Journal of Iberian Geology (2019) 45:301–316 https://doi.org/10.1007/s41513-018-0072-4 RESEARCH PAPER Morphology and preliminary biomechanical interpretation of mandibular sutures in Metoposaurus krasiejowensis (Temnospondyli, Stereospondyli) from the Upper Triassic of Poland Kamil Gruntmejer1,2 · Dorota Konietzko‑Meier1,3 · Adam Bodzioch1 · Josep Fortuny4,5 Received: 23 September 2017 / Accepted: 1 June 2018 / Published online: 3 July 2018 © The Author(s) 2018 Abstract The morphology of the mandibular sutures in the Late Triassic temnospondyl Metoposaurus krasiejowensis has been exam- ined in order to determine their role in mandible biomechanics. Until now, no histological studies of mandibular sutures in extinct vertebrates were performed, in contrast to cranial sutures. As a consequence, mandibular suture interpretations herein are based mainly on comparisons with previous studies of cranial sutures and with 3D cranial finite element analysis of this species. A total of 32 standard thin sections were studied under standard petrographic microscope observations in order to differentiate the morphology of mandibular sutures. Five mandibular suture types are present in this taxon: interdigitated, shallowly interdigitated, overlapping, tongue and groove and abutting. Based on previous work, it has generally been assumed that the shallowly interdigitated, tongue, groove and abutting suture types are associated with tension, the interdigitated type with compression and the overlapping type with absorption and counteraction of variable loads. The sutures associated with tension occur mainly in the anterior part of the mandible, principally in the dentary; overlapping sutures have been noted in medial portions of the mandible and sutures associated with compression mainly in posterior portions, i.e., in the angular and prearticular. The variability of suture types along the mandible suggests a complex loading regime of compression and tension. Sutures associated with tension and a flexible symphysis potentially allowed an increase of oral volume during gape opening, whereas sutures associated with compression represent adaptations for strong bite forces. Keywords Temnospondyli · Metoposaurus · Mandible · Sutures · Biomechanics Resumen Se ha examinado la morfología de las suturas mandibulares del temnospóndilo del Triásico Superior Metoposaurus krasie- jowensis para determinar su papel en la biomecánica mandibular. Hasta la fecha, no se han realizado estudios histológicos de las suturas mandibulares de vertebrados fósiles, en contraste con los estudios histológicos en suturas craneales. Como consecuencia, las interpretaciones sobre las suturas mandibulares están aquí basadas en la comparación con estudios previos en suturas craneales y con análisis 3D de elementos finitos para esta misma especie. En total 32 laminas delgadas estándares fueron estudiadas con observaciones de microscopio petrográfico con el fin de diferenciar la morfología de las suturas mandibulares. Cinco tipos de suturas mandibulares son presentes en este taxón: interdigitales, levemente interdigitales, superposición, lengua, ranura y lindante. En base a estudios previos, se ha asumido generalmente que las suturas levemente interdigitales, lengua, ranura y lindantes se asocian con cargas de tensión, mientras que las de tipo interdigitales se asocian con compresión y el tipo sutural de superposición con distintas cargas de absorción y neutralización. Las suturas asociadas con tensión ocurren mayormente en la parte anterior de la mandíbula, principalmente en el dentario; las suturas de super- posición se han encontrado las porciones mediales de la mandíbula y las suturas asociadas con compresión se han encontrado mayormente en las porciones posteriores, por ejemplo, en el angular y el prearticular. La variabilidad de los tipos suturales a lo largo de la mandíbula sugiere un complejo régimen de cargas de compresión y tensión. Suturas asociadas con tensión y una sínfisis flexible potencialmente permitieron un incremento del volumen oral durante la abertura bucal, mientras que las suturas asociadas con compresión representan adaptaciones a fuertes fuerzas de mordida. Extended author information available on the last page of the article 13 Vol.:(0123456789) 302 Journal of Iberian Geology (2019) 45:301–316 Palabras clave Temnospondyli · Metoposaurus · mandíbula · suturas · biomecánica 1 Introduction et al. 2011, 2012, 2016; Marcé-Nogué et al. 2015). Recently, FEA studies of the European Metoposaurus krasiejowensis With the exception of the small-sized taxon Apachesaurus, and the North American Apachesaurus gregorii have dem- metoposaurids were large, around 2–3-m-long, aquatic tem- onstrated that these temnospondyls were able to perform nospondyl amphibians with dorso-ventrally flattened bod- at least two types of biting, i.e., lateral biting utilized for ies and large and parabolic skulls (Hunt 1993; Schoch and active hunting during swimming, and bilateral biting for Milner 2000). The most characteristic anatomical features ambush hunting (Fortuny et al. 2017; Konietzko-Meier et al. of the skull were the anterolateral position of the orbits 2018). However, all conclusions were based solely on analy- (Hunt 1993). Metoposaurids had a cosmopolitan distri- sis of the skull. No similar functional morphology studies bution during the Late Triassic. Skeletal remains of these of mandibles have been performed, with the exception of temnospondyls are known from North America (Koskinono- Sulej (2007) and the description of the mandibular denti- don and Apachesaurus; Hunt 1993), North Africa (Dutui- tion of Konietzko-Meier and Wawro (2007). Sulej (2007) tosaurus ouazzoui and Arganasaurus lyazidi; Dutuit 1976; described the presence of paired mentomandibular cartilage Hunt 1993), Madagascar (Dutuit 1978), India (Phantasau- that connected the rami of the mandibles. The non-ossified rus maleriensis; Chowdhury 1965, Sengupta 1992, 2002; junction allowed ventral bending of the mandibular rami Chakravorti and Sengupta 2016) and from Europe, includ- during opening of the mouth. Later, Konietzko-Meier and ing the following species: Metoposaurus diagnosticus (von Wawro (2007) indicated the presence of sharp edges on teeth Meyer 1842), Metoposaurus krasiejowensis– previously which confirmed the ability for biting. Detailed studies of recognised as a subspecies, Metoposaurus diagnosticus structures of sutures, of bone histology and interpretations krasiejowensis (see Sulej 2002), and Metoposaurus algar- of biomechanics based on finite element analysis are not vensis (Brusatte et al. 2015). Material of the Polish taxon available, not only for metoposaurids mandible, but gener- Metoposaurus krasiejowensis, recovered at Krasiejów, has ally among Temnospondyli. Most descriptions of mandibles been examined largely osteologically and histologically focus on the localisation of the sutures and a general descrip- (Dzik et al. 2000; Sulej 2002, 2007; Dzik and Sulej 2007; tion of jaw morphology, but identifications of the nature and Konietzko-Meier and Wawro 2007; Gruntmejer 2012; Koni- type of the inner suture are very rare. In most cases, their etzko-Meier and Klein 2013; Konietzko-Meier and Sander architecture along the bones is described, but not across the 2013; Konietzko-Meier et al. 2013, 2014; Brusatte et al. bone (e.g., Jupp and Warren 1986; Kathe 1995, 1997; Bolt 2015; Gruntmejer et al. 2016; Konietzko-Meier et al. 2018; and Chatterjee 2000; Ruta and Bolt 2008; Polley and Reisz Teschner et al. 2018). However, quite of lot of unexplained 2011; Porro et al. 2015). Only Dutuit (1976) illustrated a issues surrounding the ecology and feeding of these ani- cross section of the posterior part of the mandible of Dutui- mals remain. Previously, Metoposaurus was considered as tosaurus ouazzoui, focusing on the articulation between the an ambush predator, waiting for prey at the bottom of bodies