Showing papers in "Journal of Morphology in 2013"

Postcranial morphology and the locomotor habits of living and extinct carnivorans.

Abstract: Members of the order Carnivora display a broad range of locomotor habits, including cursorial, scansorial, arboreal, semiaquatic, aquatic, and semifossorial species from multiple families. Ecomorphological analyses from osteological measurements have been used successfully in prior studies of carnivorans and rodents to accurately infer the locomotor habits of extinct species. This study uses 20 postcranial measurements that have been shown to be effective indicators of locomotor habits in rodents and incorporates an extensive sample of over 300 individuals from more than 100 living carnivoran species. We performed statistical analyses, including analysis of variance (ANOVA) and stepwise discriminant function analysis, using a set of 16 functional indices (ratios). Our ANOVA results reveal consistent differences in postcranial skeletal morphology among locomotor groups. Cursorial species display distal elongation of the limbs, gracile limb elements, and relatively narrow humeral and femoral epicondyles. Aquatic and semiaquatic species display relatively robust, shortened femora and elongate metatarsals. Semifossorial species display relatively short, robust limbs with enlarged muscular attachment sites and elongate claws. Both semiaquatic and semifossorial species have relatively elongate olecranon process of the ulna and enlarged humeral and femoral epicondyles. Terrestrial, scansorial, and arboreal species are characterized by having primarily intermediate features, but arboreal species do show relatively elongate manual digits. Morphological indices effectively discriminate locomotor groups, with cursorial and arboreal species more accurately classified than terrestrial, scansorial, or semiaquatic species. Both within and between families, species with similar locomotor habits converge toward similar postcranial morphology despite their independent evolutionary histories. The discriminant analysis worked particularly well to correctly classify members of the Canidae, but not as well for members of the Mustelidae or Ursidae. Results are used to infer the locomotor habits of extinct carnivorans, including members of several extinct families, and also 12 species from the Pleistocene of Rancho La Brea.

Intestinal morphology of the wild Atlantic salmon (Salmo salar).

Abstract: The worldwide-industrialized production of Atlantic salmon (Salmo salar) has increased dramatically during the last decades, followed by diseases related to the on-going domestication process as a growing concern. Even though the gastrointestinal tract seems to be a target for different disorders in farmed fish, a description of the normal intestinal status in healthy, wild salmon is warranted. Here, we provide such information in addition to suggesting a referable anatomical standardization for the intestine. In this study, two groups of wild Atlantic salmon were investigated, consisting of post smolts on feed caught in the sea and of sexually mature, starved individuals sampled from a river. The two groups represent different stages in the anadromous salmon life cycle, which also are part of the production cycle of farmed salmon. Selected regions of gastrointestinal tract were subjected to morphological investigations including immunohistochemical, scanning electron microscopic, and morphometric analyses. A morphology-based nomenclature was established, defining the cardiac part of the stomach and five different regions of the Atlantic salmon intestine, including pyloric caeca, first segment of the mid-intestine with pyloric caeca, first segment of the mid-intestine posterior to pyloric caeca, second segment of the mid-intestine and posterior intestinal segment. In each of the above described regions, for both groups of fish, morphometrical measurements and regional histological investigations were performed with regards to magnitude and direction of mucosal folding as well as the composition of the intestinal wall. Additionally, immunohistochemistry showing cells positive for cytokeratins, α-actin and proliferating cell nuclear antigen, in addition to alkaline phosphatase reactivity in the segments is presented.

Embryological staging of the Zebra Finch, Taeniopygia guttata.

Abstract: Zebra Finches (Taeniopygia guttata) are the most commonly used laboratory songbird species, yet their embryological development has been poorly characterized. Most studies to date apply Hamburger and Hamilton stages derived from chicken development; however, significant differences in development between precocial and altricial species suggest that they may not be directly comparable. We provide the first detailed description of embryological development in the Zebra Finch under standard artificial incubation. These descriptions confirm that some of the features used to classify chicken embryos into stages are not applicable in an altricial bird such as the Zebra Finch. This staging protocol will help to standardize future studies of embryological development in the Zebra Finch. J. Morphol. 274:1090–1110, 2013. © 2013 The Authors. Journal of Morphology Published by Wiley Periodicals, Inc.

The filter pads and filtration mechanisms of the devil rays: Variation at macro and microscopic scales

Abstract: Three lineages of cartilaginous fishes have independently evolved filter feeding (Lamniformes: Megachasma and Cetorhinus, Orectolobiformes: Rhincodon, and Mobulidae: Manta and Mobula); and the structure of the branchial filters is different in each group. The filter in Rhincodon typus has been described; species within the Lamniformes have simple filamentous filters, but the anatomy and ultrastructure of the branchial filter in the mobulid rays varies and is of functional interest. In most fishes, branchial gill rakers are elongated structures located along the anterior ceratobranchial and/or epibranchial arches; however, mobulid gill rakers are highly modified, flattened, lobe-like structures located on the anterior and posterior epibranchial elements as well as the ceratobranchials. The ultrastructure of the filter lobes can be smooth or covered by a layer of microcilia, and some are denticulated along the dorsal and ventral lobe surface. Flow through the mobulid oropharyngeal cavity differs from other filter-feeding fishes in that water must rapidly deviate from the free stream direction. There is an abrupt 90° turn from the initial inflowing path to move through the laterally directed branchial filter pores, over the gill tissue, and out the ventrally located gill slits. The deviation in the flow must result in tangential shearing stress across the filter surface. This implies that mobulids can use cross-flow filtration in which this shearing force serves as a mechanism to resuspend food particles initially caught by sieving or another capture mode. These particles will be transported by the cross filter flow toward the esophagus. We propose that species with cilia on the rakers augment the shear mediated movement of particles along the filter with ciliary transport.

