Experimental Studies of Carpenter Bee (Xylocopa: Apidae) Thorax Mechanics During Defensive Buzzing

Bees and other Hymenoptera utilize thorax vibration to realize an extensive range of behaviors ranging from flight to pollination. Strong indirect flight muscles contract to deform the thoracic walls and the resulting oscillation is sustained through a mechanism called stretch activation. While the mechanics of the insect thorax and muscles have been studied extensively during flight, relatively little is known about the thorax mechanics during non-flight behaviors. In this work, we investigate the thorax mechanics of the carpenter bee Xylocopa californica during defensive buzzing. During defensive buzzing, the insect folds its wings over its abdomen and rapidly fires it flight muscles, resulting in a loud audible buzz and large forces intended to deter predators. We devised a novel experiment to measure thorax oscillation and directional force production from a defensively buzzing carpenter bee. The largest peak forces were on average 175 mN and were oriented with the insect's dorsal-ventral muscle group. Peak forces oriented with the insect's dorsal-longitudinal muscle group averaged 117 mN. Thorax velocities were about 90 mm s^-1 p-p and velocity amplitude was positively correlated to peak force. Thorax oscillation frequency averaged 132 Hz but was highly variable both within individuals and across the tested population. From our measurements, we estimated the peak mechanical power required by defensive buzzing at 8.7 mW, which we hypothesize is greater than the power required during flight. Overall, this study provides insight into the function and capabilities of the Hymenopteran indirect flight muscle during non-flight behaviors.

A myosin-based mechanism for stretch activation and its possible role revealed by varying phosphate concentration in fast and slow mouse skeletal muscle fibers

Stretch activation (SA) is a delayed increase in force following a rapid muscle length increase. SA is best known for its role in asynchronous insect flight muscle, where it has replaced calcium’s typical role of modulating muscle force levels during a contraction cycle. SA also occurs in mammalian skeletal muscle but has previously been thought to be too low in magnitude, relative to calcium-activated (CA) force, to be a significant contributor to force generation during locomotion. To test this supposition, we compared SA and CA force at different Pi concentrations (0–16 mM) in skinned mouse soleus (slow-twitch) and extensor digitorum longus (EDL; fast-twitch) muscle fibers. CA isometric force decreased similarly in both muscles with increasing Pi, as expected. SA force decreased with Pi in EDL (40%), leaving the SA to CA force ratio relatively constant across Pi concentrations (17–25%). In contrast, SA force increased in soleus (42%), causing a quadrupling of the SA to CA force ratio, from 11% at 0 mM Pi to 43% at 16 mM Pi, showing that SA is a significant force modulator in slow-twitch mammalian fibers. This modulation would be most prominent during prolonged muscle use, which increases Pi concentration and impairs calcium cycling. Based upon our previous Drosophila myosin isoform studies and this work, we propose that in slow-twitch fibers a rapid stretch in the presence of Pi reverses myosin’s power stroke, enabling quick rebinding to actin and enhanced force production, while in fast-twitch fibers, stretch and Pi cause myosin to detach from actin.