Histological study of the cloacal region and associated structures in the hedgehog tenrec Echinops telfairi

The present investigation is based on several careful dissections and on extensive series of histological sections. It has led us to the conclusion that adult male and female Echinops telfairi are in the possession of a cloaca which represents a primitive feature among mammals. This cloaca is a small, bowl-shaped pouch at the ventro-posterior end of the body. Intestinal, genital and urinary tract open into this cloaca. The opening of the intestinal tract into the cloaca is regulated by a sphincter muscle. In the female the genital and the urinary tract open into the urogenital sinus, a subcompartment of the cloaca. The cloaca of the lesser hedgehog tenrec is lined by a multilayered, non-keratinized squamous epithelium without skin glands. In a small transitory zone between the cloaca and the outer skin the epithelium changes into the keratinized, multilayered squamous epithelium of the epidermis with eccrine and holocrine glands as well as hairs. In addition, there is a distinct circular cloacal sphincter muscle, built up by cross-striated skeletal muscle tissue.

In the terminal parts of intestinal, urinary and genital tracts of male animals the following glandular structures were observed: prostate gland, Cowper's glands and strongly pigmented seminal vesicles; in female animals: the urethral and the Bartholin glands. Both males and females, in addition, possess (a) a cloacal gland, the excretory ducts of which open into the cloaca and (b) a pericloacal gland which is located in the adipose tissue on both sides of the cloaca; it presumably also opens into the cloaca.     

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.     

The Cloaca and Spermatheca of the Female Smooth Newt, Triturus vulgaris L. (Amphibia: Urodela: Salamandridae)

The anatomy and histology of the cloaca and spermatheca of 13 female smooth newts ( Triturus vulgaris ) were studied by light microscopy. The cloaca consists of a short, anterior tube (which receives the oviducts), which opens into a larger, more posterior chamber. The spermatheca, which is the only gland in the cloaca, consists of a mass of exocrine, acinar tubules which empty individually and dorsolaterally into the posterior part of the cloacal tube and all but the most posterior part of the cloacal chamber. Stored sperm are most abundant in the spermathecal tubules during the peak of the breeding season (in May and June); during their period of storage, the sperm do not appear to make intimate contact with the epithelial cells lining the spermathecal tubules. Longterm storage of viable sperm from one breeding season to the next is probably absent in the smooth newt. Sperm storage by and multiple insemination of females both occur in this species and are necessary preconditions for competition between the sperm of different males for the fertilization of eggs. However, sperm competition has not been demonstrated in the smooth newt.     

The female cloaca of an oviparous caecilian amphibian (Gymnophiona): functional and seasonal aspects

Kuehnel, S., Herzen, J., Kleinteich, T., Beckmann, F. and Kupfer, A. 2011. The female cloaca of an oviparous caecilian amphibian (Gymnophiona): functional and seasonal aspects. —Acta Zoologica (Stockholm) 00 :1–14. Reproductive morphology is receiving increased attention in animals that have variable reproductive modes combined with internal fertilization. Exceptionally among amphibians all caecilian species practice internal fertilization via an intromittent organ: an everted part of the male cloaca (phallodeum or phallus). Because research has mostly concentrated on males, knowledge of the female cloacal morphology is scarce. Here, we present the first single‐species study of the functional morphology of the female cloaca of an oviparous, phylogenetically basal caecilian (Ichthyophis cf. kohtaoensis). We have analyzed female cloacal shape during the reproductive cycle combining conventional histology with 3D‐reconstruction. All females are similar in their overall cloacal structure with some differences in size and histology associated with the reproductive cycle. The female cloaca is divided into two distinct chambers similar to the male condition. The cranial chamber contains urogenital pockets into which oviducts and Wolffian ducts open and which may have function during oviposition. The caudal cloacal chamber bears a novel feature – dorsolateral blind sacs, which are homologous to the male condition, but are considerably smaller. The study of female cloacal morphology is essential to understanding the evolution of the caecilian reproductive system and contributes to the understanding of tetrapod genital morphology in general.     