Histology of "placoderm" dermal skeletons: Implications for the nature of the ancestral gnathostome.

Abstract: The vertebrate dermal skeleton has long been interpreted to have evolved from a primitive condition exemplified by chondrichthyans. However, chondrichthyans and osteichthyans evolved from an an- cestral gnathostome stem-lineage in which the dermal skeleton was more extensively developed. To elucidate the histology and skeletal structure of the gnathostome crown-ancestor we conducted a histological survey of the diversity of the dermal skeleton among the placoderms, a diverse clade or grade of early jawed vertebrates. The dermal skeleton of all placoderms is composed largely of a cancellar architecture of cellular dermal bone, sur- mounted by dermal tubercles in the most ancestral clades, including antiarchs. Acanthothoracids retain an ancestral condition for the dermal skeleton, and we re- cord its secondary reduction in antiarchs. We also find that mechanisms for remodeling bone and facilitating different growth rates between adjoining plates are widespread throughout the placoderms. J. Morphol.

Skin wound healing in different aged Xenopus laevis.

Abstract: Xenopus froglets can perfectly heal skin wounds without scarring. To explore whether this capacity is maintained as development proceeds, we examined the cellular responses during the repair of skin injury in 8- and 15-month-old Xenopus laevis. The morphology and sequence of healing phases (i.e., inflammation, new tissue formation, and remodeling) were independent of age, while the timing was delayed in older frogs. At the beginning of postinjury, wound re-epithelialization occurred in form of a thin epithelium followed by a multilayered epidermis containing cells with apoptotic patterns and keratinocytes stained by anti-inducible nitric oxide synthase (iNOS) antibody. The inflammatory response, early activated by recruitment of blood cells immunoreactive to anti-tumor necrosis factor (TNF)-α, iNOS, transforming growth factor (TGF)-β1, and matrix metalloproteinase (MMP)-9, persisted over time. The dermis repaired by a granulation tissue with extensive angiogenesis, inflammatory cells, fibroblasts, and anti-α-SMA positive myofibroblasts. As the healing progressed, wounded areas displayed vascular regression, decrease in cellularity, and rearrangement of provisional matrix. The epidermis restored to a prewound morphology while granulation tissue was replaced by a fibrous tissue in a scar-like pattern. The quantitative PCR analysis demonstrated an up-regulated expression of Xenopus suppressor of cytokine signaling 3 (XSOCS-3) and Xenopus transforming growth factor-β2 (XTGF-β2) soon after wounding and peak levels were detected when granulation tissue was well developed with a large number of inflammatory cells. The findings indicate that X. laevis skin wound healing occurred by a combination of regeneration (in epidermis) and repair (in dermis) and, in contrast to froglet scarless wound healing, the growth to a more mature adult stage is associated with a decrease in regenerative capacity with scar-like tissue formation.

A review of cetacean lung morphology and mechanics.

Abstract: Cetaceans possess diverse adaptations in respiratory structure and mechanics that are highly specialized for an array of surfacing and diving behaviors. Some of these adaptations and air management strategies are still not completely understood despite over a century of study. We have compiled the historical and contemporary knowledge of cetacean lung anatomy and mechanics in regards to normal lung function during ventilation and air management while diving. New techniques are emerging utilizing pulmonary mechanics to measure lung function in live cetaceans. Given the diversity of respiratory adaptations in cetaceans, interpretations of these results should consider species-specific anatomy, mechanics, and behavior.

Architectural specialization of the intrinsic thoracic limb musculature of the American badger (Taxidea taxus).

Abstract: Evaluation of the relationships between muscle structure and digging function in fossorial species is limited. Badgers and other fossorial specialists are expected to have massive forelimb muscles with long fascicles capable of substantial shortening for high power and applying high out-force to the substrate. To explore this hypothesis, we quantified muscle architecture in the thoracic limb of the American badger (Taxidea taxus) and estimated the force, power, and joint torque of its intrinsic musculature in relation to the use of scratch-digging behavior. Architectural properties measured were muscle mass, belly length, fascicle length, pennation angle, and physiological cross-sectional area. Badgers possess hypertrophied shoulder flexors/humeral retractors, elbow extensors, and digital flexors. The triceps brachii is particularly massive and has long fascicles with little pennation, muscle architecture consistent with substantial shortening capability, and high power. A unique feature of badgers is that, in addition to elbow joint extension, two biarticular heads (long and medial) of the triceps are capable of applying high torques to the shoulder joint to facilitate retraction of the forelimb throughout the power stroke. The massive and complex digital flexors show relatively greater pennation and shorter fascicle lengths than the triceps brachii, as well as compartmentalization of muscle heads to accentuate both force production and range of shortening during flexion of the carpus and digits. Muscles of most functional groups exhibit some degree of specialization for high force production and are important for stabilizing the shoulder, elbow, and carpal joints against high limb forces generated during powerful digging motions. Overall, our findings support the hypothesis and indicate that forelimb muscle architecture is consistent with specializations for scratch-digging. Quantified muscle properties in the American badger serve as a comparator to evaluate the range of diversity in muscle structure and contractile function that exists in mammals specialized for fossorial habits. J. Morphol. 2013. © 2012 Wiley Periodicals, Inc.

