Ontogenetic variation in the stratum granulosum of the epidermis of Chaetophractus vellerosus (Xenarthra,Dasypodidae) in relation to the development of cornified scales

The epidermis of mammals is characterized by having a stratum granulosum that produces an orthokeratotic stratum corneum, different from the typical reptilian parakeratotic stratum. Nonetheless, some mammals show distinct degrees of parakeratosis in epidermal regions with few or no pilose follicles (e.g., areas subjacent to cornified scales). With respect to the epidermis and the development of cornified scales in the Dasypodidae, previous studies have supported the presence of a continuous stratum granulosum without any variations during ontogeny. This condition, in which the cornified scales develop without a loss of the stratum granulosum, was interpreted as primitive for eutherians. The present contribution expands the knowledge on the epidermis of Chaetophractus vellerosus in distinct ontogenetic stages in order to determine whether the cornified scales show the same developmental pattern as in other eutherians. The presence of a stratum granulosum in C. vellerosus neonates and its reduction in more advanced ontogenetic stages, in direct relationship with cornified scale development, supports the hypothesis that the partial parakeratosis in the xenarthran integument is secondary, as in other eutherians, and can be interpreted as a derived character state.     

Ontogenetic criteria to distinguish vertebral types on the debated xenarthran synsacrum

The presence of a synsacrum formed by the fusion of vertebrae that come into closed contact with the ilium and ischium is a feature that characterizes the clade Xenarthra. Nevertheless, the proper identity of each vertebral element that forms it is a matter of discussion. In this article, we provide ontogenetic information about skeletal ossification of the xenarthran synsacrum and define the position of the sacrocaudal limit within it. We analyzed the synsacrum of 25 specimens of nonadult and 101 adult armadillos and anteaters: Dasypus hybridus, D. novemcinctus, Chaetophractus vellerosus, C. villosus, Tamandua tetradactyla, and Myrmecophaga tridactyla. Two sets of vertebrae were identified: an anterior set, often attached to the iliac bones, in which transverse processes are originated mainly from an expansion of the base of the neural arches, and secondarily from a lateroventral ossification center. A posterior set is characterized by a series of vertebrae along which extra lateral ossifications (described here for the first time) are developed and form exclusively the transverse processes. Among armadillos, the sacrocaudal limit is set between the last vertebrae attached to the iliac bones and the first vertebrae that form the dorsal border of the sacroischial fenestra. In addition, anterior free caudals also showed extra lateral ossifications forming exclusively the transverse processes, supporting the notion that more posterior synsacrals are in fact caudal vertebrae that were incorporated to the synsacrum. In pilosans, the sacrocaudal limit is set between the first vertebrae that come into contact with the ischial bones and the immediately anterior one. However, the pattern of homologies is obscured by the low resolution in the ontogenetic sequence when compared to that of armadillos. J. Morphol. 276:494–502, 2015. © 2014 Wiley Periodicals, Inc.     

Morphology and ultrastructure of possible integumentary sense organs in the estuarine crocodile (Crocodylus porosus)

The skins of crocodylids and gavialids can be distinguished from those of alligatorids by the presence of darkly pigmented pits, known as integumentary sense organs (ISOs), on the postcranial scales. The structure of ISOs, in Crocodylus porosus, was studied using light microscopy and scanning and transmission electron microscopy. The stratum corneum of the epidermis in the area of the ISO is thinner, while the stratum germinativum is thicker, relative to other regions of the integument. Beneath the epidermal layer the ISO region has a paucity of collagen fibers relative to the rest of the dermis. Widely dispersed fibrocytes, nerve terminals, and chromatophores occur throughout the ISO region of the dermis, but these elements are concentrated in the area immediately beneath the stratum germinativum in the ISO region. The morphology of the ISOs suggests that they are sensory organs. It has traditionally been assumed that sensory organs on the amniote integument have a mechanosensory function. However, alternate functional interpretations of this structure are possible, and a resolution awaits further work. © 1996 Wiley-Liss, Inc.     

