The sauropterygian clade Plesiosauria arose in the Late Triassic and survived to the very end of the Cretaceous. A long, flexible neck with over 35 cervicals (the highest number of cervicals in any tetrapod clade) is a synapomorphy of Pistosauroidea, the clade that contains Plesiosauria. Basal plesiosaurians retain this very long neck but greatly reduce neck flexibility. In addition, plesiosaurian cervicals have large, paired, and highly symmetrical foramina on the ventral side of the centrum, traditionally termed “subcentral foramina”, and on the floor of the neural canal. We found that these dorsal and the ventral foramina are connected by a canal that extends across the center of ossification of the vertebral centrum. We posit that these foramina are not for nutrient transfer to the vertebral centrum but that they are the osteological correlates of a highly paedomorphic vascular system in the neck of plesiosaurs. This is the retention of intersegmental arteries within the vertebral centrum that are usually obliterated during sclerotome re-segmentation in early embryonic development. The foramina and canals are a rare osteological correlate of the non-cranial vascular (arterial) system in fossil reptiles. The adaptive value of the retention of the intersegmental arteries may be improved oxygen transport during deep diving and thermoregulation. These features may have been important in the global dispersal of plesiosaurians.
Plesiosauria are Mesozoic marine reptiles that had a global distribution
almost from their origin in the Late Triassic (Benson et al., 2012) to their
extinction at the end of the Cretaceous (Ketchum and Benson,
2010; Fischer et al., 2017).
Plesiosauria belong to the clade Sauropterygia and are its most derived and
only post-Triassic representatives, being among the most taxonomically
diverse of all Mesozoic marine reptiles (Motani, 2009). Sauropterygia
originated in the Early Triassic, diversifying into Placodontia and
Eosauropterygia. Eosauropterygia include the Pistosauroidea, which in turn
include Plesiosauria and non-plesiosaurian pistosauroids (Benson et al.,
2012), most notably the genera
Plesiosauria have a unique bauplan, with an unique mode of aquatic locomotion: four-winged underwater flight using limbs modified into pointed flippers (Ketchum and Benson, 2010; Wintrich et al., 2017). Morphological disparity within the group is mainly found in the evolution of different neck lengths and skull sizes. Neck length evolution involves a long neck at the base of the clade, with at least 35 cervical vertebrae, which is unique to “Pistosauridae” and Plesiosauria, all other amniotes having less than 30 cervical vertebrae (Müller et al., 2010). In Pistosauroidea, the increase in neck length evolves by an increase in vertebral number, not by an increase in centrum length as in other well-known long-necked animals, like sauropod dinosaurs (Sander et al., 2011; Taylor and Wedel, 2013). Neck elongation in plesiosaurians culminates in Elasmosauridae with cervical numbers exceeding 70 (O'Keefe, 2001; Zammit et al., 2008; Müller et al., 2010; Noe et al., 2017). The plesiosaurian neck was remarkably stiff (Taylor, 1981; Massare, 1988, 1994; Noe et al., 2017), which appears counterintuitive especially in the long-necked forms.
All plesiosaurian cervical vertebrae show a pair of large foramina on the
ventral surface of the vertebral centra (Romer, 1956). These foramina are
generally termed “subcentral foramina” (Storrs, 1991; Noe et al., 2017).