Functional morphology of the fin rays of teleost fishes

Abstract: Ray-finned fishes are notable for having flexible fins that allow for the control of fluid forces. A number of studies have addressed the muscular con- trol, kinematics, and hydrodynamics of flexible fins, but little work has investigated just how flexible ray-finned fish fin rays are, and how flexibility affects their response to environmental perturbations. Analysis of pectoral fin rays of bluegill sunfish showed that the more proximal portion of the fin ray is unsegmented while the distal 60% of the fin ray is segmented. We examined the range of motion and curvatures of the pectoral fin rays of bluegill sunfish during steady swim- ming, turning maneuvers, and hovering behaviors and during a vortex perturbation impacting the fin during the fin beat. Under normal swimming conditions, cur- vatures did not exceed 0.029 mm 21 in the proximal, unsegmented portion of the fin ray and 0.065 mm 21 in the distal, segmented portion of the fin ray. When per- turbed by a vortex jet traveling at approximately 1m s 21 (67 6 2.3 mN s.e. of force at impact), the fin ray underwent a maximum curvature of 9.38 mm 21 .B uck- ling of the fin ray was constrained to the area of impact and did not disrupt the motion of the pectoral fin dur- ing swimming. Flexural stiffness of the fin ray was cal- culated to be 565 3 10 26 Nm 2 . In computational fluid dynamic simulations of the fin-vortex interaction, very flexible fin rays showed a combination of attraction and repulsion to impacting vortex dipoles. Due to their small bending rigidity (or flexural stiffness), impacting vortices transferred little force to the fin ray. Con- versely, stiffer fin rays experienced rapid small-ampli- tude oscillations from vortex impacts, with large impact forces all along the length of the fin ray. Seg- mentation is a key design feature of ray-finned fish fin rays, and may serve as a means of making a flexible fin ray out of a rigid material (bone). This flexibility may offer intrinsic damping of environmental fluid pertur- bations encountered by swimming fish. J. Morphol.

Fetal nutrition in lecithotrophic squamate reptiles: Toward a comprehensive model for evolution of viviparity and placentation

Abstract: The primary pattern of embryonic nutrition for squamate reptiles is lecithotrophy; with few exceptions, all squamate embryos mobilize nutrients from yolk. The evolution of viviparity presents an opportunity for an additional source of embryonic nutrition through delivery of uterine secretions, or placentotrophy. This pattern of embryonic nutrition is thought to evolve through placental supplementation of lecithotrophy, followed by increasing dependence on placentotrophy. This review analyzes the relationship between reproductive mode and pattern of embryonic nutrition in three lecithotrophic viviparous species, and oviparous counterparts, for concordance with a current model for the evolution of viviparity and placentation. The assumptions of the model, that nutrients for oviparous embryos are mobilized from yolk, and that this source is not disrupted in the transition to viviparity, are supported for most nutrients. In contrast, calcium, an essential nutrient for embryonic development, is mobilized from both yolk and eggshell by oviparous embryos and reduction of eggshell calcium is correlated with viviparity. If embryonic fitness is compromised by disruption of a primary source of calcium, selection may not favor evolution of viviparity, yet viviparity has arisen independently in numerous squamate lineages. Studies of fetal nutrition in reproductively bimodal species suggest a resolution to this paradox. If uterine calcium secretion occurs during prolonged intrauterine egg retention, calcium placentotrophy evolves prior to viviparity as a replacement for eggshell calcium and embryonic nutrition will not be compromised. This hypothesis is integrated into the current model for evolution of viviparity and placentation to address the unique attributes of calcium nutrition. The sequence of events requires a shift in timing of uterine calcium secretion and the embryonic mechanism of calcium retrieval to be responsive to calcium availability. Regulation of uterine calcium secretion and the mechanism of embryonic uptake of calcium are important elements to understanding evolution of viviparity and placentation.

Cuttlefish skin papilla morphology suggests a muscular hydrostatic function for rapid changeability.

Abstract: Coleoid cephalopods adaptively change their body patterns (color, contrast, locomotion, posture, and texture) for camouflage and signaling. Benthic octopuses and cuttlefish possess the capability, unique in the animal kingdom, to dramatically and quickly change their skin from smooth and flat to rugose and three-dimensional. The organs responsible for this physical change are the skin papillae, whose biomechanics have not been investigated. In this study, small dorsal papillae from cuttlefish (Sepia officinalis) were preserved in their retracted or extended state, and examined with a variety of histological techniques including brightfield, confocal, and scanning electron microscopy. Analyses revealed that papillae are composed of an extensive network of dermal erector muscles, some of which are arranged in concentric rings while others extend across each papilla's diameter. Like cephalopod arms, tentacles, and suckers, skin papillae appear to function as muscular hydrostats. The collective action of dermal erector muscles provides both movement and structural support in the absence of rigid supporting elements. Specifically, concentric circular dermal erector muscles near the papilla's base contract and push the overlying tissue upward and away from the mantle surface, while horizontally arranged dermal erector muscles pull the papilla's perimeter toward its center and determine its shape. Each papilla has a white tip, which is produced by structural light reflectors (leucophores and iridophores) that lie between the papilla's muscular core and the skin layer that contains the pigmented chromatophores. In extended papillae, the connective tissue layer appeared thinner above the papilla's apex than in surrounding areas. This result suggests that papilla extension might create tension in the overlying connective tissue and chromatophore layers, storing energy for elastic retraction. Numerous, thin subepidermal muscles form a meshwork between the chromatophore layer and the epidermis and putatively provide active papillary retraction.

