Epidermal glands in squamata: Fine structure of pre-cloacal glands in Amphisbaena alba (Amphisbaenia,Amphisbaenidae)

The femoral or cloacal region in lizards and amphisbaenians displays epidermal glands; these are commonly used for purposes of systematics. In spite of being recognized as semiochemical sources (Maderson [1986] Plenum Press, pp. 13–25), their precise role remains uncertain. The glands of lizards are assumed to be principally associated with reproduction and the demarcation of territory. Their function in amphisbaenians remains unknown. The histology of these glands has only been described for lizards. There are no ultrastructural studies of glands of either type. This study concentrates on the fine morphology of the pre-cloacal glands in Amphisbaena alba using routine histological and ultrastructural techniques. The pre-cloacal glands of amphisbaenians are, like those of lizards (Chiu and Maderson [1975] J. Morphol. 147:23–40), made up by a layer of germinative cells and various layers of polyhedral cells. The latter display three well-characterized stages of differentiation. Granules form and pass through two distinct stages. Thereafter, the granules fuse in the third stage. The glandular secretion is formed by cellular units that constitute the plug. Comparison of these morphological data with those available for lizards allows speculation about the function of the glands in amphisbaenians. © 1994 Wiley-Liss, Inc.     

Morphology of the femoral glands in the lizard Ameiva ameiva (teiidae) and their possible role in semiochemical dispersion

Many lizards have epidermal glands in the cloacal or femoral region with semiochemical function related to sexual behavior and/or territorial demarcation. Externally, these glands are recognized as a row of pores, opening individually in the center of a modified scale. In many species the pores are used as systematic characters. They form a glandular cord or, in some species, a row of glandular beads below the dermis, and are connected to the exterior through the ducts, which continuously liberate a solid secretion. Dead cells, desquamated from the secretory epithelium, constitute the secretion, known as "a secretion plug." The present work focuses on the morphology of the femoral glands of the teiid lizard Ameiva ameiva, correlating it to the way in which the secretion is deposited in the environment. The results here obtained are compared to those available for other lizards and amphisbaenians. We observed that the diameter of the glandular pores did not show significant differences between males and females. The glands comprise germinative and secretory cells, which pass through at least three stages of differentiation, during which an accumulation of cytoplasmic granules, with a glycoprotein content, occurs. The cells eventually die and desquamate from the secretory epithelium, forming a secretory plug mostly constituted by juxtaposed nonfragmented secretory cells. Because of the arrangement of the rosette-like scales surrounding the femoral pores, we suggest that when the animal is in a resting position, with its femoral regions touching the ground, these scales may be involved in the breakage of their respective plugs, depositing tiny portions on the substrate. In this manner, it seems that the method for signal dispersion in this species involves specifically adapted structures and does not simply involve the chance breakage of the plug, as the gland secretes it. Signal dispersion must also be intimately associated with the animal's movement within its territory.     

Chemical composition of femoral secretions of oviparous and viviparous types of male common lizards Lacerta vivipara

In spite of the importance of chemoreception in intraspecific communication of lizards, only a few studies have examined chemical composition of secretions of lizards. The secretion of the femoral glands of adult male lizards Lacerta vivipara contains a relatively low number (18) of lipophilic compounds in comparison with other related lacertid lizards. These compounds were identified on the basis of mass spectra, obtained by GC-MS. Chemicals included ten steroids (mainly cholesterol) and four carboxylic acids between n-C₁₂ and n-C₁₈, and minor components such as squalene, α-tocopherol, and two waxy esters, which may contribute to avoid oxidation of other lipophilic components in the fairly humid environments occupied by this lizard. Secretions of adult males from oviparous and viviparous populations did not differ in the numbers and quality of chemical compounds, but there were some differences in the relative proportion of some compounds. Males from oviparous populations had lower proportions of hexadecanoic acid and cholestan-3-one, and higher proportions of squalene than viviparous males. These differences might be explained by either small genetic differences between types or due to different microclimatic conditions in the original populations.     

