Abstract
At low ambient temperature Helicoverpa zea male moths engage in warm-up behavior prior to taking flight in response to an attractive female pheromone blend. Male H. zea warm up at a faster rate when sensing the attractive pheromone blend compared with unattractive blends or blank controls (Crespo et al. 2012), but the mechanisms involved in this olfactory modulation of the heating rate during preflight warm-up are unknown. Here, we test three possible mechanisms for increasing heat production: 1) increased rate of muscle contraction; 2) reduction in mechanical movement by increased overlap in activation of the antagonistic flight muscles; and 3) increased activation of motor units. To test which mechanisms play a role, we simultaneously recorded electrical activation patterns of the main flight muscles (dorsolongitudinal and dorsoventral muscles), wing movement, and thoracic temperature in moths exposed to both the attractive pheromone blend and a blank control. Results indicate that the main mechanism responsible for the observed increase in thoracic heating rate with pheromone stimulation is the differential activation of motor units during each muscle contraction cycle in both antagonistic flight muscles. This additional activation lengthens the contracted state within each cycle and thus accounts for the greater heat production. Interestingly, the rate of activation (frequency of contraction cycles) of motor units, which is temperature dependent, did not vary between treatments. This result suggests that the activation rate is determined by a temperature-dependent oscillator, which is not affected by the olfactory stimulus, but activation of motor units is modulated during each cycle.
Highlights
MANY INSECTS OF MEDIUM TO large size have evolved to take advantage of the metabolic heat produced during flight muscle contraction for regulating their thoracic temperature (Heinrich 1974)
When the female pheromone is present, male moths heat at higher rates than without pheromone, suggesting that modulation of thoracic heat production occurs during natural behavior (Crespo et al 2012), but the mechanisms for modulating heat generation are not known
We investigate to what degree three putative motor control mechanisms contribute to the observed increase in heating rate in the pheromone-stimulated males: 1) increase in the rate of flight muscle contractions; 2) increased heat production as the result of minimizing mechanical energy use through more simultaneous contraction of the antagonistic flight muscles; and 3) differential activation of motor units
Summary
MANY INSECTS OF MEDIUM TO large size have evolved to take advantage of the metabolic heat produced during flight muscle contraction for regulating their thoracic temperature (Heinrich 1974). The main antagonistic flight muscles, the dorsolongitudinal wing depressors (DLMs) and the dorsoventral wing elevators (DVMs) are the main heat source prior to take-off (Kammer 1970) Their kinetics are, like that of other invertebrate and vertebrate muscles, strongly affected by temperature. During the preflight warm-up behavior of Lepidoptera, DLMs and DVMs as well as several (and probably most) of the direct flight muscles (e.g., subalar, tergosternal, anterior and posterior tergocoxals, and dorso oblique; Kammer 1968) are activated almost simultaneously (Fig. 1), generating only small-amplitude wing movements (as opposed to the alternate contraction seen in flight; Kammer 1981). DVMs include an anterior and two posterior tergocoxals, one or a few tergosternals, a tergotrochanteral, and an extracoxal depressor (whose function in flight is unknown) muscle (Kammer 1985), and almost all of these are involved in the preflight warm-up behavior seen in moths (Kammer 1968). No information regarding the synchronization of these muscles during flight and warm-up behaviors has been collected so far
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