Morphological integration versus ecological plasticity in the avian pelvic limb skeleton

Abstract: Understanding patterns and distributions of morphological traits is essential for discerning underpinning processes of morphological variation. We report on the variation in the avian pelvic limb skeleton. Length and width variables were measured in the skeletons of 236 avian species in order to examine the importance of body mass, ecological factors, phylogeny and integration in the formation of specific hindlimb morphology. Scaling relationships with body mass were analyzed across Aves and in individual avian subclades. Principal component analysis and multiple regressions were performed to examine the relationship between morphology, ecology, and phylogeny. Finally, the occurrence of within-limb morphological integration was tested by partial correlation analysis of the residuals from element lengths vs. body mass and correlation analysis of avian hindlimb proportions. Body mass is the greatest contributor to variation, and it strongly influences variation in avian skeletal lengths. Lengthening of the leg typically comes from disproportionate increases in tibiotarsal and tarsometatarsal length. Partial correlation analysis showed that only these two elements are distinctly integrated consistently across all bird taxa, whereas relation of femur and third toe to other limb elements displays no clear pattern. Hence, morphological integration of all elements is not a prerequisite for limb design, and variation between taxa is mainly to be found in femoral and digital length. Furthermore, variation in tibiotarsal relative length is much lower than in other elements likely due to geometric constrains. Clear ecological adaptations are obscured by multifunctionality of the avian hindlimb, and phylogeny significantly constrains the morphology. Finally, when looking at relative lengths segmented limbs meet the requirements of many-to-one-mapping of phenotype to functional property, in line with a common concept of evolvability of function and morphology.

Homology of lungs and gas bladders: Insights from arterial vasculature

Abstract: Gas bladders of ray-finned fishes serve a variety of vital functions and are thus an important novelty of most living vertebrates. The gas bladder has long been regarded as an evolutionary modification of lungs. Critical evidence for this hypothesized homology is whether pulmonary arteries supply the gas bladder as well as the lungs. Pulmonary arteries, paired branches of the fourth efferent branchial arteries, deliver blood to the lungs in osteichthyans with functional lungs (lungfishes, tetrapods, and the ray-finned polypterid fishes). The fact that pulmonary arteries also supply the respiratory gas bladder of Amia calva (bowfin) has been used to support the homology of lungs and gas bladders, collectively termed air-filled organs (AO). However, the homology of pulmonary arteries in bowfin and lunged osteichthyans has been uncertain, given the apparent lack of pulmonary arteries in critical taxa. To re-evaluate the homology of pulmonary arteries in bowfin and lunged osteichthyans, we studied, using micro-CT technology, the arterial vasculature of Protopterus, Polypterus, Acipenser, Polyodon, Amia, and Lepisosteus, and analyzed these data using a phylogenetic approach. Our data reveal that Acipenser and Polyodon have paired posterior branches of the fourth efferent branchial arteries, which are thus similar in origin to pulmonary arteries. We hypothesize that these arteries are vestigial pulmonary arteries that have been coopted for new functions due to the dorsal shift of the AO and/or the loss of respiration in these taxa. Ancestral state reconstructions support pulmonary arteries as a synapomorphy of the Osteichthyes, provide the first concrete evidence for the retention of pulmonary arteries in Amia, and support thehomology of lungs and gas bladders due to a shared vascular supply. Finally, we use ancestral state reconstructions to show that arterial AO supplies from the celiacomesenteric artery or dorsal aorta appear to be convergent between teleosts and nonteleost actinopterygians.

Inner architecture of vertebral centra in terrestrial and aquatic mammals: A two-dimensionnal comparative study

Abstract: Inner vertebral architecture is poorly known, except in human and laboratory animals. In order to document this topic at a broad comparative level, a 2D-histomorphometric study of vertebral centra was conducted in a sample of 98 therian mammal species, spanning most of the size range and representing the main locomotor adaptations known in therian taxa. Eleven variables relative to the development and geometry of trabecular networks were extracted from CT scan mid-sagittal sections. Phylogeny-informed statistical tests were used to reveal the respective influences of phylogeny, size, and locomotion adaptations on mammalian vertebral structure. The use of random taxon reshuffling and squared change parsimony reveals that 9 of the 11 characteristics (the two exceptions are total sectional area and structural polarization) contain a phylogenetic signal. Linear discriminant analyses suggest that the sampled taxa can be arranged into three categories with respect to locomotion mode: a) terrestrial + flying + digging + amphibious forms, b) coastal oscillatory aquatic taxa, and c) pelagic oscillatory aquatic forms represented by oceanic cetaceans. Pairwise comparison tests and linear regressions show that, when specific size increases, the length of trabecular network (Tt.Tb.Le), as well as trabecular proliferation in total sections (Pr.Tb.Tt), increase with positive allometry. This process occurs in all locomotion categories but is particularly pronounced in pelagic oscillators. Conversely, mean trabecular width has a lesser increase with size in pelagic oscillators. Trabecular orientation is not influenced by size. All tests were corrected for multiple testing. By using six structural variables or indices, locomotion mode can be predicted with a 97.4% success rate for terrestrial forms, 66.7% for coastal oscillatory, and 81.3% for pelagic oscillatory. The possible functional meaning of these results and their potential use for paleobiological inference of locomotion in extinct taxa are discussed. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.

Comparative ultrastructure of the spermatozoa of three crayfish species: Austropotamobius torrentium, Pacifastacus leniusculus, and Astacus astacus (Decapoda: Astacidae).

Abstract: This study reports about the spermatozoal ultrastructure of three species of astacid crayfish, i.e., the stone crayfish Austropotamobius torrentium, signal crayfish Pacifastacus leniusculus, and noble crayfish Astacus astacus. The acrosome is a cup shaped and electron-dense structure at the anterior of the spermatozoon and comprises three layers of differing electron densities filled with parallel filaments that extend from the base to the apical zone. The acrosome was significantly longer in A. astacus than in P. leniusculus and the shortest acrosome belongs to A. torrentium. The width of the acrosome was significantly narrower in A. torrentium than in P. leniusculus and the widest acrosome belongs to A. astacus. The L:W ratio was significantly greater in A. torrentium than in P. leniusculus and the lowest ratio belongs to A. astacus. Radial arms are visible on each side of the acrosome or nucleus in sagittal view and wrap around the spermatozoon. Each radial arm comprises a parallel bundle of microtubules arranged along the long axis within a sheath. The nucleus, with decondensed material, is located in the posterior of the cell. All parts of the spermatozoon are tightly enclosed within an extracellular capsule. Despite a well-conserved general structure and similarity of pattern among these spermatozoa, differences in the dimensions of the acrosome within the studied species may be useful to help distinguish the different crayfish species. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.