The normal development of the anorectum in the pig

The development of the anorectum was studied in forty-four embryos and foetuses of pig varying in length from 9 mm total length to 210 mm crownrump length and in three newborn pigs. The presence of some features during critical stages in the development of the cloaca in the pig such as an epithelial mass protruding into the dorsal cloaca near its intestinal orifice and distinct differences in the type of epithelium in different regions of the cloacal system greatly facilitated the study of the developmental process. Thus it could be established that a change in position of the dorsal cloaca and adjacent structures such as the distal part of the gut and the urorectal septum via the dorsal part of the cloacal plate towards the tailgroove is of major importance for the partition of the cloaca into a separate intestinal and urogenital division. A subsequent disintegration of the dorsal part of the cloacal plate results in two separate openings for both the systems at the same time. Disintegration of the ventral part of the cloacal plate leads only to a further widening of the external opening of the urogenital system. In the cloacal system three distinct zones were discerned, a dorsal and ventral cloacal and a cloacal plate region. From the dorsal cloacal epithelium the whole anorectal segment between the intestinal mucosa and the anal epidermis develops. The epithelium of ventral cloacal origin seems to disappear completely . Cloacal plate epithelium forms the epithelial lining of distal parts of the urogenital system. The penile urethra in the male is formed by a ventralward movement of the urogenital opening by the growing perineum and not by fusion of genital folds.     

Sex Difference in the Cloacal Gland in the Hagfish,Eptatretus burgeri,and its Possible Significance in Reproduction

The cloacal gland of the hagfish, Eptatretus burgeri, was studied histologically in four seasons. Before the breeding season (spring and summer) the male cloacal gland was larger than the female cloacal gland. The gland was largest in the males with a more mature testis. After the breeding season (autumn and winter) there was no sex difference in the size of the cloacal gland. The cloacal gland consists of mucus and thread cells, as do the lateral slime glands. The sperm may be entangled within slime in the cloacal gland and be shed outside as a slimy sperm mass. Such a slimy sperm mass may play an important role in reproduction of the hagfish.     

On cloacal gestation in angel sharks from southern Brazil

The anatomy of the reproductive organs of the gravid female angel sharks Squatina Guggenheim and S. occulta was studied in specimens obtained by bottom trawling off southern Brazil from 1980 to 1992. Gestation of the species is lecithotrophic, lasts 11 months and is synchronized at the population level. The ovulation and onset of gestation occur in summer (January–February) and parturition takes place in spring (November-December). The gestation of Squatina has two phases: uterine gestation during the first 4 months and cloacal gestation during the last 6 months. The transition between these phases occurs in the 5th month (May). During uterine gestation the uteri are turgid, distended longitudinally and transversally, and constricted at both ends. Embryos develop within the closed uteri. During cloacal gestation the dome-shaped uteri are contracted longitudinally and are constricted near the nidamental gland. At the posterior end, they are distended transversally to form a wide opening into the cloaca. The cloaca is distended longitudinally and transversally. The embryos complete their development within the single, heart-shaped, uterine-cloacal chamber, that is open to the exterior through the cloacal Vent.     

A re-examination of the cloacal sacs and gland of the blind snake,Leptotyphlops dulcis (Reptilia: Leptotyphlopidae)

The cloacal sacs of Leptotyphlops dulcis are nonglandular, posterior evaginations of the cloaca. The median cloacal gland is tubuloalveolar. Similar unpaired cloacal glands as well as paired sacs are noted in certain colubrid snakes. Terminology applied to these cloacal derivatives is discussed, and a standardization of names is provided.     

Evolutionary morphology of the caecilian urogenital system. IV. The cloaca

The gross and microscopic anatomy of male and female cloacae of caecilians (Amphibia: Apoda or Gymnophiona) is described and analyzed in terms of structure and function. The arrangement of musculature and cloacal accessory structures is species-specific in males. Contraction of certain cloacal and body wall musculature facilitates eversion of the male cloaca for use as an intromittent organ. The cloacae of females show less marked morphological differences from species to species, and are modified as receptors of male phallodea.     

扬子鳄皮肤腺结构与发育的初步观察

扬子鳄有三种皮肤腺:背腺、泄殖腔麝腺和下颌腺。背腺位于背中线左右两侧第二行鳞片下方,其确切位置个体间差异很大,如表1。幼鳄背腺形态多种多样,但显示出是一种退化器官,未观察到腺开口,也未观察到半成鳄和成鳄的背腺,因此扬子鳄背腺可能不具功能。泄殖腔麝腺位于泄殖腔腹唇内,梨形,腺管开口于泄殖腔腹壁,成体腺腔很大,腺的底部壁较厚,腺细胞明显地分成若干小叶,其它部位壁较薄,小叶不明显,属全泌腺,分泌油脂物,繁殖期特别发达,但性未成熟个体亦具功能,是一种信息素下颌腺位于下颌后方两侧皮肤内,圆柱状,脉管开口于下颌腹侧皮肤表面,成体腺腔不规则,腺壁厚,从包囊到腺腔,腺细胞可明显地分成三个区,属全泌腺,分泌油脂物,在繁殖期特别发达,此腺到性成熟才具功能。     

