The existence of tonsils in the oropharynx of ratite species was first reported by Cho et al. who noted that “The ostrich tonsils and tongue are smooth, blunt and U-shaped. In the Darwin's rhea both tongue and tonsils have simple, pointed V-shaped tips. The tonsils in the emu are similar to the rhea but have a small flap laterally”. However, the term ‘tonsil’ appears to have been used inappropriately and it seems more probable from the foregoing description, that what is referred to as ‘tonsils’ are in fact the pharyngeal folds. The relatively large amount of lymphoid tissue present in the pharyngeal folds of D. novaehollandiae and S. camelus has also prompted more recent reference to these structures as tonsils. The question therefore arises as to whether the pharyngeal folds in D. novaehollandiae and S. camelus represent true pharyngeal tonsils? Tadjalli et al. briefly mention the presence of pharyngeal tonsils in S. camelus, describing them as “…two pockets like diverticuli that are bordered by a prominent circular pharyngeal fold. Each pocket has an oval structure, called pharyngeal tonsil” [sic]. Although the opening to the tonsil and its oval shape were depicted and the structures correctly identified as tonsils, no macro- or microscopic evidence was provided to support this conclusion. A pharyngeal tonsil has recently been reported in D. novaehollandiae but the distinction between this structure and the pharyngeal folds is still unclear.
The present study provides definitive morphological evidence that the pharyngeal folds per se do not represent tonsils (as defined in mammals), but rather lymphoid tissue-rich regions which are closely associated with true pharyngeal tonsils. Much of the confusion surrounding the naming of “tonsils” in birds stems from the fact that the GALT, in the form of aggregated lymph nodules, observed in the oropharynx of a number of bird species[4–7, 9], has traditionally been interpreted as constituting pharyngeal tonsils.
GALT occurs in two forms, namely, (1) as solitary and aggregated lymph nodules and inter-nodular lymphoid tissue assembled below the surface epithelium, and (2) as tonsils. Two types of tonsils are recognised, those with follicles, and those without[1, 3]. A follicular tonsil comprises one or more tonsillar follicles of which each follicle is “composed of a crypt, its orifice (fossula), and its surrounding lymphatic tissue, which contains Lymphonoduli”. Non-follicular tonsils bulge into the oropharynx and have a slightly folded epithelium, are devoid of crypts but contain lymph nodules and inter-nodular lymphoid tissue, an example being the tonsil of the soft palate and tubal tonsil of the ruminant. According to Nomina Anatomica Veterinaria (NAV) the term “tonsil” (Tonsilla) is applied to GALT present in the pharynx. Immunologically active lymphoid tissue in other parts of the digestive tract not associated with crypts or fossula is referred to as Lymphonoduli solitarii (solitary lymph nodules) and Lymphonoduli aggregati (aggregated lymph nodules) in the small and large intestine and as Lymphonoduli gastrici, which are associated with the glands in the stomach. Similarly, the aggregated lymph nodules of GALT found in specific anatomical locations in birds have been grouped under the term Lymphonoduli aggregati apparatus digestorii according to Nomina Anatomica Avium. These include the Lymphonoduli pharyngeales, Lymphonoduli esophageales, Lymphonoduli cecales and Lymphonoduli rectales. However, the term Lymphonoduli is deemed, in avians at least, to be synonymous with tonsils and these tonsils are defined as “Lymphonoduli aggregati of relatively constant occurrence and relatively large size”. The definition of an avian tonsil thus clearly differs from that of a mammalian tonsil. Further complicating this anomalous situation is the occurrence in Gallus domesticus of tonsils conforming to the classical description of the mammalian tonsil (except that they are not located in the pharynx). These include esophageal[10, 23], cecal and pyloric tonsils. Thus in the avian literature the distinction between Lymphonoduli (solitarii and aggregati) and Tonsilla has become blurred, leading to the term tonsil being used synonymously for both forms of GALT in birds. The fact that a typical “mammalian” tonsil has not previously been described in the avian oropharynx has also contributed to the inappropriate use of nomenclature.
The identification of a follicular pharyngeal tonsil (Tonsilla pharyngea) (as defined by NAV) as a component of GALT in the oropharynx of D. novaehollandiae and S. camelus warrants stricter and more consistent use of the terms “aggregated lymph nodules (Lymphonoduli aggregati)” and “tonsils (Tonsilla)” in birds. Thus to avoid confusion these terms should no longer be considered synonymous and the GALT present in the pharyngeal region (including the pharyngeal folds) of birds not forming typical tonsils (follicular or non-follicular), should be named pharyngeal lymph nodules (Lymphonoduli pharyngeales). However, it should be noted that the large aggregations of lymph nodules and inter-nodular lymphoid tissue situated directly below the pharyngeal epithelium on the dorsal surface of the pharyngeal folds in D. novaehollandiae and S. camelus, also represents a small pharyngeal tonsil. The lack of tonsillar crypts in this concentration of lymphoid tissue defines this tonsil as a non-follicular pharyngeal tonsil. True tonsils which display similar morphological features to those described in D. novaehollandiae and S. camelus have been described in Gallus domesticus. However, these tonsils are not located in the pharyngeal region and are positioned in other parts of the digestive tract such as the cecum, esophagus and pylorus.
