Cranial ontogeny of otariid seals

Over 2000 otariid skulls were measured for a morphometric study of cranial ontogeny in fur seals and sea lions. Few interspecific differences in cranial ontogeny were observed in the Otariidae, with only minor differences in rates of growth. Sexual dimorphism was significant in all otariids but was more apparent in the larger species. Female otariids of each species showed monophasic development in all characteristics, whereas males expressed monophasic growth for some characters and biphasic growth for others. Biphasic development in skulls of male otariids occurred well after physical maturity had been reached, usually at a suture index of 27. The rate of development varied between skull characters; components relating to the nervous system completed growth well before the rest of the skull, whereas those related to feeding, respiration and vocalisation developed in synchrony with the overall growth of total skull length. Sutures of the calvaria, or braincase, were the first to show partial closure and those uniting the facial bones were usually the last to fuse. As with the calvaria, the orbits and otic capsules developed quickly, suggesting a need for good hearing and vision early in independent postnatal life. Development of the rostral and palatal regions required significantly longer to complete growth.     

Response of the longitudinal growth of cranium and long bones to early weaning in the rabbit

To study the problem whether the growth rates of the cranium and of long bones are different from one another, in 13 age groups of 5 rabbits each three distances of the skull (SSO-SL, SSO-P and N-NSA) and the length of the femur, tibia and calcaneus were measured. Following the early weaning of the rabbits (41/2 weeks), the increase of all measurements was strongly delayed for about one week. Thereafter, during a two weeks' period a typical catch-up growth was observed. From these results the conclusion was drawn that the growth rates of cranium and long bones do not differ from each other, and that a temporary deficiency of food intake affects intramembranous bone growth and cartilaginous growth in a similar way.     

The fate of the arachnoid villi in humans

Villi arachnoidales undergoes in the course of life changes in relation to the skull bones and sinuses. Our aim was to determine the relations of the villi arachnoidales to the skull bone and/or sinuses from the neonatal period to adults. The investigations were performed on collection of 50 disarticulated macerated skull bones from the new-born to 30 years of age and on 20 skulls from individuals in the life period from 30 to 80 years of age. Villi arachnoidales produced imprints on the skull bones in the shape of holes and/or furrows corresponding to different shape of the villi arachnoidales. These imprints appeared very early in the period when the bony sprouts of the large skull bones received a thin covering of compact bone, the future lamina vitrea. At that time villi arachnoidales had no connection with the dural sinuses but with the diploe and with the diploic veins. By agglomeration of the villi in larger and large formations, granula meningea, Pacchionian granulations, the contact to sinuses was realized by means of short channels. The structural changes of villi arachnoidales may produce thrombophlebitis and hydrocephalus externus, especially in children. The fate and the relations of the villi arachnoidales are therefore of great importance for neurologist, neurosurgeon and otorhinolaryngologist.     

Effects of maternal food restriction during lactation on craniofacial growth in weanling rats

Adult Holtzman rats were submitted during suckling period to a food restriction with or without protein or carbohydrate restoration. Twenty-one-day-old weanling pups were compared with controls of 9, 13, 17, and 21 days of age. Lateral craniofacial roentgenographies were taken. The length in midsagittal plane of each bone and its angle with respect to the vestibular line were measured in males. In females, the brain and the left masseter muscle were weighed, and the muscle/brain ratios (neuromuscular index) were calculated. Food restriction altered skull size and shape. Size changes were due to arrested lengths in all studied skull bones. Shape variation was evident by orthocephalization changes, reflected in angulation changes of bones belonging to the frontoethmofacial (frontal, nasal, and maxillary bones) and to the occipitointerparietal (interparietal bone) complexes. Partial restorations by both protein or carbohydrate supplementation were found. Nutritional stresses during lactation affected orthocephalization through an altered growth ratio between two soft tissues functionally associated to the craniofacial complex: brain and masticatory muscles.     

