Research Article |
Corresponding author: Gerald Mayr ( gerald.mayr@senckenberg.de ) Academic editor: Martin Päckert
© 2021 Gerald Mayr.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Mayr G (2021) On the occurrence of lateral openings and fossae (pleurocoels) in the thoracic vertebrae of neornithine birds and their functional significance. Vertebrate Zoology 71: 453-463. https://doi.org/10.3897/vz.71.e71268
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Abstract
The occurrence of lateral openings and pleurocoels (lateral fossae) in the corpus of the thoracic vertebrae of extant and fossil neornithine birds is reviewed, with both features having been identified as osteological correlates of the avian pulmonary system. Openings mainly occur in larger species with a high overall bone pneumatization but do not seem to serve for the passage of lung or air sac diverticula. Pleurocoels, on the other hand, are not directly related to pneumatic features and constitute a plesiomorphic trait that was widespread in Mesozoic non-neornithine birds. It is noted that an inverse correlation exists between the occurrence of pleurocoels and the pneumatization of the humerus, with pleurocoels being mainly found in extant and fossil taxa, in which the humerus is not pneumatized by diverticula of the clavicular air sac. Here it is hypothesized that pleurocoels primarily serve to increase the structural resistance of the vertebral body and were reduced multiple times in neornithine birds. In some taxa, their reduction may be related to the development of the furcula, which assists ventilation of the clavicular and cervical air sacs and may thereby contribute to the pneumatization of both, the humerus and the thoracic vertebrae. If so, Mesozoic non-neornithine birds, which had a rigid furcula with massive shafts as well as non-pneumatic humeri and pronounced pleurocoels, are likely to have differed in functional aspects of their air sac system from extant birds.
Aves, bone pneumatization, evolution, functional morphology, osteology
Birds have a unique respiratory system, which is very different from that of all extant non-avian land vertebrates. Unlike in other tetrapods, the lungs of birds are rigid and dorsally fixed to the vertebral column and ribs, and their ventilation is enhanced by a system of air sacs, which regulate a unidirectional air flow through the lungs (
Skeletal features related to bone pneumatization are distributed over the entire avian skeleton and involve traits (such as pneumatic foramina, heavily trabeculated bone structures, and hollow bone shafts) associated with the skull, major limb and pectoral girdle bones, as well as the vertebral column (e.g.,
An overview of pneumatic structures associated with the vertebrae of archosaurs was given by
Centrally situated openings in the lateral surfaces of the body of the thoracic vertebrae occur in crocodilians (
As detailed below, pleurocoels were identified in various Cenozoic neornithine birds, the closest extant relatives of which lack these structures. The present study not only aims at providing an overview of lateral openings and pleurocoels in the bodies of the thoracic vertebrae of extant and fossil neornithine birds, but also addresses some functional aspects of these features. For the first time, a correlation between the occurrence of pleurocoels and the absence of a pneumatization of the humerus is noted, which may open a new view on the correlated evolution of some postcranial skeletal features of birds.
Concerning extant birds, this study is based on an examination of skeletons of multiple representatives of all extant higher-level clades in the collection of Senckenberg Research Institute Frankfurt (
Institutional abbreviations:
In crocodilians, centrally situated foramina on each of the lateral surfaces of the body of the thoracic (dorsal) vertebrae serve for the passage of blood vessels and nerves (
Lateral openings in the thoracic vertebrae are particularly well developed in the anseriform Anhimidae (Fig.
