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      What prevents Struthio camelus and Dromaius novaehollandiae (Palaeognathae) from choking? A novel anatomical mechanism in ratites, the linguo-laryngeal apparatus

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          Abstract

          Background

          The avian glottis channels air from the oropharynx to the trachea and is situated on an elevated structure, the laryngeal mound. It is imperative that the glottis be protected and closed during swallowing, which in mammals is achieved by covering the glottis with the epiglottis, as well as by adduction of the arytenoid cartilages. An epiglottis, however, is reportedly absent in birds. Ratites such as Struthio camelus and Dromaius novaehollandiae possess a very wide glottis in comparison to other birds. The question therefore arises as to how these large birds avoid inhalation of ingesta through a wide glottis, with apparently little protection, particularly as their feeding method involves throwing the food over the glottis to land in the proximal esophagus.

          Results

          In S. camelus when the glottis was closed and the tongue body retracted, the smooth tongue root became highly folded and the rostral portion of the laryngeal mound was encased by the pocket in the base of the ∩ − shaped tongue body. In this position the lingual papillae also hooked over the most rostral laryngeal projections. However, in D. novaehollandiae, retraction of the tongue body over the closed glottis resulted in the prominent, triangular tongue root sliding over the rostral portion of the laryngeal mound. In both S. camelus and D. novaehollandiae these actions resulted in the rostral portion of the laryngeal mound and weakest point of the adducted glottis being enclosed and stabilised.

          Conclusions

          Only after conducting a comparative study between these two birds using fresh specimens did it become clear how specific morphological peculiarities were perfectly specialised to assist in the closure and protection of the wide glottis. We identify, describe and propose a unique anatomical mechanism in ratites, which may functionally replace an epiglottis; the linguo-laryngeal apparatus.

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          Most cited references8

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          The kinematics of feeding and drinking in palaeognathous birds in relation to cranial morphology.

          Cranial kinesis is an important feature in avian feeding behaviour and involves the transmission of quadrate movement to the upper bill by the Pterygoid-Palatinum Complex (PPC). The PPC in Palaeognathae is remarkably different from that found in Neognathae. In this study we analyse whether the special morphology of the PPC is an adaptation to the feeding behaviour of the Palaeognathae. Behavioural analyses of the rhea Rhea americana showed that the feeding behaviour of the rhea is typical ;Catch and Throw' behaviour, independent of the size of the food item. Drinking is achieved by a scooping movement followed by a low-amplitude tip-up phase. During feeding rhynchokinetic movements of the upper bill were observed. However, cranial kinesis was limited and may differ from rhynchokinesis in neognathes as a clear bending zone seemed absent. Since the movement patterns are considered very similar to the basic feeding behaviour in neognathous birds it is concluded that the specific morphology of the PPC is not the result of specific functional demands from palaeognathous feeding behaviour.
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            A modified differential stain for cartilage and bone in whole mount preparations of mammalian fetuses and small vertebrates.

            Fixation in formol-acetic-alcohol as a prelude to the staining of whole mount vertebrate skeletons with alcian blue and alizarin red S has greatly facilitated the enzyme clearing step of the method outlined by Dingerkus and Uhler. The modified method has been tested on fetal and neonatal mice, and on a variety of vertebrates including bony fish, reptiles, amphibia and birds, and shown to be rapid, reproducible and permanent. The method is not so rapid as that reported by Kimmel and Trammell but is superior at least in certain circumstances. In the present study, optimal results were obtained by fixing in formol-acetic-alcohol for 40 minutes, staining cartilage with alcian blue 8GX, then clearing with trypsin. The time taken to complete the latter step was reduced significantly by incubation at 37 C. The next step was to stain bone using alizarin red S in a weak solution of potassium hydroxide, followed by clearing in a potassium hydroxide-glycerol series.
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              Light and scanning electron microscopic study of the structure of the ostrich (Strutio camelus) tongue.

              The ostrich's tongue is situated in the posterior part of the oropharyngeal cavity and its length is only about a quarter of the beak cavity. The triangular shortened tongue has retained the usual division into the apex, the body and the root. There are no conical papillae between the body and the root of the tongue, and the presence of the flat fold with lateral processes sliding over the tongue root in the posterior part of the lingual body is a unique morphological feature. All lingual mucosa covers non-keratinised stratified epithelium, and the lamina propria of the mucosa is filled with mucous glands whose round or semilunar openings are found on both the dorsal and ventral surface of the tongue. The complex glands found in the lingual body are composed of alveoli and/or tubules. Moreover, simple tubular glands seen in the posterior part of the tongue root are an exception. Numerous observations have shown that the ostrich's tongue is a modified structure, though not a rudimentary one, whose main function is to produce the secretion moisturising the beak cavity surface and the ingested semidry plant food in this savannah species.
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                Author and article information

                Journal
                Front Zool
                Front. Zool
                Frontiers in Zoology
                BioMed Central
                1742-9994
                2012
                31 May 2012
                : 9
                : 11
                Affiliations
                [1 ]Department of Anatomy and Physiology, Faculty of Veterinary Science, University of Pretoria, Private Bag X04, Onderstepoort, 0110, South Africa
                Article
                1742-9994-9-11
                10.1186/1742-9994-9-11
                3404984
                22650266
                519439e3-197f-4ce0-889d-48c1d7cd1ab1
                Copyright ©2012 Crole and Soley; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the CreativeCommons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 29 February 2012
                : 31 May 2012
                Categories
                Research

                Animal science & Zoology
                swallowing,glottis,struthio camelus,protection,linguo-laryngeal apparatus,dromaius novaehollandiae

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