The large, highly symmetrical subcentral foramina are an autapomorphy
of plesiosaurs and are found with great regularity in members of the clade
(Wintrich et al., 2017; Benson and Druckenmiller, 2014; Storrs, 1991;
O'Keefe, 2001), but smaller and less symmetrical foramina are found in some
pistosaurids (non-plesiosaurian Pistosauroidea) such as
The usage of the descriptive term subcentral foramina has a long tradition, and such paired foramina are seen in many taxa of different lineages outside of Sauropterygia. However, the term subcentral foramen is also somewhat of a wastebasket term. In the case of Plesiosauria, foramina subcentralia (subcentral foramina) were defined by Storrs (1991). He described them as a uniquely derived character shared by virtually all plesiosaurs and as being unknown among other Sauropterygia like pachypleurosaurs, placodonts, and nothosaurid-grade Nothosauriformes. Furthermore, he interpreted the foramina subcentralia as vertebral nutritive foramina in cervical vertebrae. Rothschild and Storrs (2003) hypothesized that the foramina indicated a rich blood supply to the interior of the centra (i.e., acting as nutrient foramina), protecting the vertebrae from decompression syndrome. However, they noted that the foramina showed a “large degree of variability” which is not what we observe (see below).
In addition to these ventral, paired foramina, plesiosaurian cervicals show a pair of large, highly symmetrical foramina on the floor of the neural canal. This character has not received much attention in the literature before (but see Martin and Parris, 2007), probably because it is harder to observe due to its location inside the neural canal. Damaged or sectioned vertebral centra as well as CT scans reveal that the two sets of foramina appear to be connected by two canals that pass through the center of the vertebral centrum. This raises the question as to what occupied the canals in the living animal, with vascular tissue coming to mind.
The vascular system in fossil vertebrates is hard to reconstruct because blood vessels such as arteries and veins as well as the heart are not preserved in fossils (see Maldanis et al., 2016, for an exception). In addition, osteological correlates for features of the vascular systems in fossil reptiles remain little studied (Schwarz et al., 2007, p. 181), particularly outside the head. Some basic principles apply, though, that aid in possibly identifying such correlates. In addition, an understanding of the development of the vascular system is important. During development, some arteries in the embryo become remodeled or resorbed, and during growth, bone will grow around arteries but arteries will not lead to bone resorption. This is seen also in the structure of the human skull bone. Note that this is unlike the situation in postcranial skeletal pneumaticity in dinosaurs including birds, where respiratory tissue invades the interior of bone by inducing bone resorption (Wedel, 2009), a process that continues throughout ontogeny.
At face value, subcentral foramen is a descriptive term for any foramen on the ventral side of a vertebral centrum. However, there are different vascular structures that may have occupied a subcentral foramen. First, the foramina could each have housed a normal nutrient blood vessel pair, consisting of an artery which enters the bone, delivering the oxygenated blood to the interior of the bone, and a vein draining the bone interior. This is the classical situation seen in long bones with a single large nutrient canal (e.g., Seymour et al., 2012; Nakajima et al., 2014) through which a terminal artery, known as arteria nutricia, enters and then ends inside the bone. Since osteogenesis of the vertebral centrum follows the same rules as that of a long bone, this is a plausible hypothesis for the ventral foramina, as recognized by Storrs (1991). The pairing would then be due to bilateral symmetry of the centrum. The second hypothesis would be that the foramina are the entries for arteries which traverse the vertebral centrum in a dorsoventral (or vice versa) direction. These could develop in two different fashions. The arteries could either have been initially located laterally to the vertebral anlage and subsequently been incorporated into the centrum by the growth expansion of the centrum, as has been described in the posterior caudal and fluke vertebrae of whales by Slijper (1939). Alternatively, they could represent persisting intersegmental arteries which develop in the early embryo and are primarily located within the paraxial mesoderm, first between adjacent somites and later, after somite re-segmentation, inside the vertebral anlage.
Development of intersegmental arteries is seen in all vertebrates at an early ontogenetic stage. At the onset of the development of the axial skeleton in vertebrate embryos, in a process called somitogenesis, primary segments form in craniocaudal sequence within the paraxial mesoderm (Benazeraf and Pourquie, 2013). These segments, which are formed synchronously on either side of the neural tube and the notochord, are called somites. While the newly formed somites are epithelial spheres, they subsequently undergo several steps of differentiation to form their tissue derivatives, which include axial skeleton, skeletal muscle, and connective tissue of the trunk. In amniotes, the ventral somite half becomes a mesenchymal mass of cells, the sclerotome, which gives rise to all elements of the vertebral column, including the ribs. The dorsal half, in contrast, forms the dermomyotomal epithelium, which again differentiates into the myotome giving rise to axial muscle and the dermatome giving rise to the connective tissue of the skin. A sub-compartment of the sclerotome, the syndetome, gives rise to vertebral ligaments (Brent et al., 2003) and another sub-compartment, the arthrotome, gives rise to intervertebral joints (Mittapalli et al., 2005; Christ et al., 2007).