Pulmonary injection preparations from the collection of Hans-Rainer Duncker: A‒D, Chauna torquata (Anseriformes, Anhimidae); A depicts the latex cast of the right lung (rotated by 180°), in C the corresponding part of the vertebral column (caudalmost thoracic vertebrae, right side) of the same specimen is shown; B and D are details of the framed areas in A and C. E‒G, Fulmarus glacialis (Procellariiformes, Procellariidae); E depicts the latex cast of the right lung (rotated by 180°), in G the corresponding part of the vertebral column (caudalmost thoracic vertebrae, right side) of the same specimen is shown; F is a detail of the framed area in E showing a “pulmonary protuberance” (encircled) sensu
Lateral openings also occur in the thoracic vertebrae of other anseriform birds, in which their occurrence is, however, more variable. These openings are present in some individuals of Anseranas semipalmata (Anseranatidae; Fig.
Caudalmost thoracic vertebrae of anseriform birds in right lateral view. A, Chauna torquata (Anhimidae;
Centrally located lateral openings in the corpus of all or most thoracic vertebrae are likewise present in the gruiform Gruoidea (Gruidae, Aramidae, and Psophiidae; Fig.
Caudalmost section of thoracic spine and isolated thoracic vertebrae of various neornithine birds with lateral openings (lop) and pleurocoels (plc) in the vertebral corpus (lateral or lateroventral view). A, Sula leucogaster (Sulidae;
Caudalmost thoracic vertebrae of procellariiform (A‒E) and charadriiform (F‒M) birds in right lateral view. A, Diomedea melanophris (Diomedeidae;
Concerning fossil neognathous taxa, centrally positioned lateral openings in the bodies of the thoracic vertebrae occur in the early Paleogene Lithornithidae (Fig.
Thoracic vertebrae of fossil taxa with lateral openings (lop) or pleurocoels (plc). A, Lithornis vulturinus from the early Eocene Fur Formation in Denmark (Lithornithidae;
Little is known on the ontogenetic development of lateral openings and there appear to be taxon-specific differences in their development. The thoracic vertebrae of a juvenile individual of Phoebastria irrorata (Diomedeidae) do not exhibit lateral openings, whereas numerous openings are present in a juvenile individual of Ardeotis kori (Otididae; Fig.
Pleurocoels on the thoracic vertebrae adjoin the lungs and encompass protuberances of the mediodorsal bronchi (“pulmonary protuberances” of
Among extant birds, pronounced pleurocoels mainly occur in taxa of the Procellariiformes and Charadriiformes. In the Procellariiformes, they are present in most Procellariidae (Fig.
In the Charadriiformes, pleurocoels occur in all taxa of the Charadrii (Fig.
As yet, pleurocoels have not been reported for species outside the Procellariiformes and Charadriiformes, but here their presence is noted for a few species of the Anatidae (Aythya australis, Merganetta armata; Fig.
Thoracic vertebrae with well-developed pleurocoels were reported for various stem group representatives of higher-level taxa, the extant members of which lack such fossae. This is true for the stem group galliform Paraortygoides radagasti, which belongs to the Gallinuloididae (Fig.
Owing to their absence in all Mesozoic birds outside Neornithes, large openings in the lateral surfaces of the vertebral body probably represent a derived neornithine trait and evolved multiple times independently in only distantly related lineages. Even though such openings also occur in small species (e.g., some representatives of the anseriform Aythyini), they are mainly found in large-sized birds and appear to be due to an increased skeletal pneumatization. Lateral openings in the bodies of the thoracic vertebrae are often correlated with pneumatic foramina in the sternal extremity of the coracoid, which are present in the Anhimidae, Anseranatidae, Psophiidae, Gruidae, and Opisthocomiformes. Such coracoideal foramina are, however, absent in other taxa that exhibit openings in the bodies of the thoracic vertebrae, so that their presence in the above taxa is likely to be due to a higher overall degree of pneumatization in different parts of the skeleton and not due to an immediate functional correlation.
