Mller F. Zur embryonalen Kopfentwicklung von Crocodylus cataphractus CUV. In the ostrich Struthio sp. Article 1888;43:4827. https://doi.org/10.1007/978-3-642-73999-6. Philos Trans R Soc London. Anat Anz. The ossicles are the first bones to become fully ossified, with their ossification beginning in the fourth month of gestation. young cartilage), which is more advanced than in the earliest stages described in the other birds. Suschkin [48] and Sonies [64] provided a more detailed description of the posterior portion of the trabeculae (trabecular-polar region). de Beer GR, Barrington EJW. Article The vertebral column develops from a resegmentation process of the somites, while the ribs develop as extensions from the thoracic vertebrae. Read more. The atrioturbinal is located in the anterior region of the nasal capsule. The only exception is Apteryx [50], whose external nares are positioned at the tip of the beak [50, 57, 63, 92, 98], and therefore, a prenasal process is mentioned to be missing [50]. Malformation of the entire limbs include amelia, meromelia, phocomelia, and micromelia. In Spheniscus [47] and Struthio [65], an independent origin and the chondrification of the process was mentioned, but in most birds, the process developed in continuity with the trabecular-polar bar. J Morphol. Data from sources without a detailed description of the staining were treated more carefully. Ulbrich KP. In Streptopelia [55], the tectum was mainly formed by the coalescence of the occipital arches, although the contribution of the otic capsule to its formation was mentioned. Schultze MS. Untersuchungen ber den Bau der Nasenschleimhaut, namentlich die Structur und Endigungsweise der Geruchsnerven bei dem Mensch und den Wirbelthieren; 1862. In total, 23 characters were analyzed. 2010;48(4):33247. In the developing skull, from the earliest mesenchymal anlagen to the first ossifications, different cartilaginous states occur in parallel and distinct borders between the developing elements and the surrounding tissue do not exist [24, 42, 48]. 2002;252(2):13144. 9). Syndactyly involves the fusion of two or more digits. The notable synthesis of de Beer [11] did not benefit from the phylogenetic, methodological, and conceptual framework we now have available, and several studies have been performed since then. Development of chondrocranium in Silonia, Pangasius and Ailia (Schilbeidae) Proceedings of the National Institute of Sciences of India, 22B 335-356 Parker [57] described and figured in a chondrocranial stage before the formation of the trabecula communis a structure called presphenoid (Table S3, Additionalfile3), which in regard to its position (between the eyes) and spatial relation (the orbito-sphenoid plates grow out of the presphenoid) [57] (Plate10, figs. For homologous structures, various anatomical terms were used by authors in the last two centuries (Table S3, Additional file 3). 1991;215:10371. 11b) were the last elements of the avian chondrocranium that chondrify (Fig. Most of the samples were in toto trypsin cleared and stained, some specimens were used for serial histological sectioning. Frank [65] worked with a more extensive series of Struthio embryos, but could not find evidence for the fenestra. Rieppel O. III. Ossification sequence of the common tern (Sterna hirundo) and its implications for the interrelationships of the Lari (Aves, Charadriiformes). 13a, Table 3). 2018;279(1):6274. 2012; The Egyptian German Society for Zoology. Its persisting small portion at the dorsal edge of the interorbital septum is the planum supraseptale [21, 46] (Fig. 2015;526(7574):56973. Differences between non-avian sauropsids and birds can be explained by the development of the chondrocranium in close connection with the sense organs and the brain [12, 17]. Danny Ly BSc, MSc Slab [61] could not tell with certainty whether it was a tectum synoticum or posterius. 7a). The musculoskeletal system develops from three sources: The development of bone and muscle begins at the fourth gestational week, when the paraxial mesoderm differentiates into somites; the latter gives rise to sclerotomes and dermomyotomes. Evolution and development of the bird chondrocranium Acta Zool. By the eighth week, three primary ossification centers develop: one at the center of the cartilaginous vertebral body and one on each side of the cartilaginous vertebral arch. The infrapolar process is a feature shared with crocodilians (Crocodylus [66], Alligator [86], Mecistops [20], Caiman [19, 22]) (Table 1). Bhullar BAS, Marugn-Lobn J, Racimo F, Bever GS, Rowe TB, Norell MA, et al. It uses developmental timing data (Table 2) scaled between 0 (conception) and 1 (last element to appear) and, using parsimony, it optimizes these continuous scores on a given tree (Fig. Zool Scr. Malformations of the limbs vary greatly and can include defects in the entirety of the limb, the hand or the foot, and the digits. 