Chemical signalling behaviour in intrasexual communication of lizards lacking femoral pores

Signals that are used in animal communication may have multiple sensorial channels and functions. Animal communication integrates very distinct mechanisms such as behaviour, morphology and physiological secretions. Chemical signals occur in several contexts and are known to have a role in sexual selection. In many lizards, pheromones secreted through femoral pores are used to attract females and demark territory dominance. In lizard species without femoral pores, however, study of chemical signalling is negligible. Lizards of the genus Tropidurus have no ventral pores, but express melanic patches in their ventral thighs and cloacae (body regions linked to chemical communication in other lizards), which may play a role in both visual signalling and chemical signalling. Here, we describe the occurrence of pelvic rubbing—a chemical signalling behaviour—in two Tropidurus species, displayed in intraspecific agonistic intrasexual staged encounters. In addition, we compile a list of currently reported species that display this behaviour, checking for its social contexts and presence/absence of secretion pores. We analysed behaviours in conspecific trials between males of Tropidurus semitaeniatus and of T. hispidus during their breeding season. In T. semitaeniatus, displays of pelvic rubbing elicited aggressive responses from the opponents. Tropidurus hispidus, however, did not react to these conspecific displays. Pelvic rubbings were also partially linked to defecation in both species, which is likely due to secretions from internal urodeal glands expelled during defecation. Also, high rates of tongue flick behaviours during the encounters support the hypothesis that these lizards make use of chemical communication. Our observations corroborate previous suggestions that glandular scales — scales covered by generation glands produced at the epidermis across the lizards’ shedding cycles — are present in their melanic ventral patches. Our work also highlights the potential of characterizing such ventral patches as multimodal signalling badges. Further, we investigated the contexts in which pelvic rubbing is displayed adding to our understanding of the role played by chemical signalling in lizards without femoral pores.     

Epidermal glands in cordylid lizards,with special reference to generation glands

We investigated inter‐ and intraspecific variation in epidermal gland characteristics in cordylid lizards. Our particular interest was whether a causal relationship exists between the presence of generation glands and lifestyle, i.e. in rock‐dwelling or ground‐dwelling lizards. We established that both femoral and generation glands are always present in adult males, but that species can be divided into three categories on the basis of the presence of these glands in adult females: both femoral and generation glands absent; femoral glands present, but generation glands absent; and both femoral and generation glands present. The absence of epidermal glands in females appears to be the basal condition in the Cordylidae. All cordylid species are sexually dimorphic as far as generation gland number is concerned, with females having consistently less glands than males. Gland number in females is strongly affected by climate, being lower in cooler compared with warmer environments. In males, there is no clear geographical pattern, although in some clades males of high‐altitude species have more generation glands than males of species occurring at lower altitudes. At least four of the five ground‐dwelling species in the family display unique generation gland characteristics, compared with rock‐dwelling species, reflecting the continued importance of generation glands in terrestrial environments. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 158 , 312–324.     

Chemosensory discrimination of male age by female Psammodromus algirus lizards based on femoral secretions and feces

Chemical communication plays an essential role in several social and reproductive behaviors of many animals. In lizards, the main sources of semiochemicals are femoral or pre‐anal gland secretions and feces. In male lizards Psammodromus algirus, there are age‐related differences in the chemical composition of femoral gland secretions and in the reproductive strategies, with older males defending territories and females, while younger males adopting sneak‐mating strategies. Females flee more often from mating advances of young males than from those of old males, which are more successful in obtaining matings. This suggests that age discrimination of males may be important for females. We tested here whether females showed differential chemosensory responses to chemical cues (femoral gland secretion and feces) of males of two age classes, and whether females use information from substrate scent marks of males of different ages to select where to stay. We found that females elicited more tongue‐flicks to the secretion and feces of old males than to control or secretion and feces of young males. Also, the time spent by females on a scented paper depended on the treatment, suggesting that females tended to spend more time on scent marks made with femoral secretions of old males. Adult females seemed capable to discriminate between young and old males based on chemical cues alone and showed more interest in scents of old males. However, substrate scent marks did not seem to entirely determine site selection by females, suggesting that females might need additional cues to perform the choice. These results can be explained by the different age‐dependent reproductive strategies of males, which can affect differentially to females.     

Lipids in femoral gland secretions of male lizards, Psammodromus hispanicus

Many lizards produce chemical secretions that may be used as pheromones in reproductive behavior, but only a few studies have identified chemical compounds in secretions. By using GC–MS, we found only 20 lipophilic compounds in femoral glands secretion of male lizards, Psammodromus hispanicus. Main compounds were six steroids (mainly cholesterol and campesterol) and seven n-C₉ to n-C₁₈ carboxylic acids (especially dodecanoic acid), and minor components were six alcohols between C₁₆ and C₂₉ and squalene. We compared these chemicals with those previously found in secretions of the closely related sister species Psammodromus algirus and other lizard species.     