skull and mandible; however, no detailed information on the of water (Ochev 1966; Murry 1989). Later, the capability of structure of the suture was provided. active swimming was considered to suggest that the feeding behaviour in metoposaurids was similar to that of extant 1.1 Sutures: morphology, types and function crocodilians and alligators (i.e., “mid-water feeder”) (Hunt in vertebrates 1993) and it was hypothesised that Metoposaurus was an active swimmer, using its limbs in the process (Sulej 2007). Absorption and dispersion of stress probably occurred A histological analysis of intercentra has recently postulated mainly during feeding behaviour and were directly related that the long and laterally flattened tail was the main propul- with cranial and mandibular sutures. These structures are sion organ during swimming (Konietzko-Meier et al. 2013). fibrous joints composed of collagen fibres that connect From a different point of view, food acquisition has been dis- adjacent bones and provide biomechanical and growth func- cussed by different authors. Dzik et al. (2000) proposed that tions (Jasinoski and Reddy 2012). The morphology of cra- prey was captured by suction, whereas 3D-computational nial sutures in extinct non-amniotes (fish and amphibians) finite element analysis (FEA) of large temnospondyl taxa holds valuable data for our understanding of cranial function (e.g., capitosaurids) has revealed that these animals were during feeding (Markey et al. 2006). Most studies of the active hunters, able to attack their prey by direct biting dur- mechanical role of cranial sutures were conducted as in vivo ing swimming as well. It is because of the limited compari- stress measurements across sutures in extant vertebrates sons with extant taxa and demonstrating the peculiar ecolog- such as mammals, for example, Sus scrofa (Rafferty and ical niche occupied by gigantic temnospondyl taxa (Fortuny Herring 1999) and actinopterygian fish such as Polypterus 13 Journal of Iberian Geology (2019) 45:301–316 303 endlicherii (Markey and Marshall 2007a). These two phy- dicynodonts Lystrosaurus declivis and Oudenodon bainii logenetically widely separated groups inhabit different envi- were also based on histological thin sections (Jasinoski et al. ronments, with a diverse spectrum of prey capture. Actinop- 2010b). Pioneer studies of the morphology and function of terygians obtain their food using a wide variety of methods, cranial sutures were those of Discosauriscus austriacus and including suction feeding, ram feeding, filter feeding and Onchiodon labyrinthicus (Kathe 1995, 1997). Markey and biting (Markey et al. 2006). In contrast, in terrestrial settings Marshall (2007a) compared cranial suture morphology and almost all vertebrates (mammals, reptiles and amphibians) its function in the extant Polypterus endlicherii, the Devo- use practically a single technique of feeding, i.e., biting or, nian Acanthostega gunnari and Eusthenopteron foordi and in herbivores, chewing. Despite these differences, sutures the Early Permian Phonerpeton pricei. Their goal was to in fish and mammals exhibit closely similar stress patterns evaluate at what moment in the fish-tetrapod transition suc- (Markey and Marshall 2007a). The interdigitated suture is tion feeding evolved into direct biting on prey. Their study characteristic of skull regions that experience high compres- revealed that suction feeders were characterised mainly by sive loads, while shallowly interdigitated, abutting (or butt- sutures associated with tension anteriorly and sutures associ- ended) and tongue-and-groove sutures are associated with ated with compression posteriorly, whereas animals capable tension (Jasinoski et al. 2010a, b). The overlapping (or scarf) of direct biting mostly showed only sutures associated with sutures represent a morphological compromise, which can compression (Markey and Marshall 2007b). accommodate both tensile and compressive stresses (Mar- In a similar manner to those studies, the morphology key et al. 2006). Porro et al. (2015) distinguished a similar and assumed function of cranial sutures in the Late Triassic sutural morphology and biomechanical function in the skull temnospondyl Metoposaurus krasiejowensis were studied of the Devonian Acanthostega gunnari. According to those histologically (Gruntmejer 2012). The presence of interdigi- authors, butt joints and tongue-and-groove joints are associ- tated sutures, which counteract compression loads, along ated with tension, the interdigitated sutures with compres- the entire skull of Metoposaurus, may indicate direct biting sion. In contrast to Markey et al. (2006), the scarf joints were on prey. Markey and Marshall (2007b) proposed the same defined as having been adapted to resist torsion and shear way of feeding (biting) in Acanthostega gunnari. Data on (Porro et al. 2015). the feeding behaviour in Acanthostega gunnari have been Moreover, the presence and arrangement of collagen undermined following a 3D-computational analysis of their fibres along the sutural edges also have a significant impact skull anatomy (Porro et al. 2015). Those studies revealed on stress distribution (Rafferty and Herring 1999; Herring that the differentiation of sutural morphology in the skull and Teng 2000). In interdigitated sutures, which experience of Acanthostega gunnari was more consistent with suction compression, the fibres are oriented obliquely in the direc- feeding, rather than with biting (Porro et al. 2015). Fortuny tion of the apex of the interdigitation, while in shallowly et al. (2015) proposed a correlation of cranial sutural func- interdigitated sutures, which experience tension, the fibres tion with biomechanical results derived from finite element radiate outwards at the apex of the interdigitation, and some analysis (FEA) on the extant Chinese giant salamander, fibres have an oblique arrangement along the straight limbs Andrias davidianus, documenting the role of sutures to dis- of the sutural interdigitation (Rafferty and Herring 1999; sipate stress during feeding. Herring and Teng 2000; Jasinoski et al. 2010a). The pres- However, mandibular sutures and their biomechanical ence of well-mineralised Sharpey’s fibres on the sutural function in temnospondyls are still unknown and no taxa edges is a good indicator for differentiating these two types have been analysed to date. Similar to the skull, the mandi- of sutural morphologies (Jasinoski et al. 2010b), and deter- ble of Metoposaurus krasiejowensis is a conglomerate of ten mine which bones contacts underwent compression or ten- bones (dentary, splenial, postsplenial, angular, surangular, sion. Moreover, the occurrence of Sharpey’s fibres is not articular, prearticular, coronoid, intercoronoid, precoronoid) limited to sutural edges. These structures indicate the point that are adapted to resist various loads during feeding (Jupp of attachment of skin, ligaments and skeletal muscles into and Warren 1986). Among non-amniote, extinct tetrapods, the bone (Francillon-Vieillot et al. 1990). Sharpey’s fibres sutures and their biomechanical implications for the lower are very numerous in the skull bones of Metoposaurus jaw have only been studied in the Devonian Acanthostega krasiejowensis, but are short and thin (Gruntmejer et al. gunnari (Neenan et al. 2014; Porro et al. 2015). The mandi- 2016; Konietzko-Meier et al. 2018), whereas they are much bles of extinct taxa have been sectioned/histologically sam- thicker and longer in the mandible (Gruntmejer 2015). pled (e.g., Carroll 1964; Heaton 1979; Haridy et al. 2017a, Previous studies that focused on cranial sutures relied on in press) but without a similar treatment or level of detailed correlations of sutural morphology and related biomechani- study to that presented here. cal function among extant animals, using quantitative and computational research methodologies. Detailed descrip- tions of cranial suture morphology and its function in the 13 304 Journal of Iberian Geology (2019) 45:301–316 1.2 Pursued goals Sutures play an important role in skull/mandible biomechan- ics. For this reason it is important to recognise the nature and function of the sutures along the lower jaw, not only on the morphological level, but also on the histological one. The main goal of the present study is to investigate, for the first time, mandibular sutural morphology in the Late Triassic temnospondyl Metoposaurus krasiejowensis using histologi- cal thin sections. Comparisons of mandibular sutural mor- phology in three specimens of Metoposaurus krasiejowensis are made in order to assess the variability of sutural typology along the entire mandible. Based on comparisons of suture morphology, interpretative functions of the mandibular sutures are proposed. 