Muscle architecture and out-force potential of the thoracic limb in the Eastern mole (Scalopus aquaticus).

Abstract: Moles have modified thoracic limbs with hypertrophied pectoral girdle muscles that allow them to apply remarkably high lateral out-forces during the power stroke when burrowing. To further understand the high force capabilities of mole forelimbs, architec- tural properties of the thoracic limb muscles were quantified in the Eastern mole (Scalopus aquaticus). Architectural properties measured included muscle mass, moment arm, belly length, fascicle length, and pennation angle, and these were used to provide esti- mates of maximum isometric force, joint torque, and power. Measurements of muscle moment arms and limb lever lengths were additionally used to analyze the out-force contributions of the major pectoral girdle muscles. Most muscles have relatively long fascicles and little-to-no pennation. The humeral abductor/rota- tors as a functional group are massive and are capable of relatively high force, power, and joint torque. Of this group, the bipennate m. teres major is the most mas- sive and has the capacity to produce the highest force and joint torque to abduct and axially rotate the humerus. In general, the distal limb muscles are rela- tively small, but have the capacity for high force and mechanical work by fascicle shortening. The muscle architectural properties of the elbow extensors (e.g., m. triceps brachii) and carpal flexors (e.g., m. palmaris longus) are consistent with the function of these muscles to augment lateral out-force application. The humeral abductor/rotators m. latissimus dorsi, m. teres major, m. pectoralis, and m. subscapularis are calcu- lated to contribute 13.9 N to out-force during the power stroke, and this force is applied in a 'frontal' plane causing abduction of the humerus about the sternocla- vicular joint. Moles have several specializations of their digging apparatus that greatly enhance the application of out-force, and these morphological features suggest convergence on limb form and burrowing function between New and Old World moles. J. Morphol. 000:000-000, 2013. V C 2013 Wiley Periodicals, Inc.

Comparative Cryo-SEM and AFM studies of hylid and rhacophorid tree frog toe pads.

Abstract: Cryo-scanning electron microscopy (cryo-SEM) and atomic force microscopy (AFM) offer new avenues for the study of the morphology of tree frog adhesive toe pads. Using these techniques, we compare toe pad microstructure in two distantly related species of tree frog, Litoria caerulea, White (Hylidae) and Rhacophorus prominanus, Smith (Rhacophoridae), in which the toe pads are considered to be convergent. AFM demonstrates the extraordinary similarity of both surface microstructures (largely hexagonal epithelial cells surrounded by deep channels) and nanostructures (an array of nanopillars, ca. 350 nm in diameter, all with a small dimple at the apex). The cryo-SEM studies examined the distribution of the fibrillar cytoskeleton within the different layers of the stratified toe pad epithelium, demonstrating that the cytoskeletal elements (keratin tonofilaments) that lie at an angle to the surface are relatively poorly developed in L. caerulea, clearly so in comparison to R. prominanus. Cryo-SEM also enabled the visualization of the fluid layer that is critical to a toe pad's adhesive function. This was achieved by examination of the frozen fluid residues left behind after removal of a toe within the cryo-SEM's experimental chamber. Such 'toeprints' demonstrated the presence of a wedge of fluid surrounding each toe pad, as well as fluid filling the channels that surround each epithelial cell. Cryo-SEM was used to examine epithelial cell shape. In a sample of 582 cells, 59.5% were hexagonal, the remainder being mainly pentagonal (23.1%) or heptagonal (16.1%). The distribution of differently-shaped cells was not random, but was not associated with either pad curvature or the distribution of mucous pores that provide fluid for the frogs' wet adhesion mechanism. Our main finding, the great similarity of toe pad structure in these two species, has important implications for biomimetics, for such convergent evolution suggests a good starting point for attempts to develop adhesives that will function in wet conditions.

The anatomy of vocal divergence in North American Elk and European red deer

Abstract: Loud and frequent vocalizations play an important role in courtship behavior in Cervus species. European red deer (Cervus elaphus) produce low-pitched calls, whereas North American elk (Cervus canadensis) produce high-pitched calls, which is remarkable for one of the biggest land mammals. Both species engage their vocal organs in elaborate maneuvers but the precise mechanism is unknown. Vocal organs were compared by macroscopic and microscopic dissection. The larynx is sexually dimorphic in red deer but not in elk. The laryngeal lumen is more constricted in elk, and narrows further during ontogeny. Several elements of the hyoid skeleton and two of four vocal tract segments are longer in red deer than in elk allowing greater vocal tract expansion and elongation. We conclude that elk submit the larynx and vocal tract to much higher tension than red deer, whereby, enormously stressed vocal folds of reduced effective length create a high resistance glottal source. The narrow, high impedance laryngeal vestibulum matches glottal and vocal tract impedance allowing maximum power transfer. In red deer longer and relaxed vocal folds create a less resistant glottal source and a wider vestibulum matches the low glottal impedance to the vocal tract, thereby also ensuring maximum power transfer.