Age-related variation in lipophilic chemical compounds from femoral gland secretions of male lizards Psammodromus algirus

In spite of the importance of chemoreception in social organization of lizards, only a few studies have examined chemical composition of secretions of lizards. The secretion of the femoral glands of male lizards Psammodromus algirus contains 59 lipophilic compounds, mainly carboxylic acids between n-C₉ and n-C₂₀, and steroids (mainly campesterol, ergosterol and cholesterol), and minor components such as five alcohols, six aldehydes, squalene, α-tocopherol, ketones, and a furanone. These compounds were identified on the basis of mass spectra, obtained by GC–MS. Secretions of adult males of different age were different. Older lizards had secretions with relatively lower proportions of octadecadienoic, oleic and eicosatetraenoic acids, and higher proportions of campesterol, ergosterol, ergostenol, 4,4-dimethy-cholest-7-en-3-ol, and ergosta-5,22-dien-3-ol. These differences might allow conspecifics to get information on the age of the sender based on chemicals alone, which may have an important role in social behavior of this lizard.     

The surface of the ovine omasum as seen with the scanning electron microscope (Mammalia,Bovidae)

The omasal surface with a range of horny papillae and stratum corneum has been examined using scanning electron microscopy. Other features of interest described include pits or holes in the surface of these corneal cells and hair-like structures associated with the lamina.     

Chemical compounds from femoral gland secretions of male Iberian rock lizards, Lacerta monticola cyreni

In spite of the importance of chemoreception and chemical signals in the social organization of lizards, there are only a few studies examining the chemical composition of secretions of lizards used for scent marking. The secretion of the femoral glands of male Iberian rock lizards (Lacerta monticola cyreni) contains 44 lipophilic compounds, including several steroids (mainly cholesterol), and n-C6 to n-C22 carboxylic acids, and minor components such as esters of carboxylic acids, alcohols, squalene, and one lactone. These compounds were identified on the basis of mass spectra, obtained by GC-MS. Most lipids were detected in all individuals, although relative proportions of each chemical show a high interindividual variability. This variability might be related to the characteristics or physical and health condition of males and might be the basis of female choice based on chemical cues observed in this lizard species.     

Transdermal Delivery of a Tetrapeptide: Evaluation of Passive Diffusion

Skin penetration of the tetrapeptide Ac-Ala-Ala-Pro-Val-NH₂ was assessed. This peptide sequence fits the P-P₁ subsites of elastase and inhibits human neutrophil elastase competitively. Consequently this peptide may be therapeutically useful in a variety of inflammatory disorders, including psoriasis, in which elevated levels of human neutrophil elastase have been reported. Peptide penetration was assessed across whole human skin, whole skin with the stratum corneum removed by tape stripping and epidermis, which had been removed from the dermis by heat separation. The influence of 75 aqueous ethanol as a potential penetration enhancer of the tetrapeptide across epidermis was also assessed. The tetrapeptide did not penetrate whole human skin or epidermis, even under the influence of 75 aqueous ethanol. However, when the stratum corneum was removed tetrapeptide flux of 73.39 μg cm² h⁻¹ was achieved. The study demonstrates that the stratum corneum is the main barrier to tetrapeptide skin penetration and must be overcome if therapeutically relevant amounts of tetrapeptide are to be delivered to the skin.     

A Model of Solute Transport through Stratum Corneum Using Solute Capture and Release

A one-dimensional model of solute transport through the stratum corneum is presented. Solute is assumed to diffuse through lipid bi-layers surrounding impermeable corneocytes. Transverse diffusion (perpendicular to the skin surface) through lipids separating adjacent corneocytes, is modeled in the usual way. Longitudinal diffusion (parallel to the skin surface) through lipids between corneocyte layers, is modeled as temporary trapping of solute, with subsequent release in the transverse direction. This leads to a linear equation for one-dimensional transport in the transverse direction. The model involves an arbitrary function whose precise form is uncertain. For a specific choice of this function, closed form expressions for the Laplace transform of solute out-flux at the inner boundary, and for the time lag are obtained in the case that a constant solute concentration is maintained at the outer skin surface, with the inner boundary of the stratum corneum kept at zero concentration, and with the stratum corneum initially free of solute.     