Morphology of female genital tracts in Dasypodidae (Xenarthra,Mammalia): a comparative survey

Previous works about comparative spermatology in Dasypodidae determined that sperm morphology is a striking variable among genera. It was suggested that this sperm feature may be related to specific morphologies of the female reproductive tract. The present comparative study of the morphology of the female genital tract from seven species corresponding to six genera of Dasypodidae is aimed to determine the main similarities and differences between the species and to establish a possible correlation with the sperm shapes and sizes. Genital tracts were studied macroscopically and histologically. Dasypus hybridus has disk-shaped ovaries and the cortex occupies almost all the organ with a single oocyte in each follicle. Tolypeutes matacus, Chaetophractus villosus, Chaetophractus vellerosus, Zaedyus pichiy, Cabassous chacoensis and Clamyphorus truncatus possess ovoid and elongated ovaries, with both longitudinally polarized cortex and medulla, and the peculiar presence of several oocytes in the same follicle. D. hybridus and T. matacus have a simple pear-shaped uterus, but in the other species the uterus is pyramid shaped and bicornuate. The uterine cervix is very long in all studied species. Only T. matacus presents a true vagina as in most eutherian mammals; on the other hand, in the other species a urogenital sinus is observed. The structure of female reproductive tracts in Dasypodidae contains a mixture of assumedly primary and other derived features. According to the different morphologies of the regions analyzed, a classification of the female genital tracts in three groups can be performed (group 1: Dasypus; group 2: Tolypeutes; group 3: Chaetophractus, Zaedyus, Cabassous, Clamyphorus) and a correlation between each group and a specific sperm morphology can be established.     

Comparative ossification sequence and skeletal development of the postcranium of palaeognathous birds (Aves: Palaeognathae)

Palaeognaths constitute one of the most basal lineages of extant birds, and are also one of the most morphologically diverse avian orders. Their skeletal development is relatively unknown, in spite of their important phylogenetic position. Here, we compare the development of the postcranial skeleton in the emu (Dromaius novaehollandiae), ostrich (Struthio camelus), greater rhea (Rhea americana) and elegant crested‐tinamou (Eudromia elegans), focusing on ossification. All of these taxa are characterized by element loss in the appendicular skeleton, but there are several developmental mechanisms through which this loss occurs, including failure to chondrify, failure to ossify and fusion of cartilages prior to ossification. Further evidence is presented here to support a reduction in size of skeletal elements resulting in a delay in the timing of ossification. This study provides an important first look at the timing and sequence of postcranial ossification in palaeognathous birds, and discusses the influence of changes in the pattern of skeletal development on morphological evolution.     

Ecological differences between two sympatric species of armadillos (Xenarthra,Mammalia) in a temperate region of Argentina

Morpho-physiological specialization related to foraging can act as constraints on behaviour and ecological patterns of abundance and distribution. We tested this prediction in two species (weeping or screaming hairy armadillos Chaetophractus vellerosus Gray, 1865 and mulitas Dasypus hybridus Desmarest, 1804) that represent the two subfamilies of armadillos (Dasypodidae, Xenarthra): Euphractinae and Dasypodinae. The first subfamily possesses a well-developed masticatory apparatus that is considered primitive within the Xenarthra, while Dasypodinae show reductions in various aspects of cranial morphology. We sampled signs (burrows and foraging holes) and captured both species on 34 farms randomly selected in the north-eastern Pampas region of Argentina. We analyzed several niche dimensions. The two species showed significant differences in habitat use, seasonal patterns and diet. Weeping armadillos were generalists in their diet and active throughout the year. They were associated with calcareous-sand soil, as expected for a burrowing animal of the deserts. They tolerated a wide range of environmental conditions. We found that mulitas are myrmecophagous, and that they demonstrated a reduction in body temperature and activity during the cold season. As expected from their geographical distribution, mulitas used mainly vegetation with high cover and were associated with humic soils. Niche segregation between the two species of armadillos appeared to originate from different degrees of dietary specialization.     