7c and 12), which connects the otic capsules, is occasionally associated with a tectum posterius (Fig. In turn, the dermomyotome will differentiate into dermatome cells forming the dermis of the back and the neck, and myotome cells forming the skeletal muscles. 2015;298(4):7719. 10a, b) is a median structure located anterior to the hypophyseal fenestra between the eyes. In the embryonic cartilaginous skull, however, Palaeognathae and Neognathae cannot be distinguished from each other [28] as a robust criterion for comparing chondrocrania among species is lacking so far. The majority of bird species belong to the latter. 4) that joins the occipital arches [11] (Fig. 2018:147. In most non-avian sauropsids [23], the basal plate is the first part to chondrify (Mecistops [20]) (Table 2), followed shortly by the trabeculae. An independent origin of the cochlear portion was mentioned for Columba [67], Anas [46, 64], Spheniscus [47], and Streptopelia [54]. The morphology of the ostrich Chondrocranium. Corfield JR, Eisthen HL, Iwaniuk AN, Parsons S. Anatomical specializations for enhanced olfactory sensitivity in kiwi, Apteryx mantelli. Acta Zool. 6a). Anat Rec. Drawings by Timea Bodogn, modified from cited source. Musculoskeletal anatomy is fascinating since it gives us insights as to how our body utilizes our muscles, bones, and joints to give us the ability to navigate in the world. J Anat. The otic capsule, which surrounds the anlage of the labyrinth, consists of two parts. The situation in Spheniscus [47] was described as being more complicated. Developmental studies on the neurocranium of the intermediate stages of Coturnix coturnix japonica (Phasianidae, Galliformes). The authors declare that they have no competing interests. Evolution and development of the cartilaginous skull: A similar continuity between the two fenestrae was described for the sparrow Passer sp. Adv Anat Embryol Cell Biol. a Struthio camelus (NMB 5516), b Gallus domesticus (PIMUZ 154), c Meleagris gallopavo (NMB 881), d Coturnix japonica (SMF 7180), e Anas platyrhynchos (NMB C. 833), f Spheniscus demersus (NMB 5634), g Falco tinnunculus (NMB 1351), H) Melopsittacus undulates (NMB 5898), and I) Euplectes orix franciscanus (SMF 2763). 1999;16(5):80318. . This has been done for many clades of non-avian amniotes [29,30,31,32] and for birds [33,34,35,36,37,38,39,40,41]. Correspondence to This concordance has been discussed as supporting a closer relationship of birds and crocodilians to each other than to other sauropsids [18, 19, 21]. Bony skull development in the Argus monitor (Squamata, Varanidae, Varanus panoptes) with comments on developmental timing and adult anatomy. Various patterns of development are described in the literature [49]. Reportedly, only a few chondrocranial features distinguish birds from non-avian sauropsids, in particular from crocodilians [11]. The variation in the onset of chondrification is large (Fig. 7a and 10c), which chondrifies as an anterolateral outgrowth of the acrochordal cartilage [11] (Figs. 13b, Table 4). Scale bars equal 10mm. In His, W., Braune, W. & E. du Bois-Reymond (Eds. Recall that the paraxial mesoderm forms segmented series of tissue blocks on each side of the neural tube, the somites. In Struthio [25, 65], the metotic cartilage appeared late in sequence relative to other birds (Fig. 2015. https://doi.org/10.1016/j.zool.2015.02.004. The development of the base of the skull is complete when these cartilaginous structures fuse and undergo endochondral ossification. He clarified that this attachment cannot be seen as distinct element. De Beer [11] stated that the formation of the septum is associated with the large size of the eyes. https://doi.org/10.5962/bhl.part.117709. 