Neural Control of Fibrillar Muscles in Bees During Shivering and Flight

Abstract

The big indirect flight muscles in the thorax of honeybees and bumblebees show two modes of action: they contract with ‘conventional’ twitches in response to slowly repeated muscle potentials and go into tetanus at higher muscle potential frequencies. They can also contract much faster when quickly stretched (stretch activation). We observed contractions of DV (dorsoventral) and DL (dorsal longitudinal) muscles optically with the help of a tiny mirror glued to the scutellum. We noticed that DL muscles contracted much more than DV muscles during pre-flight warmup. During warm-up, muscle potential frequencies in DL muscles were higher than in DV muscles (DL frequency/DV frequency =1.3), whereas during flight the ratio reversed (DL/DV=0.8). The scutal fissure was completely closed during shivering warm-up, apparently because the DL muscles shortened as much as they could. As a consequence, fast antagonistic stretching was not possible. However, the scutal fissure oscillated between wide open and closed during flight, and antagonists could stretch each other quickly. Flight was started by highly synchronized ‘conventional’ contractions of many muscle elements in DV muscles. Antagonistic stretch-activation during flight led to faster shortening than during shivering warm-up and synchronized all activated muscle elements to produce maximal contractions. The indirect flight muscles of bumblebees were in tetanic contractions during shivering warm-up over the whole range of temperatures between 8 and 36°C. These tetanic contractions probably prevented other researchers from observing mechanical muscle activity. Our results, which for the first time allow us to detect tetanic contractions directly, make it very improbable that non-shivering thermogenesis occurs in bumblebees, as has been proposed previously.