ORIGINAL ARTICLE: Medical and surgical management of reproductive neoplasia in two western lowland gorillas (Gorilla gorilla gorilla)

Background Reports of female reproductive tract neoplasia are infrequent in great apes. Methods Two captive‐born, female western lowland gorillas (Gorilla gorilla gorilla) housed at the North Carolina Zoological Park were diagnosed with reproductive neoplasia. Results The first gorilla had uterine endometrial thickening and uterine fibroids diagnosed during a routine annual examination. Subsequently, the animal underwent several uterine curettage procedures in an attempt to debulk the uterine mass. Biopsy results indicated uterine adenocarcinoma. The animal was treated with an ovariohysterectomy followed by a combination of megestrol acetate and medroxyprogesterone acetate. The second gorilla was diagnosed with squamous cell carcinoma of the vagina, cervix, and uterus after presenting for intermittent vaginal bleeding of 1‐month duration. This animal underwent palliative radiation therapy, receiving two rounds of radiation treatment 8 weeks apart. Conclusions The following report describes the diagnosis and management of the two cases.     

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

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

Morphology of the reproductive tract in a lizard exhibiting incipient viviparity (Sphenomorphus fragilis) and its implications for the evolution of the reptilian placenta

The morphology of the female reproductive tract and corpus luteum is examined in Sphenomorphus fragilis, a lizard from the lowland regions of New Guinea exhibiting incipient viviparity. Females oviposit eggs that hatch either immediately or within a few hours. Corpora lutea form from ovulated follicles and decrease in diameter as embryonic development progresses. The oviduct from vitellogenic females is sparsely populated with well developed uterine glands containing secretory granules. The eggs are covered with a relatively thin shell (10 μm thick) composed of an inner boundary layer and proteinacous fibers. The secreted shell is complete by early neurulation. Shell morphology does not change throughout the remainder of the in utero incubation period. A well vascularized uterus and chorioallantoic membrane provide simple placentation. These findings suggest that the reduction in shell thickness associated with the evolution of a placenta is due to a decrease in the number of shell glands in the uterus and is not a delay or inhibition of the shelling process per se. This hypothesis further suggests that the selective forces favoring shell gland loss act on the vitellogenic female during gland recruitment which occurs prior to ovulation and not on the pregnant female. © 1992 Wiley-Liss, Inc.     

Ovarian morphology and folliculogenesis and ovulation process in the flat-faced fruit-eating bat Artibeus planirostris and the Argentine brown bat Eptesicus furinalis: A comparative analysis

The Neotropical bat species Artibeus planirostris and Eptesicus furinalis present a different morphology of the female reproductive organs: the first presents a simplex uterus, while the second presents a bicornuate uterus, but there is no information about their ovaries. Our aim was to compare the general ovary morphology and the folliculogenesis process in these species to increase the knowledge about the reproductive diversity of tropical bats. We observed a morphological distinction between the ovaries of both species: A. planirostris presents the primordial follicles located in a cranial portion of the ovary and the interstitial gland cells are not distinctive, while in E. furinalis, the primordial follicles are located throughout the cortex, and there is an abundance of interstitial gland cells. Both species present binovular or triovular follicles. Artibeus planirostris is a monovular species, with a preferential ovulation in the left side. Some females of E. furinalis exhibited two corpora lutea in the same ovary, and others presented a corpus luteum in both right and left ovaries at the same time; thus, E. furinalis is a polyovular species. Our results express the variation between two Neotropical species, reflecting the great variation in the reproductive aspects in Chiroptera.     

Uterine and eggshell structure and histochemistry in a lizard with prolonged uterine egg retention (Lacertilia,Scincidae, Saiphos)

The eggshell of lizards is a complex structure composed of organic and inorganic molecules secreted by the oviduct, which protects the embryo by providing a barrier to the external environment and also allows the exchange of respiratory gases and water for life support. Calcium deposited on the surface of the eggshell provides an important nutrient source for the embryo. Variation in physical conditions encountered by eggs results in a tradeoff among these functions and influences eggshell structure. Evolution of prolonged uterine egg retention results in a significant change in the incubation environment, notably reduction in efficiency of gas exchange, and selection should favor a concomitant reduction in eggshell thickness. This model is supported by studies that demonstrate an inverse correlation between eggshell thickness and length of uterine egg retention. One mechanism leading to thinning of the eggshell is reduction in size of uterine shell glands. Saiphos equalis is an Australian scincid lizard with an unusual pattern of geographic variation in reproductive mode. All populations retain eggs in the uterus beyond the embryonic stage at oviposition typical for lizards, and some are viviparous. We compared structure and histochemistry of the uterus and eggshell of two populations of S. equalis, prolonged egg retention, and viviparous to test the hypotheses: 1) eggshell thickness is inversely correlated with length of egg retention and 2) eggshell thickness is positively correlated with size of shell glands. We found support for the first hypothesis but also found that eggshells of both populations are surprisingly thick compared with other lizards. Our histochemical data support prior conclusions that uterine shell glands are the source of protein fiber matrix of the eggshell, but we did not find a correlation between size of shell glands and eggshell thickness. Eggshell thickness is likely determined by density of uterine shell glands in this species. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Effect of low colostrum intake on gastrointestinal development and uterine and cervical morphometrical architecture in the neonatal gilt