2008;111(3):24257. Bellairs A dA. The first stage of any type of bone formation involves a mesenchymal condensation, where cells become densely packed together. Either the acrochordal cartilage (Fig. Bone formation can occur either by intramembranous ossification or endochondral ossification. Werneburg I, Snchez-Villagra MR. Skeletal heterochrony is associated with the anatomical specializations of snakes among squamate reptiles. WebPhysical Description. The relative position of the interorbital and nasal septum has a direct influence on their origin and, therefore, on their homology. In contrast to crocodilians [11], a cupola anterior (Figs. Filatoff D. Zur Frage ber die Anlage des Knorpelschdels bei einigen Wirbeltieren. CAS In other birds, the pila antotica did not break down completely (Anas, Passer [46], Struthio [25, 65], Spheniscus [47], Euplectes [50], Melopsittacus [49]) (Figs. Cells in the dorsal part form the dermatome and two edges, the ventrolateral lip and the dorsomedial lip. Univ. The unpaired structure delimits the fenestra basicranialis posterior anteriorly and forms the posterior border of the hypophyseal fenestra [11]. 2003;20(6):74958. In Rhea and Dromaius [45], an independent planum antorbitale was missing. A morphological study of skeletal development in Turkey during the pre-hatching stage. 2). https://doi.org/10.1111/j.1096-3642.1937.tb00005.x. J Vet Med Ser C Anat Histol Embryol. Front Zool. A high interorbital septum (Fig. 5) chondrified slightly earlier than the parachordal cartilage (Apteryx [57], Gallus [64, 69], Anas [46, 64], the quail Coturnix japonica [75], Columba [68]) (Fig. The formation of these structures begin by the end of the fourth gestational week, where limb buds become visible as outpocketings from the ventrolateral body wall. The true nature of the cranial ribs is still unclear [65, 89]. The sternum develops from a pair of separate vertical, condensed bands of mesenchymal cells, known as the sternal bars. In birds, the roof of the chondrocranium is reduced to a strip of cartilaginous structures that form the posterodorsal border of the foramen magnum. By using this website, you agree to our Gegenbaurs Morphologisches Jahrbuch , 122 , 796 814 . Anat Anz. 1998;79(1):24550. 4 and 7a) are situated angled in front of the basal plate and rostral to the notochord. An additional uncertainty factor is that it is not known for which stages of a series which staining or, in the case of Anas [46] which method was used. Poland sequence involves the absence of the pectoralis minor, partial absence of the pectoralis major, the absence or displacement of the nipple and areola, and the accompanying presence of digital defects. The site at which more than two bones meet are called the fontanelles (anterior, posterior, and two posterolateral). 22)|Kevin Killiany, The Seaman's Vade-mecum, And Defensive War By Sea: Containing The Proportions Of The chondrification in the metotic cartilage (Fig. 2009;6:114. Privacy In Meleagris, the relative late appearance is an issue of the selected stages [37] and missing information [33], as these studies focused on ossification and not chondrification. https://doi.org/10.1111/azo.12260. Benha: Thesis, Benha University; 2011. 7a). Fibroblasts form the epimysium and perimysium layers of the muscle, whereas the external lamina and reticular fibers form the endomysium. 3). Vertebr Zool. Chondrocranium Patterns of diversity in the avian skull. Cookies policy. J Morphol. The chondrocranial characters on the X-axis are ordered chronologically for Neornithes. Stages increasing in age from left to right. The development of the chondrocranium in the golden hamster, Mesocricetus auratus (waterhouse). Larson PM. But circumvented the issue by using only data for species for which at least four stages have been described and only considered chondrocranial elements when they were reported at least in six species. Fernandez Blanco MV. 1972;237(5353):25763. We detected apomorphies to discriminate between Palaeognathae and Neognathae. WebThe Development Of The Chondrocranium Of Melopsittacus Undulatus ( Advances In Anatomy, Embryology And Cell Biology)| Johannes M De Kock, Birds Of Prey: Sticker Book (Funfax)|Steve Parker, Wolf Hunters (Mechwarrior: Dark Age, No. 10a). Clade-specific morphological diversification and adaptive radiation in Hawaiian songbirds. In crocodilians, the fenestration of the interorbital septum was reported as missing (Crocodylus [66], Melanosuchus [72], Caiman [19]). Herein, development of The structural development of the upper limbs and lower limbs are similar but with two exceptions: the development of the lower limb is approximately 1 to 2 days behind that of the upper limb, whereas the upper and lower limbs rotate in opposite directions. Lang C. Das Cranium der Ratiten mit besonderer Bercksichtigung von Struthio camelus. Between the trabeculae and