Superfast Muscles Set Maximum Call Rate in Echolocating Bats

Abstract

As an echolocating bat closes in on a flying insect, it increases call emission to rates beyond 160 calls per second. This high call rate phase, dubbed the terminal buzz, has proven enigmatic because it is unknown how bats are able to produce calls so quickly. We found that previously unknown and highly specialized superfast muscles power rapid call rates in the terminal buzz. Additionally, we show that laryngeal motor performance, not overlap between call production and the arrival of echoes at the bat's ears, limits maximum call rate. Superfast muscles are rare in vertebrates and always associated with extraordinary motor demands on acoustic communication. We propose that the advantages of rapid auditory updates on prey movement selected for superfast laryngeal muscle in echolocating bats.

Is sexual dimorphism in singing behavior related to syringeal muscle composition?

“…Superfast muscle fibers are known from sound-producing organs in species as diverse as fishes (e.g., Kéver et al 2014), snakes (e.g., Rome et al 1996), birds (Elemans et al 2008, Fuxjager et al 2016, and mammals (e.g., Elemans et al 2011). These fibers contract faster than typical vertebrate ''fast'' muscle and display a trade-off between force generation and speed (Rome 2006).…”

How the bat got its buzz

“…, rates occurring during the buzz [6]. At these high cycling rates, however, we also observed that the superfast vocal muscles could not completely relax to baseline tension (figure 2).…”

“…We now know that rare superfast muscles power the buzz [6]. For laryngeal echolocating bats, each call emitted is under active neuromuscular control [6,7]; we therefore assume that all bats that buzz possess superfast laryngeal muscles. During the buzz, some bats (figures 1 and 2) produce a distinct second phase, buzz II, characterized by up to a one-octave drop in the F 0 of their calls [3,5,10].…”

“…Laryngeally echolocating bats produce sound by airflowinduced oscillation of the specialized vocal membranes in the larynx (figures 1 and 2; [6,7]). These oscillations cause pressure changes in the vocal tract, radiated as sound.…”

Vocal production complexity correlates with neural instructions in the oyster toadfish (Opsanus tau)

“…The performance demands on motor systems associated with sound production and modulation have selected for the evolution of extreme superfast muscles (Elemans et al, 2011;Elemans et al, 2008;Elemans et al, 2004;Rome, 2006;Rome et al, 1996;Young and Rome, 2001) and highly synchronised and specialised motor neurons (Chagnaud et al, 2012). Our results show that complex signals, even in a simple sound-producing organ, can emerge from reliable neural inputs.…”