Journal of Morphology

Higashiyama, Hiroki; Kuratani, Shigeru

doi: 10.1002/jmor.20241pmid: N/A

Cover illustration. Morphology of the trigeminal nerve is closely related to the embryonic composition of the jaw or oral apparatus of vertebrates. In this issue of the Journal of Morphology, Higashiyama and Kuratani (pp. 17–38) investigate the development of the maxillary nerve, a component of the trigeminal nerve, generally regarded as a branch specifically assigned to the upper jaw of gnathostomes. The authors tried to reconstruct this branch's evolution by comparative embryological observation. The cover image shows the embryos of the Mus musculus (left) and Scyliorhinus torazame (right) immunostained to visualize peripheral nerves. Trigeminal nerves are highlighted by hand drawing.

Wilpe, Erna; Groenewald, Hermanus Bernardus

doi: 10.1002/jmor.20188pmid: 24142864

The morphology of Kupffer cells was examined in the liver of the juvenile Nile crocodile using light microscopy and transmission electron microscopy. Pleomorphic Kupffer cells were located in the sinusoids, in the space of Disse, in the hepatic parenchyma and often connected adjacent sinusoids. The cell surfaces were irregular due to the presence of filopodia and lamelliapodia with phagocytosis of white blood cells, red blood cells and thrombocytes being evident. The cells were in close contact with endothelial cells and pit cells in the sinusoidal lumen and with stellate cells in the space of Disse. The cytoplasm contained large phagosomes comprising a combination of ceroid pigment, melanosomes and siderosomes. The nuclei were often indented and eccentrically placed due to the presence of the phagosomes. Conspicuous clusters of membrane‐bound tubular organelles with a filamentous or crystalline interior were observed in the cytoplasm. The clusters were sometimes separated into smaller groups around phagosomes. A clear zone existed between the limiting membrane and the interior of these tubular organelles with the electron‐dense interior profiles being, respectively, circular, angular or divided. The tubular organelles have not previously been described in Kupffer cells and possibly represent lysosomes with specialized functions. Mitochondria, microtubules, Golgi profiles, granular and smooth endoplasmic reticulum, and a few cytoplasmic lipid droplets were also present. The presence of the tubular organelles and the occurrence of the Kupffer cells in different locations in the liver of the juvenile Nile crocodile are indicative of particularly active and mobile cells. J. Morphol. 275:1–8, 2014. © 2013 Wiley Periodicals, Inc.

Oliveira, Cléo D.C.; Sartori, André F.

doi: 10.1002/jmor.20190pmid: 24027039

The arenophilic system of anomalodesmatan clams comprises multicellular glands, muscular papillae, and radial lines of adhesive secretion, which glue sand grains and other extraneous particles to the external surface of the shell. The presence and morphology of these organs have been established in an increasing number of taxa, but arenophilic glands were not previously known to occur in the deep‐sea, carnivorous family Cuspidariidae. Dissections, histological sections and ultrastructural examination of members of the cuspidariid genera Cuspidaria and Cardiomya revealed a functional arenophilic system positioned around the siphonal apparatus. Glands are contained in muscular papillae at the posterior tip of the siphonal sheath, from where they deposit their adhesive secretion onto the shell rostrum. Discovery of an arenophilic system in cuspidariid clams adds support to the idea that the glands are a synapomorphy of Anomalodesmata, secondarily absent in only one of the major component branches (the clade joining Thraciidae, Cleidothaeridae, and Myochamidae). Moreover, similarity between the arenophilic papillae we observed on the siphonal sheath of Cuspidaria, Cardiomya, and Myonera, and literature reports on the crown of tentacles of Multitentacula is puzzling and highlights the need for further studies of the latter genus. J. Morphol. 275:9–16, 2014. © 2013 Wiley Periodicals, Inc.