Responses to Femoral Gland Secretions by Visually Adept Male and Female Collared Lizards

Although visually transmitted social signals are well documented in many diurnal iguanians, including collared lizards, secretory femoral glands also suggest a role of chemical signals in intraspecific communication. We conducted laboratory trials to test the extent to which male and female collared lizards responded by tongue‐flicking femoral gland secretions, neutral (water), and odoriferous (cologne) control substances, males distinguished self‐secretions from those produced by unfamiliar rival males, and females distinguish secretions from unfamiliar vs. familiar males. Both males and females spent similar amounts of time in four arena quadrants each with a Petri dish treated with one of the four test compounds. Males gave more tongue flicks/trial to secretions produced by unfamiliar rivals and cologne than they tongue‐flicked their own secretions and water. By contrast, the number of tongue flicks by females on control substances and familiar and unfamiliar males was similar. Results support the hypothesis that femoral gland secretions function in intrasexual signaling among male collared lizards, perhaps allowing them to distinguish unfamiliar rivals. Females tongue‐flicked secretions from familiar and unfamiliar males with similar frequency that was high relative to that of males, suggesting a possible role of secretions in assessment of males. Ours is the first evidence of a signaling role of femoral gland secretions in collared lizards and adds to a growing body of evidence that chemical signaling has evolved in diurnal lizards that also have highly developed visual‐based signaling.     

The epidermis and feather follicles of the king penguin (Aptenodytes patagonica) (aves)

The King penguin epidermis has a stratum corneum of flattened solidly keratinized cells without basophilic nuclear remnants. It contains keratin bound substances and is without an underlying stratum granulosum. The insunken feather follicles and the thick phospholipid-rich cornified layer appear to be adaptations for aquatic life.     

Chemical signalling in lizards: an interspecific comparison of femoral pore numbers in Lacertidae

Animals communicate via a variety of sensory channels and signals. Studies on acoustic and visual communication systems suggest that differences in the physical environment contribute to the variety of signalling behaviour, with species investing in those signals that are transmitted best under the local conditions. Whether or not environmental tuning also occurs in chemical communication systems has received much less attention. In the present study, we examined the effect of several aspects of the physical environment on the chemical communication system of lacertid lizards (family Lacertidae). The numbers of femoral pores are used as a proxy reflecting how much a particular species invests in and relies upon chemical signalling. Femoral pores are specialized epidermal structures that function as a secretion channel for the waxy substance produced by glands. In some lacertid species, the secretion carries infochemicals that play an important role in social communication. The number of femoral pores varies considerably among species. We have compiled data on femoral pore numbers for 162 species and tested for the effects of climate and substrate use. After correcting for body size and taking the phylogenetic relationships among the species into account, we found no effect of climate conditions or latitude on species pore numbers. Substrate use did affect pore numbers: shrub‐climbing species tended to have fewer femoral pores than species inhabiting other substrates. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 114 , 44–57.     

The hind limb step cycle of Iguana and primitive reptiles

The hind limb step cycle of Iguana is described and compared with other lizards. In generalized lizards with well developed limbs, the femur retracts through a large arc and rotates as it retracts, flexion of the crus on the metatarsus occurs during the initial part of the propulsive phase and extension of the knee and ankle during the final part, the crus rotates to face laterally, the metatarsus is laterally directed at the time of pedal plantarflexion, and pedal plantarflexion involves an initial rotation of the metatarsus around its long axis followed by an extension of the ankle joint. The evolutionary significance of the differences in the hind limb step cycle of lizards and salamanders is considered and it is shown that in many, but not all, features, primitive reptiles would have been like salamanders. The primitive step cycle differs from the mammalian pattern in the large amount of rotation of the limb segments, the large amount of femoral retraction, and the reduced amount of lateral movement of the hip relative to the knee that occurs during femoral retraction.     

Functional morphology and neuronal innervation of the prothoracic defence gland in Timema

Timema is the most basal genus of Phasmatodea and the sister group to the remaining stick and leaf-insects (Euphasmatodea). An autapomorphy of all phasmids is the paired prothoracic exocrine defence glands. In this study, the anatomy and innervation of the defence glands in Timema petita and Timema chumash are described and compared with the data on Euphasmatodea. In all phasmids, the glands consist of a cuticular epithelium, a secretory epithelium and muscular fibres that compress the lumen. In Timematodea, the muscular part of the gland is less developed than in Euphasmatodea and the ejection of the defence secretion depends on the dorsal longitudinal neck muscles. On the neuroanatomical level, Timema petita and Timema chumash lack neurons that are involved in the independent contraction of the gland in euphasmids. In both studied species of Timema, neck muscles play an active role in the gland function which is not observed in any other phasmid. Considering the basal position of this genus, this supports the hypothesis that in euphasmids, the muscular part of the gland evolved from the dorsal longitudinal neck muscles. Additionally, the same nerves that innervate the dorsal longitudinal neck muscles in all Polyneoptera also innervate the defence glands in phasmids.     

