Research Article |
Corresponding author: M. Alejandra Sosa ( alejandrasosa@fcnym.unlp.edu.ar ) Academic editor: Martin Päckert
© 2024 M. Alejandra Sosa, Carolina Acosta Hospitaleche.
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:
Sosa MA, Acosta Hospitaleche C (2024) Vertebral formula and numerical variations in the spine of the Antarctic and southern South American penguins (Aves: Sphenisciformes). Vertebrate Zoology 74: 209-219. https://doi.org/10.3897/vz.74.e114112
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Abstract
The vertebral column in tetrapods consists of several constant regions, namely the cervical, thoracic, lumbar, sacral, and caudal regions. Each of these regions is characterized by a specific number of vertebrae, contributing to the overall vertebral formula. Supernumerary and/or missing vertebrae have only been sporadically mentioned for penguins, and the specific vertebral formula is only determined for some non-passeres orders. Variations in the anatomy and vertebral number of South American and Antarctic penguin species are evaluated here. Sixty-six specimens of Aptenodytes forsteri, Pygoscelis adeliae, P. antarcticus, P. papua, Spheniscus magellanicus, and Eudyptes chrysocome were examined to establish the vertebral formula for six South American and Antarctic species, reporting the type and frequency of the variations found in the generalized configuration. We found no intraspecific variation in respect of the number of cervical as well as cervicothoracic vertebrae in all penguin species studied. Intra- and interspecific variation occur in the thoracic, synsacral, and caudal regions comprising 6–7, 13–14 and 5–8 vertebrae, respectively. Particularly, the variations were found in the transitional zones between one region and another and/or between synsacral segments.
Axial formula, numerical anomalies, Spheniscidae, synsacral segments, vertebral column
The vertebral column is the part of the axial skeleton that protects the spinal cord, provides support and stability to the body, and serves as the origin and insertion of the musculature (
In tetrapods, in general, the most common and well-known vertebral regions correspond to the cervical, thoracic, lumbar, sacral, and coccygeal or caudal regions (
It is difficult to establish a general vertebral formula in birds because the regionalization of the spine is related to the presence of modifications such as the notarium formed by the fusion of some thoracic vertebrae; the synsacrum formed by ankylosis of thoracic, lumbar, sacral, and caudal vertebrae; and the pygostyle formed by the fusion of the last caudal vertebrae (
Beyond that, numerical differences have also been found in the same region in several tetrapods. Such is the case of goats and humans among mammals (Simoens et al. 1982;
Particularly in penguins, the total number of vertebrae also varies, from 42 in Eudyptes chrysocome (Forster, 1781), Eudyptes chrysolophus (von Brandt, 1837), Eudyptula minor (Forster, 1781), Pygoscelis papua (Forster, 1781), Aptenodytes patagonicus (Miller, 1778), and Aptenodytes forsteri Gray, 1844 (
Recently, an extra vertebra in the thoracic region was detected in a specimen of Aptenodytes forsteri (
The vertebral column of 66 specimens of six South American and Antarctic penguin species, housed in the collections of the Vertebrate Zoology Division of the Museo Argentino de Ciencias Naturales Bernardino Rivadavia (MACN-Or) of the Ciudad Autónoma de Buenos Aires and the Ornithological Section of the Museo de La Plata (MLP-ORN), La Plata, were analyzed. The sample includes the emperor penguin Aptenodytes forsteri (n = 3), Adélie penguin Pygoscelis adeliae (Hombron and Jacquinot, 1841) (n = 20), chinstrap penguin Pygoscelis antarcticus (Forster, 1781) (n = 1), gentoo penguin Pygoscelis papua (n = 9), Magellanic penguin Spheniscus magellanicus (n = 32), and rockhopper penguin Eudyptes chrysocome (n = 1) (see Table S1). Only subadult and adult penguins were selected based on their fully development of vertebrae, allowing precise allocation within vertebral column regions. Specimen ages were determined following
The number of vertebrae was determined by counting each individual, morphologically identifying the regions as follows. Cervical (C): the ribs are fused to the vertebrae, they have a foramen transversarium, and the vertebral body is heterocoelus; cervicothoracic (CT): the ribs are not fused to the vertebrae but do not articulate with the sternum, and the vertebral body is heterocoelus; thoracic (T): the ribs are not fused to the vertebrae and articulate with the sternum, and the vertebral body is opisthocoelus, except for the cranial articular facet of the first thoracic vertebra which is heterocoelus; synsacrum (S): total or partially ankylosed thoracic, lumbar, sacral, and caudal vertebrae; free caudal (Ca): cylindrical vertebral body, triangular vertebral arch, well-developed and rectangular processus transversi, all similar in size and shape; and pygostyle (P): total or partially ossified vertebrae with cylindrical vertebral body compressing and reducing in size caudally.
