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. 2020 Feb 6;10(1):2007.
doi: 10.1038/s41598-020-58843-5.

The Vocal Organ of Hummingbirds Shows Convergence With Songbirds

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Free PMC article

The Vocal Organ of Hummingbirds Shows Convergence With Songbirds

Tobias Riede et al. Sci Rep. .
Free PMC article

Abstract

How sound is generated in the hummingbird syrinx is largely unknown despite their complex vocal behavior. To fill this gap, syrinx anatomy of four North American hummingbird species were investigated by histological dissection and contrast-enhanced microCT imaging, as well as measurement of vocalizations in a heliox atmosphere. The placement of the hummingbird syrinx is uniquely located in the neck rather than inside the thorax as in other birds, while the internal structure is bipartite with songbird-like anatomical features, including multiple pairs of intrinsic muscles, a robust tympanum and several accessory cartilages. Lateral labia and medial tympaniform membranes consist of an extracellular matrix containing hyaluronic acid, collagen fibers, but few elastic fibers. Their upper vocal tract, including the trachea, is shorter than predicted for their body size. There are between-species differences in syrinx measurements, despite similar overall morphology. In heliox, fundamental frequency is unchanged while upper-harmonic spectral content decrease in amplitude, indicating that syringeal sounds are produced by airflow-induced labia and membrane vibration. Our findings predict that hummingbirds have fine control of labia and membrane position in the syrinx; adaptations that set them apart from closely related swifts, yet shows convergence in their vocal organs with those of oscines.

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
(a) The “bee” hummingbirds (Mellisugini) have undergone rapid speciation relative to related groups. Hummingbirds(Trochilidae) along with swifts and swiftlets are grouped within the Apodiformes, while Caprimulgiformes and Apodiformes are within the clade Strisores. (b) The hummingbird vocal organ is located in the neck, unlike in other birds where it is located in the body cavity. The hummingbird tracheobronchial junction is positioned much higher in the respiratory tract than most other avian vocal organs. Consequently, the tracheal (i.e. the tracheal vocal tract filter) is much shorter than for example that of a zebra finch, a relatively small songbird. Tracheal and bronchial measurements of hummingbirds represent mean values of four similar species (mean ± standard deviation). Zebra finch dimensions after Daley & Goller. Zebra finch syrinx schematic after Riede & Goller. (c) Lateral view of a segmented 3D surface of the skeleton (white), the tracheal and bronchial airway (green), the tympanum (blue) and the larynx (purple) of an Anna’s hummingbird adult male that was microCT scanned at 50 μm resolution in a fixed position. (d) Ventral view of the same bird. Note that the calcified tympanum of the syrinx is located on the bird’s left side of the neck. The bird was salvaged after a window collision which resulted in the rostral part of the beak being lost.
Figure 2
Figure 2
Three-dimensional models of the tympanum and four accessory cartilages from three hummingbird species reflecting qualitative differences in shape and size between the species. P, pessulus; B1 through B4 denote four accessory cartilages that are embedded in the lateral wall (B1–B3) and the MTM (B4). The large surface area of the tympanum serves as attachment area for intrinsic syringeal muscles. The arrows in the top left panel indicate attachment area and fiber orientation of three intrinsic muscles (M1, M2, M3). The accessory cartilages are in part inserted by those syringeal muscles and thereby help to posture and tension the vibrating tissue inside the syrinx.
Figure 3
Figure 3
Histological sections of a hummingbird syrinx. Sections are coronal sections from three male Costa’s hummingbird syrinxes. (a) Overview of trachea, syrinx and two bronchi (trichrome stain). The square in (a) indicates the location of the higher magnification image in (b) and the squares in (b) indicate the location of the higher magnification images in (cm). (c) B1 and B2 are accessory cartilages situated caudal from the tympanum (Ty). There are one or two expansions at the caudal end (d) and a single smaller expansion at the cranial end. Accessory cartilages (B1, B2, B3, B4) are positioned caudal to the tympanum. B1 occurs as a flattened structure that extends into the lumen, and at its lateral edge it is connected to the tympanum and to B2 by connective fibrous tissue (d, arrows). Note that B1 points almost horizontally into the lumen near the tracheobronchial junction, thereby seeming to obstruct airflow at this location. (e) Tracheal ring cross sectional area is oval-shaped at mid-organ level. (f) Bronchial half-rings were flat and long-shaped cross sections at mid-organ level. Arrows point to regions of high collagen density that connect the three cartilaginous structures. (g,h) The lateral labia consists of a single layer of cuboidal ciliated epithelium and a small amount of connective tissue below the epithelial layers. (collagen, blue stain in (g); no black elastin EVG stain in (h). (i,j) Hyaluronan (blue stain in (i), removal of hyaluronan by hyaluronidase digestion with subsequent AB staining (absent blue stain in (j)). (km) Medial tympaniform membrane (MTM) consists of two cellular layers (lumen side epithelium and airsac endothelium) with embedded elastic fibers (l). A thick layer of collagen fibers occurs near the dorsal end (m). Ty, tympanum; B1 and B2, first and second accessory cartilage; P, pessulus; LL, lateral labium; MTM, medial tympaniform membrane.
Figure 4
Figure 4
Coronal cross-sections of the tympanum at mid-organ level in four hummingbird species: (a) male Anna’s hummingbird, (b) male Costa’s hummingbird, (c) female Costa’s hummingbird, (d) male black-chinned hummingbird, (e) male rufus hummingbird. p = pessulus, B4 = fourth bronchial element, MTM = medial tympaniform membrane.
Figure 5
Figure 5
Three intrinsic muscles have been identified in the hummingbird syrinx. Ventral (a), dorsal (b) and mid-organ coronal (c) view of the segmented three dimensional surfaces of the syrinx of an adult male Anna’s hummingbird. The interactive pdf files corresponding to those images can be accessed via Supplementary Fig. 1. (di) Coronal cross sections of the syrinx (H & E stain) from dorsal (df) to ventral (gi) of a male Anna’s hummingbird at 20 μm intervals. Two pairs of muscles move the syringeal cartilages. M1, M2, M3 – Muscles 1–3; B1–8, bronchial elements; T1–3, tracheal rings; Ty, tympanum; LL, lateral labium; MTM, medial tympaniform membrane.
Figure 6
Figure 6
Species-level analysis of hummingbird syrinx morphology (n = 18 birds). (a) Schematic of the syrinx measurements used in a representative serial section, for (a) top syrinx diameter, (b) bottom syrinx diameter, (c) pessulus height, (d) pessulus width, (e) length of cartilage B1, (f) mean tympanum height, (g) mean muscle diameter, (h) mean muscle length and (i) is the MTM length (the only curvilinear measurement). (b) Individual character measurements for each species, where different letters represent honestly significant differences from post-hoc Tukey tests for each trait independently. Quartile differences are represented by box-whisker plots and female samples are denoted by ‘F’. Y-axes are in μm. (c) Eigenvalues from a correlation-based PCA of the 9 characters in this analysis. (d) Eigenvectors with heavily loading characters represented as bold text within each vector. (e) Biplot of PC 1 versus PC 2. Species are represented by different colors clustered around the abbreviation for each species, and females are represented by ‘F’.

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