2 Materials and methods 2.1 Material and geological setting The bony material used in the present study comes from the Upper Triassic bone bed at Krasiejów (southwest Poland). Disarticulated skeletal remains of large vertebrates (fishes, temnospondyls and archosaurs) occur in two horizons (Dzik and Sulej 2007; Sulej 2007; Gruszka and Zieliński 2008; Bodzioch and Kowal-Linka 2012). The stratigraphical age of the Upper Silesian Keuper is still a matter of debate. Strati- graphical data indicate that the bone bed at Krasiejów was deposited during the early Norian (Racki and Szulc 2014; Szulc et al. 2015a, b), whereas biochronological data suggest a late Carnian age (Dzik and Sulej 2007; Lucas et al. 2007; Lucas 2015). Fig. 1  Mandibles of Metoposaurus krasiejowensis (UOPB 01027, Three mandibles of Metoposaurus krasiejowensis (all in UOPB 01144 and UOPB 01145) from the Upper Triassic of Poland, the collections of Opole University, Department of Biosys- and schematic drawings with marked locations of sectioning planes. The colour grey is used to indicate preserved parts of the mandible; tematics, Laboratory of Palaeobiology; abbreviation: UOPB) damaged or matrix-covered regions are shown in light yellow. Scale have been studied histologically. UOPB 01145 (38 cm in bar equals 50 mm. An angular, Ar articular, C coronoid, D dentary, length) is a complete, well-preserved left ramus (Fig. 1), Ic intercoronoid, Par prearticular, Pc precoronoid, Psp postsplenial, while UOPB 01144 (9 cm in length) is a small piece of the Sp splenial, fma anterior Meckelian foramen, fmp posterior Meckelian foramen symphysial part of the left ramus and UOPB 01027 (34 cm in length) is a near-complete right hemimandible, albeit poorly preserved. standard petrographic procedures to a thickness of about 60–80 µm (Chinsamy and Raath 1992) at the Institute of 2.2 Methods Geology, Adam Mickiewicz University (Poznań, Poland). Qualitative observations on mandibular sutures in Metopo- Three mandibular rami of Metoposaurus krasiejowensis saurus krasiejowensis were made using a LEICA DMPL were studied in order to obtain information on the structure light microscope in plane and cross polarised light in order of sutures, visible on the surface and in the cross sections. to differentiate their morphology. Schematic illustrations in In total, 32 thin sections were studied histologically, 20 of cross sectional view of all sutural morphologies recognised UOPB 01145, seven of UOPB 01144 and the remaining in the mandible of Metoposaurus krasiejowensis are illus- five of UOPB 01027 (Fig. 1; Table 1). Overall, in thin sec- trated in Fig. 2. In cross section, the abutting suture is a tions, a total of 93 sutures were visible and histologically contact between two relatively vertical edges of adjacent analysed (Table 2). Thin sections were prepared following bones (Fig. 2a). The interdigitated suture is characterised by 13 Journal of Iberian Geology (2019) 45:301–316 305 Table 1  The mandibular sutures Sutures Anatomical Number of Number of sutures examined in individual analyzed in Metoposaurus abbreviations samples specimens krasiejowensis from the Late Triassic of Poland UOPB 01145 UOPB 01144 UOPB 01027 Angular-dentary An-D 7 6 – 1 Angular-postsplenial An-Psp 6 5 – 1 Angular-prearticular An-Par 6 5 – 1 Angular-surangular An-Sa 6 6 – – Articular-prearticular Ar-Par 3 2 – 1 Articular-surangular Ar-Sa 3 2 – 1 Coronoid-dentary C-D 7 6 – 1 Coronoid-postsplenial C-Psp 3 2 – 1 Coronoid-prearticular C-Par 6 6 – – Dentary-intercoronoid D-Ic 6 3 2 1 Dentary-postsplenial D-Psp 1 – – 1 Dentary-precoronoid D-Pc 6 2 3 1 Dentary-splenial D-Sp 14 6 7 1 Dentary-surangular D-Sa 2 2 – – Intercoronoid-postsplenial Ic-Psp 1 – – 1 Intercoronoid-splenial Ic-Sp 5 3 2 – Postsplenial-splenial Psp-Sp 5 3 2 – Precoronoid-splenial Pc-Sp 6 2 3 1 complex and numerous deep interdigitating processes, where or compression (Markey et al. 2006; Jasinoski et al. 2010a) the adjacent bony edges dovetail into each other (Fig. 2b), or torsion and shearing (Porro et al. 2015). while the shallowly interdigitated suture is characterised by low interdigitating processes (Fig. 2c). Moreover, the ori- entation of Sharpey’s fibre arrangements on sutural edges is 3 Results useful to distinguish these two latter sutural morphologies (see above). The tongue-and-groove suture is characterised 3.1 Description of mandibular sutural morphology by insertion of one bone into a groove of another (Fig. 2d). in Metoposaurus krasiejowensis In the overlapping suture, the surfaces of adjacent bones greatly overlap each other without interdigitation (Fig. 2e). 3.1.1 Externally visible sutures We used thin sections with a large number of samples, combined with observations of suture morphology in super- Mandibular sutures between individual bones were exter- ficial views. The advantage of this method is that histologi- nally discernible on the surface of the mandible (Fig. 3a–g). cal details can be determined, such as orientation of collagen Sutural traces disappear in some places where the mandibles fibres, that normally are not visible in digital imaging. (especially in UOPB 01145) are covered by claystone matrix Based on previous studies of cranial sutures in extant (Fig. 3a, f). Over the entire length of all analysed specimens, and extinct vertebrates (Rafferty and Herring 1999; Markey the external suture morphology appears as a straight-line et al. 2006; Markey and Marshall 2007a, b; Jasinoski et al. connection between adjacent bones. The morphology of 2010b; Porro et al. 2015), it was assumed that the biome- each suture is constant and usually does not change along the chanical function of each sutural type could be correlated contact between individual bones, the sole exception being with the corresponding suture type in the mandible. Accord- the upper area of the coronoid-prearticular suture on the ingly, interdigitated sutures of the mandible in Metoposau- lingual side where the straight trace of this suture becomes rus krasiejowensis are herein associated with compression interdigitated (Fig. 3d). The coronoid-intercoronoid joint (Rafferty and Herring 1999; Markey et al. 2006; Markey and (Fig. 3b) and dentary-surangular suture (Fig. 3f) are visible Marshall 2007a, b; Jasinoski et al. 2010b; Porro et al. 2015), as a tongue-and-groove connection. whereas the shallowly interdigitated, tongue-and-groove and abutting sutures are associated with tension (Markey et al. 2006; Jasinoski et al. 2010b; Porro et al. 2015) and the overlapping counteracted variable loads, i.e., with tension 13 306 Journal of Iberian Geology (2019) 45:301–316 Table 2  Comparison of sutural morphology and its predicted stress resistance among three specimens Suture Specimen Number of sections Morphology Sharpey’s fibres Predicted stress An-D UOPB 01145 22, 23, 26, 27, 28, 29 Overlapping Partly visible, oriented almost perpendicular Variable stresses An-D UOPB 01027 1d Overlapping Partly visible, oriented almost perpendicular Variable stresses An-Psp UOPB 01145 22, 23, 26, 27, 28 Interdigitated Well-visible, oblique oriented