Anatomical and Functional Study of the Ostrich

Simple Summary

Ostrich is increasingly becoming an important livestock due to its high-quality products, especially its healthy meat. We studied the morphology of the ostrich lung using various imaging techniques in order to understand how it functions. The major conducting intrapulmonary airways, the secondary bronchi, were superficially placed in close proximity to the intercostal muscles and had thin collapsible external walls, implying their plausible role in gas propulsion. Many attributes of the bronchi, including categories, numbers, and topographical arrangement, were comparable to those of the Chicken. The paleopulmonic region of the lung was better developed than the neopulmonic one, which appeared rudimentary. Adjacent parabronchi were not delineated by connective tissue septa as is the case in the archetypical avian lung, and the exchange tissue was only interrupted where conducting blood vessels occurred. The parabronchi were lined with shallow atria, and, in many cases, infundibulate were absent. Air capillaries formed the terminal gas exchange units in most cases, but occasionally atria were the terminal units. Air capillaries were associated with secretory cells, and blood capillaries were supported by epithelial plates

Abstract

The Ostrich occupies a unique position as the largest bird on the planet. Like other ratites, it has been reputed to have a phylogenetically primitive lung. We used macroscopy, light microscopy, transmission and scanning electron microscopy as well as silicon rubber casting to elucidate the functional design of its lung and compare it with what is already documented for the avian species. The neopulmonic region was very small and poorly developed. The categories of the secondary bronchi (SB) present and their respective numbers included laterodorsal (8–10), lateroventral (4–5), medioventral (4–6) and posterior (16–24). The lateral aspects of the laterodorsals were covered with a transparent collapsible membrane internally lined with a squamous to cuboidal epithelium. The bulk of these SB were in close proximity to intercostal spaces and the intercostal muscles and were thought to be important in the propulsion of gases. The lung parenchyma was rigid, with the atria well supported by septa containing smooth muscles, connective tissue interparabronchial septa were absent, and blood capillaries were supported by epithelial bridges. There were two categories of epithelia bridges: the homogenous squamous type comprising two leaflets of type I cells and the heterogeneous type consisting of a type I pneumocyte and type II cell. Additional type two cells were found at the atrial openings as well as the walls of the infundibulae and the air capillaries. The atria were shallow and opened either directly into several air capillaries or into a few infundibulae. The presence of numerous type II cells and the absence of interparabronchial connective tissue septa may imply that the ostrich lung could be capable of some degree of compliance.

Introduction

The Ostrich (Struthio camelus) is the largest of all extant birds and belongs to the Ratite group that also includes the Emu (Dromaius novaehollandiae), Cassowary (Casuarius casuarius), Rhea (Rhea americana) and Kiwi (Apteryx australis). It is an important animal in many livestock industries because of its healthy red meat and skin [1]. The successful growth and reproductive performance of the ostrich are dependent on good nutrition and the ability of the bird to utilize semi-arid conditions in its natural habitat. The ratites are considered to be among the most primitive extant avian species [2], and they lack the distinct neopulmonic region that characterizes more phylogenetically advanced species. Ostriches are becoming increasingly important species as domestic animals, providing high-quality protein as well as non-consumable items. Furthermore, the ostrich’s embryonated egg is gaining traction as an important model for varied research [3,4], especially cancer pathogenesis [5]. There is little information published on the morphology of the ostrich lung. The only detailed investigation was based on one individual animal, and as such does not provide adequate details regarding the numbers and topography of the secondary bronchi [6]. Nonetheless, the structure of the ostrich lung was seen to generally conform to that of the other avian species. The air sacs in the ostrich are capacious and well developed, and the numbers are comparable to those of other avian species [7].

Some investigations have highlighted some salient gaps in the literature relating to the avian lung [8,9]. It would, for example, be interesting to find out whether the newly described category of secondary bronchi is characteristic of one of the most primitive avian species and whether the spatial disposition of the secondary bronchi has similarities among species [8,9,10]. As reported elsewhere, the mediodorsal secondary bronchi (MDSB) in the ostrich are superficially located, making them easily accessible for sampling respiratory gases and experimental investigations of processes such as airflow dynamics [3]. The disposition of the secondary bronchi in the duck lung [11] appears to conform to that of the Chicken (Gallus gallus variant domesticus) but the situation in the Ostrich has not been clarified.

