Research Article |
Corresponding author: Ingmar Werneburg ( ingmar.werneburg@senckenberg.de ) Academic editor: Irina Ruf
© 2021 Ingmar Werneburg, Serjoscha W. Evers, Gabriel Ferreira.
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:
Werneburg I, Evers SW, Ferreira G (2021) On the “cartilaginous rider” in the endocasts of turtle brain cavities. Vertebrate Zoology 71: 403-418. https://doi.org/10.3897/vz.71.e66756
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Abstract
In recent years, paleoneurology became a very popular research field and hundreds of brain-endocasts were described. The interpretation of a dorsal protuberance of the brain-endocast puzzled researchers for a long time, the so-called (cartilaginous) rider. This is mainly because of technical limitations in the past and due to non-accessibility of comparative material. Using turtles as a case-study, we conducted a literature review and studied embryological data in addition to fossil and extant species’ endocasts. We assessed three hypotheses on the origin of the rider as relating to 1) the pineal gland, to 2) the blood vessel system, and to 3) skull roof elements. Based on our integrated anatomical observations, we refute the pineal gland hypothesis (1) and an exclusive blood vessel explanation (2). However, we show that, in most cases, the cartilaginous origin applies (3). The related cartilages, mainly the anterior process of the chondrocranial tectum synoticum, can persist until adulthood. Its diversity is interpreted in regard to the mechanical support for the temporal skull region, the shape of which has been shown to be in turn related to neck retraction and jaw mechanics. Finally, we highlight the value of embryological data to provide profound hypotheses for evolutionary research despite its low quantitative evaluability. We argue that it should be studied in conjunction with modern computer-aided data acquisition whenever possible.
brain, chondrocranium, pila antotica, primary braincase wall, tectum cranii, Testudinata
Thanks to the development of computed tomography (CT) in the last 20 years and its increasing application to earth and life sciences, non-destructive analyses of anatomical structures, otherwise not assessable for macroscopical research, became possible (
Paleoneurology was established as a research program almost 100 years ago (
Rider diversity and skull categories. A) Braincase endocast in Emydura subglobosa (IW92) with no rider on the endocast; B) Brain tissue of the same specimen as in A in lateral (B1) and dorsal view (B2); C) an elongated rider in Chelydra serpentina (UFR VP1); D) a bulbus-like rider in Caretta caretta (NHMUK1940.3.15.1); E–F) † Plesiochelys etalloni (modified after
Only little work has been done to correlate endocast shape to actual brain anatomy in living vertebrates (e.g.,
In turtles, for example, neck retraction largely influences the shaping of the whole skull and already embryologically, the cartilaginous elements of the developing skull experience reorientations. Embryonic neck forces push the palatoquadrate against the braincase, closing the originally wide spaced cranioquadrate passage (
In recent years, knowledge on endocast anatomy of fossil and extant turtle species has increased enormously, and all major taxa were analyzed by at least one specimen (
Histological sections of late term embryos and a juvenile turtle. A–B, G–H) Pelomedusa subrufa (ZIUT, carapace length, CL = 96 mm); C) Chelonia mydas (ZIUT, CL = 24 mm); D–F) Chelydra serpentina (CL = 31 mm); I) Chelodina longicollis (ZIUT, CL = 18 mm; head length, HL = 11.7 mm). Section numbers in the right lower corner. A–C, G–I) cross, D–F) sagittal sections.
We compared a series of µCT-scans and brain-endocast reconstructions that we prepared for other studies (i.e.,
Endocast specimens compared in this study. Rider category (Fig.