Compression An-Psp UOPB 01027 1d Interdigitated Well-visible, oblique oriented Compression An-Par UOPB 01145 32, 34, 36, 39, 41 Interdigitated Well-visible, oblique oriented Compression An-Par UOPB 01027 1f Interdigitated Well-visible, oblique oriented Compression An-Sa UOPB 01145 31, 32 Overlapping Partly visible, oriented almost perpendicular Variable stresses An-Sa UOPB 01145 34, 36, 41, 44 Interdigitated Well-visible, oblique oriented Compression Ar-Par UOPB 01145 41, 43 Abutting Well-visible, variable oriented Tension Ar-Par UOPB 01027 1e Abutting Well-visible, variable oriented Tension Ar-Sa UOPB 01145 41, 43 Abutting Well-visible, variable oriented Tension Ar-Sa UOPB 01027 1e Abutting Well-visible, variable oriented Tension C-D UOPB 01145 22, 23 Tongue and groove Poorly visible, orientation difficult to determine Tension C-D UOPB 01145 26, 27, 28, 29 Shallowly interdigitated Partly visible, slightly oblique oriented Tension C-D UOPB 01027 1d Tongue and groove Poorly visible, orientation difficult to determine Tension C-Par UOPB 01145 26 Interdigitated Well-visible, oblique oriented Compression C-Par UOPB 01145 27, 28, 29 Overlapping Partly visible, oriented almost perpendicular Variable stresses C-Par UOPB 01145 31, 32 Interdigitated Well-visible, oblique oriented Compression C-Psp UOPB 01145 22 Overlapping Partly visible, oriented almost perpendicular Variable stresses C-Psp UOPB 01145 23 Interdigitated Well-visible, oblique oriented Compression C-Psp UOPB 01027 1d Interdigitated Well-visible, oblique oriented Compression D-Ic UOPB 01145 14 Shallowly interdigitated Partly visible, slightly oblique oriented Tension D-Ic UOPB 01145 17, 18 Tongue and groove Poorly visible, orientation difficult to determine Tension D-Ic UOPB 01144 6, 7 Tongue and groove Poorly visible, orientation difficult to determine Tension D-Ic UOPB 01027 1c Tongue and groove Poorly visible, orientation difficult to determine Tension D-Psp UOPB 01027 1c Overlapping Visible, oriented almost perpendicular Variable stresses D-Pc UOPB 01145 8, 10 Shallowly interdigitated Partly visible, slightly oblique oriented Tension D-Pc UOPB 01144 3, 4, 5 Shallowly interdigitated Partly visible, slightly oblique oriented Tension D-Pc UOPB 01027 1a Shallowly interdigitated Partly visible, slightly oblique oriented Tension D-Sa UOPB 01145 31, 32 Shallowly interdigitated Partly visible, slightly oblique oriented Tension D-Sp UOPB 01145 4, 8, 10, 17, 18 Shallowly interdigitated Partly visible, slightly oblique oriented Tension D-Sp UOPB 01145 14 Tongue and groove Poorly visible, orientation difficult to determine Tension D-Sp UOPB 01144 1, 2, 3, 4, 5, 6, 7 Interdigitated Well-visible, oriented almost perpendicular Compression D-Sp UOPB 01027 1a Shallowly interdigitated Partly visible, slightly oblique oriented Tension Ic-Psp UOPB 01027 1c Interdigitated Well-visible, oblique oriented Compression Ic-Sp UOPB 01145 14 Shallowly interdigitated Partly visible, slightly oblique oriented Tension Ic-Sp UOPB 01145 17, 18 Interdigitated Well-visible, oblique oriented Compression Ic-Sp UOPB 01144 6, 7 Shallowly interdigitated Partly visible, slightly oblique oriented Tension Pc-Sp UOPB 01145 8, 10 Shallowly interdigitated Partly visible, slightly oblique oriented Tension Pc-Sp UOPB 01144 3 Shallowly interdigitated Partly visible, slightly oblique oriented Tension Pc-Sp UOPB 01144 4, 5 Interdigitated Well-visible, oblique oriented Compression Pc-Sp UOPB 01027 1a Abutting Poorly visible, orientation difficult to determine Tension Psp-Sp UOPB 01145 14 Interdigitated Well-visible, oblique oriented Compression Psp-Sp UOPB 01145 17, 18 Shallowly interdigitated Partly visible, slightly oblique oriented Tension Psp-Sp UOPB 01144 6, 7 Interdigitated Well-visible, oblique oriented Compression 3.1.2 Sutures visible in cross sections interdigitated, overlapping, tongue and groove and abutting (Table 2, Fig. 4). Five types of sutural morphology have been recognised Interdigitated sutures occur both on the labial and lin- in the mandible of this taxon: interdigitated, shallowly gual sides of the mandible (Fig. 4). On the lingual part, this 13 Journal of Iberian Geology (2019) 45:301–316 307 Fig. 2  Schematic profiles of different types of sutures rec- ognised in the mandible of the Metoposaurus krasiejowensis. a Abutting suture; b inter- digitated suture; c shallowly interdigitated suture; d tongue and groove suture; e overlap- ping suture Fig. 3  External traces of mandibular sutures visible on the lingual (a–d, g) and labial surface (e, f). Scale bar equals 50 mm. An angular, C coronoid, D dentary, Ic intercoronoid, Par prearticular, Pc precoronoid, Psp postsplenial, Sa surangula, Sp splenial type of suture occurs at the following contacts: precoronoid- can be observed at the dentary-splenial, angular-surangular splenial (Fig. 5a, b), intercoronoid-postsplenial, coronoid- (Fig. 5e) and angular-postsplenial contact (Fig. 5f). In some postsplenial, coronoid-prearticular, angular-prearticular samples (e.g., UOPB 01144), an interdigitated suture has (Fig. 5c, d) and angular-postsplenial. On the labial part, it been noted at the postsplenial-splenial contact (Fig. 5g, h). 13 308 Journal of Iberian Geology (2019) 45:301–316 Fig. 4  Photographs and schematic drawings of selected thin sec- digitated dentary-surangular suture; no. 41, interdigitated angular- tions of specimens UOPB 01145 (a) and UOPB 01027 (b). Scale prearticular suture, interdigitated angular-surangular suture, abutting bar equals 10 mm. a No. 14, shallowly interdigitated dentary-inter- articular-prearticular suture and abutting articular-surangular suture; coronoid suture, tongue and groove dentary-splenial suture, shal- b No. 1a, shallowly interdigitated dentary-precoronoid suture, shal- lowly interdigitated intercoronoid-splenial suture and interdigitated lowly interdigitated dentary-splenial suture and abutting precoronoid- postsplenial-splenial suture; no. 23, overlapping angular-dentary splenial suture; no. 1c, tongue and groove dentary-intercoronoid suture, interdigitated angular-postsplenial suture, tongue and groove suture, overlapping dentary-postsplenial suture and interdigitated coronoid-dentary suture and interdigitated coronoid-postsplenial intercoronoid-postsplenial suture; no. 1d, overlapping angular-dentary suture; no. 26, overlapping angular-dentary suture, interdigitated suture, interdigitated angular-postsplenial suture, tongue and groove angular-postsplenial suture, shallowly interdigitated coronoid-dentary coronoid-dentary suture and interdigitated coronoid-postsplenial suture and interdigitated coronoid-prearticular suture; no. 32, inter- suture; no. 1f, interdigitated angular-prearticular suture. no. number digitated angular-prearticular suture, overlapping angular-surangular of section suture, interdigitated coronoid-prearticular suture and shallowly inter- A shallowly interdigitated suture occurs over the entire angular-surangular (Fig. 6b), dentary-postsplenial (Fig. 6c), length of the dentary contact: dentary-splenial, dentary- coronoid-postsplenial and coronoid-prearticular contact. precoronoid (Fig. 5a, b), coronoid-dentary and dentary- Tongue and groove suture types have been recognised surangular. Shallowly interdigitated sutures have been noted only at the dentary contact: dentary-splenial, dentary-inter- additionally at the following contacts: precoronoid-splenial, coronoid (Figs. 5g, 6d, e) and coronoid-dentary. intercoronoid-splenial (Fig. 5g, h) and postsplenial-splenial. The abutting suture type occurs especially in the articular Overlapping types can be observed in the central part of the mandible: at the articular-surangular and articu- part of the mandible, at the angular-dentary (Fig. 6a), lar-prearticular contacts (Fig. 6f, g). Moreover, one sample 13 Journal of Iberian Geology (2019) 45:301–316 309 Fig. 5  Photographs and interpretative line drawing of the variable interdigitated