Higashiyama, Hiroki; Kuratani, Shigeru

doi: 10.1002/jmor.20193pmid: 24151219

The trigeminal, the fifth cranial nerve of vertebrates, represents the rostralmost component of the nerves assigned to pharyngeal arches. It consists of the ophthalmic and maxillomandibular nerves, and in jawed vertebrates, the latter is further divided into two major branches dorsoventrally. Of these, the dorsal one is called the maxillary nerve because it predominantly innervates the upper jaw, as seen in the human anatomy. However, developmentally, the upper jaw is derived not only from the dorsal part of the mandibular arch, but also from the premandibular primordium: the medial nasal prominence rostral to the mandibular arch domain. The latter component forms the premaxillary region of the upper jaw in mammals. Thus, there is an apparent discrepancy between the morphological trigeminal innervation pattern and the developmental derivation of the gnathostome upper jaw. To reconcile this, we compared the embryonic developmental patterns of the trigeminal nerve in a variety of gnathostome species. With the exception of the diapsid species studied, we found that the maxillary nerve issues a branch (nasopalatine nerve in human) that innervates the medial nasal prominence derivatives. Because the trigeminal nerve in cyclostomes also possesses a similar branch, we conclude that the vertebrate maxillomandibular nerve primarily has had a premandibular branch as its dorsal element. The presence of this branch would thus represent the plesiomorphic condition for the gnathostomes, implying its secondary loss within some lineages. The branch for the maxillary process, more appropriately called the palatoquadrate component of the maxillary nerve (V2), represents the apomorphic gnathostome trait that has evolved in association with the acquisition of an upper jaw. J. Morphol. 275:17–38, 2014. © 2013 Wiley Periodicals, Inc.

Arbour, Victoria M.; Burns, Michael E.; Bell, Phil R.; Currie, Philip J.

doi: 10.1002/jmor.20194pmid: 24105904

Ankylosaurian dinosaurs are most notable for their abundant and morphologically diverse osteoderms, which would have given them a spiky appearance in life. Isolated osteoderms are relatively common and provide important information about the structure of the ankylosaur dermis, but fossilized impressions of the soft‐tissue epidermis of ankylosaurs are rare. Nevertheless, well‐preserved integument exists on several ankylosaur fossils that shows osteoderms were covered by a single epidermal scale, but one or many millimeter‐sized ossicles may be present under polygonal, basement epidermal scales. Evidence for the taxonomic utility of ankylosaurid epidermal scale architecture is presented for the first time. This study builds on previous osteological work that argues for a greater diversity of ankylosaurids in the Dinosaur Park Formation of Alberta than has been traditionally recognized and adds to the hypothesis that epidermal skin impressions are taxonomically relevant across diverse dinosaur clades. J. Morphol. 275:39–50, 2014. © 2013 Wiley Periodicals, Inc.

Faszewski, Ellen E.; Sljivo, Selsebil; Kriszun, Lisa; Kaltenbach, Jane C.

doi: 10.1002/jmor.20195pmid: 24127169

Apoptosis (programmed cell death) occurs during normal development of anurans in organs such as gills, gut, and tail. For example, apoptotic cells have been reported in the luminal epithelium along the length of the digestive tract of both larvae and frogs; however, timing of the peak number of such cells varies in different species. The purpose of the present study was to ascertain whether apoptosis also varies by species during metamorphic restructuring of the skin (as larval epithelium is replaced by adult epidermis). To determine this, cross‐sections of dorsal skin from representative larval stages and frogs of Rana pipiens, R. catesbeiana, and Ceratophrys ornata were incubated with monoclonal antibody against active caspase‐3, one of the main enzymes in the apoptotic cascade. We observed apoptotic cells in the epidermis of the skin of the three species and found that such cells were more numerous in larval stages than in frogs and more abundant in the two ranid species than in C. ornata. These results contribute to our understanding of metamorphic changes in anuran skin. J. Morphol. 275:51–56, 2014. © 2013 Wiley Periodicals, Inc.

Kellis, Eleftherios; Balidou, Anna

doi: 10.1002/jmor.20196pmid: 24127198

A tendinous inscription divides the semitendinosus muscle in two parts and it may have an effect on its function. The purpose of this study was to determine the effects of joint position and gender on the tendinous inscription morphology. Ultrasonography scans were taken from 76 young males and females at rest, in nine combinations of hip and knee joint angles. The length of the tendinous inscription arms and the angles formed by the two arms (apex angle), the tendinous inscription with the superficial (surface angle), and deep (deep angle) aponeurosis were determined. The tendinous inscription was clearly visible in 70 (out of 76) subjects. Analysis of variance designs showed that increasing hip flexion angle from 0 to 90° increased the long arm and muscle thickness but decreased the short tendinous inscription arm (P < 0.05). Changing knee flexion angle from 0 to 90° was accompanied by a longer tendinous inscription arm and an increased apex angle (P < 0.05). Long arm length and muscle thickness significantly increased from the shortest (hip 0° – knee 90°) to the longest muscle lengths (hip 0° – knee 90°). Males had a significantly higher surface, apex, and deep angle and a lower normalized tendinous inscription long arm than females (P < 0.05). These results indicate that the effect of the tendinous inscription (if any) on semitendinous muscle function depends on hip and knee joint angle while it may be gender dependent. J. Morphol. 275:57–64, 2014. © 2013 Wiley Periodicals, Inc.

