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.2013 May 28;110(22):8852-7.
doi: 10.1073/pnas.1222726110. Epub 2013 May 6.

Specialized bat tongue is a hemodynamic nectar mop

Affiliations

Specialized bat tongue is a hemodynamic nectar mop

Cally J Harper et al. Proc Natl Acad Sci U S A..

Abstract

Nectarivorous birds and bats have evolved highly specialized tongues to gather nectar from flowers. Here, we show that a nectar-feeding bat, Glossophaga soricina, uses dynamic erectile papillae to collect nectar. In G. soricina, the tip of the tongue is covered with long filamentous papillae and resembles a brush or mop. During nectar feeding, blood vessels within the tongue tip become engorged with blood and the papillae become erect. Tumescence and papilla erection persist throughout tongue retraction, and nectar, trapped between the rows of erect papillae, is carried into the mouth. The tongue tip does not increase in overall volume as it elongates, suggesting that muscle contraction against the tongue's fixed volume (i.e., a muscular hydrostat) is primarily responsible for tip elongation, whereas papilla erection is a hydraulic process driven by blood flow. The hydraulic system is embedded within the muscular hydrostat, and, thus, intrinsic muscle contraction may simultaneously increase the length of the tongue and displace blood into the tip. The tongue of G. soricina, together with the tongues of nectar-feeding bees and hummingbirds, which also have dynamic surfaces, could serve as valuable models for developing miniature surgical robots that are both protrusible and have highly dynamic surface configurations.

Keywords: biomechanics; feeding kinematics; fluid dynamics; lingual papillae; soft robots.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Elongated tongue of a nectar-feeding bat,G. soricina, and its characteristic hair-like papillae. (A)G. soricina hovers in front of a feeder filled with artificial nectar and laps nectar with its long tongue. The white arrow highlights the distal tip of the tongue, which is covered in hair-like papillae. (B) Scanning electron micrograph of the tongue tip, showing a mop-like structure made of elongated lingual papillae. In this micrograph, the hair-like papillae are in their resting condition. (Scale bar: 1 mm.) (C) Scanning electron micrograph of the medial surface of the hair-like papillae, demonstrating that they are arranged in horizontal rows along the tongue tip. (Scale bar: 100 µm.) (D) Scanning electron micrograph of small filiform papillae located on the middle and proximal regions of the dorsal surface of the tongue. (Scale bar: 30 µm.)
Fig. 2.
Fig. 2.
Anatomy of theG. soricina tongue tip. (A) Line tracings of three transverse sections through the proximal (Upper), middle (Middle), and distal (Lower) region of the tongue. The dorsal surface of the tongue is directed up. These drawings highlight the location of the epidermis/dermis/papillae (light gray), skeletal muscle (white), hypoglossal nerve (yellow), arteries (red), and veins (blue). (Scale bar: 1 mm.) (B) Schematic of the arteries and veins within theG. soricina tongue. Arteries are shown in red and veins in blue. The dotted lines in the tongue tip illustrate the position of the arteriovenous anastomoses. (C) Transverse section and line tracing of the tongue tip showing the direct connection between the vascular sinus and papillary vein. This micrograph shows only the left side of the tongue tip. The color scheme in the line tracing matches the schematics shown above except, here, the orthogonally arranged skeletal muscle fibers are illustrated as dark gray lines. (Scale bar: 0.1 mm.) ava, arteriovenous anastomoses; bh, base of hair-like papilla; ca, central artery; dla, deep lingual artery; dlv, deep lingual vein; f, frenulum; ft, filamentous tip of hair-like papilla; pv, papillary vein; vs., vascular sinus.
Fig. 3.
Fig. 3.
Blood flow and papilla erection in actively feedingG. soricina. (Upper) Frames from a color high-speed movie. (Lower) Line tracings of the rostrum, tongue, and nectar. The bat hovered in front of an acrylic feeder filled with sugar water and only the tip of the rostrum and dorsal surface of the tongue are in the camera’s field of view. In the line tracings, the tongue is shown in pink, the vascular sinuses and papillary veins in red, and the sugar water in light gray.
Fig. 4.
Fig. 4.
Artificial papilla erection produced by saline injection in aG. soricina tongue (postmortem). (A) Photographs taken with a dissecting microscope before, during, and after saline injection into the vascular sinus. The papillae become erect and the tongue tip lengthens when saline is injected into the vascular spaces. (B andC) Scanning electron micrographs of the injected tongue in dorsal (B) and lateral (C) views. In both micrographs, the tongue tip is on the right and the proximal end of the tongue is on the left. The proximal tongue was ligated with suture after inflation to prevent saline from draining out of the vascular spaces. InA andB, a star demarcates the saline injection site and small arrows point to the horny papillae. (Scale bars: 1 mm.)
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References

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