Dental patterning in the earliest sharks: Implications for tooth evolution

Abstract: Doliodus problematicus is the oldest known fossil shark-like fish with an almost intact dentition (Emsian, Lower Devonian, c. 397Ma). We provide a detailed description of the teeth and dentition in D. problematicus, based on tomographic analysis of NBMG 10127 (New Brunswick Museum, Canada). Comparisons with modern shark dentitions suggest that Doliodus was a ram-feeding predator with a dentition adapted to seizing and disabling prey. Doliodus provides several clues about the early evolution of the "shark-like" dentition in chondrichthyans and also raises new questions about the evolution of oral teeth in jawed vertebrates. As in modern sharks, teeth in Doliodus were replaced in a linguo-labial sequence within tooth families at fixed positions along the jaws (12-14 tooth families per jaw quadrant in NBMG 10127). Doliodus teeth were replaced much more slowly than in modern sharks. Nevertheless, its tooth formation was apparently as highly organized as in modern elasmobranchs, in which future tooth positions are indicated by synchronized expression of shh at fixed loci within the dental epithelium. Comparable dental arrays are absent in osteichthyans, placoderms, and many "acanthodians"; a "shark-like" dentition, therefore, may be a synapomorphy of chondrichthyans and gnathostomes such as Ptomacanthus. The upper anterior teeth in Doliodus were not attached to the palatoquadrates, but were instead supported by the ethmoid region of the prechordal basicranium, as in some other Paleozoic taxa (e.g., Triodus, Ptomacanthus). This suggests that the chondrichthyan dental lamina was originally associated with prechordal basicranial cartilage as well as jaw cartilage, and that the modern elasmobranch condition (in which the oral dentition is confined to the jaws) is phylogenetically advanced. Thus, oral tooth development in modern elasmobranchs does not provide a complete developmental model for chondrichthyans or gnathostomes.

The Reproductive Cycle of the Male Sleep Snake Sibynomorphus mikanii (Schlegel, 1837) From Southeastern Brazil

Abstract: This study describes the male reproductive cycle of Sibynomorphus mikanii from southeastern Brazil considering macroscopic and microscopic variables. Sper- matogenesis occurs during spring-summer (September- December) and spermiogenesis or maturation occurs in summer (December-February). The length and width of the kidney, the tubular diameter, and the epithelium height of the sexual segment of the kidney (SSK) are larger in summer-autumn (December-May). Histochemi- cal reaction of the SSK (periodic acid-Schiff (PAS) and bro- mophenol blue (BB)) shows stronger results during summer-autumn, indicating an increase in the secretory activity of the granules. Testicular regression is observed in autumn and early winter (March-June) when a peak in the width of the ductus deferens occurs. The distal duc- tus deferens as well as the ampulla ductus deferentis ex- hibit secretory activities with positive reaction for PAS and BB. These results suggest that this secretion may nourish the spermatozoa while they are being stored in the ductus deferens. The increase in the Leydig cell nu- clear diameter in association with SSK hypertrophy and the presence of sperm in the female indicate that the mat- ing season occurs in autumn when testes begin to decrease their activity. The peak activity of Leydig cells and SSK exhibits an associated pattern with the mating season. However, spermatogenesis is dissociated of the copulation characterizing a complex reproductive cycle. At the individual level, S. mikanii males present a continu- ous cyclical reproductive pattern in the testes and kidneys (SSK), whereas at the populational level the reproductive pattern may be classified as seasonal semisynchronous. J.

Evolutionary morphology of the hemolymph vascular system in hermit and king crabs (Crustacea: Decapoda: Anomala).

Abstract: The morphological transformation of hermit crabs into crab-like king crabs in the evolution of decapod crustaceans represents a remarkable case of carcinization or evolutionary shaping into a crab-like form. In this study, we focus on internal organs such as the hemolymph vascular system and adjacent anatomical structures of several Recent hermit crab (Paguridae) and king crab (Lithodidae) species. There are various correspondences in the morphology of the arterial systems in the dorsal cephalothorax of the two taxa, especially with regard to the anterior aorta, anterior lateral arteries, and hepatic arteries. In the pleon, the posterior aorta in both taxa displays a proximal bifurcation and follows an asymmetrical course. The ventral vessel system, on the other hand, which mainly supplies the limbs, differs significantly between the taxa, with pagurids displaying the plesiomorphic condition. The pattern of the ventral vessel system in Lithodidae is influenced by morphological transformations of integumental structures during carcinization. One of these transformations was the broadening of the sternites, which resulted in a widening of the space between the endosternites. In addition, changes in the morphology of the endophragmal skeleton in Lithodidae led to an increase in the potential for intraspecific variability and interspecific variation in the arterial branching pattern. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.

Extracellular matrix proteins secreted from both the endometrium and the embryo are required for attachment: A study using a co-culture model of rat blastocysts and Ishikawa cells

Abstract: Integrins are expressed in a highly regulated manner at the maternal-fetal interface during implantation. However, the significance of extracellular matrix (ECM) ligands during the integrin-mediated embryo attachment to the endometrium is not fully understood. Thus, the distribution of fibronectin in the rat uterus and blastocyst was studied at the time of implantation. Fibronectin was absent in the uterine luminal epithelial cells but was intensely expressed in the trophoblast cells and the inner cell mass suggesting that fibronectin secreted from the blastocyst may be a possible bridging ligand for the integrins expressed at the maternal-fetal interface. An Arg-Gly-Asp (RGD) peptide was used to block the RGD recognition sites on integrins, and the effect on rat blastocyst attachment to Ishikawa cells was examined. There was a significant reduction in blastocyst attachment when either the blastocysts or the Ishikawa cells were pre-incubated with the RGD-blocking peptide. Thus, successful attachment of the embryo to the endometrium requires the interaction of integrins on both the endometrium and the blastocyst with the RGD sequence of ECM ligands, such as fibronectin. Pre-treatment of both blastocysts and Ishikawa cells with the RGD peptide also inhibited blastocyst attachment, but not completely, suggesting that ECM bridging ligands that do not contain the RGD sequence are also involved in embryo attachment. J. Morphol. 2013. © 2012 Wiley Periodicals, Inc.

Morphological variation in the appendicular skeleton of Atlantic Forest sigmodontine rodents.

