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Amphibians & Reptilomorphs

 

AMPHIBIANS & REPTILOMORPHS

Fossilized remains of fish-like vertebrates with four limbs and the earliest amphibians are found before the end of the Devonian period (363 Ma). Reptile-like tetrapods evolved during the Carboniferous period (363-290 Ma). From them, mammals differentiated at the end of the Triassic period (208 Ma) and birds at the end of the Jurassic period (146 Ma) (1995LundbergJG; 2023CohenKM_CarN).

The taxa of early tetrapodomorphs are now arranged in the following order: Tinirau, Eusthenopteron, Megalichthys, Panderichthys, Qikiqtania, Tiktaalik, Elpistostege, Parmastega, Ventastega, Acanthostega, Elginerpeton, Ymeria, Ichthyostega (2022StewartTA_ShubinNH).

The study of ligamentum capitis femoris (LCF) in the listed extinct animal species is associated with significant difficulties. They are primarily due to the long time that has passed since the disappearance of the creatures. The situation is aggravated by the fact that LCF is an anatomical structure of small size, formed from soft tissues that are unstable in natural conditions. Confirmation of the fact of its presence in the extinct species can be the presence of a similar element in closely related living tetrapods.

Soft tissues can be preserved in fossilized resin. Thus, in Myanmar, an insect was found in amber that is approximately 99 Ma (2024CaiC_KundrataR). X-ray scanning of fossils allows us to study the shape and internal structure of insects that are approximately 300 Ma (2024LhéritierM_PerrierV). Perhaps, the improvement of 3D tomography will eventually help to establish the fine structure of hip joint tissue and LCF of dinosaur embryos in fossilized eggs (2009LiangX_WuS). Preservation of LCF is possible during mummification of bodies buried in conditions that promote dehydration with subsequent lack of contact with water. A striking example of this is the Gebelein mummies, which are approximately 3400 years old. Natural preservation of remains in peat bogs in northern European regions is known. In particular, the body of the «Kølbjerg man» was discovered, who died approximately 8000 years ago. It is possible to detect LCF in bodies buried at sub-zero temperatures: in a glacier or frozen ground. An example is the Sopkarginsky mammoth, which died almost 45000 years ago. At longer periods, soft tissues decompose, and direct detection of LCF is excluded.

Under certain conditions, bones are preserved, being replaced by minerals (fossilization). LCF of a particular species can be judged based on the analysis of fossilized bones of the pelvis and femur. On the femur, these are the fossa of the head of the femur, the groove of the head of the femur, the tuberosity of the head of the femur, the gap of the head of the femur. In the pelvic area, the presence of LCF can be indicated by: the notch of the acetabulum, the fossa of the acetabulum, the opening of the floor of the acetabulum, irregularities on the articular surface of the acetabulum, such as tuberosities and depressions. Some of the best-studied early tetrapods: Acanthostega and Ichthyostega (clade Ichthyostegalia) lived in the Upper Devonian, or 382.7-358.9 Ma (1993RieppelO; 2023CohenKM_CarN).

Ichthyostega stensiӧvi, skeleton reconstruction of the middle XX; exposition of the Orlov Paleontological Museum (Moscow), photo by the author.


Their fossil remains are found up to approximately 359.2 Ma (2012SmithsonTR_ClackJA). The acetabulum of Acanthostega was rounded, subtriangular in shape, elongated in the horizontal direction (1996CoatesMI). The elongated shape of the acetabulum in Acanthostega had a maximum length-to-height ratio of 0.45 (2012SwartzB). A three-dimensional reconstruction of the Ichthyostega skeleton showed that its hip joint had significantly limited pronation-supination, and the femur with a boomerang-shaped head swung in an elongated acetabulum in two planes (2012PierceSE_HutchinsonJR).

A cast of the pelvic limb skeleton of Ichthyostega (Late Devonian, Famennian stage, 372.2-358.9 Ma), showing a flattened proximal end of the femur; exposition of the Orlov Paleontological Museum (Moscow), photo by the author.


Articular fossae and pelvic limbs of some stem tetrapods (from 2012SwartzB: Fig. 5).