Anatomy of ovary and ovule in dandelions (Taraxacum, Asteraceae)

The genus Taraxacum Wigg. (Asteraceae) forms a polyploid complex within which there are strong links between the ploidy level and the mode of reproduction. Diploids are obligate sexual, whereas polyploids are usually apomictic. The paper reports on a comparative study of the ovary and especially the ovule anatomy in the diploid dandelion T. linearisquameum and the triploid T. gentile. Observations with light and electron microscopy revealed no essential differences in the anatomy of both the ovary and ovule in the examined species. Dandelion ovules are anatropous, unitegmic and tenuinucellate. In both sexual and apomictic species, a zonal differentiation of the integument is characteristic of the ovule. In the integumentary layers situated next to the endothelium, the cell walls are extremely thick and PAS positive. Data obtained from TEM indicate that these special walls have an open spongy structure and their cytoplasm shows evidence of gradual degeneration. Increased deposition of wall material in the integumentary cells surrounding the endothelium takes place especially around the chalazal pole of the embryo sac as well as around the central cell. In contrast, the integumentary cells surrounding the micropylar region have thin walls and exhibit a high metabolic activity. The role of the thick-walled integumentary layers in the dandelion ovule is discussed. We also consider whether this may be a feature of taxonomic importance.     

Skeletogenesis and sequence heterochrony in rodent evolution, with particular emphasis on the African striped mouse, Rhabdomys pumilio (Mammalia)

Data documenting skeletal development in rodents, the most species-rich ‘order’ of mammals, are at present restricted to a few model species, a shortcoming that hinders exploration of the morphological and ecological diversification of the group. In this study we provide the most comprehensive sampling of rodent ossification sequences to date, with the aim of exploring whether heterochrony is ubiquitous in rodent evolution at the onset of skeletal formation. The onset of ossification in 17 cranial elements and 24 postcranial elements was examined for eight muroid and caviomorph rodent species. New data are provided for two non-model species. For one of these, the African striped mouse, Rhabdomys pumilio, sampling was extended by studying 53 autopodial elements and examining intraspecific variation. The Parsimov method of studying sequence heterochrony was used to explore the role that changes in developmental timing play in early skeletal formation. Few heterochronies were found to diagnose the muroid and caviomorph clades, suggesting conserved patterning in skeletal development. Mechanisms leading to the generation of the wide range of morphological diversity encapsulated within Rodentia may be restricted to later periods in development than those studied in this work. Documentation of skeletogenesis in Rhabdomys indicates that intraspecifc variation in ossification sequence pattern is present, though not extensive. Our study suggests that sequence heterochrony is neither pivotal nor prevalent during early skeletal formation in rodents.     

Origin of archosaurian integumentary appendages: the bristles of the wild turkey beard express feather-type beta keratins

The discovery that structurally unique "filamentous integumentary appendages" are associated with several different non-avian dinosaurs continues to stimulate the development of models to explain the evolutionary origin of feathers. Taking the phylogenetic relationships of the non-avian dinosaurs into consideration, some models propose that the "filamentous integumentary appendages" represent intermediate stages in the sequential evolution of feathers. Here we present observations on a unique integumentary structure, the bristle of the wild turkey beard, and suggest that this non-feather appendage provides another explanation for some of the "filamentous integumentary appendages." Unlike feathers, beard bristles grow continuously from finger-like outgrows of the integument lacking follicles. We find that these beard bristles, which show simple branching, are hollow, distally, and express the feather-type beta keratins. The significance of these observations to explanations for the evolution of archosaurian integumentary appendages is discussed.     

