No full-text available
To read the full-text of this research,
you can request a copy directly from the authors.
Reproduction in some Pinnipedia
Abstract
S ummary
The reproductive organs have been described in a series of seals, including foetal, neonatal and adult specimens. The collection includes seals from the Antarctic, European waters and from the North Pacific. The species are:— Leptonychotes weddelli, Lobodon carcinophagus, Hydrurga leptonyx, Phoca vitulina, Halichoerus grypus, Otaria byronia. Zalophus californianus, Eumetopias stelleri , and Callorhinus ursinus.
The gross and histological appearances of the testis are described. There is evidence of a breeding season and cyclic testicular activity in the Wed dell and Crabeater Seals. Some measurements of the os penis are given.
A description is given on the gross anatomy of the urinogenitai tract in the female. The ovarian bursa is much enlarged during pregnancy. The urinary papilla is large, partly owing to the presence of lymphoid tissue.
Unimplanted blastocysts have been found in the Crabeater Seal at a time that confirms the occurrence of delayed implantation. Other evidence suggests that delayed implantation is universal in most, if not all, seal.
In at least two species, the Grey and Common Seals, there is marked enlargement of the late foetal and neonatal gonads to a size near or surpassing that of the maternal gonads. This enlargement is primarily due to an increase in the volume of interstitial tissue.
Invaginations of the epithelium forming sub‐surface crypts have been observed in all species of pinniped examined. There is evidence of cyclical activity in the number and development of these crypts. Their relationship to oogenesis is discussed.
The changes in the corpus luteum are described during early and late pregnancy. During the period of delay in implantation the majority of the luteal cells are heavily vacuolated.
The changes in the uterus and vagina are correlated with the changes in the ovary, both in the foetal, neonatal and adult. Coiling of the uterine glands and secretory activity is found in the neonatal specimens.
A short note is appended on the foetal membranes.
... Inferences on leopard seal reproduction are further confounded by the lack of basic anatomical data for their reproductive anatomy, currently limited to the female reproductive tract (Hamilton, 1939;Harrison et al., 1952) and the ex situ baculum (Didier, 1952;Hamilton, 1939). The baculum (os penis) size and structure has been shown to be related to reproductive life history strategies in pinnipeds (Brassey et al., 2020;Dixson, 1995;Fitzpatrick et al., 2012). ...
... The baculum (os penis) size and structure has been shown to be related to reproductive life history strategies in pinnipeds (Brassey et al., 2020;Dixson, 1995;Fitzpatrick et al., 2012). Any additional anatomical data for the baculum anatomy of the leopard seal, particularly its relationship with soft tissues (Harrison et al., 1952), would therefore represent a notable contribution to understanding their reproductive mating strategies. Here we provide some basic soft tissue and in situ skeletal data on the reproductive anatomy of an adult male leopard seal specimen, based on observations made during dissection and CT scanning. ...
... The testes were located between the skin/blubber and abdominal muscles. Despite testis size having a long history of study in pinnipeds (Fitzpatrick et al., 2012;Harrison et al., 1952), this is (to our knowledge) the first observation of thinning of blubber in this region. However, it is possible that the thin blubber was due to malnourishment and poor health, as the blubber thickness of the leopard seal was well below the average for phocids ($3.8 cm, Liwanag et al., 2012) and the expected variability outside of winter (>1.2 cm; Mellish et al., 2007). ...
... Uteri of older individuals are tougher and more fibrous, and placentation scars are not visible for > 1 year (Bengtson and Siniff 1981). Nulliparous females have a conspicuous hymen at the urinary papilla, where the urethra opens into the vagina (Harrison et al. 1952). Ovaries are encapsulated in tentoria and are bean-shaped and smooth in juveniles but pocked with follicles in adults (Tikhomirov 1975). ...
... Penis is pink with a black apex (Barrett-Hamilton 1901). Testes are inguinal and penis is concealed within body contour (Harrison et al. 1952). Testes are lobulate, with each lobule containing 8-10 seminiferous tubules. ...