An investigation of the ostrich lung parenchyma using 3D reconstruction of histological sections revealed that atria were shallow, infundibulae were few, and the majority of the air capillaries emanated directly from the atria [12]. Lack of connective tissue-based interparabronchial septa, structural features that epitomize the lungs of most highly derived metabolically active volant birds, was observed in the latter study. The complexity of the avian lung has been highlighted before [13,14,15], with the notion that its structural organization continues to draw controversy. In 3D reconstructions of the parabronchial unit, it was revealed that the terminal gas exchange units in the avian lung are not straight tubular structures but rather rotund structures that interconnect with their cognates [14]. The problem in the latter studies has been confounded by the limitations of the method since only a limited number of sections could be computed. Additionally, a 3D reconstruction based on larger amounts of sections [16] does not adequately discriminate the secondary bronchi since some categories have dimensions similar to those of parabronchi [9,10]. Failure by contemporary investigators to recognize the fifth category of secondary bronchi, namely the posterior secondary bronchi, or even failure to recognize the new nomenclature of the secondary bronchi [17] has further fueled the confusion, with some very recent publications using the old names, such as ventrobronchi [18].

It was reported earlier that incorporating several visualization techniques, coupled with study in both adult and developing subjects, greatly improves the understanding of the structure of the avian lung [19]. The current study aims to elucidate both the three-dimensional organization of the air conduits in the ostrich lung with an insight into the functional organization of the gas exchange unit

Discussion
Despite many contemporary investigations, the structure of the avian lung continues to draw controversies, with conflicting reports appearing in the literature from time to time [13,15]. In the current study, it was observed that the ostrich lung conforms to the general rhomboid shape described for the Chicken [10] although it was much larger. The topographical positioning of the laterodorsal secondary bronchi was similar to that of the Domestic Duck (Cairinia mochata) with thin collapsible membranes [11]. Using ultrasound scanning, such secondary bronchi were shown to participate in the propulsion of gases toward the lung parenchyma [19]. The categories, numbers, and spatial disposition of the secondary bronchi are important because they may have significant implications in the implementation of unidirectional airflow [10]. A single morphometric study performed by Maina and Nathaniel [6] noted that the atria are shallow and the lung lacks interparabronchial septa. The significance of such modifications was unclear, but the pulmonary morphometric refinements closely resembled those of highly energetic volant birds [6]. It was previously reported that the neopulmo is very poorly developed, consisting of a few laterodorsal secondary bronchi that arise from the most caudal part of the primary bronchus [6], and their parabronchi are lateral. One new category of secondary bronchi, the posterior secondary bronchi (POSB), which has been missed out previously, was described in chicken [10] and duck [11] lungs. As elucidated elsewhere, the latter category had often been confused with either the laterodorsals or the lateroventrals, but their structure and disposition have now been well explicated [9].

In the ostrich, the categories and the disposition were found to be similar to those of the Chicken and duck, although the numbers were slightly different, with the ostrich having fewer posterior secondary bronchi. These latter categories of secondary bronchi (POSB) have previously been missed by contemporary investigators firstly because they resemble parabronchi (so-called tertiary bronchi) both in structure and size, with the exception that they emerge directly from the mesobronchus and their initial parts have no openings to the atria [10]

The arrangement of the LDSB in the ostrich in close adherence to the intercostal muscles and their collapsible nature are strong pointers to their possible participation in gas propulsion, a phenomenon demonstrated previously in the Domestic Duck [19]. The other categories of the secondary bronchi do not differ much in numbers but are more in the current study than those documented earlier where MVSB were said to be 3, mediodorsal (currently named laterodorsal) were 5, one LVSB but no POSB were recognized [3]. The techniques used to elucidate the types, topography, and categories in the latter study were not elucidated, and the entire study was based on only one juvenile animal [6]. These findings authenticate earlier observations that the structure of the avian lung remains a subject of debate and a lot is yet to be clarified