Osteoderm morphology and development in the nine-banded armadillo, Dasypus novemcinctus (Mammalia, Xenarthra, Cingulata)

Among modern mammals, armadillos (Xenarthra, Cingulata) are the only group that possesses osteoderms, bony inclusions within the integument. Along the body, osteoderms are organized into five discrete assemblages: the head, pectoral, banded, pelvic, and tail shields. The pectoral, banded, and pelvic shields articulate to form the carapace. We examined osteoderm skeletogenesis in the armadillo Dasypus novemcinctus using serial and whole-mount histochemistry. Compared with the rest of the skeleton, osteoderms have a delayed onset of development. Skeletogenesis begins as condensations of osteoblasts secreting osteoid, localized within the papillary layer of the dermis. Osteoderm formation is asynchronous both within each shield and across the body. The first osteoderms to mineralize are situated within the pectoral shield of the carapace, followed by elements within the banded, head, pelvic, and tail shields. In general, within each shield ossification begins craniomedially and proceeds caudally and laterally, except over the head, where the earliest elements form over the frontal and parietal bones. The absence of cartilage precursors indicates that osteoderms are dermal elements, possibly related to the all-encompassing vertebrate dermal skeleton (exoskeleton). The mode of development of D. novemcinctus osteoderms is unlike that described for squamate osteoderms, which arise via bone metaplasia, and instead is comparable with intramembranously derived elements of the skull.     

Ossification heterochrony in the therian postcranial skeleton and the marsupial-placental dichotomy.

Postcranial ossification sequences in 24 therian mammals and three outgroup taxa were obtained using clear staining and computed tomography to test the hypothesis that the marsupial forelimb is developmentally accelerated, and to assess patterns of therian postcranial ossification. Sequence rank variation of individual bones, phylogenetic analysis, and algorithm-based heterochrony optimization using event pairs were employed. Phylogenetic analysis only recovers Marsupialia, Australidelphia, and Eulipotyphla. Little heterochrony is found within marsupials and placentals. However, heterochrony was observed between marsupials and placentals, relating to late ossification in hind limb long bones and early ossification of the anterior axial skeleton. Also, ossification rank position of marsupial forelimb and shoulder girdle elements is more conservative than that of placentals; in placentals the hind limb area is more conservative. The differing ossification patterns in marsupials can be explained with a combination of muscular strain and energy allocation constraints, both resulting from the requirement of active movement of the altricial marsupial neonates toward the teat. Peramelemorphs, which are comparatively passive at birth and include species with relatively derived forelimbs, differ little from other marsupials in ossification sequence. This suggests that ossification heterochrony in marsupials is not directly related to diversity constraints on the marsupial forelimb and shoulder girdle.     

Skeletal Morphogenesis of Microbrachis and Hyloplesion (Tetrapoda: Lepospondyli), and Implications for the Developmental Patterns of Extinct,Early Tetrapods

The ontogeny of extant amphibians often is used as a model for that of extinct early tetrapods, despite evidence for a spectrum of developmental modes in temnospondyls and a paucity of ontogenetic data for lepospondyls. I describe the skeletal morphogenesis of the extinct lepospondyls Microbrachis pelikani and Hyloplesion longicostatum using the largest samples examined for either taxon. Nearly all known specimens were re-examined, allowing for substantial anatomical revisions that affect the scoring of characters commonly used in phylogenetic analyses of early tetrapods. The palate of H. longicostatum is re-interpreted and suggested to be more similar to that of M. pelikani, especially in the nature of the contact between the pterygoids. Both taxa possess lateral lines, and M. pelikani additionally exhibits branchial plates. However, early and rapid ossification of the postcranial skeleton, including a well-developed pubis and ossified epipodials, suggests that neither taxon metamorphosed nor were they neotenic in the sense of branchiosaurids and salamanders. Morphogenetic patterns in the foot suggest that digit 5 was developmentally delayed and the final digit to ossify in M. pelikani and H. longicostatum. Overall patterns of postcranial ossification may indicate postaxial dominance in limb and digit formation, but also more developmental variation in early tetrapods than has been appreciated. The phylogenetic position and developmental patterns of M. pelikani and H. longicostatum are congruent with the hypothesis that early tetrapods lacked metamorphosis ancestrally and that stem-amniotes exhibited derived features of development, such as rapid and complete ossification of the skeleton, potentially prior to the evolution of the amniotic egg.     