The vertebral formula for each species was determined as follows: Cx + CTx + Tx + Sx + Cax + Px(x) = Ntotal. Capital letters indicate the vertebrae of the cervical, cervicothoracic, thoracic, synsacral, free caudal, and pygostyle regions, respectively. In addition, the subscript “x” shows the number of vertebrae for each region being, for the synsacrum and pygostyle, the total number of ankylosed vertebrae. It is worth noting that for practical purposes, in the total number of vertebrae (N), the pygostyle was counted as a single vertebral element regardless of the number of fused vertebrae indicated in brackets.
The synsacral segments, that form the synsacrum, were analyzed according to
The vertebral column across all examined penguin species demonstrates a consistent configuration, yet our scrutiny reveals subtle distinctions in the presence, absence, or developmental degree of specific processes, as well as variations in the number of elements within each region.
The subsequent section underscores both intra- and interspecific morphological variations, offering a detailed examination of the penguin vertebral column. Our focus centers on the vertebral formula providing an overview of numerical variations within each region.
Cervical vertebrae.
The processus ventralis corporis appears from C2 to C4 in Aptenodytes forsteri (Fig.
General aspects: A C4 in left lateral view, Aptenodytes forsteri (MLP-ORN 15192); B C8 in cranial view, Aptenodytes forsteri (MLP-ORN 15192); C C11 in left lateral view, Aptenodytes forsteri (MLP-ORN 15192); D C1–C13 in dorsal view, Pygoscelis papua (MLP-ORN 783); E CT1 in left lateral view, Aptenodytes forsteri (MLP-ORN 15192); F CT1 in cranial view, Pygoscelis adeliae (MLP-ORN 1134); G CT2 in cranial view, Pygoscelis adeliae (MLP-ORN 1134); H CT1 in cranial view, Spheniscus magellanicus (MLP-ORN 1598); I CT2 in cranial view, Spheniscus magellanicus (MLP-ORN 1598); J T1–T6 and synsacrum in left lateral view, Eudyptes chrysocome (MLP-ORN 1596); K T2 in cranial view, Aptenodytes forsteri (MLP-ORN 15192); L T6, T7 and the cranial end of the synsacrum in left lateral view, Pygoscelis adeliae (MACN-Or 68557); M T1–T7 in left lateral view, Spheniscus magellanicus (MACN-Or 71167); N T7 in left lateral view, Aptenodytes forsteri (MLP-ORN 15192); O T7 in cranial view, Spheniscus magellanicus (MACN-Or 71167); P Ca1–Ca7 in cranial view, Eudyptes chrysocome (MLP-ORN 1596); Q Ca1–Ca6 and pygostyle in left lateral view, Pygoscelis antarcticus (MLP-ORN 1138). R pygostyle in left lateral view, Eudyptes chrysocome (MLP-ORN 1596), adult; S pygostyle in left lateral view, Spheniscus magellanicus (MACN-Or 71167), juvenile, where the first vertebra is still unfused. Abbreviations: api – ala praeacetabularis ilii; av – arcus vertebrae; cv – corpus vertebrae; ec – eminentia costolateralis; fa – facies articularis; pc – processus costalis; pca – processus caroticus; ph – processus haemalis; ps – processus spinosus; pt – processus transversus; pvc – processus ventralis corporis. Scale bar: 10 mm.
Cervicothoracic vertebrae
. The vertebral body exhibits subtle variations, being slightly rectangular in A. forsteri and quadrangular in the remaining species (Fig.
Thoracic vertebrae. All vertebrae are opisthocoelus, but the cranial articular facet of T1 acquires a saddle-shape in all species. The processus ventralis corporis decreases cranio-caudally in length (Fig.
Synsacrum
. The synsacral body, robust and slightly curved, is divided into the classical five segments (Fig.