the basal plate is the polar cartilage (Fig. Chondrocranium Definition & Meaning | Dictionary.com Suschkin [48] further specified that a paired anlage of the parachordal cartilage may exist in the precartilaginous state, while chondrification takes place in the fused parachordal anlage. Eight stages in the development of skull elements, commencing from the first day to twentyfive days after hatching, have been studied.The mesenchymato Structures derived from the membranous neurocranium include the parietal bones, part of the temporal bones, and the occipital bone. The different names for the same process refer to its origin, namely the posterior end of trabecular-polar bar. Evol Dev. Zeitschrift fr wissenschaftliche Zool. Embryonic remnants of intercentra and cervical ribs in turtles. 2009;18:193208. From this point on, there are two ways osteogenesis can occur: intramembranous ossification and endochondral ossification. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Together with the anteriorly located acrochordal cartilage (Fig. Parker [58] was the first who mentioned a structure that grows out from the posterior end of the trabeculae as lingulae sphenoidales, followed by Parker [57], who called it basipterygoid process. The first seven pairs of ribs attach to the sternum through their own cartilages. Further, in the black caiman Melanosuchus niger too, a barely evident basicranial fenestra was reported [72] (p. 11). Chondrification involves the condensation and differentiation of mesenchymal cells into chondrocytes (cartilage cells). 2019;234(6):899916. De Beer and Barrington [46] assumed that the metotic cartilage is probably a modification of the cranial ribs. https://doi.org/10.1080/00445096.1972.11447457. In crocodilians, which have the external nares like Apteryx at the tip of their snout, the prenasal process is small [11, 22, 86, 93]. In contrast to the sequence of turbinals in other birds, in Coturnix [75], the atrioturbinal appeared before the other turbinals. Brachydactyly involves shortened digits. The tip of the chorda does not pierce the anterior surface of the 2015;70:5304. Observations on the anatomy and development of Apteryx. Brock GT. This is as exemplified by the case of Apteryx. II. 1900;15:149290. https://doi.org/10.1038/nature15697. For the following stage, growth of the cartilage was mentioned, and this stage was taken as proxy for the onset of chondrification, and might be a reason for the relative early appearance of the element in the sequence. Although different, the occurrence of both processes first require the condensation of mesenchymal cells - the loosely organized embryonic connective tissue. The chondrocranial characters are ordered chronologically for Neornithes. Even the development from an independent chondrification centre was described (Anas [46], Euplectes [50], Coturnix [75]). Summary. The middle third of his supraorbital plate becomes resorbed and corresponds to the actual supraorbital part of the orbital cartilage, while the anterior third, that originates from the intertrabecula and is homologous to the anterior orbital cartilage, fuses to the interorbital septum. During the sixth gestational week, joints begin to develop with the formation of condensed mesenchyme in the interzone, the region between two bone primordia. Palaeontogr Abteilung A. In Falco [48], the planum supraseptale was described to form a discrete chondrification. In the case of the processes of the trabecular region we did not consider them in the chondrification sequence, because of the unclear homology. Crompton AW. Slab O. Only Sonies [64] stated that in Anas and Gallus, the fenestra was formed by incomplete fusion of the cochlear and canalicular part in the region of the stapes (primary origin). 1951;63:848. development Parker [57] himself described a prenasal cartilage in Apteryx, although he also described the nasal capsule extending from the turbinal region to the tip of the beak. The pattern of chondrification is generally similar among birds (Fig. Similarly, in squamates the primary basicranial fenestra is filled with a layer of undifferentiated cells [12, 15]. Before the formation of the interorbital fenestra, a thinning of the cartilaginous septum occurs, followed by resorption of cartilage. Engelbrecht DVZ. https://doi.org/10.1111/j.1463-6395.1953.tb00368.x. 9), was first described by Sonies [64]. In birds, the parachordal cartilage is continuous below and above the notochord from its first chondrification on [11] (Table1), and is therefore occasionally called perichordal [46, 47, 65]. J Morphol. Terminology of the processes of the trabecular-polar region and their presumed homology [25, 47, 48, 50, 64]. 