angular-surangular suture; f UOPB 01145, no. 23, inter- morphology of selected sutures in specimens UOPB 01144 (a, b, digitated angular-postsplenial suture, g UOPB 01144, no. 6, tongue g, h), UOPB 01145 (c, e, f) and UOPB 01027 (d). Scale bar equals and groove dentary-intercoronoid suture, shallowly interdigitated 5 mm. a UOPB 01144, no. 4, shallowly interdigitated dentary-precor- intercoronoid-splenial suture and interdigitated postsplenial-splenial onoid suture and interdigitated precoronoid-splenial suture; b UOPB suture; h UOPB 01144, no. 7, shallowly interdigitated intercoronoid- 01144, no. 5, shallowly interdigitated dentary-precoronoid suture splenial suture and interdigitated postsplenial-splenial suture. An and interdigitated precoronoid-splenial suture; c UOPB 01145, no. angular, D dentary, Ic intercoronoid, Par prearticular, Pc precoronoid, 32, interdigitated angular-prearticular suture; d UOPB 01027, no. Psp postsplenial, Sa surangular, Sp splenial, no. number of section 1f, interdigitated angular-prearticular suture, e UOPB 01145, no. 34, (UOPB 01027) presents an abutting type of suture at the difficult to follow along all bony edges. Their orientation precoronoid-splenial contact. in the shallowly interdigitated type is radiating outwards at The presence of distinct and dense clumps of Sharpey’s the apex of the interdigitation. In abutting sutures, mainly fibres has been noted in all sutural edges (Table 2). The in the articular-prearticular (Fig. 7e; Table 2) and articular- longest and thickest fibres are present in the symphyseal surangular (Fig. 7f; Table 2), Sharpey’s fibres occur along region, and in the posterior part of the mandible, and they the entire sutural edges in very dense bundles, resembling are well visible at the following contacts: dentary-splenial, interwoven structural fibres (ISF). postsplenial-splenial, coronoid-postsplenial, angular- postsplenial and articular-prearticular sutures (Fig. 7a–f; 3.2 Sutural changes along the mandible Table 2). The inclination angle of Sharpey’s fibres in inter- digitated sutures varies, starting from near-perpendicular as External traces of mandibular sutures are well visible in the dentary-splenial (Fig. 7a; Table 2) to more oblique (especially in UOPB 01145) on the surface and indi- as in the postsplenial-splenial (Fig. 7b; Table 2), coronoid- vidual bones are easily differentiated (Fig. 3a–g). Over postsplenial (Fig. 7c; Table 2) and angular-postsplenial their entire length the sutural courses are straight and (Fig. 7d; Table 2). Moreover, interdigitated sutures show constant both on the labial and lingual side. Only in the the longest and most densely packed bundles of Sharpey’s upper part of the coronoid-prearticular contact, does the fibres, whereas in the tongue-and-groove, overlapping, and sutural morphology become interdigitated (Fig. 3d); in the shallowly interdigitated sutures these are very short, and coronoid-intercoronoid (Fig. 3b) and dentary-surangular 13 310 Journal of Iberian Geology (2019) 45:301–316 Fig. 6  Photographs and interpretative line drawing of cross sectional tongue and groove dentary-intercoronoid suture; f UOPB 01027, no. morphology of selected sutures in specimens UOPB 01145 (a, b, d, 1e, abutting articular-prearticular suture and abutting articular-suran- g) and UOPB 01027 (c, e, f). Scale bar equals 5 mm. a UOPB 01145, gular suture; g UOPB 01145, no. 43, abutting articular-prearticular no. 26, overlapping angular-dentary suture; b UOPB 01145, no. 31, suture and abutting articular-surangular suture. An angular, Ar articu- overlapping angular-surangular suture; c UOPB 01027, no. 1c, over- lar, D dentary, Ic intercoronoid, Par prearticular, Psp postsplenial, Sa lapping dentary-postsplenial suture; d UOPB 01145, no. 18, tongue surangular, no. number of section and groove dentary-intercoronoid suture; e UOPB 01027, no. 1c, contacts (Fig. 3f) the sutural connection becomes tongue- present an overlapping suture type anteriorly (Fig. 6b), but and-groove. However, in cross sections the variability evolve into an interdigitated suture posteriorly (Fig. 5e). This of mandibular sutural typology in Metoposaurus krasie- tendency of change in sutural morphology, i.e., a predomi- jowensis is high, both on the labial and lingual sides. The nance of shallowly interdigitated suture in the anterior part highest variation can be observed along the dentary, with of the mandible, and interdigitated sutures in its posterior four suture typologies distinguished. On the lingual sur- part has been noted in all three specimens, in particular in face, the dentary contacts other bones as a shallowly inter- UOPB 01145 and UOPB 01027. digitated suture, i.e., in the dentary-precoronoid (Fig. 5a, b), and as tongue and groove sutures, especially in the dentary-intercoronoid (Figs. 5g, 6d, e). However, on the 4 Discussion labial surface, interdigitated, shallowly interdigitated and overlapping sutures (Fig. 6a) are present at the following 4.1 Interpretation of suture biomechanical function contacts: dentary-splenial, dentary-postsplenial, angular- dentary and dentary-surangular. External traces of sutures occurring at the mandibular sur- Moreover, in many cases, suture morphology changes face appear as straight connections between adjacent bones, along the same contact between two bones, for instance in and their morphology is usually constant along the entire the dentary-splenial. This is interdigitated anteriorly, but length of the mandible. In contrast, the cross sectional changes into a tongue and groove suture type posteriorly and morphology of sutures varies along the length of even a finally becomes shallowly interdigitated. The precoronoid- single contact. Thus, only sutures visible in cross section splenial is shallowly interdigitated anteriorly, but becomes are interpreted where their biomechanical function is con- interdigitated posteriorly (Fig. 5a, b), while the postsplenial- cerned. Markey and Marshall (2007b) demonstrated that splenial is interdigitated anteriorly (Fig. 5g, h), becoming cross sectional suture morphology was a better indicator for shallowly interdigitated posteriorly. The angular-surangular 13 Journal of Iberian Geology (2019) 45:301–316 311 Fig. 7  Distinct Sharpey’s fibres in polarised light along the sutural angular-postsplenial suture; e UOPB 01145, no. 43, abutting artic- edges of mandibular bones. a UOPB 01144, no. 6, interdigitated ular-prearticular suture; f UOPB 01027, no. 1e, abutting articular- dentary-splenial suture; b UOPB 01144, no. 6, interdigitated post- prearticular suture. An angular, Ar articular, C coronoid, D dentary, splenial-splenial suture; c UOPB 01027, no. 1d, interdigitated cor- Par prearticular, Psp postsplenial, Sp splenial, no. number of section onoid-postsplenial suture; d UOPB 01027, no. 1d, interdigitated deduction of its function than were sutures visible on the interdigitated sutures comes from Sharpey´s fibres: obliquely surface of the bone. oriented fibres on the direction of the apex of the interdigi- The interpretation of biomechanical function of mandibu- tation indicate compression and in shallowly interdigitated lar sutures in Metoposaurus krasiejowensis was conducted sutures, which experience tension, the fibres radiate out- following previous studies based on non-amniote cranial wards at the apex of the interdigitation (Rafferty and Her- biomechanics (Markey et al. 2006; Jasinoski et al. 2010a; ring 1999; Herring and Teng 2000; Jasinoski et al. 2010a). Porro et al. 2015). Additional information on loading on Well-mineralised Sharpey’s fibres occur along sutural 13 312 Journal of Iberian Geology (2019) 45:301–316 edges in all samples examined, but not in all cases can their The most problematic biomechanical interpretation con- arrangements be determined. In deeply interdigitated sutures cerns overlapping sutures. Several authors (e.g., Markey (Fig. 7a–d) they are long and packed in