Abstract: Departamento de Zoologia, Instituto de Zoologia, Universidade Federal do Rio de Janeiro,Rio de Janeiro, RJ, BrazilABSTRACT Rodents of the subfamily Sigmodontinaecomprise a highly diversified group in the Atlantic For-est, with semifossorial, terrestrial, semiaquatic, scanso-rial, and arboreal forms. In this study, we analyzed mor-phometric variation in humerus, scapula, ulna, radius,femur, tibia, and pelvis to investigate its possible rela-tionship with the different types of locomotion recordedin the literature. Skeletal characters were measured in321 specimens belonging to 29 species and 19 genera ei-ther restricted to or recorded in this ecoregion. Multivar-iate morphometric analyses (principal component andcanonical variate analyses) arranged individuals of dif-ferent genera in groups congruent with the differenttypes of locomotion. This arrangement was more clearlydefined when analyses included only forelimb measure-ments, indicating that most of the variation in appendic-ular traits associated with the different locomotor modesoccurs in the forelimb skeleton. Semifossorial formsexhibited the most distinct appendicular morphology, aswell as the greatest frequency of endemism among ana-lyzed species. These results suggest that this mode oflocomotion led to greater differentiation in semifossorialAtlantic forest sigmodontines than in terrestrial and ar-boreal forms, which were found to have more subtle dif-ferentiation and fewer endemics. Scansorial speciescould not be set apart from terrestrial ones in terms ofappendicular morphology, suggesting that these twomodes of locomotion are the most similar and general-ized for the group, as they occur in most lineages in thesubfamily. The results of this study corroborate previousobservations on the relevance of appendicular charactersin the differentiation of species and genera in the sub-family Sigmodontinae. J. Morphol. 274:779–792,2013.

Trabecular bone structure in the primate wrist

Abstract: Trabecular (or cancellous) bone has been shown to respond to mechanical loading throughout ontogeny and thus can provide unique insight into skeletal function and locomotion in comparative studies of living and fossil mammalian morphology. Trabecular bone of the hand may be particularly functionally informative because the hand has more direct contact with the substrate compared with the remainder of the forelimb during locomotion in quadrupedal mammals. This study investigates the trabecular structure within the wrist across a sample of haplorhine primates that vary in locomotor behaviour (and thus hand use) and body size. High-resolution microtomographic scans were collected of the lunate, scaphoid, and capitate in 41 individuals and eight genera (Homo, Gorilla, Pan, Papio, Pongo, Symphalangus, Hylobates, and Ateles). We predicted that particular trabecular parameters would 1) vary across suspensory, quadrupedal, and bipedal primates based on differences in hand use and load, and 2) scale with carpal size following similar allometric patterns found previously in other skeletal elements across a larger sample of mammals and primates. Analyses of variance (trabecular parameters analysed separately) and principal component analyses (trabecular parameters analysed together) revealed no clear functional signal in the trabecular structure of any of the three wrist bones. Instead, there was a large degree of variation within suspensory and quadrupedal locomotor groups, as well as high intrageneric variation within some taxa, particularly Pongo and Gorilla. However, as predicted, Homo sapiens, which rarely use their hands for locomotion and weight support, were unique in showing lower relative bone volume (BV/TV) compared with all other taxa. Furthermore, parameters used to quantify trabecular structure within the wrist scale with size generally following similar allometric patterns found in trabeculae of other mammalian skeletal elements. We discuss the challenges associated with quantifying and interpreting trabecular bone within the wrist.

Apodemes associated with limbs support serial homology of claws and jaws in Onychophora (velvet worms).

Abstract: Although the onychophoran jaw blades are believed to be derivatives of foot claws, serial homology of these structures has not been demonstrated. To shed light on the evolutionary origin of the onychophoran jaws, we searched for morphological landmarks and compared the internal and external anatomy of jaws and distal leg portions in representatives of the two major onychophoran subgroups, the Peripatidae and Peripatopsidae. Our data revealed hitherto unknown structures associated with the onychophoran limbs, such as a soft diastemal membrane separating the anterior and posterior portions of the inner jaw blade (present only in Peripatidae), apodemes associated with feet, an eversible dorsal sac at the basis of each foot claw, and a specific arrangement of musculature associated with the sclerotised claws, jaws and their apodemes. Specific correspondences in structure and position of apodemes support serial homology of claws and jaws, suggesting that the onychophoran jaw evolved from the distal portion rather than the entire limb in the last common ancestor of Onychophora. J. Morphol. 274:1180–1190, 2013. © 2013 Wiley Periodicals, Inc.

Primary homologies of the circumorbital bones of snakes.

Abstract: Some snakes have two circumorbital ossifications that in the current literature are usually referred to as the postorbital and supraorbital. We review the arguments that have been proposed to justify this interpretation and provide counter-arguments that reject those conjectures of primary homology based on the observation of 32 species of lizards and 81 species of snakes (both extant and fossil). We present similarity arguments, both topological and structural, for reinterpretation of the primary homologies of the dorsal and posterior orbital ossifications of snakes. Applying the test of similarity, we conclude that the posterior orbital ossification of snakes is topologically consistent as the homolog of the lacertilian jugal, and that the dorsal orbital ossification present in some snakes (e.g., pythons, Loxocemus, and Calabaria) is the homolog of the lacertilian postfrontal. We therefore propose that the terms postorbital and supraorbital should be abandoned as reference language for the circumorbital bones of snakes, and be replaced with the terms jugal and postfrontal, respectively. The primary homology claim for the snake “postorbital” fails the test of similarity, while the term “supraorbital” is an unnecessary and inaccurate application of the concept of a neomorphic ossification, for an element that passes the test of similarity as a postfrontal. This reinterpretation of the circumorbital bones of snakes is bound to have important repercussions for future phylogenetic analyses and consequently for our understanding of the origin and evolution of snakes. J. Morphol. 274:973–986, 2013. © 2013 Wiley Periodicals, Inc.