... seminiferous tubules and epididymides are full. Polygonal Leydig cells of nonreproductive testes are 11-18 urn in diameter and have degenerated organelles (Harrison et al. 1952;Sinha et al. 1977aSinha et al. , 1977b). ...
... Similar vaginal structures are present in hippopotamuses (e.g., Hippopotamus amphibius [17]), which are the closest terrestrial relatives to cetaceans and also mate in the water. Vaginal folds appear to be unique to cetaceans and their closest relatives, the artiodactyls; no similar structures have been reported in non-cetacean marine mammals (phocids [18]; Australian sea lion, Neophoca cinerea [19]; California sea lion, Zalophus californianus [20]; Amazonian manatee, Trichechus inunguis [21]; sea otter, Enhydra lutris [22]). ...
... As it is commonly thought that all water (including freshwater) is lethal to mammalian sperm [63][64], the presence of vaginal folds in a river dolphin, which inhabits only freshwater environments, does not preclude the barrier to water functional hypothesis (baiji, Lipotes vexillifer [26]). However, if vaginal folds serve as physical barriers to water flow, it is unclear why other, non-cetacean marine mammals, which mate only in the water, also lack vaginal folds (e.g., phocids [18], Amazonian manatees [21], sea otters [22]). Collectively, these observations suggest that other factors are needed to explain the variability in the presence and development of vaginal folds in cetaceans. ...
Complex foldings of the vaginal wall are unique to some cetaceans and artiodactyls and are of unknown function(s). The patterns of vaginal length and cumulative vaginal fold length were assessed in relation to body length and to each other in a phylogenetic context to derive insights into functionality. The reproductive tracts of 59 female cetaceans (20 species , 6 families) were dissected. Phylogenetically-controlled reduced major axis regressions were used to establish a scaling trend for the female genitalia of cetaceans. An unparalleled level of vaginal diversity within a mammalian order was found. Vaginal folds varied in number and size across species, and vaginal fold length was positively allometric with body length. Vaginal length was not a significant predictor of vaginal fold length. Functional hypotheses regarding the role of vaginal folds and the potential selection pressures that could lead to evolution of these structures are discussed. Vaginal folds may present physical barriers, which obscure the pathway of seawater and/or sperm travelling through the vagina. This study contributes broad insights to the evolution of reproductive morphology and aquatic adaptations and lays the foundation for future functional morphology analyses.
... Testis and epididymis Harrison et al. (1952), Laws (1956b}, Mansfield (1958) and Harrison (1969) have described the histology of the testis and epididymis of Antarctic phocids. The most detailed general account is by Laws (1956b) on the southern elephant seal; he described the development of the tubules and interstitial tissue up to the attainment of sexual maturity, and the yearly cycle in the mature male in which seven phases of tubule activity were described (Fig. 12.5). ...
... Interstitial cells of the testis enlarge during the breeding season, but regress and often degenerate after breeding is over (Sinha et al., 1977a). Harrison et al. (1952) and Mansfield (1958) showed peak activity (as indicated by testis and seminiferous tubule diameter) in the testes of Weddell and crabeater seals, during October. Sinha et al. (1977a) noted associated changes in the vascularization of the tunica albuginea at this time. ...
Typescript. Thesis (Ph. D.)--University of Missouri--Columbia, 1965. Vita.
... Previously, the sexual maturity of male pinnipeds was investigated through histological observation of their genital organs and endocrinal examination of their reproductive hormones. In addition, histological observations have focused on characterizing spermatogenesis in seminiferous tubules in crabeater seals, Lobodon carcinophagus, leopard seals, Hydrurga leptonyx, and Weddell seals, Leptonychotes weddellii (Harrison et al. 1952). The process of spermatogenesis involves the cell division of spermatogonia, primary and secondary spermatocytes, round and elongated spermatids, and eventually spermatozoa (Mori et al. 1995;Oochi et al. 1998;Tsubota 1998). ...