Importantly, the somites do not represent the definitive segments of the vertebral column as seen in the individual vertebral bones. In a process called re-segmentation, the adjacent cranial and caudal halves of neighboring sclerotomes unite to give rise to a single vertebra, whereas intervertebral muscles and ligaments arising from the myotome and syndetome maintain the original somitic segmentation pattern. In other words, the derivative of a single somite is not a single vertebra, but a so-called motion segment, which includes two vertebral halves tethered together in a flexible fashion by muscles and ligaments. Without re-segmentation a mobile vertebral column would not be possible (Hall, 2015, chap. 16; Scaal, 2016).
Prior to re-segmentation, neighboring sclerotomes are separated by a pair of embryonic blood vessels called the intersegmental artery and vein, which are ventrally connected to the dorsal aorta and posterior cardinal vein, respectively. In a process which is not yet well understood, these vessels usually disappear or undergo remodeling during the re-segmentation process. While at trunk level, the segmental array of vessels is still visible in the adult as, e.g., intercostal vessels, the cervical intersegmental vessels are lost and likely form the vertebral artery and vein.
We hypothesize that in plesiosaurians the intersegmental arteries were retained in cervical vertebrae into the postembryonic stage. Thus, in plesiosaurians, the process of the obliteration of the cervical intersegmental arteries did not happen, and the intersegmental arteries stayed in position and remained functional, extending (following the direction of blood flow) through the center of the cervical vertebral centrum from the ventral surface of the centrum to the floor of the neural canal. Accordingly, we here propose a new term for the large, highly symmetrical paired foramina in plesiosaurian cervicals, i.e., intersegmental artery foramen (IAF), to obtain a more precise terminology in relation to its putative embryological origin. We differentiate between the ventral IAF (vIAF), which corresponds to the traditional subcentral foramen, and the dorsal IAF (dIAF) on the floor of the neural canal. The two foramina are connected by a canal running across the center of ossification of the vertebral centrum, the intersegmental artery canal (IAC). Blood flow in the intersegmental artery located in the IAC would have been from ventral to dorsal, the artery entering through the vIAF and exiting through the dorsal dIAF.
Our study of the internal structure of plesiosaur cervical centra is based on
a small but representative sample set. It includes a latest Triassic fetal
specimen and two Jurassic vertebrae from two different locations. The
Triassic fetal cervical is of uncertain systematic affinity and derives from
the newly discovered Rhaetian (latest Triassic) bone bed of Bonenburg,
Germany (Sander et al., 2016). The Bonenburg quarry exposes an unusually
thick stratigraphic section of Rhaetic sediments, including 11 m of dark
grey mudstones which contain three different bone beds (BB1 to BB3) of the
type known from SW England (Storrs, 1994) and southern Germany (Sander et
al., 2016). In BB 2, there are several finds of plesiosaur remains, including
about 20 isolated plesiosaur vertebrae with and without neural arch in a good
state of preservation, including the fetal centrum studied here. The specimen
can be assigned to Plesiosauria based on its platycoelous articular surfaces,
the ventral keel, and the large paired ventral and dorsal foramina. Similar
plesiosaur vertebrae are also known from Rhaetian bone bed localities in
France (Fischer et al., 2014) and England (Storrs, 1994). These Triassic
vertebrae can be subdivided into different morphotypes that presumably
represent different taxa (Sander et al., 2016), but the fetal centrum
currently cannot be assigned to any of these. In addition, we included the
cervical vertebrae of an articulated skeleton from the Bonenburg locality,
the only articulated Triassic plesiosaur skeleton (Wintrich et al., 2017;
Sander et al., 2016). The Jurassic vertebrae studied by us include one
isolated posterior cervical (SMNS 50845) of an indeterminate plesiosaur from
the Posidonienschiefer Formation (Toarcian, Lower Jurassic) of the famous
Holzmaden locality, Germany (see also O'Keefe, 2004) and a cervical vertebra
that is part of an articulated skeleton of
Finally, we used morphological data on cervical vertebral morphology from the literature, specifically character descriptions compiled for phylogenetic analysis (Benson and Druckenmiller, 2014). Therefore, we transformed the information in the phylogenetic character matrix, consisting of the character descriptions and character states, into the morphological information.