Chiarini‐Garcia, Hélio; Vieira, Francisco O.; Godinho, Hugo P.

doi: 10.1002/jmor.20197pmid: 24127235

The reproductive system of some fish species presents elaborate mechanisms by which the females store spermatozoa inside their ovaries, keeping them viable for fertilization for an extended period of time. However, as intriguing as this sperm storage is, it is not yet understood how the sperm can remain viable in the ovary. Aiming to understand this phenomenon, the epithelium covering the ovarian lamellae, that is, the germinal epithelium, of the Cangati (Trachelyopterus galeatus), an inseminating catfish, was evaluated taking into account the different stages of the annual reproductive cycle. The germinal epithelium morphology changed during the annual reproductive cycle, presumably in preparation to receive the spermatozoa and keep them viable until fertilization. There was a progressive increase of the epithelium height. Also the number of intercellular junctions, desmosomes, and extended tight junctions, apparently increased forming chains that could be regarded as a barrier to isolate the sperm from the female immune system. Synthetic organelles were active releasing cytoplasmic granules and secretion in the epithelial enfolds in which the spermatozoa were deeply embedded. Concomitantly, oogonium nests were formed in the germinal epithelium during early folliculogenesis. J. Morphol. 275:65–75, 2014. © 2013 Wiley Periodicals, Inc.

Kaptan, Engin; Bolkent, Sehnaz

doi: 10.1002/jmor.20198pmid: 24127244

The thumb pad is one of the most common secondary sexual characteristics in frogs. Although it is known that amphibian skin has affinity for several lectins, there is no report regarding lectin‐binding affinity of the thumb pad or its structural components. This study investigated localization and seasonal variation of specific carbohydrate moieties of glycoconjugates in both the epidermal and dermal components of the frog thumb pad at the light microscopic level using lectin histochemistry. The study consisted of four seasonal groups of the frog species, Pelophylax ridibundus (Synonym of Rana ridibunda): active, prehibernating, hibernating and posthibernating. Four horseradish peroxidase conjugated lectins were employed. It was found that dolichos biflorus agglutinin (DBA), wheat germ agglutinin (WGA), and ulex europaeus (UEAI) gave positive reactions in both epidermal layers and breeding glands. These three lectins bound specific secretory cells in the breeding glands, and the distribution of the cells and epithelial lectin reactions exhibited seasonal changes. In addition, UEA‐I and peanut agglutinin (PNA) showed an affinity in granular glands and the granular zone of mixed glands. Generally, epidermal lectin binding showed dense affinity during the posthibernation period. DBA, UEA‐I, and WGA‐specific cells in the mucous gland decreased gradually until the posthibernation period. These findings suggest that differences of lectin binding in the thumb pad may be related to functional activities and, thus, seasonal adaptations. Moreover, the presence of specific lectin‐binding cells in the breeding glands indicated that they consisted of heterogeneous secretory cell composition or that the cells were at different secretory stages. J. Morphol. 275:76–86, 2014. © 2013 Wiley Periodicals, Inc.

Oliveira, Leonardo; Costa Prudente, Ana Lúcia; Zaher, Hussam

doi: 10.1002/jmor.20199pmid: 24127255

Geophis belongs to the goo‐eating dipsadine assemblage of snakes that are known to feed exclusively on earthworms, snails, and slugs. Although the unusual feeding strategies of the goo‐eating dipsadines are well known (but poorly documented), little attention has been paid to their internal anatomy. Here, we describe a new and noteworthy morphological and histochemical condition of the infralabial glands in three species of Geophis (G. brachycephalus, G. nasalis and G. semidoliatus), all earthworm feeders. Their infralabial glands are constituted of two distinct parts: an anterolateral portion composed of mucous and seromucous cells that stretches from the tip of the dentary to the corner of the mouth, and a tubular posteromedial portion that is exclusively seromucous. The anterolateral portion receives fibers of the levator anguli oris muscle that attaches on its posterodorsal extremity while the posteromedial portion extends posteriorly to the corner of the mouth where it receives fibers of the adductor mandibulae externus medialis muscle. Furthermore, the posteromedial portion of the infralabial gland is constituted by large acini filled with secretion that is periodic acid‐Schiff positive. These acini release their secretion directly into a large lumen located in the middle of the glandular portion. In the three species examined, the supralabial glands show a traditional configuration, being constituted of mucous and seromucous cells and retaining an enlarged part in its caudal region that resembles a Duvernoy's gland. The presence in Geophis of an expanded lumen in part of the infralabial gland that is compressed by an adjacent muscle suggests a more specialized role for the secretion produced by these glands that may not be related to envenomation but rather to prey transport and mucus control. J. Morphol. 275:87–99, 2014. © 2013 Wiley Periodicals, Inc.