To assess the importance of natural variation in colostrum intake on piglet gastrointestinal and reproductive development, two equally sized female piglets from each of 27 litters were selected, one with low (average 226 g) and one with high (average 401 g) colostrum intake. At weaning (23 d of age), piglets were euthanised to perform macromorphological measurements on ileum, colon, cervix and uterus tissues, and to obtain tissue samples from the cervix and uterus for histology. Sections of uterine and cervical preparations were analysed using digital image analysis. Despite being selected for the same birth weight (average 1.1 kg, standard deviation 0.18 kg), piglets with low colostrum intake weighed 5.91 ± 0.17 kg and piglets with high colostrum intake weighed 6.96 ± 0.19 kg at weaning (P < 0.05). Most of the micro- and macroscopic measures such as length and weight of ileum and colon, cervix and uterus, luminal size of cervix and uterus, number of cervical crypts and uterine glands, were greater in gilts with high colostrum intake. The histological architecture of the uterus and cervix in gilts with high colostrum intake showed more complexity, reflecting more advanced development in these piglets. In conclusion, these data demonstrate that independent of birth weight, natural variation in colostrum intake is related to the overall development of neonatal piglets, affecting body growth, as well as growth and development of the gut and reproductive tract.     

Female reproductive tract of the lesser anteater (Tamandua tetradactyla,myrmecophagidae, Xenarthra). Anatomy and histology

The morphological and histological features of the unusual reproductive tract of the female lesser anteater, Tamandua tetradactyla (Myrmecophagidae, Xenarthra), are described for the first time. The present study aimed to establish the main similarities and differences between this species and other xenarthrans. The populations of this species are declining rapidly for a number of reasons and our study is relevant to diverse programs related to its conservation. Studies were carried out on five female genital tracts of adult specimens. Ovaries were ovoid, presenting a medulla completely surrounded by the cortex, differently from that described in other xenarthans. Like in Dasypus but different from all other armadillos studied, single oocyte follicles were observed and a simple the uterus. The uterovaginal canal connects the uterus with the urogenital sinus. The simple columnar epithelium of the uterovaginal canal ends abruptly at a septum which resembles a hymen, where the transitional epithelium of the urogenital sinus appears. This ancestral feature is shared with that of other armadillos, except Tolypeutes matacus, which has a true vagina. Characteristics of the reproductive tract and sperm morphology of other Xenarthra are comparatively discussed. These observations suggest that important reproductive features are shared between the family Myrmecophagidae and the genus Dasypus, a basal group in the phylogeny of Xenarthra. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.     

Neuromuscular organization and aminergic modulation of contractions in the Drosophila ovary

Background  

The processes by which eggs develop in the insect ovary are well characterized. Despite a large number of Drosophila mutants that cannot lay eggs, the way that the egg is moved along the reproductive tract from ovary to uterus is less well understood. We remedy this with an integrative study on the reproductive tract muscles (anatomy, innervation, contractions, aminergic modulation) in female flies.     

Seasonal changes in daily torpor patterns of free-ranging female and male Daubenton’s bats (Myotis daubentonii)

Daily torpor can provide significant energy and water savings in bats during cold ambient temperatures and food scarcity. However, it may reduce rates of foetal and juvenile development. Therefore, reproductive females should optimize development by minimizing times in torpor. To test this hypothesis, the use of torpor by female and male free-ranging Daubenton’s bats (Myotis daubentonii) during reproduction (gestation, lactation, and post-lactation period) was investigated in 1998 and 1999. Temperature-sensitive radio transmitters were attached to the bats to measure skin temperature. Simultaneously, ambient temperature was recorded. While both sexes became torpid during daytime, male bats used daily torpor (>6°C below individual active temperature) significantly more often during reproductive period (mean: 78.4 % of day time in May and 43 % in June) than females. Female bats went into daily torpor, particularly in late summer when juveniles were weaned (mean: 66.6 % of daytime). Lowest skin temperatures occurred in a female bat with 21.0°C during post-lactation. Skin temperatures of male bats fluctuated from 16.8°C in torpor to 37.2°C during times of activity. There was a significant effect of reproductive period on skin temperature in females whereas mean ambient temperature had no significant effect. However, mean ambient temperature affected mean skin temperatures in males. Our findings indicate that female Daubenton’s bats adopt their thermoregulatory behaviour in particular to optimize the juvenile development.     