To test competing hypotheses regarding vascular features, i.e., nutrient
canals vs. intersegmental artery canals, the internal morphology of the
vertebral centra needs to be revealed, which can be done by
In the study of the IAC in plesiosaur vertebra, obviously an accurate plane of the section that will intersect the canal is crucial. This will be the transverse plane of the vertebral centrum (perpendicular to the body axis), passing through the center of ossification of the bone (Fig. 1). The proper plane can be detected easily if the floor of the neural canal and thus the dorsal IAF is visible in addition to the ventral surface of the centrum. Before sectioning, vertebra SMNS 50845 was molded and cast for reconstruction after sectioning. Next, the area of the surface trace of the plane of the section was covered by a removable epoxy putty (Technovit) to ensure a clean cut of the outer bone surface. Then, two cuts spaced about 5 mm apart were placed on either side of the plane of sectioning to obtain a thin slice of bone containing the IAC. After sectioning, the putty was removed from the bone surface and the gap in the bone was filled in with plaster, with the two halves of the bone being held in place by the mold.
The transverse slice of bone was then processed into a petrographic thin
section 50 to 80
Transversal histological thin section of the posterior cervical vertebra SMNS 50845 from Holzmaden. The left and the right canals appear to meet in the center of ossification (C). However, CT data from other vertebrae suggest that the canals do not meet in the center of ossification, and the apparent connection in this section is probably caused by bone resorption during the formation of the medullary cavity and by damage during grinding of the section.
Fetal vertebral centrum of a plesiosaur (LWL-MFN P 64372) from the
Rhaetian (latest Triassic) bone bed of Bonenburg (Germany).
The
We reconstructed a surface model of the scanned vertebrae with the program
Avizo 7.1.1. In order to process the data from the
In order to evaluate the distribution of the ventral vertebral foramina in plesiosaurs, we use published information. Our analysis was based on the phylogenetic character matrix of Benson and Druckenmiller (2014), with updates for this study. The matrix consists of 80 taxa from the Late Triassic to the Late Cretaceous and of 270 characters: the character description and character state description as well as the coding. Eight characters (141, 152, 156, 166, 177, 179, 187, 191) of the 270 characters deal with special aspects of vertebral morphology such as nutrient foramina, subcentral foramina, and the number of cervical vertebrae that have implications for the reconstruction of the plesiosaurian neck arterial system.
Based on the analysis of the phylogenetic character list, the cervical vertebrae of all plesiosaurian terminal taxa in the matrix have large, paired symmetrical foramina on the ventral side of the cervical vertebral centra, conforming to the definition of vIAF. In the dorsal vertebrae there is no evidence of subcentral or nutrient foramina. The absence/presence and possible morphology of ventral foramina is unknown in the transitional pectoral vertebrae, which we consider as part of the trunk because of a lack of sufficiently informative material and a lack of published descriptive information.