numerous clumps. et al. 2006; Jasinoski et al. 2010a) recognised that this type Additionally, their arrangements and direction of orientation of suture was capable to resist both compression and tension, is easy to follow as perpendicular or oblique to the apex of whereas Porro et al. (2015) suggested the association of this the interdigitation. Numerous and long Sharpey’s fibres are suture with torsion and shearing. In Metoposaurus krasie- predominant in interdigitated sutures and may suggest that jowensis overlapping sutures are located in the middle part this type of bone connection was adapted to resist strong of the jaw ramus, both on the lingual and labial sides (Fig. 8; compression stresses acting on the bone, and may be the Table 2), but Sharpey’s fibres present there invariably are most heavily involved one during feeding. short, but well developed and perpendicular to the edges of In contrast, Sharpey’s fibres are very short, and less the bone. Generally, in long bones, fibres that are aligned numerous in overlapping, tongue-and-groove, and shal- longitudinally relative to the load are associated with ten- lowly interdigitated sutures. For this reason, their arrange- sion, while compression is most effectively resisted by fibres ment is particularly difficult to determine and follow along that are aligned transversely (Ascenzi and Bonucci 1967, these types of joints. Partially preserved clumps of Sharpey’s 1968; Vincentelli and Evans 1971). Overlapping sutures are fibres in shallowly interdigitated sutures represent an out- aggregated in the medial part of the lower jaw, which in wardly radiating arrangement at the apex of the interdigita- Temnospondyli has the shape of relatively straight, but long, tion, while in overlapping sutures Sharpey’s fibres are usu- cylinder. Thus, it could be assumed that this region experi- ally oriented perpendicular to the edges of the bone. The less enced various forces related to mouth opening and eventu- abundant accumulation of Sharpey’s fibres in these sutural ally lateral bending of the rami. In this case the overlapping morphologies may suggest lesser stress capability in these joints should should work as a stable but elastic structure types of sutures. In abutting sutures (Fig. 7e, f), especially of the medial region and should be adapted to counteract in the articular part of the mandible, Sharpey’s fibres occur variable loads. along the entire length of bony edges with a differentiated Sutures associated with tension occur in particular direction in their arrangement. Moreover, dense bundles of along the entire lingual length of the dentary and at the Sharpey’s fibres occurring in abutting sutures at the articular articular, prearticular, and surangular contacts (Figs. 5a, connection may have caused elastic mobility of this joint, b, g, 6d–g, 8). The symphyseal region was elastic (Sulej and counteracting tension stresses during jaw opening. 2007), meaning that the tensed sutures across the dentary Fig. 8  Schematic illustration of the mandible of Metoposaurus stress in cross section; blue lines indicate areas undergoing variable krasiejowensis with interpretative demonstration of stress distribu- loads (tension and compression or torsion and shear) in cross sec- tion. An angular, Ar articular, C coronoid, D dentary, Ic intercoro- tion; black arrows indicate areas of well-visible accumulations of noid, Par prearticular, Pc precoronoid, Psp postsplenial, Sa suran- Sharpey’s fibres, and slope of the arrows shows accurate orientation gular, Sp splenial. Red lines indicate areas undergoing compression of Sharpey’s fibres along the sutural edges stress in cross section; yellow lines indicate areas undergoing tension 13 Journal of Iberian Geology (2019) 45:301–316 313 may have been adapted to permit the jaws to open very et al. 2016), the external course of all sutures in the mandible wide during feeding. Wide opening of the mouth was pro- is visible and can be followed. In addition, well-mineralised posed for metoposaurids (Sulej 2007), in a similar fashion Sharpey’s fibres occur in dense bundles along the periphery to other groups (see below). The medial part of the man- of the sutural edges. This indicates that sutures were not dible was under the influence of variable stresses, mainly fully ossified and still elastic. Based on this observation, along the labial part of the dentary and in the anterior they probably could absorb strain and stress. This feature part of the angular (Figs. 6a–c, 8). The posterior part of could be important in our understanding of the mechanical the mandible was subject to compression, especially in system for flat and relatively large cranial bones, but also in the angular, surangular and prearticular (Figs. 5a–f, 8). mandibles. Together with the highly fibred matrix of dermal The compression impact in these areas may have resulted bones (Gruntmejer 2015; Gruntmejer et al. 2016), the entire from muscle insertion in these areas (Sulej 2007) and may skull and lower jaw were strongly, yet elastically, connected indicate adaptation to generate great biting capabilities. to the external cover of the body, but also the bones to each The presence of strong mandibular muscle attachment is other. In contrast to the skull, mandibular sutures in Metopo- additionally supported by the occurrence of very numerous saurus reveal a complex variability as far as cross sectional and densely packed Sharpey’s fibres (Gruntmejer 2015). morphology is concerned and suggest the important role of Such abundant accumulations of Sharpey’s fibres in these the mandible in feeding behaviours. areas suggest that the most anterior and posterior regions of the mandible were elastic, playing a significant role during feeding behaviour. 5 Conclusions Another issue is the presence of interwoven structural fibres (ISF) along the sutural surfaces of the prearticu- The mandible sutures in Metoposaurus krasiejowensis are of lar (Fig. 7e, f) and the surangular with the articular. The different types: interdigitated, shallowly interdigitated, over- prearticular and surangular are dermal bones, i.e., they lapping, tongue and groove and abutting. A comparison of ossify directly from soft tissues without a cartilaginous pre- the morphology of mandibular sutures in three specimens of decessor, whereas the articular undergoes periosteal ossi- Metoposaurus krasiejowensis indicates that suture morphol- fication. Thus, the presence of ISF in this case represent ogy varies along the mandible. The morphology of mandibu- the connection between two ossification systems. However, lar sutures reveals the particular importance of the mandible IFS also represent a strong connection of bone with the soft during feeding. Extensive variability of sutural morphology tissues, increasing the biomechanical strength of the bony along the entire mandible of Metoposaurus krasiejowensis tissue and, similar to the skull dermal bones of Metoposau- suggests a complex loading regime, including simultaneous rus krasiejowensis (Gruntmejer et al. 2016), the occurrence compression and tension regimes. Due to a lack of histologi- of ISF in mandible dermal bones also indicates their meta- cal data of cross sectional morphology of mandibular sutures plastic origin. and related biomechanical functions in temnospondyls, it is difficult to correlate the results found for Metoposaurus 4.2 Comparison of sutural morphology krasiejowensis with other temnospondyl taxa. Additional between the skull and mandible studies are called for, inclusive of quantitative and compu- of Metoposaurus krasiejowensis and functional tational analyses. For the time being, we can state that, on interpretation the basis of current investigations of the skull of Metoposau- rus krasiejowensis, including dermal bone histology, cranial The majority of cranial sutures studied in one of the skulls suture morphology and computational biomechanics (finite (UOPB 