Estrogen target sites in the cloacal region of female and male chick embryos

Summary After intravenous injection of ³H-estradiol in the 12-day old chick embryo, radioactivity is concentrated in nuclei of certain cells in the cloacal area. The nuclear labeling is observed in mesenchymal cells along the different portions of the cloaca, and in an unidentified tissue located laterally to the cloaca. The labeled mesenchymal cells display a definite pattern of distribution along the epithelial wall of the cloaca, identical both in male and in female embryos. In the adjacent bursa of Fabricius, cells do not concentrate labeled hormone in their nuclei. The presence of estrogen receptors in the cloacal area of embryos of either sex adds evidence, at the cellular level, to support the concept of a neutral, or undifferentiated, sex with estradiol inhibiting this neutral male differentiation.Visiting scientistSupported by a Fellowship from the Délégation Générale à la Recherche scientifique et technique, Paris, France     

Sexual conflict over mating in red-sided garter snakes (Thamnophis sirtalis) as indicated by experimental manipulation of genitalia

Sexual conflict over mating can result in sex-specific morphologies and behaviours that allow each sex to exert control over the outcome of reproduction. Genital traits, in particular, are often directly involved in conflict interactions. Via genital manipulation, we experimentally investigated whether genital traits in red-sided garter snakes influence copulation duration and formation of a copulatory plug. The hemipenes of male red-sided garter snakes have a large basal spine that inserts into the female cloaca during mating. We ablated the spine and found that males were still capable of copulation but copulation duration was much shorter and copulatory plugs were smaller than those produced by intact males. We also anaesthetized the female cloacal region and found that anaesthetized females copulated longer than control females, suggesting that female cloacal and vaginal contractions play a role in controlling copulation duration. Both results, combined with known aspects of the breeding biology of red-sided garter snakes, strongly support the idea that sexual conflict is involved in mating interactions in this species. Our results demonstrate the complex interactions among male and female traits generated by coevolutionary processes in a wild population. Such complexity highlights the importance of simultaneous examination of male and female traits.     

Annulate lamellae and crystalline inclusions in granular endoplasmic reticulum of the islet organ and associated tissues of a cyclostome,Myxine glutinosa

Cytoplasmic annylate lamellae were found in the islet organ of a cyclostome, the hagfish (Myxine glutinosa), predominantly in cells interpreted as young proliferating beta-cells, and also in endocrine cells and enterocytes of the bile duct and gut and in the endothelial cells of small blood vessels. A close association was observed annulate lamellae and granular endoplasmic reticulum. Both in cells with and in those without annulate lamellae, crystalline inclusions of proteinaceous nature were seen in granular endoplasmic reticulum. These inclusions were occasionally closely associated to annulate lamellae, and a direct continuity could be seen between granular endoplasmic reticulum and the outer nuclear membrane surrounding an inclusion partially situated in the perinuclear cisterna. Rod-shaped structures and rounded electron dense bodies were seen in the nuclei of some islet parenchymal cells. The presence of annulate lamellae in the islet organ and associated tissues of Myxine glutinosa is believed to be related to the very high phylogenetic age of this species. The close association observed between annulate lamellae, granular endoplasmic reticulum, crystalline inclusions, and sometimes also nuclear membranes, may be of functional significance.     

Effects of surgical deafening and exposure to continuous darkness on cloacal gland size in scotorefractory Japanese quail

Adult male quail were transferred to short days (SD) and exposed simultaneously to conspecific vocalizations of males on long days (CVMLD). Cloacal glands did not regress in some males while in others their glands regressed then spontaneously recrudesced. Of the birds that exhibited cloacal gland regression, 80% recrudesced by 8 weeks and all birds recrudesced by 25 weeks on SD. Three experiments are reported. The first experiment analyzed the effects of transfer to SD. The remaining two experiments examined the role of auditory stimuli. In Experiment 2, deafening males whose cloacal glands had not regressed after 17 days exposure to SD and CVMLD produced a significant decrease in cloacal gland size. In Experiment 3, quail whose cloacal glands had regressed and recrudesced while exposed to SD and CVMLD were deafened and/or transferred to complete darkness (DD). Cloacal gland size was significantly smaller in deafened males kept on SD or kept in DD than in sham controls retained on SD. Surprisingly, the cloacal glands of sham controls in DD were similar to those of intact birds which remained on SD. These results suggest that scotorefractoriness which has been attributed to an insensitivity to short photoperiods may be due to a sensitivity to vocalizations of birds on LD. Perhaps there is a hierarchy of physical and social cues so that a decrease in the photoperiod unmasks the effects of auditory stimuli. Furthermore, an interval timer mechanism or some alternative to the external coincidence model of time keeping seems to account for the refractoriness to SD.     