Gape size, its morphological basis, and the validity of gape indices in western diamond-backed rattlesnakes (Crotalus atrox).

Abstract: Maximum gape is important to the ecology and evolution of many vertebrates, particularly gape-limited predators, because it can restrict the sizes and shapes of prey that can be eaten. Although many cranial elements probably contribute to gape, it is typically estimated from jaw length or jaw width, or occasionally from a combination of these two measures. We measured maximum gape directly for 18 individuals of the western diamond-backed rattlesnake, Crotalus atrox. We measured each individual's body length, several external cranial dimensions, several cranial osteological dimensions from cleaned skeletons, and we calculated gape index values from two published gape indices (GI). Cranial bone lengths and gape circumference showed negative allometry with snout–vent length (SVL), indicating that small individuals have relatively larger heads and gapes than their larger conspecifics. We then used Akaike's Information Criterion to determine which external and osteological measurements were the best predictors of gape. Body size (SVL) was the best predictor of maximum gape overall; however, when SVL was excluded from the analysis, quadrate (QL) and mandible lengths (MdLs) were the best predictors of maximum gape using both external and osteological measurements. Quadrate length probably contributes directly to gape; however, the importance of MdL to gape is less clear and may be due largely to its allometric relationships with head length and SVL. The two published GI did not prove to be better indicators of actual gape than the jaw and QLs in this study, and the gape values they produced differed significantly from our empirically determined gapes. For these reasons, we urge caution with the use and interpretation of computed GI in future studies. The extensive variation in quadrate and mandible morphology among lineages suggest that these bones are more important to variation in gape among species and lineages than within a single species. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.

The need for data standards in zoomorphology

Abstract: eScience is a new approach to research that focuses on data mining and exploration rather than data generation or simulation. This new approach is arguably a driving force for scientific progress and requires data to be openly available, easily accessible via the Internet, and compatible with each other. eScience relies on modern standards for the reporting and documentation of data and metadata. Here, we suggest necessary components (i.e., content, concept, nomenclature, format) of such standards in the context of zoomorphology. We document the need for using data repositories to prevent data loss and how publication practice is currently changing, with the emergence of dynamic publications and the publication of digital datasets. Subsequently, we demonstrate that in zoomorphology the scientific record is still limited to published literature and that zoomorphological data are usually not accessible through data repositories. The underlying problem is that zoomorphology lacks the standards for data and metadata. As a consequence, zoomorphology cannot participate in eScience. We argue that the standardization of morphological data requires i) a standardized framework for terminologies for anatomy and ii) a formalized method of description that allows computer-parsable morphological data to be communicable, compatible, and comparable. The role of controlled vocabularies (e.g., ontologies) for developing respective terminologies and methods of description is discussed, especially in the context of data annotation and semantic enhancement of publications. Finally, we introduce the International Consortium for Zoomorphology Standards, a working group that is open to everyone and whose aim is to stimulate and synthesize dialog about standards. It is the Consortium's ultimate goal to assist the zoomorphology community in developing modern data and metadata standards, including anatomy ontologies, thereby facilitating the participation of zoomorphology in eScience. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.

Functional nasal morphology of chimaerid fishes

Abstract: Holocephalans (chimaeras) are a group of marine fishes comprising three families: the Callorhinchidae (callorhinchid fishes), the Rhinochimaeridae (rhinochimaerid fishes) and the Chimaeridae (chimaerid fishes). We have used X-ray microcomputed tomography and magnetic resonance imaging to characterise in detail the nasal anatomy of three species of chimaerid fishes: Chimaera monstrosa, C. phantasma and Hydrolagus colliei. We have shown that the nasal chamber of these three species is linked to the external environment by an incurrent channel and to the oral cavity by an excurrent channel via an oral groove. A protrusion of variable morphology is present on the medial wall of the incurrent channel in all three species, but is absent in members of the two other holocephalan families that we inspected. A third nasal channel, the lateral channel, functionally connects the incurrent nostril to the oral cavity, by-passing the nasal chamber. From anatomical reconstructions, we have proposed a model for the circulation of water, and therefore the transport of odorant, in the chimaerid nasal region. In this model, water could flow through the nasal region via the nasal chamber or the lateral channel. In either case, the direction of flow could be reversed. Circulation through the entire nasal region is likely to be driven primarily by the respiratory pump. We have identified several anatomical features that may segregate, distribute, facilitate and regulate flow in the nasal region and have considered the consequences of flow reversal. The non-sensory cilia lining the olfactory sensory channels appear to be mucus-propelling, suggesting that these cilia have a common protective role in cartilaginous fishes (sharks, rays and chimaeras). The nasal region of chimaerid fishes shows at least two adaptations to a benthic lifestyle, and suggests good olfactory sensitivity, with secondary folding enhancing the hypothetical flat sensory surface area by up to 70%. J. Morphol. 274:987–1009, 2013. © 2013 Wiley Periodicals, Inc.

Histological variability in fossil and recent alligatoroid osteoderms: Systematic and functional implications

Abstract: Statements about morphological variation in extinct taxa often suffer from insufficient sampling that can be remedied by taking advantage of larger sample sizes provided by related, extant taxa. This anal- ysis quantitatively and qualitatively examines histologi- cal and morphological variation of osteoderms from extant and extinct alligatoroid specimens. Statistically significant differences were correlated with changes in osteoderm size and shape. These differences are inde- pendent of position on the body, taxonomy, or evolution. Histological variation in alligatoroid osteoderms is due to morphological constraints on the elements them- selves, and not taxonomic differences. This has implica- tions for the recognition of histological characters in the osteoderms of extinct archosaur groups that lack extant representatives. J. Morphol. 274:676-686, 2013. 2013