FURTHER CYTOLOGICAL STUDIES OF A PERIODIC ACID-SCHIFF'S SUBSTANCE IN THE OVULES OF PASPALUM ORBICULARE AND P. LONGIFOLIUM

A periodic acid-Schiff's substance present in the micropylar end of the ovules of Paspalum orbiculare and P. longifolium was further studied by light and electron microscopy of glutaraldehyde-osmium-fixed and freeze-substituted, osmium-fixed tissues. The PAS substance is water soluble and is found in intercellular spaces between the nucellus and inner integument, the inner and outer integuments, the outer integument and ovary wall, and in the micropyle. Structurally the substance consists of fibrils embedded in a dense, amorphous matrix and may be associated with membranous structures in special layers between the plasmalemma and the cell wall in nucellar and integumentary cells. Part of the water soluble substance is believed to be secreted from the nucellar and integumentary cells. A large amount of this substance may be formed as a result of the dissolution of about one third of the distal micopylar portion of the outer integument prior to anthesis. Many of the electron-dense fibrils seem to be fibrillar intercellular substances and others appear to originate from the cell walls, including the cuticle. Both the matrix and the fibrils may be chemically heterogeneous and together form a mucilagenous substance which may facilitate the final growth of pollen tubes in these two species.     

Osteoderm morphology in recent and fossil euphractine xenarthrans

The presence of osteoderms within the integument, forming a carapace, is one of the most distinctive features of armadillos with the external morphology of these elements forming the basis of most systematic schemes. This is especially true for fossil taxa, where these elements are most frequent in the palaeontological record. A detailed study of osteoderms from the cephalic shield and different regions of the dorsal armour of Chaetophractus villosus (Euphractinae, Xenarthra) was made and compared to those of the extant genus Dasypus (Dasypodinae, Xenarthra), and the extinct genus ?Eutatus. Three distinct histological zones were recognized: outer and inner zones are thin, formed by regular compact bone, the middle zone is thicker, with large cavities that contain mainly adipose tissue, hair follicles, and sweat and sebaceous glands. The internal structure of ?Eutatus (also a member of Euphractinae) osteoderms is close to that of C. villosus, consistent with the notion that these taxa are phylogenetically closely related. In contrast, Dasypus shows marked differences. Dasypus shows hair follicles associated with both gland types (sweat and sebaceous) and connected to foramina on the external surface. Although not observed in adult C. villosus, it has been documented during embryonic development, only to atrophy later in ontogeny. Furthermore, the presence of red bone marrow is rare in C. villosus, but widespread in Dasypus novemcinctus osteoderms. These results suggest an early split of both subfamilies and support the hypothesis that the Euphractinae are more derived than the Dasypodinae.     

Palatability of the tissues of the holothurian Thyone briareus (Lesueur) to fish

The evolutionary adaptations of Thyone briareus (Lesueur) for predator repulsion were investigated. Killifish, Fundulus diaphanus (Lesueur) were fed bite-sized pieces of the integument, gonads, stomach, intestines, longitudinal muscle bands, and retractor muscles of Thyone briareus to determine palatability. Of the tissues tested, gravid ovaries and integument were least palatable to the fish.Noxiousness of the integument and gonads of T. briareus would enhance the survival of sea cucumbers more than noxiousness of other tissues. This indicates that the mechanisms involved in the repulsion of fish predators have evolved as antipredator adaptations.     

GLANDULAR HAIRS IN THE ARBUTUS XALAPENSIS COMPLEX IN RELATION TO HERBIVORY

The morphological boundaries between Arbutus xalapensis and A. glandulosa are diffuse. Many individuals share traits of both species. The character most commonly used to distinguish the species is the presence of glandular hairs in A. glandulosa. Comparisons in the field of the number of colonies and level of defoliation by Eucheira socialis (Lepidoptera, Pieridae), an Arbutus-specific herbivore, showed that the damage is greater for glabrous than pilose trees and greater for pilose than glandular trees. Additionally, the geographic distribution of glandular trees is strongly correlated with that of E. socialis while that of non-glandular trees is not. We suggest that the glandular and non-glandular forms could belong to one single polymorphic species in which the glandular characteristic is maintained by differential herbivory.     