A histochemical study of the secretions of reproductive glands and of the egg envelopes of Achatina fulica (Pulmonata: Stylommatophora)

Histochemical investigations of the secretions of reproductive glands—albumen gland, apical uterus, basal uterus and prostate gland—indicate the presence of galactogen in the albumen gland, acid mucopolysaccharide in the apical uterus, and lipoprotein in the basal uterus and prostate gland of A. fulica. The proteinaceous secretions produced by the glands do differ in their terminal reactive sites. Intense alkaline phosphatase reaction is found in albumen gland and apical uterus; carbonic anhydrase activity could be detected mainly in the uterine glands. The cyclical secretory activity of the reproductive glands has been studied preparatory to egg-laying and in the spent phase. Histochemical characteristics of the egg envelopes—albumen, shell membrane and egg-shell—suggest a possible sequential deposition of glandular products during the descent of eggs through the repv. ductive tract. The factors contributing to the stability and resistant nature of the egg envelopes, and the possible role of nutritive materials contained in reproductive gland secretions in the development of the embryo (even while the eggs are inside the uterus), are discussed.     

Differential expression and estrogen response of lactoferrin gene in the female reproductive tract of mouse,rat, and hamster

Lactoferrin, an iron-binding glycoprotein, kills bacteria and modulates inflammatory and immune responses. Presence of lactoferrin in the female reproductive tract suggests that the protein may be part of the mucosal immune system and act as the first line of defense against pathogenic organisms. We have discovered that lactoferrin is a major estrogen-inducible protein in the uterus of immature mice and is up-regulated by physiological levels of estrogen during proestrous in mature mice. In the present study, we examined lactoferrin gene expression and its response to estrogen stimulation in the female reproductive tract of several strains of immature mouse, rat, and hamster. The lactoferrin expression in the cycling adult female rat was also evaluated. Lactoferrin gene polymorphism exists among the different mouse strains. In the three inbred mouse strains studied, lactoferrin gene expression is stimulated by estrogen in the immature uterus, although it is less robust than in the outbred CD-1 mouse. We found that the lactoferrin gene is constitutively expressed in the epithelium of the vagina and the isthmus oviduct; however, it is estrogen inducible in the uterus of immature mice and rats. Furthermore, lactoferrin is elevated in the uterine epithelium of the mature rat during the proestrous and estrous stages of the estrous cycle. Estrogen stimulation of lactoferrin gene expression in the reproductive tract of an immature hamster is limited to the vaginal epithelium. The present study demonstrates differential expression and estrogen responsiveness of the lactoferrin gene in different regions of the female rodent reproductive tract and variation among the rodent species studied.     

Seasonal variation of the oviduct of the American alligator,Alligator mississippiensis (Reptilia: Crocodylia)

The annual oviductal cycle of the American alligator, Alligator mississippiensis, is described using light and electron microscopy. Previous work done by Palmer and Guillette ([ 1992 ] Biol Reprod 46:39–47) shed some light on the reproductive morphology of the female alligator oviduct; however, their study was limited and did not report details relating to variation across the reproductive season. We recognize six variable regions of the oviduct: infundibulum, tube, isthmus, anterior uterus, posterior uterus, and vagina. Each area shows variation, to some degree, in the histochemistry and ultrastructure of oviductal secretions. Peak secretory activity occurs during the months of May and June, with the greatest variation occurring in the tube and anterior uterus. During the month of May, high densities of neutral carbohydrates and proteins are found within the tubal and anterior uterine glands. The epithelium of the entire oviduct secretes neutral carbohydrates throughout the year, but many regions lack protein secretions, and the posterior uterine glands show little secretory activity of any type throughout the year. After oviposition, secretory activity decreases drastically, andthe oviduct resembles that of the premating season. This study also provides evidence to support the homology between alligator and bird oviducts. Sperm were observed in glands at the tubal‐isthmus and utero‐vaginal junctions in preovulatory, postovulatory and postovipository females. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Food Uptake by the Insect-Parasitic Nematode,Sphaerularia bombi (Tylenchida)