The sulcus ventralis synsacri varies in depth and width, being deep and broad in E. chrysocome, narrow in P. adeliae, P. antarcticus, P. papua, and S. magellanicus, and absent in A. forsteri. The processus costales are developed between S4–S6 in S. magellanicus, P. adeliae, A. forsteri, P. papua, and P. antarcticus, S5–S6 in E. chrysocome, and then in S8–S9 in E. chrysocome, S9– S10 in S. magellanicus, and P. adeliae, and S10–S11 in A. forsteri, P. papua, and P. antarcticus. The crista spinosa synsacri, compressed at the cranial end, decreases in height craniocaudally toward the last synsacral vertebra.
A significant interspecific variation is observed in the fusion of the synsacrum to the pelvic girdle. Aptenodytes forsteri, S. magellanicus, and E. chrysocome do not exhibit fusion. On the contrary, in P. adeliae fusion occurs to varying degrees, involving the last two vertebrae of the TLS, all vertebrae of the LS and SS, and the first two (e.g., MLP-ORN 15476) or three (MACN-Or 68826) vertebrae of the CS. Pygoscelis antarcticus presents full fusion, with the processus transversi and the processus costales of all synsacral vertebrae fused to the pelvic girdle. In P. papua, fusion affects the last three vertebrae of the TLS, all vertebrae of the LS and SS, and the first (MACN-Or 68596) or second (MLP-ORN 14767) vertebrae of the CS.
Free caudal vertebrae.
They exhibit a cylindrical vertebral body (Fig.
Pygostyle
. It results from the ankylosis of five caudal vertebrae, progressively decreasing craniocaudally in size, forming a triangular single structure (Fig.
The cervical and cervicothoracic regions exhibits a consistent configuration across all species. In the majority of species, the thoracic region typically comprises six vertebrae; however, exceptions are noted. Specifically, T7 is present in MLP-ORN 1586 (A. forsteri) and MACN-Or 71167 (S. magellanicus). On the other hand, specimens MACN-Or 73283 (P. adeliae) and MLP-ORN 135 (S. magellanicus) display a unique variation, featuring only five thoracic vertebrae.
General vertebral formula for the six species analyzed. Abbreviations: C – Cervical region; CT – Cervicothoracic region; T – Thoracic region; S – Synsacrum; Ca – Free caudal region; P – Pygostyle.
Species | Vertebral formula |
Aptenodytes forsteri | C13 + CT2 + T6 + S13 + Ca7 + P1(5) = 42 |
Eudyptes chrysocome | C13 + CT2 + T6 + S13 + Ca7 + P1(5) = 42 |
Pygoscelis adeliae | C13 + CT2 + T6 + S14 + Ca6 + P1(5) = 42 |
Pygoscelis antarcticus | C13 + CT2 + T6 + S14 + Ca6 + P1(5) = 42 |
Pygoscelis papua | C13 + CT2 + T6 + S14 + Ca6 + P1(5) = 42 |
Spheniscus magellanicus | C13 + CT2 + T6 + S13 + Ca6 + P1(5) = 41 |
The synsacrum comprises 13 ankylosed vertebrae in A. forsteri, E. chrysocome, 19 specimens of S. magellanicus, and two specimens of P. adeliae (MACN-Or 68557 and MLP-ORN 15137), as well as one specimen of P. papua (MLP-ORN 15410). In contrast, P. adeliae, P. antarcticus, P. papua, and 11 specimens of S. magellanicus exhibit a synsacrum formed by14 ankylosed vertebrae.
Additionally, all species exhibit five discernible synsacral segments, with variations in the number of vertebrae. In S. magellanicus and P. adeliae (Fig.
Synsacra and pelves (in B, D–F) in ventral view. A Spheniscus magellanicus (MLP-ORN 1598); B Pygoscelis adeliae (MACN-Or 68557); C Aptenodytes forsteri (MLP-ORN 15192); D Pygoscelis papua (MLP-ORN 783); E Pygoscelis antarcticus (MLP-ORN 1138); F Eudyptes chrysocome (MLP-ORN 1596). Synsacral segments: TS – Thoracal Segment; TLS – Thoracolumbar Segment; LS – Lumbar Segment; SS – Sacral Segment; CS – Caudal Segment. Abbreviations: api – ala praeacetabularis ilii; pc – processus costalis; pt – processus transversus; T – thoracic vertebra. Black circles indicate each individual vertebra. Scale bar: 10 mm.