01029) of Metoposaurus krasiejowensis were element simulations), these animals were capable of direct defined as interdigitated (Gruntmejer 2012), which are biting of prey items by using different feeding behaviours associated with compression (Rafferty and Herring 1999; such as ambush strategy (bilateral bite) and active predation Markey et al. 2006; Markey and Marshall 2007a, b; Jasinoski by lateral head movements (lateral bite). et al. 2010b). Moreover, sutural morphology does not change along the skull bones (Gruntmejer 2012). A predominance of Acknowledgements The authors are grateful to Michał Jankowiak (Adam Mickiewicz University, Institute of Geology, Poland) for prep- interdigitated sutures across the postorbital and medial part aration of thin sections and to John Jagt (Natuurhistorisch Museum of the skull roof was confirmed in other early non-amniotes Maastricht, Maastricht) for improving the English. J. Fortuny acknowl- (Kathe 1997). Interestingly, in the entire skull examined, edges receiving a postdoc Grant, “Beatriu de Pinós” 2014—BP-A sutures associated with tension (i.e., abutting or tongue- 00048 (Generalitat de Catalunya), the Spanish Ministerio de Economía, Industria y Competitividad, the European Regional Development Fund and-groove) do not occur (Gruntmejer 2012). In contrast to of the European Union (MINECO/FEDER EU, project CGL2014- the skull, where the external traces of sutures between skull 54373-P) and the CERCA Programme (Generalitat de Catalunya). We bones are fused and invisible (Gruntmejer 2012; Gruntmejer thank also both reviewers (Michael Buchwitz and Bryan Gee) and the 13 314 Journal of Iberian Geology (2019) 45:301–316 invited editor (Jean-Sébastien Steyer) for all comments which greatly largest living amphibian, the Chinese giant salamander Andrias improved our paper. davidianus (Amphibia: Urodela). PLoS One, 10, e0121885. Fortuny, J., Marcé-Nogué, J., & Konietzko-Meier, D. (2017). Feeding Open Access This article is distributed under the terms of the Crea- with Late Triassic metoposaurids: A 3D finite element analysis tive Commons Attribution 4.0 International License (http://creat​iveco​ approach. Journal of Anatomy, 230, 752–765. mmons​.org/licen​ses/by/4.0/), which permits unrestricted use, distribu- Fortuny, J., Marcé-Nogué, J., Steyer, J. S., De Esteban-Trivigno, S., tion, and reproduction in any medium, provided you give appropriate Mujal, E., & Gil, L. (2016). Comparative 3D analyses and palaeo- credit to the original author(s) and the source, provide a link to the ecology of giant early amphibians (Temnospondyli: Stereospon- Creative Commons license, and indicate if changes were made. dyli). Scientific Reports, 6, 30387. Francillon-Vieillot, H., de Buffrénil, V., Castanet, J., Géraudie, J., Meu- nier, F. J., Sire, J. Y., et al. (1990). Microstructure and mineraliza- tion of vertebrate skeletal tissues. In J. G. Carter (Ed.), Skeletal biomineralization: patterns, processes and evolutionary trends References (Vol. I, pp. 471–530). New York: Van Nostrand Reinhold. Gruntmejer, K. (2012). Morphology and function of cranial sutures Ascenzi, A., & Bonucci, E. (1967). The tensile properties of single of the Triassic amphibian Metoposaurus diagnosticus (Temno- osteons. The Anatomical Record, 158, 375–386. spondyli) from southwest Poland. In E. Jagt-Yazykova, J. Jagt, A. Ascenzi, A., & Bonucci, E. (1968). The compressive properties of Bodzioch, et al. (Eds.), Krasiejów—Palaeontological inspirations single osteons. The Anatomical Record, 161, 377–391. (pp. 34–54). Bytom: ZPW Plik. Bodzioch, A., & Kowal-Linka, M. (2012). Unraveling the origin of Gruntmejer, K. (2015). Mandible histology in Metoposaurus diagnos- the Late Triassic multitaxic bone accumulation at Krasiejów (S ticus krasiejowensis (Amphibia, Temnospondyli) from the Upper Poland) by diagenetic analysis. Palaeogeography, Palaeoclimatol- Triassic of Poland—Preliminary results. In J. Jagt, G. Hebda & S. ogy, Palaeoecology, 346(347), 25–36. Mitrus et al. (Eds.), XIII Annual Meeting of European Association Bolt, J. R., & Chatterjee, S. (2000). A new temnospondyl amphib- of Vertebrate Palaeontologists—Abstract Book (p. 28). ian from the Late Triassic of Texas. Journal of Paleontology, 74, Gruntmejer, K., Konietzko-Meier, D., & Bodzioch, A. (2016). Cranial 670–683. bone histology of Metoposaurus krasiejowensis (Amphibia, Tem- Brusatte, S. L., Butler, R. J., Mateus, O., & Steyer, J. S. (2015). A new nospondyli) from the Late Triassic of Poland. PeerJ, 4, e2685. species of Metoposaurus from the Late Triassic of Portugal and Gruszka, B., & Zieliński, T. (2008). Evidence for a very low-energy comments of the systematics and biogeography of metoposaurid fluvial system: A case study from the dinosaur-bearing Upper temnospondyls. Journal of Vertebrate Paleontology, 35, e912988. Triassic rocks of southern Poland. Geological Quarterly, 52, Carroll, R. L. (1964). Early evolution of the dissorophid amphibians. 239–252. Bulletin of the Museum of Comparative Zoology, 131, 161–250. Haridy, Y., LeBlanc, A. R., & Reisz, R. R. (2017a). The Permian reptile Chakravorti, S., & Sengupta, D. P. (2016). Indian metoposaurid Opisthodontosaurus carrolli: A model for acrodont tooth replace- amphibians: morphometry, taxonomy and dispersal. In F. Holw- ment and dental ontogeny. Journal of Anatomy, 232, 371–382. erda, A. Madern & D. Voeten et al. (Eds.), XIV Annual Meeting of Haridy, Y., MacDougall, M. J., & Reisz, R. R.. The lower jaw of the European Association of Vertebrate Palaeontologists—Abstract Early Permian parareptile Delorhynchus, first evidence of multiple Book (p. 96). denticulate coronoids in a reptile. Zoological Journal of the Lin- Chinsamy, A., & Raath, M. A. (1992). Preparation of fossil bone for nean Society (in press). https:​ //doi.org/10.1093/zoolin​ nean/​ zlx085​ histological examination. Palaeontologia Africana, 29, 39–44. Heaton, M. J. (1979). Cranial anatomy of primitive captorhinid reptiles Chowdhury, T. R. (1965). A new metoposaurid amphibian from the from the Late Pennsylvanian and Early Permian, Oklahoma and Upper Triassic Maleri Formation of Central India. Philosophical Texas. Oklahoma Geological Society Bulletin, 127, 1–84. Transactions of the Royal Society of London, Series B, 250(761), Herring, S. W., & Teng, S. (2000). Strain in the braincase and its 1–52. sutures during function. American Journal of Physical Anthro- Dutuit, J. M. (1976). Introduction à l’étude paléontologique du Trias pology, 112, 575–593. continental marocain. Descriptions des premiers Stégocéphales Hunt, A. P. (1993). Revision of the Metoposauridae (Amphibia: Tem- receuillis dans le couloir d’Argana (Atlas Occidental). Mémoires nospondyli) and description of a new genus from western North du Muséum national d’Histoire naturelle Paris, 36, 1–253. America. Museum of Northern Arizona Bulletin, 59, 67–97. Dutuit, J. M. (1978). Description de quelques fragments osseux prov- Jasinoski, S. C., Rayfield, E. J., & Chinsamy, A. (2010a). Functional enant de la région de Folakara (Trias supérieur malgache). Bul- implications of dicynodont cranial suture morphology. Journal of letin du Muséum national d’Histoire naturelle Paris, 69, 79–89. Morphology, 271, 705–728. Dzik, J., & Sulej, T. (2007). A review of the early Late Triassic Krasie- Jasinoski, S. C., & Reddy, B. D. (2012). Mechanics of cranial sutures jów biota from Silesia, Poland. Palaeontologia Polonica, 64, during simulated cyclic loading. Journal of Biomechanics, 45, 3–27. 