As detailed in the introduction, and in contrast to lateral openings, pleurocoelous thoracic vertebrae occur in virtually all Mesozoic non-neornithine birds except for the Archaeopterygiformes. Pleurocoels are therefore probably plesiomorphic for the Pygostylia, the clade including the Confuciusornithiformes, Enantiornithes, and Ornithuromorpha. They are found in the closest Mesozoic relatives of neornithine birds (Ichthyornithiformes, Hesperornithiformes), but it is not straightforward to determine whether pleurocoels were also present in the stem species of the Neornithes. If only the extant species are considered, it is most parsimonious to assume that the pronounced pleurocoels of the Procellariiformes and Charadriiformes are autapomorphic for these two taxa. However, the occurrence of pleurocoels in phylogenetically early diverging and geologically old stem group representatives of taxa whose extant representatives lack these structures, such as the Galliformes (Paraortygoides), Passeriformes (Parapsittacopes), and the coraciiform Coracii (Septencoracias), suggests that they were independently reduced in only distantly related neornithine clades. Accordingly, it is here hypothesized that pleurocoels were present in the last common ancestor of at least neognathous birds and possibly also in that of Neornithes as a whole.
Instead, there actually exists a negative correlation between pleurocoels and pneumatic features, with pleurocoels being present in taxa that lack pneumatic foramina in the fossa pneumotricipitalis of the humerus. Such is the case in the Procellariiformes, in which all taxa except for the Diomedeidae have non-pneumatic humeri. The Diomedeidae, by contrast, lack pleurocoels on the thoracic vertebrae but are the only procellariiform birds that exhibit pneumatic foramina in the fossa pneumotricipitalis. The thoracic vertebrae of the Oceanitidae, Hydrobatidae, and the procellariid taxon Pelecanoides are mediolaterally compressed, which may account for the absence of pleurocoels in these taxa. In the Charadriiformes, pneumatic foramina in the fossa pneumotricipitalis of the humerus are absent in all taxa except for the Stercorariidae, Rynchopidae, and Anous (Lari) (
All Mesozoic non-neornithine birds with pleurocoels likewise have a non-pneumatic humerus, and pneumatic foramina in the humerus are also absent in all fossil neornithine taxa, for which pleurocoels have been reported. Such is true for the Halcyornithidae and Messelasturidae (
There are a few extant taxa with non-pneumatic humeri that lack pleurocoels (
The fact that most taxa with distinct pleurocoels have non-pneumatic humeri raises the question about a possible functional correlation between the pneumatization of the humerus and the morphology of the thoracic vertebrae. Most extant birds have nine air sacs. The humerus is pneumatized by diverticula of the clavicular air sac (
In birds that have a furcula with narrow shafts, the bone acts as a spring during flight, and “the coupled actions of the sternum and furcula appear to be part of a respiratory cycling mechanism between the lungs and air sacs” (
The contribution of furcula movements to the ventilation of the clavicular and cervical air sacs suggests that Mesozoic non-neornithine birds, which had a rigid furcula with massive shafts, differed in some functional aspects of their air sac system from extant birds. Here it is hypothesized that well-developed diverticula of the clavicular and cervical air sacs evolved late in avian evolution and characterize neornithine subclades.
Pleurocoels appear to have been reduced in taxa, in which the thoracic vertebrae are pneumatized (e.g., Anhimidae, Gruoidea), and in those, in which these vertebrae are mediolaterally compressed (e.g., diving birds, taxa of the charadriiform Scolopaci) or are co-ossified to form a notarium (e.g., crown group Galliformes). This suggests a correlation with structural properties of the vertebral column. The cross section of the body of a pleurocoelous thoracic vertebra recalls that of an I-beam, and pleurocoels may increase the dorsoventral bending strength of the corpus of the thoracic vertebrae in taxa, in which the vertebral column of the thorax is subjected to little mediolateral flexion load (see, e.g.,
I thank Sven Tränkner for taking the photographs. Hans-Rainer Duncker is thanked for donating his invaluable collection of pulmonary injection preparations to Senckenberg Research Institute. Comments from Claudia Tambussi, Federico Degrange, an anonymous reviewer, and the Associate Editor Martin Päckert improved the manuscript.