Transmissions- und rasterelektronen-mikroskopische Untersuchung an den Sinnesknospen der Tentakeln von Myxine glutinosa L. (Cyclostomata)

Sensory buds of different sizes have been found in the epidermis from the barbels of Myxine glutinosa. The electron microscopic investigations reveal their composition as one type of receptor cells and two types of supporting cells. The receptor cells have apical stereocilia with filamentous internal structure and there are microvilli on the supporting cells. The cytoplasma of the receptor cells contain fibrils and fibril bundles. The sensory buds are innervated by a nerve plexus below the basal lamina with nerve endings between the basal cells, which lie below the sensory buds. A comparison with sensory buds in some other vertebrates is drawn.     

Sexually transmitted bacteria affect female cloacal assemblages in a wild bird

Ecology Letters (2010) 13: 1515-1524 ABSTRACT: Sexual transmission is an important mode of disease propagation, yet its mechanisms remain largely unknown in wild populations. Birds comprise an important model for studying sexually transmitted microbes because their cloaca provides a potential for both gastrointestinal pathogens and endosymbionts to become incorporated into ejaculates. We experimentally demonstrate in a wild population of kittiwakes (Rissa tridactyla) that bacteria are transmitted during copulation and affect the composition and diversity of female bacterial communities. We used an anti-insemination device attached to males in combination with a molecular technique (automated ribosomal intergenic spacer analysis) that describes bacterial communities. After inseminations were experimentally blocked, the cloacal communities of mates became increasingly dissimilar. Moreover, female cloacal diversity decreased and the extinction of mate-shared bacteria increased, indicating that female cloacal assemblages revert to their pre-copulatory state and that the cloaca comprises a resilient microbial ecosystem.     

A dual fate of the hindlimb muscle mass: cloacal/perineal musculature develops from leg muscle cells

The cloaca serves as a common opening to the urinary and digestive systems. In most mammals, the cloaca is present only during embryogenesis, after which it undergoes a series of septation events leading to the formation of the anal canal and parts of the urogenital tract. During embryogenesis it is surrounded by skeletal muscle. The origin and the mechanisms regulating the development of these muscles have never been determined. Here, we show that the cloacal muscles of the chick originate from somites 30-34, which overlap the domain that gives rise to leg muscles (somites 26-33). Using molecular and cell labelling protocols, we have determined the aetiology of cloacal muscles. Surprisingly, we found that chick cloacal myoblasts first migrate into the developing leg bud and then extend out of the ventral muscle mass towards the cloacal tubercle. The development of homologous cloacal/perineal muscles was also examined in the mouse. Concordant with the results in birds, we found that perineal muscles in mammals also develop from the ventral muscle mass of the hindlimb. We provide genetic evidence that the perineal muscles are migratory, like limb muscles, by showing that they are absent in metd/d mutants. Using experimental embryological procedures (in chick) and genetic models (in chick and mouse), we show that the development of the cloacal musculature is dependent on proximal leg field formation. Thus, we have discovered a novel developmental mechanism in vertebrates whereby muscle cells first migrate from axially located somites to the pelvic limb, then extend towards the midline and only then differentiate into the single cloacal/perineal muscles.     

Male Courtship Pheromones Induce Cloacal Gaping in Female Newts (Salamandridae)

Pheromones are an important component of sexual communication in courting salamanders, but the number of species in which their use has been demonstrated with behavioral evidence remains limited. Here we developed a behavioral assay for demonstrating courtship pheromone use in the aquatically courting Iberian ribbed newt Pleurodeles waltl. By performing an in-depth study of the courtship behavior, we show that females invariably open their cloaca (cloacal gaping) before engaging in pinwheel behavior, the circling movement that is the prelude to spermatophore uptake. In contrast, cloacal gaping was not observed in failed courtships, where females escaped or displayed thanatosis. Since gaping mainly occurred during male amplexus and cloacal imposition, which is the obvious period of pheromone transfer, we next investigated whether male courtship water (i.e., water holding courtship pheromones) alone was able to induce this reaction in females. These tests showed that courtship water induced cloacal gaping significantly more than water, even in the absence of a male. Cloacal gaping thus provides a simple and robust test for demonstrating courtship pheromone use in the Iberian ribbed newt. Since opening the cloaca is an essential prerequisite for spermatophore pick-up in all internally fertilizing salamanders, we hypothesize that variations on this assay will also be useful in several other species.