Major taxon | Species | Collection number | reference | Rider category | Posterior emargination |
---|---|---|---|---|---|
Proganochelyidae | † Proganochelys quenstedtii* | MB 1910.45.2 (Berlin specimen) |
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Bulbus | Shallow |
† Proganochelys quenstedtii* | SMNS 16980 (Stuttgart specimen) |
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Absent/bulbus | Shallow | |
Meiolaniidae | † Gaffneylania auricularis | MPEF-PV 10556 |
|
Absent | Shallow |
† Meiolania platyceps | MMF 13825a |
|
Bulbus | Shallow | |
† Naomichelys speciosa* | FMNH-PR-273 | Paulina-Carabajal et al. (2019); |
Bulbus | Shallow | |
† Niolamia argentina | MLP 26–40 |
|
Bulbus | Shallow | |
Baenidae | † Eubaena cephalica* | DMNH 96004 |
|
Elongated | Deep |
† Plesiobaena antiqua | UCMP 49759 | Gaffney (1982) | Triangular | Shallow | |
Plesiochelyidae | † Plesiochelys etalloni | MH 435 |
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Triangular | Deep |
Testudines, Sandownidae | † Sandownia harrisi* | MIWG3480 |
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Bulbus/elongated | Deep |
Pleurodira, Bothremydidae | † Bothremys cooki | AMNH 2521 (Type skull) |
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Bulbus/ Elongated | Deep |
† Bothremys barberi | FMNH PR 247 |
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Bulbus/ Elongated | Deep | |
† Chedighaii hutchisoni | KUVP 14765 |
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Absent/bulbus | Deep | |
Pleurodira, Chelidae | Chelodina reimanni* | ZMB 49659 |
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Bulbus/ Elongated | Deep |
Emydura subglobosa* | IW92 |
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Absent | Shallow | |
Pleurodira, Podocnemidae | † Yuraramirim montealtensis | MPMA 04-0008/89 |
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Elongated | Shallow |
Podocnemis unifilis* | SMF-55470 |
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Elongated | Deep | |
Erymnochelys madagascariensis | AMNH living Reptiles 63579 |
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Absent | Deep | |
Cryptodira, Protostegidae | † Rhinochelys pulchriceps* | CAMSM_B55775 | Evers et al. (2018), |
Bulbus | Shallow |
Cryptodira, Xinjiangchelyidae | † Annemys sp.* | IVPP-V-18106 |
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Elongated | Deep |
† Xinjiangchelys radiplicatoides* | IVPP V9539 |
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Bulbus/ Elongated | Deep | |
Cryptodira, Trionychidae | Apalone spinifera* | FMNH 22178 |
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Elongated | Deep |
Pelodiscus sinensis* | IW576-2 |
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Elongated | Deep | |
Cryptodira, Emysternia | Platysternon megacephalum* | SMF-69684 |
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Absent | Shallow |
Trachemys scripta* | See |
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Bulbus | Deep | |
Cryptodira, Geoemydidae | Cuora amboinensis* | NHMUK69.42.145_4 |
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Bulbus/elongated | Deep |
Rhinoclemmys funereal* | YPM12174 |
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Bulbus | Deep | |
Cryptodira, Testudinidae | Chelonoidis chilensis | MPEF-AC 25 |
|
Bulbus | Deep |
Gopherus berlandieri* | AMNH-73816 |
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Elongated | Deep | |
Kinixys belliana* | AMNH-10028 |
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Absent | Deep | |
Malacochersus tornieri* | SMF-58702 |
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Bulbus/elongated | Deep | |
Testudo graeca* | YPM14342 |
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Bulbus | Deep | |
Testudo hermanni* | AMNH134518 |
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Bulbus/elongated | Deep | |
Cryptodira, Chelonioidea | † Corsochelys haliniches | CNHM PR 249 |
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Elongated | Shallow |
Caretta caretta | CNHM 31022 | Zangerl (1962) | Bulbus/ Elongated | Shallow | |
Caretta caretta* | NHMUK1940.3.15.1 |
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Bulbus | Shallow | |
Chelonia mydas | CNHM 22066 | Zangerl (1962) | Bulbus/ Elongated | Shallow | |
Chelonia mydas* | ZMB-37416MS |
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Absent | Shallow | |
Cryptodira, Chelydridae | Chelydra serpentina* | UFR VP1 |
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Elongated | Deep |
Macrochelys temminckii* | GPIT-PV-79430 (syn. GPIT/RE/10801) |
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Bulbus/elongated | Shallow/Deep |
For our study, we had access to the embryonic histological collection of Prof. Dr. Wolfgang Maier, Zoologisches Institut der Universität Tübingen (ZIUT), Germany, which houses a number of turtle species that were collected by Stefan Eßwein around 1990. In addition, we studied sections of Chelydra serpentina (Inv.-Nr. Rept 1214; carapace length = 31 mm) from Phyletisches Museum Jena, Germany, and Caretta caretta from the lab of Prof. Dr. Shigeru Kuratani (SK-lab) in Kōbe, Japan. Sections are mainly stained with Azan after Haidenhain (
From literature, late term embryos of following species were compared: Apalone spinifera (Fig.