Both the ventral and the dorsal IAFs are part of character 156 of Benson and
Druckenmiller (2014): “Cervical vertebrae, subcentral foramina and foramina
on the dorsal surface of the centrum, within the neural canal”. This has
three states: “both absent (0); both present (1); dorsal foramina present,
but subcentral foramina very small or absent (2)”. Character 166 is also
relevant for this study in that it captures the presence of a midline keel or
rounded ventral ridge on the centrum. Beyond this, the shape of the ventral
keel and the size of the pits and foramina differ depending on taxon. We
observed that in all cervical vertebrae (with the exception of the
atlas–axis complex) from the Rhaetic bone beds of Bonenburg and France and
in some of the Early Jurassic plesiosaur cervicals (e.g., Benson et al.,
2012), there are paired deep ventral pits. At the bottom of the pits are the
vIAFs. The cervical vertebrae of the Triassic articulated skeleton (see
Wintrich et al., 2017) and the vertebrae of the indeterminate Jurassic
plesiosaur SMNS 50845 and of
All plesiosaur cervical vertebrae in this study show the dIAF on the floor of
the neural canal if this is exposed and not covered by sediment. The dIAFs
are not coded as separate characters in the Benson and Druckenmiller (2014)
matrix but only as part of character 156, as discussed above. dIAFs have
rarely been mentioned in morphological descriptions of plesiosaurian cervical
centra, as already noted. We observed that the dorsal IAFs are present in all
vertebrae personally examined for this study where the neural canal was
exposed. State 2 of character 156, “dorsal foramina present, but subcentral
foramina very small or absent”, is particularly interesting because it
correlates with state 0 of character 152, “number of cervical vertebrae”,
which is “< 15” cervical vertebrae (Benson and Druckenmiller,
2014, appendix S2). This state is seen in the most short-necked pliosaurs
Both histological sections and segmentation of
Plesiosaur vertebral foramina have been observed and described from so many taxa and have been used as characters in phylogenetic analyses that it is clear that they are a pervasive feature of plesiosaur cervicals (Storrs, 1991; O'Keefe, 2001; Benson and Druckenmiller, 2014; Wintrich et al., 2017), with the possible exception of the pliosaur-type forms (see above). Thus, we feel that our results are representative of all plesiosaur cervicals although we only investigated three specimens in detail. The course of the paired canals through the vertebral centrum would suggest that these structures originally housed continuous arteries traversing the vertebral centrum in ventrodorsal direction, which opens up the possibility that they contained persisting intersegmental arteries, not nutrient ones, which would have ended within the central region of the vertebra. Furthermore, the crossing of the vertebral centrum is a feature which we argue should originate at an early developmental stage. This is because in the case of nutritive canals, the vascular system does spread into bone tissue (as mentioned above), whereas in continuous blood vessels, the bone tissue grows around the vessels instead. It is also known that bone tissue cannot resorb or displace features of the vascular system such as arteries because osteoclasts only resorb mineralized surfaces (Hall, 2015, chap. 15). This suggests that the arteries were already present in the vertebral primordium at the stage in early development when the sclerotomes were re-segmented and, subsequently, the cartilage primordia of the centra of the vertebra were formed. As the primordium of the centrum grew and ossified, the arteries and with them the canals also enlarged in size. The divergence of the canals is explained by the retention of the homologous locations inside the centrum and on its surface as ventral and dorsal intersegmental foramina.