Considering that the femur of Acanthostega is also flattened, its hip movements were similar to Ichthyostega, as was its gait. Apparently, the evolution of tetrapod locomotion between Panderichthys - Acanthostega, went through a stage of locomotion with body flexion, in which the pelvic fins played the role of anchors, before the emergence of a propulsive force driven by the hind limbs (2005BoisvertCA). Currently, the type of locomotion with support on the front fins is demonstrated by mudskippers (Periophthalmus) from the class of ray-finned fishes. According to the graphical reconstruction, the acetabulum of Acanthostega and Ichthyostega had a posterior notch (2018AhlbergP). More precisely, the notch of the acetabulum in these tetrapodomorphs was located in the posterosuperior section.

Pelvic morphology of elpistostegids and three early tetrapods, lateral, anterior, left view. Not drawn to scale. Tiktaalik, modified from Shubin et al. (Shubin, Daeschler and Jenkins 2014); Ichthyostega, new reconstruction based on data from Jarvik (Jarvik 1996); Acanthostega, new reconstruction based on data from Coates (Coates 1996); Eryops modified from Pawley & Warren (Pawley and Warren 2006); illustration from 2018AhlbergPE:Fig. 3, no changed.

The presence of the acetabular notch suggests that Ichthyostega and Acanthostega had at least one LCF in the hip joint. This element, by restricting hip motion, contributed to more effective support on the pelvic limb. It seems to us that the movements of the hips in Ichthyostega and Acanthostega in the elongated acetabulum were circumduction, which is well reproduced in the human wrist joint. In this case, the LCF functioned as a flexible traction, limiting the adduction of the hip and the tilt of the pelvis to the medial side. At the same time, it supplemented the upper arch of the acetabulum, providing direct support for the upper surface of the femoral head and contributed to the pressing of its to the acetabulum. According to Б.З. Перлин et al. (1977), the LCF functions in a similar way in humans, playing the role of «... a supporting component of the bone-fibrous arch ...» of the hip joint.

It seems to us that the proximal attachment area of the LCF in Ichthyostega and Acanthostega was located above and behind the center of the hip joint. The distal attachment area was probably located on the periphery of the upper part of the articular surface of the femoral head or even on the neck. It could resemble the «capsular ligament» (synovial fold) of Amantini, but was localized in the upper part of the joint. According to our opinion, the LCF in Ichthyostega and Acanthostega was formed from a portion of the articular capsule by its local intensive stretching and gradual displacement in the direction of the central longitudinal axis of the hip joint. A similar mechanism for the emergence of LCF in phylogenesis was described by a number of authors of the XIX and XX centuries (1902СаввинВН; 1927АнсеровНИ; 1939МаркизовФП; 1946ТонковВ).

Accordingly, in Ichthyostega and Acanthostega, when supporting themselves on a leg extended forward, the LCF was at an angle to the vertical. Being stretched by the weight of the pelvis tilted downwards and medially, the element was similar to a deflected pendulum thread with an upper suspension point. As a result of the ligament-bone-cartilage interaction, a force directed forward appeared, facilitating the movement of the animal.

The subsequent form of tetrapods after Acanthostega and Ichthyostega is assumed to be Tulerpeton curtum, which had longer and thinner bones than its evolutionary ancestors, but with six fingers (2009ClackJA).

Artistic reconstruction of the external appearance of Tulerpeton curtum; exposition of the Orlov Paleontological Museum (Moscow), photo by the author.


Tulerpeton curtum is recognized as a stem-group reptiliomorph amniote that lived in an aquatic environment; unfortunately, its pelvic girdle has not been preserved (1995LebedevOA_CoatesMI). In the middle of the Visean stage (346.7-330.9 Ma) of the Carboniferous period, tetrapods became effectively terrestrial (2012SmithsonTR_ClackJA; 2023CohenKM_CarN). Currently, it is assumed that the first truly terrestrial vertebrate was Pederpes finneyae. Its fossilized remains were found in deposits of the Tournaisian era, formed 354-344 Ma (2002ClackJA; 2023CohenKM_CarN). The shape of the acetabulum of the individual could not be clarified, since this part of the pelvis was irreversibly lost. However, it was noted that the shape of the femur resembled that of Ichthyostega and is no different from the shape of the femur of the closely related Whatcheeria (2005ClackJA_FinneySM). In turn, Whatcheeria deltae, which lived somewhat later, approximately 340 Ma, had a strongly concave acetabulum, an anteroposteriorly elongated and laterally flattened femoral head (1995LombardRE_BoltJR).