Observations of µCT slices of enhanced contrast stained specimens (with phosphotungstic acid, i.e. PTA, see
A survey on a variety of extinct and extant turtle adult brain-endocasts (Table
Histological analyses of late term embryos revealed detailed anatomy of the structures surrounding the cerebellum and cerebrum (Fig.
A literature survey on the diversity and the development of the tectum synoticum in late term embryos revealed that a clearly defined anterior tectal process is present in all turtles. Length of the late embryonic process differs among species and to individual degree of development. Caretta caretta and Podocnemis unifilis late term embryos show aberrant, T-shaped appearances of this process (Fig.
The origin of the rider in the dorsal part of the endocast was alternatively explained by three hypotheses in the past. Based on our comparisons, we reject the pineal-gland-hypothesis (1), we argue that the vessel-hypothesis applies, if at all, only rarely (2), and consider the skull roof hypothesis as applying in most cases (3). In particular, we show that an anterior process of the cranial tectum and other elements of the primordial (chondrocranial) skull can persist and differentiate until adulthood and leave traces in the brain cavity.
The pineal gland is a dorsal median projection of the brain, laying between the telencephalic hemispheres anteriorly and the mesencephalic optic lobes posteriorly and can be associated with other outgrowths of the dorsal diencephalon (Fig.
Like D. coriacea, other extant marine turtles (Chelonioidea) also have a relatively long pineal gland, which is, however, not surrounded by bone in a separate dorsal cavity (Fig.
In the studied late term embryos, there is – with the notable exception of Chelodina with its flattened skull (Fig.
Although we never found any indication of the following development (maybe partly also because of limited data), one could argue that later in ontogeny the brain could – completely or partly – expand such way that it pushes the blood vessels against the braincase internally. However, the skull elements surrounding the brain, the cartilaginous chondrocranium and the dermal skull roof bones – parietal and frontal mainly –, are already well-developed around hatching (Fig.
When considering the blood-vessel hypothesis,
Late term Ca. caretta embryos (
Late embryonic diversity of the anterior (tectal) process in different turtle species in lateral (normal letter) and dorsal (letter with ‘) views (redrawn from cited references). In Ad’ and C–L’, only parts of the chondrocrania are shown with the left otic capsule for orientation. Earlier stages are shown in C, D, J, M), post-hatching specimens are shown in P–R’. A) four developmental stages of Caretta caretta (
In the late embryonic skull of turtles, the chondocranium is well differentiated and already possesses some endochondral ossifications (visible in Fig.
There is a striking diversity in the relative length and orientation of this late embryonic process in different species. This is, first of all, related to the developmental age of the embryos as visible in Eretmochelys imbricata (Fig.
In this context, little research has been done on cartilaginous structures in post-hatching, juvenile, and adult turtle skulls. It is known, however, that at least in the marine turtles Dermochelys coriacea (Fig.