While posterior caudal and fluke vertebrae of extant whales have similar
canals piercing the vertebral centra and housing arteries (Slijper, 1939),
their morphology and origin is rather different, as described in detail by
Slijper (1939) and confirmed by a study of the tail segment of a complete
adult skeleton of the bottlenose dolphin
An understanding of the arteries crossing the primordium requires some
considerations of the embryonic development of the vascular system of the
head, neck, and body stem. In terms of the evolutionary patterns in the
framework of heterochrony, the retention of intersegmental arteries in
plesiosaurians would have to be considered a case of extreme paedomorphosis
(Alberch et al., 1979; McNamara, 1997). Also, regionalization of the body is
an important aspect to consider because the molecular boundary between the
neck and the trunk is distinct (Müller et al., 2010) and highly
conserved: the cervical column in the mouse, crocodile, and chicken shows
expression of
In the embryo, a paired primary dorsal aorta differentiates by vasculogenesis and is located underneath the paraxial mesoderm. The primary dorsal aortae gradually change position from lateral to medial. Eventually, both dorsal aortae fuse in the midline of the embryo ventral to the notochord, which leads to the formation of a single large median aorta (Wiegreffe et al., 2007; Garriock et al., 2010). Initially, the intersegmental arteries branch off in dorsal direction from the paired dorsal aortae, passing in between the sclerotomes before re-segmentation. Their subsequent development is not well studied. In the trunk at thoracic levels, they relocate laterally to form the intercostal arteries. In the neck, they seem to obliterate in their proximal part during re-segmentation, whereas their distal part outside the vertebral centra fuses with neighboring segments to form the vertebral artery (Arey, 1924, p. 212).
Importantly, we found evidence for intersegmental artery retention only in
the cervical vertebral centra, not in the dorsal vertebral centra. Thus, if
plesiosaurians retained intersegmental arteries, then the question arises as
to which vessels these intersegmental arteries were connected to. As
mentioned above, in principle the intersegmental arteries in extant embryos
arise from the paired aortae. In the neck, however, they form longitudinal
anastomoses which give rise to the aorta vertebralis, while the connections
to the dorsal aorta become obliterated. In snakes like
We shall now evaluate the hypotheses explaining why plesiosaurians did not resorb the intersegmental arteries, retaining the embryonic vascular system. The first hypothesis involves developmental constraints linked to the uniquely high number of cervicals in plesiosaurs (the low number of pliosaur-type plesiosaurs being secondarily derived). This, like any other hypothesis explaining the persistence of intersegmental arteries, has to be consistent with the lack of IAF in the dorsal and presumably pectoral vertebrae, the numbers of which are not unusually high in plesiosaurians compared to other amniotes (Müller et al., 2010; Coffin and Poole, 1988).
The uniquely high number of cervical vertebrae means that in the
plesiosaurian embryo there was also a uniquely high number of cervical somites and
sclerotomes. As noted above, no other vertebrate group evolved such an
enormously long neck via an increase in the number of segments, i.e.,
vertebrae (Müller et al., 2010). A model for understanding the
development of the very high number of cervical segments in plesiosaurians
might be the segmentation process in snakes, that have evolved very high
numbers of dorsal segments. There, it has been shown that the molecular
mechanisms of somitogenesis are principally the same as in vertebrates with
lower segment numbers, but that somitogenesis proceeds much faster leading to
initially smaller somites which, however, later on grow to a normal size
relative to the size of the snake species concerned (Gomez et al., 2008). In
snakes, the extremely high number of dorsal vertebrae (“precloacal” in
morphological terminology) correlates with a corresponding extension the
expression of thorax-specific
Furthermore, we do not know if plesiosaurians developed paired vertebral arteries arising from the aorta in addition to retaining the intersegmental arteries. These vertebral arteries would have extended along (?) the vertebral centrum, with nutrient arteries branching off and vascularizing the vertebral body through lateral nutrient foramina as seen in mammals (Rothman and Simeone, 1975). Such lateral nutrient foramina are common in marine mammals but differ from the vIAF of plesiosaurians in their smaller size, larger number, and asymmetrical irregular placement.
