Relating form to function in the hummingbird feeding apparatus
- Published
- Accepted
- Subject Areas
- Biophysics, Zoology, Anatomy and Physiology
- Keywords
- Anatomy, Bill, Computed tomography, Electron microscopy, Lingual apparatus, Nectar feeding, Tongue
- Copyright
- © 2017 Rico-Guevara
- Licence
- This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ Preprints) and either DOI or URL of the article must be cited.
- Cite this article
- 2017. Relating form to function in the hummingbird feeding apparatus. PeerJ Preprints 5:e2986v1 https://doi.org/10.7287/peerj.preprints.2986v1
Abstract
A complete understanding of the feeding structures is fundamental in order to study how animals survive. Some birds use long and protrusible tongues as the main tool to collect their central caloric source (e.g. woodpeckers and nectarivores). Hummingbirds are the oldest and most diverse clade of nectarivorous vertebrates, being a perfect subject to study tongue specializations. Their tongue functions to intraorally transport arthropods through their long bills and enables them to exploit the nectarivorous niche by collecting small amounts of liquid, therefore it is of vital importance to study its anatomy and structure at various scales. I focused on the portions of the hummingbird tongue that have been shown to be key for understanding their feeding mechanisms. I used histology, transmission and scanning electron microscopy, microCT, and ex-vivo experiments in order to advance the comprehension of the morphology and functioning of the hummingbird feeding apparatus. I found that hummingbird tongues are composed mainly of thin cornified epithelium, lack papillae, and completely fill the internal cast of the rostral oropharyngeal cavity. Understanding this puzzle-piece match between bill and tongue will be essential for the study of intraoral transport of nectar. Likewise, I found that the structural composition and tissue architecture of the tongue groove walls provide the rostral portion of the tongue with elastic properties that are central to the study of tongue-nectar interactions during the feeding process. Detailed studies on hummingbirds set the basis for comparisons with other nectar-feeding birds and contribute to comprehend the natural solutions to collecting liquids in the most efficient way possible.
Author Comment
This is a submission to PeerJ for review.
Supplemental Information
Video S1. MicroCT rendering (rostro-cranial coronal cross sectioning) of the bill and tongue of an Anna’s Hummingbird, overlaying TEM micrographs
This virtual model of the internal three-dimensional architecture help us to understand the fit between bill and tongue. Additionally, merging microCT, light, and electron microscopy allows us to understand the key morphological features for the tongue functioning linking them across spatial scales. Known objects are placed at the same scale at the different zoom levels in order to contextualize the structures shown.
Video S2. Control of the setup to film post-mortem tongue fluid interactions
Under a dissecting microscope (cf. Fig S2), this control system emulates reciprocating tongue movements and allows for fine control of the distance to the nectar surface using micromanipulators. I coupled a high-speed camera to capture the details of tongue fluid interactions (e.g. Video S3).
Video S3. High-speed recording of post-mortem tongue expansive filling
A slow motion (165 times slower than real time) video of the lateral view of a dissected Ruby-throated Hummingbird focusing on the bill tip – tongue – nectar interaction. The tongue protraction is controlled by micromanipulators (Video S2). Footage obtained under a dissecting microscope (cf. Fig S2) with a flat surface mirror to achieve the side view.
Video S4. Recording of post-mortem tongue fluid trapping
A real-time video of the dorsal view of a deceased Ruby-throated Hummingbird focusing on the bill tip – tongue – nectar interaction. Footage obtained under a dissecting microscope immersing the tongue in a nectar reservoir to appreciate the instantaneous change in shape when the tongue transitions form air (out of focus) to nectar (in focus) and vice versa.
Video S5. Three-dimensional digital rendering of a microCT scan of the skull of a Ruby-throated Hummingbird
This spinning reconstruction makes it possible to follow and visualize the elongated epibranchials surrounding the skull. In this case, the tongue is retracted inside the bill.