1934;223:41167. Biol Open. In other birds, the metotic cartilage was continuous with the basal plate (Falco [48], Phalacrocorax [61], Euplectes [50], Melopsittacus [49]), or continuous with the otic capsule (Struthio [25, 65], Spheniscus [47, 94]) before being cartilaginous. Maxwell EE. All data generated or analyzed during this study are included in this published article. Vorster [69] did not explicitly mention a tectum posterius but observed in Gallus that the ventral root of the tectum synoticum spreads over the occipital arch. Craniosynostosis involves the premature closure of one or more sutures of the skull. 1956;159:165224. In spina bifida cystica, the meninges and/or the neural tissue protrude through the skin at the sacral region to form a cyst-like sac. In most birds, the interorbital septum becomes fenestrated in ontogeny (Figs. In most birds, the paired trabeculae have been described to grow rostrally together in the midline (left) to form the trabecula communis (middle), whereas in Falco and Coturnix the trabeculae fused with an intertrabecula (right) to form the trabecula communis. Web1. The Chondrocranium and the Development of the Skull in Recent Reptiles. Already Sonies [64] mentioned that the connection of the polar cartilage with the basal plate is not constant in birds. At birth, the membranous bones are separated from each other by dense connective tissue membranes that form fibrous joints, known as the cranial sutures (coronal, sagittal, and lambdoid). https://doi.org/10.1159/000365564. 2019;100(4):37688. The planum supraseptale merges posteriorly into the supraorbital cartilage (Fig. Polydactyly involves the presence of extra digits. The bones that make up the vertebral column, the ribs, and sternum form only by endochondral ossification. 7b) in Gallus [64] took place before the chondrification of the metotic cartilage, whereas the fenestra ovalis was in other birds the last aspect to form in the sequence of the otic region (Fig. Comparative studies of chondocranial development of mammals can benefit from a solid phylogenetic framework, research on non-classical model organisms, and integration with imaging and sectional data derived from computer-tomography. The suprapolar cartilage appears early in the chondrification sequence, around the time when the polar cartilages and the trabeculae chondrify. A connection to the basal plate was not explicitly mentioned. 11a) were absent (Struthio [45, 65] or not reported (Apteryx [57], Dromaius [28, 45, 56], Rhea [45, 56]). WebTHE DEVELOPMENT OF THE CHONDROCRANIUM IN OPHICEPHALUS | Zoological Journal of the Linnean Society | Oxford Academic Abstract. In Coturnix [34, 75], the nasal septum appeared not earlier than in other species although an intertrabecula was described. First mentioned for the marine turtle Chelonia mydas (Chelone viridis) as a mesenchymal element [85], the intertrabecula was reported in some crocodilians too (the American alligator Alligator mississippiensis [86, 87], Crocodylus [21], Caiman [19]). Reviewer: Biol. Gussekloo SWS, Bout RG. Cerny R, Horek I, Olsson L. The trabecula cranii: development and homology of an enigmatic vertebrate head structure. For birds with relatively large eyes as Struthio, Rhea, and Caprimulgus, a dorsal position of the concha nasalis to the planum antorbitale was described [65]. Only in this group turbinals are described to be missing, such as the concha nasalis in Passeriformes (Fig. In Coturnix [75], the pila antotica was recorded when the acrochordal cartilage started to chondrify, without any information about its chondrogenesis. Sonies [64], who worked mainly with whole-mount staining (Table S1, Additionalfile1), observed a primary origin in which the basicranial fenestra was formed by leaving a space free when the cartilages of the basal plate merged whereas authors working with histological sections described a secondary origin [58, 69] in which the basicranial fenestra was formed by resorption of the previously uniform cartilage of the basal plate. These include the missing fenestrae in the nasal septum of the palaeognaths (Fig. Wilson Bull. PubMed 1957: Development of the skull in catfishes. The fully formed chondrocranium. Parker WK. The prenasal process is either described as a prolongation of the trabecula communis (Phalacrocorax [61], Spheniscus [47], Euplectes [50], Melopsittacus [49], Gallus [64, 69]), or as a prolongation of the nasal septum (Apteryx [57], Anas [46], Struthio [25], Coturnix [75]). 