Cranial growth in normal and low-protein-fed Saimiri. An environmental heterochrony

Protein malnutrition has a significant and measurable effect on the rate and timing of growth. Heterochrony is generally viewed as the study of evolutionary changes in the relative rates and timing of growth and development. Although changes in growth commonly result from experimental manipulations of diet, nobody has previously attempted to explain such changes from a heterochronic perspective. We use a heterochronic perspective to compare a group of squirrel monkeys fed a low-protein diet to individuals on a high-protein diet, but, in contrast to previous works, we focus particularly on the effects of environmental and not genetic factors. In the present study, Gould's (1977) and Godfrey and Sutherland's (1996) methodologies for studying heterochrony, as well as geometric morphometrics, are used to compare two groups of Saimiri sciureus boliviensis. Two groups of Saimiri were constructed on the basis of the protein content in their diets: a high-protein group (HP) (N=12) and a low-protein group (LP) (N=12). All individuals are males born in captivity. Two major functional components of the skull, the neurocranium and the face, were analysed. Four minor components were studied in each major component. Comparison of craniofacial ontogeny patterns based on major and minor components suggests that changes in the skull of LP animals can be explained by heterochrony. The skull of LP animals exhibits isomorphism produced by proportioned dwarfism. Our results suggest that heterochrony can be environmentally, rather than exclusively genetically, induced. The study of genetic assimilation (Waddington, 1953, 1956; see Scharloo, 1991; Hallgrimsson et al., 2002) has demonstrated that environmentally induced phenotypes often have a genetic basis, and thus parallel changes can be easily induced genetically. It is possible that proportioned dwarfism is far more common than currently appreciated.     

Comparative morphology and evolution of the otic region in toothed whales (Cetacea, Mammalia)

The otic region in the skull of archeocetes and odontocetes is compared and interpreted with special emphasis on the morphology and suspension of the ear bones. In archeocetes, the periotic was obviously separate from the mastoid but still integrated within the skull via a long anterior and posterior process. The rotation of the cochlear part of the periotic was already obvious. The tympanic bone was attached to a decreasing number of neighboring elements, with the periotic becoming more and more important in the later archeocetes. The accessory air sacs of the tympanic cavity had invaded some of the adjacent skeletal elements and attained a moderate-to-remarkable extension. In the evolution of the odontocetes, the periotic and tympanic were successively uncoupled from the skull and combined to a new morphological and functional unit (tympanoperiotic complex). This uncoupling was mainly achieved by shortening the periotical processes and simultaneously extending the tympanic air sacs. For functional reasons, however, the periotic (posterior process) stayed in immediate contact with the mastoid, the latter remaining in the lateral wall of skull. In advanced marine dolphins, the bony sheaths of the accessory air sacs are largely reduced, presumably because of volume fluctuations in the tympanic cavity during diving. The perfect uncoupling of the ear bones from the skull obviously was an essential prerequisite for directional hearing, for effective ultrasound orientation and communication, and finally, for the striking development of the dolphin brain.     

Post-natal growth of the skull in the house mouse Mus musculus Linné, 1758, and in 2 different large subspecies of the field mouse Microtus arvalis Pallas, 1779. II. Results (I)

Postnatal skull ontogeny of Mus musculus, Microtus arvalis arvalis and M. a. asturianus was studied qualitatively and quantitatively. To facilitate age determination for undated specimens, the most important stages in ossification of the skull bones are described, with drawings of selected ontogenetic stages (Part I). Using Parameter C of the growth function Y(t) = A - B exp (- Ct), it is possible to establish skull growth gradients. The growth functions are subdivided into 3 classes, based on Parameter C, associated with different growth regions of the skull. Changes in individual skull proportions are demonstrated by means of ontogenetic and intraspecific allometries.     

