Pulse sound generation, anterior swim bladder buckling and associated muscle activity in the pyramid butterflyfish, Hemitaurichthys polylepis

Abstract

Acoustic behaviors are widespread among diverse fish taxa but mechanisms of sound production are known from relatively few species, vary widely and convergent mechanisms are poorly known. We examined the sound production mechanism in the pyramid butterflyfish, Hemitaurichthys polylepis, a member of the socially and ecologically diverse reef fish family Chaetodontidae. In the field, fish produce pulse trains at dusk during social interactions that are probably related to mate attraction and courtship. In laboratory experiments, sound production was synchronized to high-speed video to determine body movement associated with sound generation. In addition, electromyography (EMG) recordings tested the activity of six candidate muscles. Fish produced individual pulses with a mean peak frequency of 97 Hz in rapid succession. EMG experiments show that anterior hypaxial muscles contract at high bilaterally synchronous rates (up to 120 Hz) in near perfect association with rapid inward buckling visible outside the body over the anterior swim bladder. Muscle activity often showed EMG doublets that occurred within the time of a single sound pulse but was not sustained. Buckling and sound pulse rates correlated strongly (R(2)≈1.00) and sound pulse rate measured over two successive pulses (maximum of 38 pulses s(-1)) was lower than muscle firing rate. These results show that the extrinsic swim bladder muscles of pyramid butterflyfish involve single contractions that produce pulses in a manner similar to distantly related teleosts, but involve a novel doublet motor-neuron firing pattern. Thus, the sound production mechanism in pyramid butterflyfish is likely convergent with several percomorph taxa and divergent from the related chaetodontid genus Forcipiger.

Sound production in the longnose butterflyfishes (genusForcipiger): cranial kinematics, muscle activity and honest signals

“…onset of EP lagged relative to sound onset (-0.08±3.68ms) compared with TEP (-0.71±3.22ms, paired t-test, N12, T2.01, P0.069). In the same individual, HP musculature, a region shown to be active during sound production in H. polylepis (Boyle & Tricas, 2010), was found to fire for only six out of 18 events, and to lag behind the onset of EP (mean EP onset-1.33±1.51ms versus HP mean6. 32±5.17s, paired t-test, N6, t-4.61, P0.006).…”

“…Territorial sounds of unknown mechanistic origin are described for pebbled butterflyfish (Tricas et al , 2006). Sound production in the pyramid butterflyfish (Hemitaurichthys polylepis) and pennant bannerfish (Heniochus chrysostomus) involves activity of anterior hypaxial musculature associated with anterior ribs and swimbladder (Boyle and Tricas, 2010;Parmentier et al, 2011). Recent phylogenetic hypotheses place the genus Forcipiger as basal within a clade that includes…”

“…Two to four muscles were tested for activity within each free-swimming subject. Candidate muscles were chosen based on preliminary analysis of high-speed video during sound emission that revealed a rapid cranial elevation component (see Results) and based on observations of a related chaetodontid, the pyramid butterflyfish (Boyle & Tricas, 2010). EMG recording electrodes (Fig.1) were placed in the anterior epaxial musculature (EP, N7) approximately 0.5cm posterior to the supraoccipital bone and at a dorso-ventral level approximately 50% of the dorso-ventral axis of the supraoccipital.…”

“…In one individual, an EMG electrode was inserted into tail epaxial musculature (TEP) midway between the caudal end of the body cavity and caudal peduncle, approximately 1cm above the midline. Based on observations of muscle activity during sound production in pyramid butterflyfish (Boyle & Tricas, 2010), we monitored the anterior hypaxial (HP) musculature caudal to the pectoral girdle and rib of the fourth vertebra, at a level approximately 25% along the ventral-dorsal axis of the supracleithrum (N1).…”

“…The direct mechanism for sound production by pebbled butterflyfish, however, remains unknown. In two closely related butterflyfish species, pyramid butterflyfish (Hemitaurichthys polylepis) and pennant bannerfish (Heniochus chrysostomus), pulse train sounds are produced that involve activity of hypaxial musculature in close association with the anterior swim bladder and ribs (Boyle and Tricas, 2010;Parmentier et al, 2011). These recent findings indicate that diversity in sound production mechanisms and behavioral contexts likely exists within the family Chaetodontidae and leads to the question of whether communicative sounds provide honest signals during interactions with conspecifics.…”