Variation within different segments are also evident. In P. adeliae the observed variation includes three vertebrae in the CS (specimens MLP-ORN 15137 and MACN-Or 68557), and three vertebrae in both LS and CS (specimen MACN-Or 73283). P. papua exhibits variations, such as in MLP-ORN 14921, which has two TS vertebrae (identified by the presence of eminentiae costolateales), and only two TLS with processus costales. Another specimen, MLP-ORN 14900, also displays only two last vertebrae of the TLS with processus costales. MLP-ORN 15410 is characterized by one missing vertebra in the TLS, with only the last two vertebrae of this segment bearing processus costales. In S. magellanicus, specimen MACN-Or 73286 features four vertebrae in the TLS, and among specimens with 13 synsacral elements, the absent vertebra corresponds to the CS segment.
The counts of free caudal vertebrae varies, ranging between five (e.g. MLP-ORN 15476 P. adeliae), six (e.g. MLP-ORN 1138 P. antarcticus), seven (e.g. MLP-ORN 15038 P. adeliae, MLP-ORN 14921 P. papua, MLP-ORN 949 S. magellanicus), or eight (e.g. MLP-ORN 929 S. magellanicus). In all species, the pygostyle is elongated and acquires a triangular shape, consistently formed by five vertebrae that fuse during postnatal ontogeny. Notably, the cranialmost vertebra composing the pygostyle is notably sturdier than the others, with shorter processus transversi compared to the free caudal vertebrae, and more expanded processus haemalis. This unique morphology distinguishes this vertebra among other free caudal vertebrae, whether free or already fused to the pygostyle.
The present work examined the complete spine of 66 specimens (Table
Total number of vertebrae by species and by region, and the number of cases in which the more general total numbers occur, and the number of cases where variations occur. N indicates the total number of specimens analyzed per species.
Species (N) | Condition | Number of casesa | Number of vertebrae | Total | |||||
Cervical | Cervicothoracic | Thoracic | Synsacrum | Free Caudals | Pygostyle | ||||
Aptenodytes forsteri (3) | General | 1 | 13 | 2 | 6 | 13 | 7 | 1(5) | 42 |
Extra vertebra | 1 | 13 | 2 | 7 | 13 | 7 | 1(5) | 43 | |
Eudyptes chrysocome (1) | General | 1 | 13 | 2 | 6 | 13 | 7 | 1(5) | 42 |
Pygoscelis adeliae (20) | General | 9 | 13 | 2 | 6 | 14 | 6 | 1(5) | 42 |
Homeotic transformation | 2 | 13 | 2 | 7 | 13 | 6 | 1(5) | 42 | |
Extra vertebra | 3 | 13 | 2 | 6 | 14 | 7 | 1(5) | 43 | |
Missing vertebra | 1 | 13 | 2 | 5 | 14 | 6 | 1(5) | 41 | |
Pygoscelis antarcticus (1) | General | 1 | 13 | 2 | 6 | 14 | 6 | 1(5) | 42 |
Pygoscelis papua (9) | General | 4 | 13 | 2 | 6 | 14 | 6 | 1(5) | 42 |
Extra vertebra | 1 | 13 | 2 | 6 | 14 | 7 | 1(5) | 43 | |
Missing vertebra | 1 | 13 | 2 | 6 | 13 | 6 | 1(5) | 41 | |
2 | 13 | 2 | 6 | 14 | 5 | 1(5) | 41 | ||
Spheniscus magellanicus (32) | General | 10 | 13 | 2 | 6 | 13 | 6 | 1(5) | 41 |
Homeotic transformation | 1 | 13 | 2 | 7 | 13 | 5 | 1(5) | 41 | |
Extra vertebra | 8 | 13 | 2 | 6 | 14 | 6 | 1(5) | 42 | |
1 | 13 | 2 | 6 | 13 | 7 | 1(5) | 42 | ||
1 | 13 | 2 | 6 | 13 | 8 | 1(5) | 43 | ||
a The number of cases does not include those specimens that were incomplete. |
Our findings reveal a total number of 42 vertebrae for E. chrysocome, P. papua, and A. forsteri, consistent with previous reports (
The cervical region consistently comprises 13 vertebrae across all analyzed species, aligning with observations by
In all species, two cervicothoracic vertebrae, also referred as “transitional” (
The thoracic vertebrae, characterized by the presence of unfused ribs articulating with the sternum (
The first vertebra, ankylosed to the synsacrum and bearing ribs, used to be included in the thoracic region (
Most species, such as P. adeliae, P. antarcticus, P. papua, and S. magellanicus, exhibit six free caudal vertebrae. However, seven free caudal vertebrae are counted in A. forsteri and E. chrysocome. Variations in the number of caudal vertebrae have also been reported in cranes (Gruidae) (Hiraga et al. 2013). The pygostyle resulted as the most conservative element, composed of five vertebrae ankylosed forming a triangular structure in all species described here (see also
Numerical changes in the vertebral series can result from meristic variations, also called numerical anomalies (Verheyen 1858a, 1858b;
We found numerical variabilities in the thoracic, synsacral, and caudal regions among species (Fig.