Skull and mandible formation in the cuckoo (Aves, Cuculidae): contributions to the nomenclature in avian osteology and systematics

The study of the contributions of different bones to the formation of the skeleton in birds is necessary: (1) to establish homologies in comparative anatomy; (2) to delimit each bone structure correctly, mainly in relation to the skull and mandible where the bones are fused to each other in adults; and (3) to standardize nomenclature in avian osteology. In this paper at least one young specimen belonging to each sub-family of Cuculidae was examined in order to identify each bone in terms of boundaries and contributions to skull and mandible formation. These cuckoos specimens were also compared with adults and young of turacos and hoatzin. The results show little variation of skull and jaw among the young cuckoos studied compared with the variations among adult specimens. However, it provides new suggestions for the boundaries and nomenclature of certain osseous structures in the skull and mandible of birds, specifically fissura zona flexoria craniofacialis, prominetia frontoparietalis, crista temporalis transversa, processus squamosalis, fossa laterosphenoidalis, tuberculum laterosphenoidale and processus retroangularis. This study also provides more reliable homologies for use in cladistic analysis and above all it contributes to the phylogenetic position of Cuculidae within Neognathae, specifically the skull formation suggest that turacos and hoatzin are more similar to each other than either is to the cuckoos.     

Early development of the cephalic skeleton of Barbus barbus (Teleostei, Cyprinidae)

The inception, and development of the cephalic skeleton of Barbus barbus from hatching to 24 days passes through periods of fast and slow growth; these rates are not the same in different parts of the skull. Trabeculae, parachordal plates, Meckelian cartilages and hyposymplectics are present at hatching. Then the cartilaginous floor of the neurocranium develops, the pars quadrata, the hyoid bars and branchial arches elements appear shortly before the first movable dermal bones, the dentaries, maxillae and opercles. The first bone of the braincase to appear is the parasphenoid; other bones develop subsequently and at the same time: the angular, quadrate, interopercle and fifth ceratobranchial. Later the splanchnocranium continues to develop at a relatively fast rate while the neurocranium shows little growth. The braincase does not begin to close before the 24th day, nor do the first bones of the skull roof appear, while the bucco-pharyngeal apparatus is complete, having the adult shape. The early constitution of the latter structures seems to be linked with the mechanical demands of biological functions such as breathing and feeding.     

The subdivisions and fusions of the exoskeletal skull bones ofDiscosauriscus austriacus (Makowsky 1876) and their possible homologues in rhipidistians

Two localities in the Boskovice Furrow region of Moravia (Czecho-Slovakia) have produced new, well preserved material of the Lower Permian tetrapodDiscosauriscus austriacus (Makowsky 1876). A relatively large number of specimens have been found with some dermal skull roof bones partly or fully subdivided, and/or fused. These are the first records of such subdivisions and fusions in this tetrapod and the following bones are discussed: frontal, postfrontal, parietal, intertemporal, supratemporal, tabular and postparietal. The subdivided bones within the skull roof ofDiscosauriscus (and some dissorophoids) are situated at the same places as those found in Devonian rhipidistians, and may relate to the homology of the bones of the cranial exoskeletal roof inDiscosauriscus and in osteolepiforms. It shows that the “orthodox” terminology of the skull roof bones used in osteolepiforms is correct.     

Study of lead accumulation in bones of Wistar rats by X-ray fluorescence analysis: aging effect

The accumulation of lead in several bones of Wistar rats with time was determined and compared for the different types of bones. Two groups were studied: a control group (n = 20), not exposed to lead and a contaminated group (n = 30), exposed to lead from birth, first indirectly through mother's milk, and then directly through a diet containing lead acetate in drinking water (0.2%). Rats age ranged from 1 to 11 months, with approximately 1 month intervals and each of the collections had 3 contaminated rats and 2 control rats. Iliac, femur, tibia-fibula and skull have been analysed by Energy Dispersive X-ray Fluorescence Technique (EDXRF). Samples of formaldehyde used to preserve the bone tissues were also analysed by Electrothermal Atomic Absorption (ETAAS), showing that there was no significant loss of lead from the tissue to the preservative. The bones mean lead concentration of exposed rats range from 100 to 300 μg g(-1) while control rats never exceeded 10 μg g(-1). Mean bone lead concentrations were compared and the concentrations were higher in iliac, femur and tibia-fibula and after that skull. However, of all the concentrations in the different collections, only those in the skull were statistically significantly different (p < 0.05) from the other types of bones. Analysis of a radar chart also allowed us to say that these differences tend to diminish with age. The Spearman correlation test applied to mean lead concentrations showed strong and very strong positive correlations between all different types of bones. This test also showed that mean lead concentrations in bones are negatively correlated with the age of the animals. This correlation is strong in iliac and femur and very strong in tibia-fibula and skull. It was also shown that the decrease of lead accumulation with age is made by three plateaus of accumulation, which coincide, in all analysed bones, between 2nd-3rd and 9th-10th months.     