It's not always possible to obtain samples from dead male pinnipeds that are fresh enough to determine the histological characteristics of spermatogenesis and their stage of sexual maturity. We propose that the morphometrics of genital organs of northern fur seals, Callorhinus ursinus, can be used as a new indicator of sexual maturity. We analyzed data from collected records of male fur seals around Hokkaido during 2011–2017 to examine morphometrics of genital organs and their stage in histological characteristics of spermatogenesis. First, we investigated ontogenetic and seasonal variation in three genital organs: testes, epididymides, and bacula. Second, we classified the stages of histological characteristics of spermatogenesis into three groups (Stage A–C) using non-linear discriminant analysis, based on the stage in histological characteristics of spermatogenesis determined by histological observation of seminiferous tubules. Testicular size, testicular mass, and epididymal mass showed seasonal variation associated with spermatogenesis. From our analysis, the stage in histological characteristics of spermatogenesis could be estimated using testicular mass with high accuracy of predicting spermatogenesis. And measurement of baculum was suggested to be an indicator of predicting sexual maturity. We conclude that this simple estimation may be used to determine sexual maturity based on individual growth patterns.
... Integrating ultrasound imaging with endocrine measures provides a broader understanding of the mechanisms critical to establishing pregnancy in northern fur seals. Previous histological analysis of northern fur seal reproductive tracts has shown that the CL remains functional for the first month following ovulation; however, luteal cells become vacuolated with little capability of steroid secretion for the remainder of embryonic diapause (Boshier, 1981;Craig, 1964;Daniel, 1971;Harrison et al., 1952). Coincident with luteal quiescence, folliculogenesis occurs primarily in the CL-bearing ovary (Craig, 1964;Skinner and Westlin-van Aarde, 1989). ...
Reproductive success is one of the central tenets of conservation management programs, yet the inability to study underlying physiological processes in a minimally-invasive manner and the unpredictable nature of wild animal populations leaves large gaps in our knowledge of factors critical to successful reproduction in wild species. This study integrated ultrasonography of the reproductive tract and analysis of reproductive hormones in 172 northern fur seals (Callorhinus ursinus) to identify intrinsic factors associated with reinitiating embryonic growth at the end of diapause. Within the first 3-4 weeks of active gestation, pregnant fur seals (n = 126) had a larger corpus luteum and fewer antral follicles than non-pregnant fur seals, or those still in diapause (n = 46). This suggests that the conceptus drives changes in ovarian status to convey its presence to the female. Morphological changes in the reproductive tract associated with pregnancy were not reflected in differences in endocrine profiles (estradiol, estrone, progesterone, and relaxin) between pregnant and non-pregnant individuals. Hormone concentrations correlated more strongly with calendar date than with the presence or size of the conceptus, demonstrating that none of these reproductive hormones were reliable markers for early pregnancy diagnosis. Instead, the northern fur seal’s long diestrus may serve to reduce the probability of a temporal mismatch between corpus luteum regression and embryo implantation. Indeed, conception rates were high and confirmed rates of pregnancy loss were relatively low (11%). In this study, minimally-invasive ultrasonography was used in wild pinnipeds to detect very early pregnancy (embryonic vesicles >2 mm) in combination with ovarian and endocrine dynamics at the time of embryo implantation, shedding light on mechanisms for maternal recognition of pregnancy. This study is also the first to track whether these same animals carried the embryo to term, by observing fur seals during the birthing season the following year. Data do not support the notion that decreased pregnancy rates or higher pregnancy loss rates are major contributing factors to the northern fur seal’s population decline.
... However, in cetaceans, it is not known whether the terminal cone or tip also penetrates through the cervix. The pinniped (seals, sea lions, fur seals and walruses) penis is vascular and not fibroelastic, and it contains a baculum (os penis bone) within its glans [29]. While pinnipeds lack the extensive vaginal folds unique to cetaceans and artiodactyls, they have a hymen (a membrane that covers all or part of the vaginal opening) that may function to prevent the incursion of seawater and debris into the reproductive tract [30]. ...