Schematic representation of the vertebral column of penguins representing the general vertebral formula and its numerical variations. A General vertebral formula of Pygoscelis; B Numerical variation with extra vertebra in the caudal region, e.g. Pygoscelis papua; C Numerical variations with a missing vertebra in the thoraric region, e.g. Pygoscelis papua; D Numerical variation with a missing vertebra in the thoracolumbar segment of the synsacrum, e.g. Pygoscelis papua; E Numerical changes in the thoracic region and the lumbar segment of the synsacrum occur due to homeotic transformations. There is a variation in the number of the vertebrae within regions (an extra thoracic vertebra and a missing vertebra in the lumbar segment of the synsacrum), but not provokes a change in the total number of vertebrae, e.g. Pygoscelis papua; F General vertebral formula of Spheniscus; G Numerical variation with an extra vertebra in the caudal segment of the synsacrum , e.g. Spheniscus magellanicus; H Numerical variation with two extra vertebrae in the free caudal region, e.g. Spheniscus magellanicus; I Numerical variation with a missing vertebra in the thoracic region, e.g. Spheniscus magellanicus; J Numerical changes in the thoracic and free caudal region occur due to homeotic transformations. There is a variation in the number of the vertebrae within regions (an extra thoracic vertebra and a missing free caudal vertebra) but not provokes a change in the total number of vertebrae, e.g. Spheniscus magellanicus; K General vertebral formula of Aptenodytes/Eudyptes. Abbreviations: C – cervical vertebrae; CT – cervicothoracic vertebrae; T – thoracic vertebrae; S – synsacrum; Ca – free caudal vertebrae; P – pygostyle.
The numerical anomalies identified in Sphenisciformes were attributed to ontogenetic causes by
Other cases of numerical variation probably caused by homeotic transformations are observed within the synsacrum, characterized by counts of either 13 or 14 vertebrae. These variations predominantly occur in the TLS and CS, although occurrences were also noted in the TS. In one specimen of P. papua (MLP-ORN 14921) the TLS displayed an unusual development: the first vertebra exhibited eminentiae costolaterales (like those of the TS), while the last two vertebrae possessed processus costales, a feature typically seen in three vertebrae among the majority of specimens of this species. This specimen presented six thoracic vertebrae and a total of 14 synsacral vertebrae, which aligns with the general count for the species. Another specimen of P. papua (MLP-ORN 15410) presented only 13 vertebrae in the synsacrum, with the missing vertebra corresponding to the TLS, where the first two vertebrae displayed processus transversi, while the last two presented processus costales. Despite this variation, this specimen exhibited six thoracic and six caudal vertebrae, representing the most common count for this species.
The most significant variability in the number and configuration of synsacral vertebrae (ranging from 13 to 14 vertebrae) among penguins was observed in S. magellanicus. Specimens with 13 synsacral vertebrae exhibit one missing element in the CS, maintaining the typical total count for the species. However, the specimen MACN-Or 73286 has one vertebra less in the TLS.
The number of vertebral elements of each region in the species analyzed ratifies previous data (e.g.,
We are grateful to Yolanda Davies from the “Museo Argentino Bernardino Rivadavia” for kindly receiving MAS in the collection under her care, to Mariana Picasso and Diego Montalti from the Museo de La Plata for their trust in accessing the materials, to María Florencia Sosa for checking the English grammar, to Alejandra Piro and Jorge La Grotteria for their help and support in preparing the manuscript, to G. Mayr, J. Watanabe, one anonymous reviewer and the editor M. Päckert for their helpful comments.
Table S1
Data type: .pdf
Explanation notes: Specimens of the six species analyzed, the number of vertebrae and the association of the synsacrum to the pelvic girdle. Abbreviation: f!: indicates the number of vertebrae fused to form the pygostyle.