? Measuring the position of the bird's centre of mass and various wing beat parameters from the movies, the duo used coefficients taken from the literature to estimate drag and calculate the bird's mechanical power output from the aerodynamic model.
But Askew points out that, ‘There has been a build up of a range of different numbers and this is one of the problems with aerodynamic models: what values should you pick for your aerodynamic coefficients and are they appropriate across all flight speeds?’ The duo tested which coefficients produced the best agreement with the powers measured from the flight muscle fascicles and Askew says, ‘We got the best match at low speeds when we used coefficients from the low end of the range and the best match at the high speeds when we used coefficients from the medium values’. He adds that although estimating mechanical power output based on the bird's flight behaviour is convenient, ‘we should be very cautious about the coefficients that we use in aerodynamics models, in particular about using the same coefficients across all flight speeds’.
Finally, Morris and Askew teamed up with Frank Nelson to find out how the mechanical power output measurements related to the metabolic energy consumed by the birds in order to estimate the pecoralis muscle efficiency and the cost of other metabolic systems during flight (p. 2788). ‘We trained the birds to fly wearing a little mask that we could connect to the respirometry apparatus to withdraw the air that the animal is breathing out and analyse it for the amount of oxygen that the animal is using and carbon dioxide that it is producing to measure their metabolic rates,’ explains Askew. Using these values to calculate the birds' metabolic rates as they flew at speeds ranging from 6 to 13 m s−1, the trio then assumed a postural cost of flight – the energy consumed by other flight muscles and the cardiovascular system – of 10% and used this to calculate the pectoral muscle's efficiency. It came out at 7–11%, which seemed quite low given that the efficiency of mammalian muscle has been measured at 10–19%, so the team decided to run the calculation the other way round.
Choosing efficiency values of 19%, they calculated the fraction of the metabolic energy that is being consumed by the pectoralis muscle and found that it could be using between 36 and 54% of the metabolic energy, while choosing a low muscle efficiency of 10% suggested that the pectoralis could use between 69–100% of the metabolic energy, with the remaining energy going to other flight muscles and the respiratory and circulatory systems. ‘Our calculations suggest that the postural costs of flight have been under-estimated perhaps because the energy used by flight muscles other than the pectoralis muscles has been ignored,’ says Askew.
Having shown that researchers should use some caution when estimating the mechanical and metabolic costs of flight, Askew says, ‘Mechanical power calculations are good for general models for understanding how animals might fly, but in terms of coming up with specific predictions I think people need to be quite cautious.’ Looking to the future Askew says, ‘We need to fill in some of these gaps and measure flight muscle efficiency,’ and adds, ‘Getting a handle on the postural costs of flight is more challenging, but probably achievable’.