Variation of resorption rates in vivo of various bones in immature rats

The ³H-tetracycline method of measuring bone resorption in vivo was applied to the comparison of various whole bones in rats of two different ages. The rat was chosen because it grows via modelling processes and contains little, if any, cortical remodelling except for a small amount of trabecular remodelling. It was found that resorption rates in vivo are high and similar in almost all of the 18 bones measured between birth and 2 weeks of age. However, in weanling rats studied at 4–6 weeks of age, resorption rates in the skull and in the long bones had decreased significantly while remaining high in the vertebrae, scapula, sternum and pelvis. Bones of neonatal rats were quite alike in their rates of bone resorption, but the bones of the weanlings manifested significant heterogeneity in their rates.It is known that anatomic heterogeneity of metabolic turnover of various bones characterizes the mature state in humans and dogs as well. The present data are unique in that they reflect absolute resorption rates in vivo uncomplicated by the extensive re-utilization of calcium inherent in other isotopic or non-isotopic protocols.     

Bone structure and the patterns of force transmission in the cat skull (Felis catus)

Projection microradiography was used to determine the density and orientation of the force transmitting structures, i.e., trabeculae and bone lying between approximately parallel vascular canals, within the bones of cat skulls. The organisation in the skulls was confirmed statistically for a total of ten cats. The results of the observations showed that within specific areas of the skull a high degree of structural orientation and an increased density of osseous structures was present. The distribution of these characters corresponded in contiguous bones such that a continuum of structural organisation was established between the alveolar region and the site of attachment of the temporalis and masseter muscles and the glenoid region. The patterns of force transmission during jaw closure were determined when a resistance was placed initially between the canines and then the carnassials. An analysis was first carried out on dry skulls using colophonium resin to determine the direction of the force distribution. The nature and the approximate magnitude of the forces were ascertained by replacing the resin with strain gauges. The basic similarities in the strain patterns recorded from the dry skulls and those from the ten anaesthetised cats in which strain gauges had been intra-vitally implanted, substantiated the recordings made on the dry skulls. Combination of the results from the three sets of experiments defined the patterns of force distribution in the cat skull during the closure of the mandible against a resistance. The results showed that: (1) the combined action of the temporalis and masseter muscles tended to reduce the overall strain in the skull bones, and that the deformations produced by the action of the masseter were greater than that exerted by the temporalis muscles; (2) during biting, whether the resistance was placed between the canines or carnassials, compressive forces predominated in the facial bones; (3) small movements observed between facial bones indicated the presence of a flexible component within the skull, thus allowing large forces to be exerted during biting without overstressing the facial bones; (4) the glenoid fossa is part of a force bearing joint; (5) forces generated during biting were resisted within the skull by forces of an opposite nature generated within the system, the incompressible nature of bone and by the effect of the soft tissues; (6) the nature and the magnitude of the strain altered when a resistance was placed at the canines and then at the carnassials; however, the pattern of force distribution within the skull remained the same; (7) there was a direct correspondence between the detailed structural organisation of the bones and the patterns of force distribution. This conclusion would appear to apply in general to mammalian skulls. The study also emphasises the importance, neglected hitherto, of carrying out a variety of experiments to determine the patterns of force distribution in bones. The Trajectorial Theory of bone organisation is discussed and, on the basis of the results obtained, a modified theory is proposed. This states that: the structural continuum is common to the compact and cancellous bone and comprises bony bars which are aligned in the optimum direction for the transmission of force to a region in the bone or bones where it is effectively resisted.     