It can be assumed that Pederpes finneyae had an acetabulum similar to Whatcheeria deltae.

Right pelvic bone of Whatcheeria deltae, lateral view (schematic), cranial end on the right; the image is based on the drawing from 1995LombardRE_BoltJR, our notations).


Analyzing the graphic reconstruction of the pelvis of Whatcheeria deltae from the work of R.E. Lombard, J.R. Bolt (1995: Fig. 8), we see the notch of the acetabulum in the upper-posterior section, caudal to the buttress located above. Accordingly, based on this observation, it can be assumed that Whatcheeria deltae and Pederpes finneyae had LCF. It was probably located, as in Acanthostega, attached above the center of the acetabulum and followed forward-outward-downward to the periphery of the head or to the neck of the femur. The most ancient amphibian anthracosaur from the lower stages of the Carboniferous period (358.9-315.2 Ma) is Eoherpeton watsoni (1975PanchenAL). T.R. Smithson (1985) provides a detailed description of its pelvis and the acetabulum region. The author notes that in Eoherpeton watsoni, below the blade of the ilium and its process under the transverse line, there is a large bulbous tubercle, which forms a supraacetabular buttress. Its incomplete surface faces posterolaterally, and its posterior margin forms the anterior border of a deep cleft: the supra-acetabular notch, which is probably the site of a ligament [LCF] similar to that found in the acetabular notch in mammals (see A.S. Romer, 1922:581). The supra-acetabular notch and buttress in Eoherpeton watsoni are much more strongly developed than in most early tetrapods, especially in Archeria and Gephyrostegus. The researcher points out that the significance of this observation is unclear, but it may indicate a closer relationship between the head of the femur and the acetabulum, providing a more powerful ligamentous connection between the hindlimb and the pelvic girdle. Neglecting the supraacetabular buttress, the acetabulum appears to have originally formed a deep ovoid depression at the junction of the ilium, ischium, and pubis. The acetabulum is oriented forward and has a greatest diameter of about 60 mm. Ventrally, there is a prominent labrum, approximately 12 mm high, running the length of the concave ventral margin and oriented at right angles to the posterior aspect of the acetabulum. At its lowest point, the labrum is horizontal. The bony surface of the acetabulum was apparently covered with cartilage (1985SmithsonT:Fig. 27).

An early tetrapod, Crassigyrinus scoticus, is an amphibian from the Namurian stage of the Carboniferous period, i.e., it lived approximately 326-313 Ma. Its ilium formed a strong articulation with the spine through the sacral rib. The ischium was separated from the ilium by cartilage, ornamented like a skin bone. The pubic bone is not preserved. The femur bears a strongly developed internal trochanter on the surface. The described structure of the femur suggests swimming, not walking (1990PanchenAL_SmithsonTR). The shape of the acetabulum of the mentioned ancient amphibian remains unknown. We do not exclude that the structure of its hip joint was similar to that of a modern salamander (1934FrancisETB). A temnospondyl (primitive amphibian) Eryops megacephalus, which flourished in the Permian, or 298.9-251.9 Ma, had significant similarities with salamanders (2022HerbstEC_HutchinsonJR; 2023CohenKM_CarN).

In the posterosuperior region of the acetabulum of Eryops megacephalus, a large notch is clearly visible. Its configuration and location resembles that of Acanthostega and Whatcheeria deltae. In our opinion, in Eryops megacephalus, the proximal end of the LCF was attached in the region of the acetabular notch and was located behind and above the center of the hip joint. Its distal part, apparently, was attached near the edge of the articular surface of the head or even to the neck of the femur. We propose that in the line from Acanthostega to Eryops megacephalus, the LCF was oriented in a mirror-opposite manner to modern mammals. It was located at the top of the hip joint. This suggests similar biomechanics of the hip joint and the gait pattern of the earliest tetrapods.

References

Cohen KM, Harper DAT, Gibbard PL, Car N. The International Commission on Stratigraphy (ICS) International Chronostratigraphic Chart. September 2023. [stratigraphy.org]

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Keywords

ligamentum capitis femoris, ligamentum teres, ligament of head of femur, doctrine, animals, reptile, amphibian


                                                                     

The original text in Russian is available at the link: Амфибии и рептиломорфы

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