The hummingbird syrinx morphome: a detailed three-dimensional description of the black jacobin\u2019s vocal organ

Amanda Monte,Daniel N Düring,Alexander F Cerwenka,Manfred Gahr,Bernhard Ruthensteiner

doi:10.1186/s40850-020-00057-3

Abstract

BackgroundThe ability to imitate sounds depends on a process called vocal production learning, a rare evolutionary trait. In addition to the few mammalian groups that possess this ability, vocal production learning has evolved independently in three avian clades: songbirds, parrots, and hummingbirds. Although the anatomy and mechanisms of sound production in songbirds are well understood, little is known about the hummingbird’s vocal anatomy.ResultsWe use high-resolution micro-computed tomography (μCT) and microdissection to reveal the three-dimensional structure of the syrinx, the vocal organ of the black jacobin (Florisuga fusca), a phylogenetically basal hummingbird species. We identify three features of the black jacobin’s syrinx: (i) a shift in the position of the syrinx to the outside of the thoracic cavity and the related loss of the sterno-tracheal muscle, (ii) complex intrinsic musculature, oriented dorso-ventrally, and (iii) ossicles embedded in the medial vibratory membranes.ConclusionsThe extra-thoracic placement of the black jacobin’s syrinx and the dorso-ventrally oriented musculature likely aid to uncoupling syrinx movements from extensive flight-related thorax constraints. The syrinx morphology further allows for vibratory decoupling, precise control of complex acoustic parameters, and a large motor redundancy that may be key biomechanical factors leading to acoustic complexity and thus facilitating the occurrence of vocal production learning.

Highlights

The ability to imitate sounds depends on a process called vocal production learning, a rare evolutionary trait
We use high-resolution micro-computed tomography and microdissection to reveal the threedimensional structure of the syrinx, the vocal organ of the black jacobin (Florisuga fusca), a phylogenetically basal hummingbird species
We identify three features of the black jacobin’s syrinx: (i) a shift in the position of the syrinx to the outside of the thoracic cavity and the related loss of the sterno-tracheal muscle, (ii) complex intrinsic musculature, oriented dorso-ventrally, and (iii) ossicles embedded in the medial vibratory membranes

Summary

Introduction

The ability to imitate sounds depends on a process called vocal production learning, a rare evolutionary trait. In addition to the few mammalian groups that possess this ability, vocal production learning has evolved independently in three avian clades: songbirds, parrots, and hummingbirds. Vocal learning evolved independently in songbirds (suborder Passeri) [3, 4], parrots (order Psittaciformes) [5] and hummingbirds (family Trochilidae) [6] due to convergent. Efforts to understand vocal learning have concentrated on the neural processes that modulate vocal output with little regard to the biomechanics of sound production in the vocal organ [12]. Gallinaceous species have none, songbird species have from three to five intrinsic muscle pairs [17, 19], while parrot species mainly have two [19, 20]

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