In the tuatara,
The probable persistence of intersegmental arteries and the possible presence
of vertebral arteries in the plesiosaurian neck raise the question of the
function and adaptive value of these features. Several advantages can be
hypothesized, beginning with what is known in the few extant amniotes that
seemingly retain intervertebral arteries. In the tree-climbing rat snake
Other functional hypotheses explaining the retention of intersegmental arteries related to deep diving involve the protection from compression of the blood vessels by their location in canals in the vertebrae. If there were anastomoses with the vertebral arteries, an increase in the number of segments would mean more anastomoses and again greater transport capacity. Other, as yet less easily hypothesized advantages might be related to the compression of the upper respiratory and digestive tracts. Hypotheses involving a long neck and high cervical vertebral numbers invite future tests based on the comparison with the cervical vertebral column of short-necked plesiosaurian (i.e., pliosaur-type) that evolved several times in the history of plesiosaurians, together with the seeming loss of ventral IAF (see phylogenetic data matrix in Benson and Druckenmiller, 2014).
As discussed above, IAFs are a unique character of plesiosaurians. However,
it is not only plesiosaurs that have paired foramina on the ventral side of
their cervical vertebrae. The non-plesiosaurian pistosauroids
Since available evidence suggests that sauropterygians originated in the
Tethys (Neenan et al., 2013) and all other Triassic pistosauroids are known
from this realm (Benson et al., 2012), the ancestors of
Plesiosaurians cervical vertebrae bear a peculiar set of bilaterally paired foramina on their ventral side, matched by paired foramina on the floor of the neural canal. CT scanning, thin sectioning, and the observation of fracture surfaces reveals that the foramina on each side are connected by a canal that passes through the center of ossification of the vertebral centrum. The foramina and canals thus did not house nutritive blood vessels supplying the center of the bone but must have contained blood vessels that entered ventrally and exited dorsally. The location of the canals in the anteroposterior middle of the centra, their high bilateral symmetry, and their course through the center of ossification suggests that the blood vessels contained in the canals represent an embryonic vascular feature, the intersegmental arteries that persisted into the adult. The plesiosaurian intersegmental arteries became incorporated into the primordium of the vertebral centrum during re-segmentation in the embryonic axial skeleton and thus were not resorbed, unlike in almost all other amniotes. The persistence of the intersegmental arteries is correlated to, and presumably linked with, the uniquely high number of cervical vertebrae, stiffening of the neck, and increased pelagic adaptation in plesiosaurs compared to non-plesiosaurian sauropterygians. Possible adaptive advantages of the persistent intersegmental arteries must be sought in deep diving and in thermoregulation in the neck.
All data needed to evaluate the conclusions in the paper are present in the paper. Additional data related to this paper may be requested from the authors.
The specimens and thin sections on which this study is based are reposited in the following institutions, here listed with their abbreviations: LWL-MFN – LWL- Museum für Naturkunde, Muünster, Germany; SMNS – Staatliches Museum für Naturkunde, Stuttgart, Germany; STIPB – Steinmann Institute Paleontology Collection, University of Bonn, Bonn, Germany.
The authors declare that they have no conflict of interest.
This article is part of the special issue “Secondary adaptation of tetrapods to life in water – Proceedings of the 8th International Meeting, Berlin 2017”. It is a result of the 8th International Meeting on the Secondary Adaptation of Tetrapods to Life in Water, Berlin, Germany, 3–8 April 2017.
First and foremost we thank Michael Mertens of Schwaney (North Rhine-Westphalia, Germany) for his untiring efforts in collecting marine reptiles from the Rhaetian bone beds of Bonenburg and facilitating their transfer to the LWL-MFN collections. We thank Olaf Dülfer (Bonn) for help with specimen preparation, Georg Oleschinski (Bonn) for photography, and Rico Schellhorn (Bonn) for help with illustrations and discussion. Reviews by Alexandra Houssaye and two anonymous reviewers are gratefully acknowledged. This project was funded by the Deutsche Forschungsgemeinschaft (DFG, grant number SA 469/47-1) and by the LWL-Museum für Naturkunde (Münster, Germany) through the archeological and paleontological heritage mitigation scheme of the State of North Rhine-Westphalia. Edited by: Florian Witzmann Reviewed by: Alexandra Houssaye and two anonymous referees