The pharyngeal folds of both D. novaehollandiae and S. camelus share similar features. In contrast, the pharyngeal folds of Rhea americana are much reduced and display no free portion. However, on the caudo-lateral edge of each pharyngeal fold in this species is an oval opening which leads to a small pocket in the fold (personal observation). This opening and pocket in R. americana is similar in its location to the pharyngeal tonsil and its opening in S. camelus and is also situated retropharyngeally (personal observation). It is therefore highly suggestive that if D. novaehollandiae and S. camelus display pharyngeal tonsils in a similar location to each other, and that if R. americana possesses a similar structure in a similar region of the pharyngeal fold to that in S. camelus, that it too possesses a pharyngeal tonsil. The three ratite species mentioned above each belong to a different order (Casuariiformes, Struthioniformes and Rheiformes) and it would appear that pharyngeal tonsils are unique to D. novaehollandiae, S. camelus and possibly also to R. americana. It would be of great interest to investigate whether the remaining orders (Apterygiformes and Tinamiformes), as well as Casuarius spp. from the same order as D. novaehollandiae, also display pharyngeal tonsils, which could make these structures a characteristic feature of the Superorder Paleognathae.
The pharyngeal folds in D. novaehollandiae and S. camelus fulfil mechanical functions (respiratory and digestive) and an immunological function. The respiratory function has been addressed in D. novaehollandiae. The digestive function of the folds is reflected by the presence of many large, simple, branched tubular mucus-secreting glands (Gl. tonsilla pharyngea) in D. novaehollandiae which provide lubrication for food boli and also protect the non-keratinised epithelium. The immunological function is expressed by the significant concentration of GALT in the form of aggregated lymph nodules (Lymphonoduli pharyngeales and the non-follicular tonsil) in the pharyngeal folds, and by the massive accumulation of GALT in the closely associated follicular tonsil. Thus, the pharyngeal folds in D. novaehollandiae and S. camelus represent the first strategic, anatomical location of GALT in these species. The placement of the pharyngeal tonsils at this specific location appears to be related to the catch and throw or cranio-inertial feeding method employed by ratite species[26, 27] which results in the food items travelling from the bill-tip to land in the proximal esophagus prior to being swallowed. Thus, the first point of contact of the food (carrying potentially harmful antigens) with a mucosal surface is that of the pharyngeal folds and the associated follicular pharyngeal tonsils.
In mammals, tonsils do not contain salivary glands but are, however, surrounded by salivary glands. The secretion from these glands washes out accumulated leukocytes along with other microorganisms from the tonsillar crypts and fossules to prevent infection. In contrast to mammals, the pharyngeal tonsils of D. novaehollandiae and S. camelus contain varying amounts of salivary glands in the form of simple, tubular mucus-secreting glands. The mucus glands in the tonsils of D. novaehollandiae and S. camelus may similarly function to prevent the accumulation of leukocytes and microorganisms in the tonsillar crypts, thus preventing infection. In mammals this is achieved by secretions from the surrounding salivary glands washing out debris and by the action of swallowing which compresses the crypts. In birds, which lack an upper esophageal sphincter, the compression force of swallowing is largely absent and the primary method of cleaning the tonsillar crypts would depend on the pressure exerted from the build-up of secreted mucus.
The follicular pharyngeal tonsils of D. novaehollandiae and S. camelus contain numerous tonsillar crypts and these invaginations reportedly result in a higher concentration of lymphoid tissue in a particular location[21, 28]. This fact points to the importance and immunological significance of the pharyngeal tonsils in D. novaehollandiae and S. camelus, as in common with other avian species, both D. novaehollandiae and S. camelus display significant accumulations of lymphoid tissue (GALT) in the oropharynx, but not necessarily forming pharyngeal tonsils. Thus, in addition to the normal component of GALT (Lymphonoduli pharyngeales) found in the avian oropharynx, D. novaehollandiae and S. camelus possess follicular tonsils, thus massively increasing the volume of lymphoid tissue present in the oropharynx. Therefore, the oropharynx of D. novaehollandiae and S. camelus is immunologically highly protected, in contrast to the situation in other described avian species.