Human epidermis reconstructed on synthetic membrane: Influence of experimental conditions on terminal differentiation

Summary Cell suspensions of human keratinocytes seeded onto cell culture inserts may undergo terminal differentiation in the absence of fibroblasts. Among the parameters that control these morphogenic events, exposure to air and the composition of the culture medium were investigated. In the latter case, three media were considered DMEM:Ham’s F12, MCDB 153, and keratinocyte SFM medium at equivalent calcium (1.5 mM) and fetal calf serum (5%) concentrations. Immunochemical methods and transmission electron microscopy show that cells cultured in DMEM:Ham’s F12 medium, and then raised at the air-liquid interface, form a basal layer plus suprabasal cell layers corresponding to thestratum spinosum, stratum granulosum, andstratum corneum. The suprabasal keratinocyte layers show morphologies that resemble intact skin in which cells are connected by desmosomes and contain intermediate filaments and keratohyalin-filaggrin granules. When the cultures are kept submerged, the keratinocytes show occasional keratohyalin granules and are connected by fewer desmosomes. Additionally, no properstratum corneum is formed. In keratinocyte SFM medium and MCDB 153, cultures raised at the air-liquid interface are not able to form an epithelium of normal architecture and do not express terminal differentiation markers. Differentiation is initiated, however, since desmosomes and bundles of keratin filaments appear; on the other hand, filaggrin is not expressed even after 28 d in culture. Membrane-bound transglutaminase is expressed throughout the entire suprabasal compartment in MCDB153 and DMEM:Ham’s F12 media but never appears in keratinocyte SFM medium. These studies show the relative independence of epidermal differentiation program to the composition (including the calcium concentration) of the media contacting the dermis and filling the extracellular space. Conversely, differentiation appears to depend on elements of basal medium and/or components synthesized by keratinocytes under the influence of the culture medium.     

Comparative anatomy and phylogeny of the cloacae of salamanders (Amphibia: Caudata). II. Cryptobranchidae,Hynobiidae, and Sirenidae

Cloacae were examined from salamanders representing the three families in which fertilization of eggs is known or inferred to occur externally. The cloacae of male and female sirenids are aglandular and lack cilia. Sexual dimorphism in sirenid cloacae occurs only in the extent of epithelial stratification in the cloacal chamber in females (entire chamber) versus males (posterior angle of the vent). Both male and female Cryptobranchus alleganiensis possess ventral glands that secrete an acid mucopolysaccharide and have ciliated cloacal linings. The ventral glands are more numerous and hypertrophied in breeding male than female C. alleganiensis, but in males, ventral glands secrete only onto the surface of the cloacal lips along the anterior three-fifths of the cloacal orifice, whereas in females, the glands secrete onto the border of the entire cloacal orifice. Except for male Onychodactylus japonicus, male and female hynobiids also possess only ventral glands and have ciliated cloacal linings. Hynobiid ventral glands secrete a glycoprotein. Much variation occurs, however, among these hynobiids in cloacal conformation, extent of epidermis into the cloaca, and anatomy of the ventral gland. Male O. japonicus possess an unciliated cloaca in which three types of cloacal glands occur, each giving unique reactions to tests for carbohydrates and proteins. The glands in male O. japonicus do not seem to be homologous to those found in spermatophore producing salamanders in the Salamandroidea, but this does not negate the possibility that O. japonicus makes spermatophores. Examination of cloacal characters in additional species of hynobiids may be useful in resolving intrafamilial phylogenetic relationships.     

Age related differences in lipophilic compounds found in femoral gland secretions of male spiny-footed lizards, Acanthodactylus erythrurus

Although chemoreception plays an important role in social organization of many lizards, only a few studies have examined the chemicals found in secretions used for intraspecific communication. We report the composition of the secretion of the femoral glands of males of the spiny-footed lizard (Acanthodactylus erythrurus). On the basis of mass spectra, obtained by GC/MS, we identified 45 lipophilic compounds, including several alcohols ranging from 10 to 29 carbon atoms (mainly hexacosanol and tetracosanol), steroids (mainly cholesterol and dehydrocholesterol), n-C9 to n-C20 carboxylic acids, esters of carboxylic acids, and minor components such as lactones, ketones, squalene and a-tocopherol. Some of these compounds are reported for the first time in lizards. Adult and subadult males differed in the composition of secretions, with C9 to C15 carboxylic acids being more abundant in younger than in older lizards, whereas C16 to C20 carboxylic acids were more abundant in older lizards. Also, older lizards had significant lower proportions of cholesterol and campesterol but higher proportions of dehydrocholesterol.