Theoretical morphology of tetrapod skull networks

Network models of the tetrapod skull in which nodes represent bones and links represent sutures have recently offered new insights into the structural constraints underlying the evolutionary reduction of bone number in the tetrapod skull, known as Williston's Law. Here, we have built null network model-derived generative morphospaces of the tetrapod skull using random, preferential attachment, and geometric proximity growth rules. Our results indicate that geometric proximity is the best null model to explain the disparity of skull structures under two structural constraints: bilateral symmetry and presence of unpaired bones. The analysis of the temporal occupation of this morphospace, concomitant with Williston's Law, indicates that the tetrapod skull has followed an evolutionary path toward more constrained morphological organizations.     

The Parietal Problem: How to Cut This Gordian Knot?

Although no one has disputed that the piscine progenitors of the tetrapods have a homologue of the human parietal bone, opinions differ as to where in the skull roof this homologue is located. One view holds it to be either of two interorbital bones that together surround the foramen neuroepiphysium (and the so-called pineal plates); another, that it is each of the two mesial bones which comes next in order, behind the orbital cavities. Both of these views are untenable because neither of the proposed bones has proved to be amenable to conversion to the parietal bone of man. In seeking a solution to this issue thoughts turn to the tentorium cerebelli, whose topographic relationships and comparative morphology place it in the key position as a plausible derivative of the posterior half of the cranium of the tetrapod forerunners. Following this line of reasoning, it can be suggested that the tentorial exoskeleton, here called the pluteal bones, originally was situated in the dermis superjacent to the synotic tectum. In early therian phylogeny, these skull bones were covered by the backwardly expanding cerebral hemispheres which, concomitantly, became overgrown and thus protected by epiotic exoskeleton. It follows that the likely homologues of the human parietal bones are those parts of the skull roof of the piscine progenitors of the tetrapods that lie dorsolateral to the otic capsules.     

Do foraging methods in winter affect morphology during growth in juvenile snow geese?

Physical exertion during growth can affect ultimate size and density of skeletal structures. Such changes from different exercise regimes may explain morphological differences between groups, such as those exhibited by lesser snow geese (Chen caerulescens caerulescens; hereafter snow geese) foraging in southwest Louisiana. In rice‐prairie habitats (hereafter rice‐prairies), snow geese bite off or graze aboveground vegetation, whereas they dig or grub for subterranean plant parts in adjacent coastal marshes. Grubbing involves considerably more muscular exertion than does grazing. Thus, we hypothesized that rates of bone formation and growth would be lower for juveniles wintering in rice‐prairies than those in coastal marshes, resulting in smaller bill and skull features at adulthood. First, we tested this exertion hypothesis by measuring bills, skulls, and associated musculature from arrival to departure (November–February) in both habitats in southwest Louisiana, using both banded birds and collected specimens. Second, we used the morphological data to test an alternative hypothesis, which states that smaller bill dimensions in rice‐prairies evolved because of hybridization with Ross's geese (C. rossii). Under the exertion hypothesis, we predicted that bill and skull bones of juveniles would grow at different rates between habitats. However, we found that bill and skull bones of juveniles grew similarly between habitats, thus failing to support the exertion hypothesis. Morphometrics were more likely to differ by sex or change with sampling date than to differ by habitat. We predicted that significant, consistent skewness toward smaller birds could indicate hybridization with Ross's geese, but no skewness was observed in our morphological data, which fails to support the hybridization hypothesis. Further research is needed to clarify whether snow geese wintering in Louisiana represent a single polymorphic population that segregates into individually preferred habitats, which we believe at present to be more likely as an explanation than two ecologically and spatially distinct morphotypes.     

Tissue origins and interactions in the mammalian skull vault.