A Correlation Between Pituitary and Integumentary Structure in the Nine-Spined Stickleback,Pungitius pungitius L.

Benjamin, M. 1980. A correlation between pituitary and integumentary structure in the nine-spined stickleback, Pungitius pungitius L. (Department of Anatomy, University College, Cardiff, Wales, U.K.) — Acta zool. (Stockh.) 61(2): 105–109. Naturally occurring, large pituitary cysts, that almost excluded prolactin cells from the pituitary of Pungitius pungitius L., offered a unique opportunity to study a target organ for prolactin (the integument) in fish that were “partially hypophysectomised” without any accompanying surgical trauma. In fish with large pituitary cysts, the epidermis from the lateral body wall was thinner and its mucocytes less abundant, than in fish with normal pituitaries and thus many prolactin cells. In support of the hypothesis that prolactin produced the observed integumentary changes, was the similarity of other pituitary cells in animals with and without cysts. Evidently, prolactin can influence the integument of Pungitius, even though it does not seem essential for freshwater survival.     

The histogenesis of integuments in some species of menispermanceae

The mode of initiation and development of integuments was investigated in six species of five genera in Menispermanceae, which have bitegmic and unitegmic ovules. The species investigated have similar integumentary structures at maturity in each of the bitegmic and unitegmic ovules. In bitegmic ovules (e.g.Cocculus), both integuments are for the most part two-cell layered. The initiation of inner integument (ii) begins with divisions of dermal cells of the nucellar primordium. The initiation of the outer integument (oi) commences with divisions of subdermal cells. In unitegmic ovules (e.g.Stephania), the integument is initiated by periclinal divisions of dermal cells, and cells of subdermal origin (which may represent the oi in case of bitegmy) form a small swelling on the raphal side and, on the antiraphal side, are included in the base of the single integument. Unitegmy of Menispermanceae (at least in the case of the genera investigated) seems to have been derived through elimination of oi, rather than through “integumentary shifting” (Bouman and Calis, 1977), a process suggested for explanation of unitegmy as in Ranunculaceae.     

Skeletal development in the Chinese soft‐shelled turtle Pelodiscus sinensis (Testudines: Trionychidae)

We investigated the development of the whole skeleton of the soft‐shelled turtle Pelodiscus sinensis, with particular emphasis on the pattern and sequence of ossification. Ossification starts at late Tokita‐Kuratani stage (TK) 18 with the maxilla, followed by the dentary and prefrontal. The quadrate is the first endoskeletal ossification and appears at TK stage 22. All adult skull elements have started ossification by TK stage 25. Plastral bones are the first postcranial bones to ossify, whereas the nuchal is the first carapacial bone to ossify, appearing as two unstained anlagen. Extensive examination of ossification sequences among autopodial elements reveals much intraspecific variation. Patterns of ossification of cranial dermal elements are more variable than those of endochondral elements, and dermal elements ossify before endochondral ones. Differences in ossification sequences with Apalone spinifera include: in Pelodiscus sinensis the jugal develops relatively early and before the frontal, whereas it appears later in A. spinifera; the frontal appears shortly before the parietal in A. spinifera whereas in P. sinensis the parietal appears several stages before the frontal. Chelydrids exhibit an early development of the postorbital bone and the palatal elements as compared to trionychids. Integration of the onset of ossification data into an analysis of the sequence of skeletal ossification in cryptodirans using the event‐pairing and Parsimov methods reveals heterochronies, some of which reflect the hypothesized phylogeny considered taxa. A functional interpretation of heterochronies is speculative. In the chondrocranium there is no contact between the nasal capsules and planum supraseptale via the sphenethmoid commissurae. The pattern of chondrification of forelimb and hind limb elements is consistent with a primary axis and digital arch. There is no evidence of anterior condensations distal to the radius and tibia. A pattern of quasi‐ simultaneity is seen in the chondrogenesis of the forelimb and the hind limb. J. Morphol. 2009. © 2009 Wiley‐Liss, Inc.