Pre-hatch lung development in the ostrich
Highlights
► Epithelial attenuation during ostrich lung development follows processes of cell cutting similar to those described in the chicken. ► Between embryonic days E24 and E39, the epithelial thickness is reduced by 90% from about 13 μm to less than 3 μm. ► Atria formation is evident from E32 while first portions of thin blood–gas barrier (BGB) form by E35. ► Blood vessel augmentation and remodeling proceeded through intussusceptive angiogenesis. ► A remarkably thin BGB was formed by E39, in readiness for hatching at E40.
Introduction
The ostrich (Struthio camelus) is the largest of all extant birds and belongs to the order Struthioniformes (generally referred to as ratites) that also includes the emu, cassowary, rhea and kiwi (Sibley and Ahlquist, 1990). The ratites are considered to be among the most primitive extant avian species (Storer, 1971a, Storer, 1971b) and their lungs have a poorly developed neopulmonic region, unlike the more phylogenetically advanced species (Duncker, 1971). Ostriches are becoming increasingly important species as domestic animals providing high quality protein as well as non-consumable items (Cooper et al., 2008). In addition, recent reports on the reservoir of Avian Influenza Virus in some farmed South African ostriches have elevated the need to understand ostrich biology (Abolnik et al., 2009, Thompson et al., 2008). The little information published on the morphology of the ostrich lung indicates that the structure conforms to that of the other avian species but is designed like that of highly aerobic volant birds (Maina and Nathaniel, 2001, Maina and Woodward, 2009).
Studies in the recent past (Makanya and Djonov, 2009, Makanya et al., 2006, Makanya et al., 2011b) have documented diverse and unique developmental mechanisms in the chicken lung that have hitherto not been described in mammals. The formation of the blood–gas barrier (BGB) in mammals entails conversion of the primordial cuboidal epithelium of the airways into surfactant producing type II cells (Schittny and Burri, 2003) most of which later convert to the thinner type I cells (Mercurio and Rhodin, 1976, Mercurio and Rhodin, 1978, Schittny and Burri, 2003). Establishment of the thin BGB subsequently entails thinning of the epithelium by elongation and extrusion of lamellar bodies and subsequent apposition of blood capillaries to the thin epithelium (Makanya et al., 2001, Makanya et al., 2007).
In the less studied avian lung, the epithelium of the primitive air conduits starts off as low cuboidal, becomes tall columnar and later stratified columnar before it is attenuated by the complex processes of secarecytosis and peremerecytosis. These processes involve cutting and constriction of the apical parts of the cells and their driving forces are currently unknown (Makanya and Djonov, 2009, Makanya et al., 2011a, Makanya et al., 2011b, Makanya et al., 2006). By studying the developmental process in the ostrich lung, the current study aims to establish whether similar mechanisms are preserved in this phylogenetically primitive species, noting also that the ratite lung differs from that of other birds in its lack of interparabronchial septa, poorly developed neopulmo and presence of granular cells at the level of the air capillaries (Maina and King, 1989, Maina and Nathaniel, 2001). Our findings indicate that though the processes are fundamentally similar a slightly different structure is formed.
Section snippets
Experimental animals
Fertilized ostrich eggs of the Struthio camelus massaicus species were incubated at 36.5 °C and a humidity of 25%. Embryonated eggs were obtained at incubation days E24, E32, E35 and E39 (incubation period till hatching is 40 days). Embryos were freed from the shells by first cutting off the blunt end of the egg with a hacksaw and then injecting the embryo with sodium pentobarbitone. The lungs were processed according to the techniques outlined below. All experimental protocols were approved by
Results
A recapitulation of the events occurring in the ostrich lung at E24 is provided in Fig. 1. The lung was made up of migrating epithelial tubes interspersed with plentiful mesenchyme with profiles of incipient vasculature. Many migrating epithelial cords of the incipient parabronchi were evident and the epithelium was cuboidal, tall columnar or pseudostratified columnar showing that the tubes were at different stages of development. At this stage also, the cells showed morphological polarization
Discussion
Study of lung development in the ostrich is interesting because it is the largest living bird, it is a ratite, meaning that it belongs to a phylogenetically primitive taxon and it is flightless. Morphometric and qualitative studies have shown that the ostrich lung closely resembles that of small highly energetic volant birds (Maina and Nathaniel, 2001). Structurally, the ostrich lung differs from that of other birds in that it has no interparabronchial septa and the neopulmo is poorly developed
Acknowledgments
We thank Maasai Ostrich Farm for providing the ostrich embryos on which this study is based. In particular we are grateful to Miss Rose Menjo and Dr. J.M. Kithuka for assisting in egg incubation for the targeted time points. In addition we would like to thank Brigitte Scolari, Clemens Weber, Regula Buergy, Jackson Gachoka, Peter Kiguru and John Kiai for their excellent technical assistance and Dr. Aikaterini Anagnostopoulou for carefully scrutinizing the final manuscript. This work was
References (42)
- et al.
Lung volume changes during respiration in ducks
Respir. Physiol.
(1985) A systematic study of the development of the airway (bronchial) system of the avian lung from days 3 to 26 of embryogenesis: a transmission electron microscopic study on the domestic fowl, Gallus gallus variant domesticus
Tissue Cell
(2003)Morphogenesis of the laminated, tripartite cytoarchitectural design of the blood–gas barrier of the avian lung: a systematic electron microscopic study on the domestic fowl, Gallus gallus variant domesticus
Tissue Cell
(2004)- et al.
The pulmonary blood–gas barrier in the avian embryo: inauguration, development and refinement
Respir. Physiol. Neurobiol.
(2011) - et al.
Risk factors for seropositivity to H5 avian influenza virus in ostrich farms in the Western Cape Province, South Africa
Prev. Vet. Med.
(2008) - et al.
Structure-function studies of blood and air capillaries in chicken lung using 3D electron microscopy
Respir. Physiol. Neurobiol.
(2010) - et al.
The honeycomb-like structure of the bird lung allows a uniquely thin blood–gas barrier
Respir. Physiol. Neurobiol.
(2006) - et al.
Characterisation of a highly pathogenic influenza A virus of subtype H5N2 isolated from ostriches in South Africa in 2004
Influenza Other Respir. Viruses
(2009) - et al.
A novel mechanism of capillary growth in the rat pulmonary microcirculation
Anat. Rec.
(1990) - et al.
Scanning electron microscope study of the developing microvasculature in the postnatal rat lung
Anat. Rec.
(1986)