The insect-parasitic female of Sphaerularia bombi everts its uterus and associated reproductive structures into the body cavity of its bumblebee host. This uterine sac then takes over the normal functions of the parasite and leads an independent existence. An examination of this sac shows that the surface of the uterine cells are differentiated into a network of saccular indentations separating off fine cytoplasmic extensions. The folding of adjacent cytoplasmic extensions around portions of the host''s hemolymph results in the formation of pinocytotic vacuoles. Intracellular vacuoles are also formed at the base of the saccular indentations. It appears that the first stage of intracellular digestion in S. bombi initially occurs by pinocytosis in the outer surface of the uterine cells. The inner and outer surfaces of the ovary and oviduct are modified into lobelike projections to increase the absorptive surface area, and electron-dense droplets originating in this tissue were also observed in the developing eggs. The hypothesis is presented that soluble nutrients are passed into the ovary-oviduct tissue where, after being reconstituted into droplets, they enter the developing eggs.     

Histological and morphological aspects of reproduction in the sandbar shark Carcharhinus plumbeus in the U.S. south‐eastern Atlantic Ocean and Gulf of Mexico

The reproduction of the sandbar shark Carcharhinus plumbeus in the U.S. south‐eastern Atlantic Ocean including the Gulf of Mexico was examined using a combination of histological and morphological characteristics of C. plumbeus collected through fishery‐dependent and ‐independent sampling programmes (n = 1,567). Indices of maturity were constructed using measurements of gonads, reproductive tracts and claspers, and sandbar sharks exhibited 50% maturity sizes of 140 and 148 cm fork length for males and females respectively. Gonado‐somatic indices and variation in reproductive tract condition were used to determine seasonal trends in reproduction of mature C. plumbeus. Sandbar sharks have discrete seasonal reproductive cycles in which males produce sperm from January to May with a peak in May and females develop eggs from January to May with ovulation occurring in June. Females were shown to exhibit a >2 year reproductive cycle. Embryonic development was assessed through measurements of masses and lengths of uterine contents. Gestation was 12 months, from July to the following June, with parturition in late June. This research highlights a difference from previously reported data on the periodicity of female reproduction in C. plumbeus in the U.S. south‐eastern Atlantic Ocean and Gulf of Mexico, which may have major effects on future C. plumbeus stock management.     

Anatomy and histology of the reproductive tract of the female Babirusa (Babyrousa celebensis)

The anatomy and histology of the female reproductive tract of the Indonesian wild pig Babyrousa celebensis was studied by means of reproductive tracts obtained from seven animals aged between two and 22 years of age. The ovary appeared to have the ability to ovulate up to four ova at one time. However, the combined ovarian output seemed to average 1.86 ova. Ovulation can take place at any time from puberty to old age (22 years). The opening to the uterine tube was indicated by a ‘flower-like' array of tall, broad epithelial ‘petals' arising from the luminal surface of the funnel. The mucosal surfaces of these structures were covered in a mixture of prominent ciliated cells and bulbous secretory cells. The uterine tube followed a tightly convoluted path to the tip of the uterine horn. The uterus was proportionately short. The anatomical construction of the uterus was similar to those of other suids in that the columnar endometrium was heavily folded, there was a rich supply of uterine glands in the lamina propria, and the uterus was provided with a good blood supply. The cervix was thick walled and had a spiral lumen.     

Observations on the female internal reproductive organs of the brown howler monkey (Alouatta guariba clamitans)

Alouatta guariba clamitans (brown howler monkey) is an endemic primate from the southeastern Brazil tropical forests, classified as near threatened by the IUCN Red List 2007. The genus Alouatta is one of the most difficult New World monkeys to breed and rear in captivity. In this study we examined the macroscopic and histological aspects of the female genital tract of wild brown howler monkeys to provide baseline information for future reproduction research. The anatomical relationship between the vagina, uterus, broad ligament, oviducts and ovaries are those of a typical primate reproductive tract. The fundic portion of the uterus is globoid, the cervix is well developed, which confers to the uterus an elongated shape, and the vagina is a long flattened channel. Histological analysis conducted in females in the follicular phase revealed large quantities of interstitial luteinized tissue in the ovaries, a stratified nonkeratinized vaginal epithelium, lack of glands in the vaginal mucosa and simple tubular endometrial glands. The observed anatomical features should be considered in the adaptation and application of assisted reproductive techniques aimed at improving captive reproduction for species conservation. Am. J. Primatol. 71:145–152, 2009. © 2008 Wiley‐Liss, Inc.     

