Comparative morphology and functional significance of mechanical and sensory structures in the upper digestive tract of the ostrich (Struthio camelus) and emu (Dromaius novaehollandiae)

Abstract

This study describes, on a comparative basis, the morphology of mechanical (the linguo-laryngeal apparatus) and sensory (Herbst corpuscles and taste buds) specialisations in the upper digestive tract (bill and oropharynx) of the ostrich and emu, with a view to a better understanding of the functional significance of these structures. The ostrich and emu are commercial entities that constitute important niche industries and are farmed intensively throughout South Africa. A lack of information on the mechanical and sensory specialisations of the upper digestive tract in these two birds hampers a sound understanding of food selection and intake. A total of 48 adult (12-14 months) ostrich heads and 48 adult emu (12-14 months) heads obtained from birds at slaughter at commercial abattoirs and farms, as well as 5 ostrich chick (2-4 weeks) heads and 1 emu chick (8 weeks) head, obtained from previous research projects, were used for this study. Morphological features were described using basic gross anatomical (dissection and stereomicroscopy) and histological techniques (H&E staining), supplemented by differential staining for cartilage and bone, transmission electron microscopy and immunohistochemistry. The findings of the study were compared with the relevant literature and hypotheses for functional significance were formed. 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 the ostrich and emu possess a very wide glottis in comparison to other birds. The question therefore arises as to how these large birds avoid inhalation of food particles 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. In the ostrich, 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 the emu, 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 the ostrich and emu these actions resulted in the rostral portion of the laryngeal mound and weakest point of the adducted glottis being enclosed and stabilised. 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. A unique anatomical mechanism in ratites was identified, described and proposed, which may functionally replace an epiglottis; the linguo-laryngeal apparatus. The oropharynx of the ostrich and emu is richly supplied with Herbst corpuscles. This widespread distribution of these mechanoreceptors has not previously been reported in birds. Specific concentrations of Herbst corpuscles within the oropharynx, which differ between the ostrich and emu, assist in the accurate positioning of the tongue and laryngeal mound for cleaning the choana (internal nares). The Herbst corpuscles are strategically located to aid in the handling and transport of food and the median palatine and ventral ridges in the ostrich display a concentration of Herbst corpuscles which denote these structures as sensory organs, namely the palatal and interramal organs. Three specific arrangements of Herbst corpuscles were noted in the oropharynx. The first arrangement consisted of groups of corpuscles located peripherally around a myelinated nerve and was present in the bill tip. The second arrangement, possibly linked to the first, was that of individual or groups of corpuscles without an obvious associated nerve and was present throughout the remaining regions of the oropharynx. The third arrangement was that of corpuscles associated with large, simple branched tubular mucus-secreting glands. The basic structure of Herbst corpuscles in the ostrich and emu, observed by light and transmission electron microscopy, of a capsule (with cellular and acellular lamella), an outer zone (collagen fibrils, fibroblasts and a fluid matrix), an inner core (formed by bilaterally symmetrical specialised Schwann cells) and a receptor axon, is similar to that noted for other avian species. However, unlike in other birds, the capsule of the Herbst corpuscle in the ostrich and emu is formed by myofibroblasts which indicates contractile properties for this component of the corpuscle in ratites. Sensory cilia were noted in the myofibroblasts of the capsule and fibroblasts of the outer zone of the ostrich Herbst corpuscle which may assist in regulating the tension of the capsule. These features have not been reported in other avian species. Although the structure of the palaeognathous palate has been widely studied, relatively little information is available on the morphology of the ratite bill. The kiwi possesses a bill tip organ and the present study confirmed the existence of this somatosensory organ in the ostrich and emu. Examination of the rhamphotheca of these two birds demonstrated numerous specialisations. In the emu, rhamphothecal serrations with intervening keratinised pegs on the rostral mandibular tomia resembled a form of pseudo-teeth. These structures may share a similar embryological origin to teeth; however, they would appear to function by channelling and enhancing vibratory stimuli to Herbst corpuscles in nearby bony pits. In the ostrich, epidermal troughs were present in the regions