2005;264(1):3452. Endochondral ossification thus begins from these primary ossification centers at the diaphysis and proceeds toward the epiphyses. Nature. Based on Brocks [25] work, de Beer [11] mentioned a basicranial fenestra for Struthio. Tracing the developmental origin of a lizard skull: Chondrocranial Zusi RL. Eo SH, Bininda-Emonds ORP, Carroll JP. In crocodilians, the absence of the fenestra basicranialis posterior was mentioned for several species ([11, 23, 59, 71], Mecistops [20], Caiman [19, 22]). This may mean that the appearance of certain elements in some species may be in reality earlier than reported in our survey. The scoop-like rostrum 3 - Description of the optimum stage of the chondrocranium: Total body length of embryo: 53 mm. The fenestrae of the nasal septum formed in most birds before the interorbital fenestra (Fig. Suschkin [48] argued that the dye (carmine) used by Parker [57] was not suitable for staining intercellular substance and that because of the difference in chondrogenesis between the median and lateral part of the parachordal cartilage, the median aspect was less obvious and gave the impression of a paired anlage. https://doi.org/10.1016/j.jobaz.2012.10.004. 13a, Table 3). In Falco [48], the nasal septum chondrified before the trabecula communis due to its origin from the intertrabecula, which was present earlier than the trabecula communis. De Kock [49] assumed a correlation with the presence of the paranasal cartilage that gave rise to the concha nasalis in some birds (Gallus [64], Anas [46], Struthio [65]). 8 and 9) chondrified subsequent to the trabeculae (Table 2). 4) was mentioned in several bird species except in Galloanserae. The skull consists of a neurocranium and a viscerocranium, with each having membranous and cartilaginous components. Modified from Wada et al. a Struthio sp. They consist of a core of mesenchymal cells - derived from the somatic layer of the lateral plate mesoderm - covered by a layer of ectoderm. pterygoideus basisphenoidei [45], although a connection to the quadrate was missing and the fusion to the basal plate was described. https://doi.org/10.1002/jmor.1051080104. PLoS One. 2014;5:19. The distinction between Palaeognathae and Neognathae is mainly based on the pterygoid-palate connection in the adult skull [26, 27]. Development The phylogenetic distribution was studied using a parsimony-based state reconstruction running on the Mesquite version 3.61 software and visualized on a phylogenetic framework from http://www.timetree.org/ [access: 2020-05-12]. Weisbecker V, Mitgutsch C. A large-scale survey of heterochrony in anuran cranial ossification patterns. Society for the Study of Amphibians and Reptiles the Recessus Scalae tympani and its bearing on the classification of reptiles. The vertebral column develops from the sclerotomes, the ventromedial part of the somite. 2020;579(7799):397401. Malformations of the vertebra include Klippel-Feil sequence and spina bifida. 2008;269(9):1095113. The Neornithes consensus line represents the mean values of the individual chondrification events of all ten bird species ordered in ascending order of relative timing of chondrification. EH gathered the data. Only Sonies [64] identified the polar cartilage continuous with the trabeculae. Evolution and development of the bird chondrocranium - PMC Cranioschisis involves the failure of the cranial vault to form, thus exposing the brain tissue to amniotic fluid, resulting in anencephaly. In Opisthocomus, Bang [99] described that the atrioturbinal (anterior concha) was missing, whereas Parker [83] mentioned that the atrioturbinal (inferior turbinal) was simpler but otherwise similar as in Gallus. 1891;5:21344. Vertebr Zool. of the Chondrocranium and Dermatocranium in Early Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. 11) is located between the nasal sacs in the nasal capsule (Fig. Drawings by Timea Bodogn, modified from cited source. 10b). Cranial ribs were first mentioned in chicken embryos by Froriep [102] and documented thereafter in several other bird species. To analyse the variation among bird chondrocrania in a phylogenetic framework, we mapped the differences of the chondrocranium and the diverging modes of structure development (Tables 3 and 4) on a given molecular tree (Fig.
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