Pollen digestion by nectarivorous and frugivorous Antillean bats

The ability to extract pollen contents may be related to the extent to which animals use this item as a regular part of their diet. In spite of the broad diversity of taxa that feed on pollen, comparative studies to test this hypothesis are scarce. We compared the extraction efficiency of pollen grains of Blue Mahoe (Talipariti elatum) by Antillean nectar bats (Brachyphylla nana) and Jamaican fruit bats (Artibeus jamaicensis). Antillean nectar bats extracted the contents of a higher percentage of pollen grains than Jamaican fruit bats, even though processing time in the gut was lower in the nectarivorous bats. Pollen extraction efficiency increased with time spent in the gut in each species. The gastrointestinal tract in both species resembled the functioning of a continuous stirred-tank reactor (CSTR) equivalent to the stomach, in series with a plug-flow reactor (PFR) equivalent to the intestine with varying degrees of longitudinal mixing. Accordingly, pollen grains flowed continuously out of the stomach and moved out through the intestine where they were mixed longitudinally. Our results support previous findings of higher extraction efficiencies in nectarivorous bats than their frugivorous relatives, and suggest that these differences may be the result of differences in the level of activity of the enzymes responsible for pollen wall degradation. Identification of enzymatic mechanisms of pollen degradation would allow a direct test of this hypothesis.     

Thermal physiology of pregnant and lactating female and male long-eared bats, Nyctophilus geoffroyi and N. gouldi

During roosting in summer, reproductive female bats appear to use torpor less frequently and at higher body temperatures (T _b) than male bats, ostensibly to maximise offspring growth. To test whether field observations result from differences in thermal physiology or behavioural thermoregulation during roosting, we measured the thermoregulatory response and energetics of captive pregnant and lactating female and male long-eared bats (Nyctophilus geoffroyi 8.9 g and N. gouldi 11.5 g) during overnight exposure to a constant ambient temperature (T _a) of 15°C. Bats were captured 1–1.5 h after sunset and measurements began at 21:22±0:36 h. All N. geoffroyi entered torpor commencing at 23:47±01:01 h. For N. gouldi, 10/10 males, 9/10 pregnant females and 7/8 lactating females entered torpor commencing at 01:10±01:40 h. The minimum T _b of torpid bats was 15.6±1.1°C and torpid metabolic rate (TMR) was reduced to 0.05±0.02 ml O₂ g⁻¹ h⁻¹. Sex or reproductive condition of either species did not affect the timing of entry into torpor (F=1.5, df=2, 19, P=0.24), minimum TMR (F=0.21, df=4, 40, P=0.93) or minimum T _b (F=0.76, df=5, 41, P=0.58). Moreover, sex or reproductive condition did not affect the allometric relationship between minimum resting metabolic rate and body mass (F=1.1, df=4, 37, P=0.37). Our study shows that under identical thermal conditions, thermal physiology of pregnant and lactating female and male bats are indistinguishable. This suggests that the observed reluctance by reproductive females to enter torpor in the field is predominantly because of ecological rather than physiological differences, which reflect the fact that females roost gregariously whereas male bats typically roost solitarily.     

Mating frequency, genetic structure, and sex ratio in the intermorphic female producing ant species Myrmecina nipponica

1. Myrmecina nipponica has two types of colonies: a queen colony type, in which the reproductive females are queens and new colonies are made by independent founding, and an intermorphic female colony type, in which reproductive females belong to a wingless intermediate morphology between queen and worker, and where colonies multiply through colonial budding. 2. The mating frequencies of reproductive females in both types indicate monoandry. The relatedness among nestmates in both types was almost 0.75, however relatedness between mother and daughter in intermorphic female colonies was slightly higher than that of queen colonies. 3. The sex ratio (corrected investment female ratio) was 0.70 at the population level, suggesting that the sex ratio is controlled by workers in this species, however the ratio differed greatly between the two types of colonies. Queen colonies (n = 37) had a female‐biased sex ratio of 0.77 while intermorphic female colonies (n = 33) had a ratio of 0.56. 4. Each reproductive intermorphic female was accompanied by an average of 2.9 workers (including virgin intermorphic females) in the colonial budding, and when the investment to those workers was added to the female investment, the sex ratio reached 0.81. 5. The frequency distribution of sex ratio was bimodal, with many colonies producing exclusively males or females, however mean estimated relatedness within colonies was almost 0.75. These data are inconsistent with the genetic variation hypothesis, which is one of the predominant hypotheses accounting for the between‐colony variation in sex ratio.