overlying the bill tip organ and functioned to enhance vibratory stimuli to the underlying Herbst corpuscles. Additionally, in the ostrich only, and not related to the structure or functioning of the bill tip organ, the rostral tomia and maxillary and mandibular nails were composed of typical tubular and inter-tubular horn. This may represent a unique feature in birds. The structure of the mandible and premaxilla was similar to that described previously for these birds. However, the persistence of Meckel’s cartilage through to the adult bird in the ostrich and emu is a novel avian feature not previously reported. The bony bill tips were adorned with numerous sensory (bony) pits which displayed similar distribution patterns in the ostrich and emu and indicated the presence, macroscopically, of a bill tip organ. The total number of pits in the bill tip of the ostrich and emu did not differ significantly, although regional differences did occur. The sub-divisions of the trigeminal nerve (N. opthalmicus R. medialis and N. intramandibularis) innervating the bill tip were well developed in both birds and displayed extensive branching. The emu displayed more myelinated nerve fibres in both nerves than in the ostrich. As myelinated nerve fibres supply Herbst corpuscles, the number of nerve fibres is correlated to the number of corpuscles. No correlation could be made between the number of pits in a particular region and the number of nerve fibres or with the relative percentage of Herbst corpuscles in that region. The bill tip organ in both species was basically similar except for the epidermal specialisations noted above. Two parts of the bill tip organ were recognised; the bony bill tip organ (Herbst corpuscles stacked in bony cavities and pits) and the peripheral bill tip organ (Herbst corpuscles in sheets or chains in the connective tissue between the epithelium and bone). The morphology of the bill tip organ in the ostrich and emu indicates that it is an organ that functions by direct touch. These two ratite species appear to possess the most elaborate bill tip organ of any pecking bird. The existence of a bill tip organ in the ostrich and emu is an enigma and points to the possibility that a bill tip organ is a basal structure in all palaeognathous birds (living and extinct). Furthermore, it is evident by observing the exploratory behaviour of the ostrich and emu, that they use their bill tip organ extensively as a tool for exploring and interpreting their environment as well as for discriminating food. The sense of taste in birds is an important motivator for feeding as well as initial food selection. The existence of this sense in ratites has remained largely speculative. In the present study taste buds were only identified in the emu and were predominantly located in the caudal region of the non-pigmented oropharyngeal roof and sparsely located on the oropharyngeal floor. The taste buds extended the full width of the epithelium in which they were located and were ovoid structures. The taste bud was composed of centrally located, vertically oriented light and dark cells (representing both receptor cells and supporting elements) and peripherally situated follicular cells which were continuous with the surrounding Str. germinativum of the stratified squamous epithelium. Positive IHC labelling for neurofilament demonstrated numerous fine nerve fibres (Neurofibra gustatoria) within the connective tissue immediately surrounding the taste bud. Taste bud morphology in the emu was similar to that described in other birds. However, when sectioned tangentially they were indistinguishable from the surrounding epithelium with H&E staining. By using IHC labelling, concentrations of nerve fibres could be demonstrated beneath apparently nondescript epidermal structures, thus indicating the presence of a taste bud. The distribution of taste buds in the oropharynx could be linked to the particular feeding method of the emu. Based on information from GenBank, it would appear that the relatively few taste buds present in the emu oropharynx would mainly function in distinguishing bitter taste. As bitter-tasting compounds can cause a negative association with a particular food type, it would appear that the sense of taste in the emu would predominantly function for protection and not food selection. This study revealed various unique findings regarding the mechanical and sensory specialisations in the upper digestive tract of the ostrich and emu.  The ostrich and emu possess a combination of structures which functionally replace an epiglottis, namely the linguo-laryngeal apparatus.  Herbst corpuscles are widely distributed in the oropharynx of the ostrich and emu and their distribution is related to the particular feeding habits of these birds.  The capsule of Herbst corpuscles in the ostrich and emu is composed of contractile elements, a feature not reported in other birds.  The ostrich and emu possess a well-developed bill tip organ, which is an unusual feature amongst pecking birds.  Taste buds are present in the emu and no structures resembling taste buds were identified in the ostrich.