During mammalian evolution, expansion of the cerebral hemispheres was accompanied by expansion of the frontal and parietal bones of the skull vault and deployment of the coronal (fronto-parietal) and sagittal (parietal-parietal) sutures as major growth centres. Using a transgenic mouse with a permanent neural crest cell lineage marker, Wnt1-Cre/R26R, we show that both sutures are formed at a neural crest-mesoderm interface: the frontal bones are neural crest-derived and the parietal bones mesodermal, with a tongue of neural crest between the two parietal bones. By detailed analysis of neural crest migration pathways using X-gal staining, and mesodermal tracing by DiI labelling, we show that the neural crest-mesodermal tissue juxtaposition that later forms the coronal suture is established at E9.5 as the caudal boundary of the frontonasal mesenchyme. As the cerebral hemispheres expand, they extend caudally, passing beneath the neural crest-mesodermal interface within the dermis, carrying with them a layer of neural crest cells that forms their meningeal covering. Exposure of embryos to retinoic acid at E10.0 reduces this meningeal neural crest and inhibits parietal ossification, suggesting that intramembranous ossification of this mesodermal bone requires interaction with neural crest-derived meninges, whereas ossification of the neural crest-derived frontal bone is autonomous. These observations provide new perspectives on skull evolution and on human genetic abnormalities of skull growth and ossification.     

Postnatal growth of skull linear measurements of Cape Hare Lepus capensis in northern China: an analysis in an adaptive context

304 skulls of Cape hare (Lepus capensis) were collected from two climatically distinct localities in northern China. With eye lens weight as a continuous age variable, postnatal growth patterns of 25 cranial linear measurements in relation to sex, growth season and region were analysed to understand the morphological basis of life history adaptation. In almost all the skull measurements, no significant differences were found between either sex or growth seasons. Principal component analysis revealed that facial elements accounted for the greatest proportion of skull morphological variation. Von Bertalanffy function was applied to describe growth trajectories of the skull elements. Based on this model, the growth rates of skull elements and the age at which they reached a certain proportion (95%) of asymptotes were compared. The results showed that skull growth exhibited an allometric pattern, with neural components attaining their final size more rapidly (at about 2–3 months old in tympanic bulla and 4–6 months old in others) than did the facial, which continued to grow well into postnatal life (at 6–10 months old). The earlier establishment of neurocranial morphology was associated with a fully developed central nervous system, which may play a key role in improving the survival of animals during the early phase of life. There was a regional difference in developmental rate of the hare skull. For all the skull parameters, northern hares had a more rapid rate of cranial growth compared to the southern, i.e. skull elements of juveniles from northern population were relatively larger at comparable ages and achieved adult size 0.5–4.0 months earlier than those from the south. In adult hares, however, no significant regional differences in any of the skull parameters were present. Adaptive explanations for the regional difference in ontogenetic pattern of skull morphology include age‐specific thermoregulation constraint, season‐related food availability and age‐dependent predation pressure. Based on the findings of this study, it is suggested that the postnatal growing period represents a crucial time of life, and that improvement of survivorship when young by growth adaptation forms an important aspect of the hare's life history strategies. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 78 , 343–353.     

Somatostatin receptors are restricted to a subpopulation of osteoblast-like cells during endochondral bone formation.

Specific binding sites for the peptide hormone somatostatin have previously been demonstrated in long bones from neonatal rats. In the present study, the distribution of somatostatin receptors during embryonic bone formation has been investigated using the stable radioiodinated somatostatin analogue, SDZ 204-090. Somatostatin receptors in rat long bones were first detectable at the time of invasion of the cartilage model by osteogenic cells. Initially, receptors were detectable throughout the region occupied by osteogenic cells. As bone growth proceeded, however, receptors were restricted to the region of most recent invasion of the hypertrophic cartilage, where osteoid had not yet been deposited. In vivo labelling studies in neonatal rats were carried out to identify the cells bearing somatostatin receptors. Receptors were present in a restricted region of the metaphysis, immediately adjacent to the hypertrophic cartilage. Chondrocytes, osteoclasts, and mature osteoblasts were not labelled by the radioligand. The labelled cells were often apposed to remnants of cartilage matrix and stained positively for the osteoblast marker, alkaline phosphatase. Thus the cells with specific somatostatin-binding sites were probably osteoblast precursor cells. Specific binding was detectable in all endochondral bones examined, including those of the skull, but no specific binding was found in the membrane bones of the skull. These data suggest that somatostatin is involved in the regulation of osteoblast differentiation during endochondral bone formation.