Illustration of the cartilaginous anterior process of the supraoccipital and hypothesis on the force transmissions in the skull. Note the different degrees of ossification in the skull in A, C, and E (note: these images are not exactly on the midline). In D. coriacea (C), tectum cranii is fully cartilaginous and continuous with the interorbital septum and – like in Chelo. mydas (A) – with the orbitotemporal region. In Chely. serpentina (E), only the cartilaginous process and few remainders of the cartilaginous cranium are present. The schematic illustrations show the approximate position of the anterior tectal process (blue). Bended arrows indicate suggested force transmissions in the skull: in lateral skull view (B, D, F), they are indicated by a thin bended arrow due to visualization reasons; in dorsal views (B’, D’, F’), those arrows correspond to the broad red bended arrows in the skull. The straight arrows indicate pulling neck forces, the relative degree of which are indicated by the depth of the posterodorsal emarginations. It is hypothesized that these forces in the skull are absorbed by the anterior tectal process, which has an altering relative length and position in each species. * in C indicates the spatial shift of the skull roof vs. the braincase resulting in a dorsal excavation, which is here filled with cartilage of tectum cranii – more medial, there is a space for the dorsally erected pineal gland (figs 192, 201 and 202 in Wyneken, 2001, and discussed by
Considering the actual presence of a dorsally covered bony or cartilaginous anterior part of the supraoccipital, the anterior process might have some relation to the architecture of the temporal region (sensu
Originally, in early Testudinata, such as † Proganochelys quenstedtii (
As there is variation in rider shape among turtles, and the tectum might serve as anchor and/or buffer for biomechanical forces, some aspects of rider diversity roughly seem to be consistent with variation in skull roof emargination with very short, bulbus-like riders being associated with no or only a shallow occiput emargination and elongated riders associated with deep occiput or complete emargination. This relation is tentative and needs rigorous quantitative examination beyond the scope of this study. If rider shape and length were ultimately found to be correlated with emargination, this would reinforce current hypotheses on how important neck functionality and associated characters are for skull disparity and development in turtles.
We speculate that forces transmitted along the reduced temporal coverage during neck retraction are buffered along the postorbital area in a posterodorsal and medial direction into the anterior process of the tectum synoticum (red arrows in Fig.
The shape of the adult endocast rider cannot be easily associated to the length of the anterior tectal process (see Table
The collected images on the late embryonic stages from the literature (Fig.
Within some extant turtle taxa, e.g. Terrapene and chelid pleurodires, a dermal coverage of the temporal region is completely lost by evolutionary expansion of the anteroventral emargination (5 in Fig.
Evaluating the origin of a rider on the top of brain endocasts requires consideration of the tissues surrounding the brain cavity, including their ontogeny. Alternative explanations for the rider in turtle endocasts, such as the cavity of the pituitary gland or blood vessel imprints on the endocranial cavity, do not hold after our analyses of histological sections and µCT scans of PTA-stained specimens. Instead, we present clear evidence for the persistence of a cartilaginous tip of the supraoccipital bone, a remnant of the embryonic tectum synoticum, which causes the occurrence of a ‘rider’ in endosseous endocasts of turtle braincases. As such, the anatomy of the chondrocranium and its persistence until adulthood needs to be studied in detail for a profound interpretation of unique endocast structures, and we consider it as the major source for morphological variation of the endocast rider herein. Our considerations on these structures can only count as a preliminary examination of this topic. Cartilaginous structures were rarely studied before. This is, because comparative anatomy is mainly a subject of paleontologists today, who – in the past – rarely integrated embryonic or non-bone data to their analyses, but the field is changing.
Our paper highlights the need to integrate paleontology, zoology, and embryology to enable a holistic view on skull evolution (sensu
We wish to thank Wolfgang Maier (Tübingen), Rolf Beutel (Jena), and Shigeru Kuratani (Kobe) for access to their collections. We thank Cathrin Pfaff and Jürgen Kriwet (Vienna) for scanning the PTA-stained specimens used here. Wolfgang Maier is thanked for continuous inspiring discussions with I.W. on the relationship of ontogenetic and phylogenetic aspects of cranial morphology. We thank Juliana Sterli and one anonymous reviewer for their suggestions to improve the manuscript. Financial support: DFG-grant WE 5440/6-1 to I.W, FAPESP 2019/10620-2 to G.S.F.