2050–2054. Dzik, J., Sulej, T., Kaim, A., & Niedźwiedzki, R. (2000). Późnotriasowe Jasinoski, S. C., Reddy, B. D., Louw, K. K., & Chinsamy, A. (2010b). cmentarzysko kręgowców lądowych w Krasiejowie na Śląsku Mechanics of cranial sutures using the finite element method. Opolskim. Przegląd Geologiczny, 48, 226–235. Journal of Biomechanics, 43, 3104–3111. Fortuny, J., Marcé-Nogué, J., De Esteban-Trivigno, S., Gil, L., & Jupp, R., & Warren, A. A. (1986). The mandibles of the Triassic Galobart, Á. (2011). Temnospondyli bite club: ecomorphologi- temnospondyl amphibians. Alcheringa, 10, 99–124. cal patterns of the most diverse group of early tetrapods. Journal Kathe, W. (1995). Morphology and function of the sutures in the of Evolutionary Biology, 24, 2040–2054. dermal skull roof of Discosauriscus austriacus Makowsky 1876 Fortuny, J., Marcé-Nogué, J., Gil, L., & Galobart, Á. (2012). Skull (Seymouriamorpha; Lower Permian of Moravia) and Onchiodon mechanics and the evolutionary patterns of the otic notch clo- labyrinthicus Geinitz 1861 (Temnospondyli; Lower Permian of sure in capitosaurs (Amphibia: Temnospondyli). The Anatomical Germany). Geobios, Mémoire Spécial, 19, 255–261. Record, 295, 1134–1146. Kathe, W. (1997). Comparative morphology and functional interpre- Fortuny, J., Marcé-Nogué, J., Heiss, E., Sanchez, M., Gil, L., & Galo- tations of the sutures in the dermal skull roof of temnospondyl bart, À. (2015). 3D bite modeling and feeding mechanics of the 13 Journal of Iberian Geology (2019) 45:301–316 315 amphibians. Zoological Journal of the Linnean Society, 126, Neenan, J. M., Ruta, M., Clack, J., & Rayfield, E. J. (2014). Feeding 1–39. biomechanics in Acanthostega and across the fish-tetrapod transi- Konietzko-Meier, D., Bodzioch, A., & Sander, P. M. (2013). Histo- tion. Proceedings of the Royal Society B, 281, 20132689. logical characteristics of the vertebral intercentra of Metopo- Ochev, V. G. (1966). Systematics and phylogeny of capitosauroid laby- saurus diagnosticus (Temnospondyli) from the Upper Triassic rinthodonts. Saratov: Saratov State University Press. (in Russian). of Krasiejów (Upper Silesia, Poland). Transactions of the Royal Polley, B. P., & Reisz, R. R. (2011). A new Lower Permian trematopid Society of Edinburgh, Earth and Environmental Sciences, 103, (Temnospondyli: Dissorophoidea) from Richards Spur, Okla- 1–14. homa. Zoological Journal of the Linnean Society, 161, 789–815. Konietzko-Meier, D., Danto, M., & Gądek, K. (2014). The microstruc- Porro, L. B., Rayfield, E. J., & Clack, J. A. (2015). Descriptive anat- tural variability of the intercentra among temnospondyl amphib- omy and three-dimensional reconstruction of the skull of the ians. Biological Journal of the Linnean Society, 112, 747–764. early tetrapod Acanthostega gunnari Jarvik, 1952. PLoS One, 10, Konietzko-Meier, D., Gruntmejer, K., Marcé-Nogué, J., Bodzioch, A., e0118882. & Fortuny, J. (2018). Merging cranial histology and 3D-compu- Racki, G., & Szulc, J. (2014). Formacja grabowska—Podstawowa tational biomechanics: a review of the feeding ecology of a Late jednostka litostratygraficzna kajpru Górnego Śląska. Przegląd Triassic temnospondyl amphibian. PeerJ, 6, e4426. Geologiczny, 63, 103–113. Konietzko-Meier, D., & Klein, N. (2013). Unique growth pattern of Rafferty, K. L., & Herring, S. W. (1999). Craniofacial sutures: Mor- Metoposaurus diagnosticus krasiejowensis (Amphibia, Temno- phology, growth, and in vivo masticatory strains. Journal of Mor- spondyli) from the Upper Triassic of Krasiejów, Poland. Palaeo- phology, 242, 167–179. geography, Palaeoclimatology, Palaeoecology, 370, 145–157. Ruta, M., & Bolt, J. R. (2008). The brachyopoid Hadrokkosaurus Konietzko-Meier, D., & Sander, P. M. (2013). Long bone histology of bradyi from the early Middle Triassic of Arizona, and a phyloge- Metoposaurus diagnosticus (Temnospondyli) from the Late Tri- netic analysis of lower jaw characters in temnospondyl amphib- assic of Krasiejów (Poland) and its paleobiological implications. ians. Acta Palaeontologica Polonica, 53, 579–592. Journal of Vertebrate Paleontology, 33, 1003–1018. Schoch, R. R., & Milner, A. R. (2000). Stereospondyli. In P. Wellnhofer Konietzko-Meier, D., & Wawro, K. (2007). Mandibular dentition in (Ed.), Handbuch der Paläoherpetologie (Vol. 3B, pp. 1–203). the Late Triassic temnospondyl amphibian Metoposaurus. Acta Munich: F. Pfeil. Palaeontologica Polonica, 52, 213–215. Sengupta, D. P. (1992). Metoposaurus maleriensis Roychowdhury Lucas, S. G. (2015). Age and correlation of the Late Triassic tetrapods from the Tiki Formation of Son-Mahanadi Valley of Central India. from southern Poland. Annales Societatis Geologorum Poloniae, Indian Journal of Geology, 64, 300–305. 85, 627–635. Sengupta, D. P. (2002). Indian metoposaurid amphibians revised. Pale- Lucas, S. G., Spielmann, J. A., & Hunt, A. P. (2007). Bio-chronological ontological Research, 6, 41–65. significance of the Late Triassic tetrapods from Krasiejów, Poland. Sulej, T. (2002). Species discrimination of the Late Triassic temno- New Mexico Museum of Natural History and Science Bulletin, spondyl amphibian Metoposaurus diagnosticus. Acta Palaeonto- 41, 248–258. logica Polonica, 47, 535–546. Marcé-Nogué, J., Fortuny, J., De Esteban-Trivigno, S., Sánchez, M., Sulej, T. (2007). Osteology, variability, and evolution of Metoposaurus, Gil, L., & Galobart, À. (2015). 3D computational mechanics a temnospondyl from the Late Triassic of Poland. Palaeontologia elucidate the evolutionary implications of orbit position and size Polonica, 64, 29–139. diversity of early amphibians. PLoS One, 10, e0131320. Szulc, J., Racki, G., & Jewuła, K. (2015a). Key aspects of the stra- Markey, M. J., Main, R. P., & Marshall, C. R. (2006). In vivo cra- tigraphy of the Upper Silesian middle Keuper, southern Poland. nial suture function and suture morphology in the extant fish Annales Societatis Geologorum Poloniae, 85, 557–586. Polypterus: Implications for inferring skull function in living and Szulc, J., Racki, G., Jewuła, K., & Środoń, J. (2015b). How many fossil fish. Journal of Experimental Biology, 209, 2085–2102. Upper Triassic bone-bearing levels are there in Upper Silesia Markey, M. J., & Marshall, C. R. (2007a). Linking form and function (southern Poland)? A critical overview of stratigraphy and facies. of the fibrous joints in the skull: a new quantification scheme for Annales Societatis Geologorum Poloniae, 85, 587–626. cranial sutures using the extant fish Polypterus endlicherii. Jour- Teschner, E. M., Sander, P. M., & Konietzko-Meier, D. (2018). Varia- nal of Morphology, 268, 89–102. bility of growth pattern observed in Metoposaurus krasiejowensis Markey, M. J., & Marshall, C. R. (2007b). Terrestrial-style feeding humeri and its biological meaning. Journal of Iberian Geology, in a very early aquatic tetrapod is supported by evidence from 44, 99–111. experimental analysis of suture morphology. Proceedings of the Vincentelli, R., & Evans, F. G. (1971). Relations among mechanical National Academy of Sciences, USA, 104, 7134–7138. properties, collagen fibers, and calcification in adult human corti- Murry, P. A. (1989). Paleoecology and vertebrate faunal relationships, cal bone. Journal of Biomechanics, 4, 193–201. of the Upper Triassic Dockum and Chinle formations, southwest- von Meyer, H. (1842). Labyrinthodonten—Genera. Neues Jahrbuch ern United States. In S. G. Lucas & A. P. Hunt (Eds.), Dawn of für Mineralogie, Geographie, Geologie und Petrefaktenkunde, dinosaurs in the American southwest (pp. 375–400). Alburquer- 1842, 301–304. que: New Mexico Museum of Natural History. Affiliations Kamil Gruntmejer1,2 · Dorota Konietzko‑Meier1,3 · Adam Bodzioch1 · Josep Fortuny4,5 1 * Kamil Gruntmejer Department of Biosystematics, Laboratory of Palaeobiology, gruntmejerkamil@gmail.com Opole University, Oleska 22, 45‑052 Opole, Poland 2 European Centre of Palaeontology, Opole University, Oleska 48, 45‑052 Opole, Poland 13 316 Journal of Iberian Geology (2019) 45:301–316 3 5 Steinmann Institute, University of Bonn, Nussallee 8, Institut Català de Paleontologia Miquel Crusafont, 53115 Bonn, Germany ICTA‑ICP Building, c/de les columnes, s/n, 4 08193 Cerdanyola Del Vallès, Spain Centre de Recherches en Paléontologie de Paris, UMR 7207 CNRS-MNHN-UPMC, Muséum national d’Histoire naturelle, Bâtiment de Paléontologie, CP38, 8 rue Buffon, 75005 Paris, France 13