Genitalia are morphologically variable across many taxa and in physical contact during intromission, but little is known about how variation in form correlates with function during copulation. Marine mammals offer important insights into the evolutionary forces that act on genital morphology because they have diverse genitalia and are adapted to aquatic living and mating. Cetaceans have a fibroelastic penis and muscular vaginal folds, while pinni-peds have a baculum and lack vaginal folds. We examined copulatory fit in naturally deceased marine mammals to identify anatomical landmarks in contact during copulation and the potential depth of penile penetration into the vagina. Excised penises were artificially inflated to erection with pressurized saline and compared with silicone vaginal endocasts and within excised vaginas in simulated copulation using high-resolution, diffusible iodine-based, contrast-enhanced computed tomography. We found evidence suggestive of both congruent and antagonistic genital coevolution, depending on the species. We suggest that sexual selection influences morphological shape. This study improves our understanding of how mechanical interactions during copulation influence the shape of genitalia and affect fertility, and has broad applications to other taxa and species conservation.
... The female reproductive tract histology has been described in various pinniped species (Buño et al., 1950;Amoroso et al., 1951;Harrison et al., 1952;Craig, 1964;Boshier, 1979Boshier, , 1981Ouellete and Ronald, 1985;Atkinson et al., 1994;Tedman, 1991;Atkinson, 1997;Colegrove et al., 2009) including a specialized vascular countercurrent mechanism of heat exchange in the reproductive tract of true seals (Rommel et al., 1995(Rommel et al., , 1998. However, in SAFS there are no references about the reproductive tract microanatomical features in pups or juvenile females in order to analyze the changes that occur during puberty and adulthood. ...
In the present study, a detailed histological description of the female reproductive tract of South American fur seal (Arctophoca australis) pups has been conducted. The uterine tube was covered by cuboidal to columnar epithelium; nerve fibers were present in the mesosalpinx and beneath the muscular layer. The uterus was bipartitus; the endometrial surface of the horns was lined by a simple cuboidal or columnar epithelium with deep tubular glands; caudally ("the transition area"), the epithelium changed to pseudostratified columnar, few tubular glands were present and the myometrium increased in width. A bistratified epithelium internally coated the uterine body, whereas it changed to cylindrical stratified epithelium with a highly vascularized lamina propria and a strong muscular layer in the cervix; no endometrial glands were observed in this region. From the transition area of the uterus to the vagina there were several nerve fibers and ganglia belonging to the uterovaginalis plexus. In the vestibule, hymenal folds were poorly developed; adnexa structures included the major vestibular glands and a neurovascular structure similar to the vestibular bulb. Minor vestibular glands were associated with the clitoris. The skin of the perineum was lined by a keratinized stratified epithelium, pigmented, with sebaceous glands, sweat glands and hair follicles. This is the first detailed histological description of the reproductive tract of South American fur seal pups, including the glandular adnexa and nerve structures. These results contribute to the reproductive biology in Pinniped species, and give a better understanding of the utero-placental perfusion mechanism during diving. This article is protected by copyright. All rights reserved.
... Otariids also differ from phocids in having the bacular apex just beneath the glans, where it may function to stimulate the female reproductive tract (this is presumably why the bacular apex of otariids, sciurids, and some other taxa is of diverse shapes and sizes; Long and Frank 1968; Kim et al. 1975; Morejohn 1975; Patterson and Thaeler 1982; Patterson 1983; Dixson 1987). The bacular apex in phocids is farther from the glans and differs little interspecifically (Harrison et al. 1952; Harrison 1969; Green 1972; Tedman 1991; Laws and Sinha 1993). In the hooded seal, the apical cartilage of the baculum comes close to the glans and thus may directly stimulate the female reproductive tract, as also seems likely in the rodent genera Neotoma and Peromyscus (Arata et al. 1965; Long and Frank 1968; Patterson and Thaeler 1982 ). ...
Growth and size-scaling of the baculum and testes in the moderately polygynous hooded seal (Cystophora cristata) were studied using 107 specimens of known age (1 month to 28 years) from the northwestern Atlantic. Bacular growth was rapid between 2 and 5 years of age: length increased 150% and "density" (i.e., mass/length) increased 8-fold and mass 20-fold. Growth continued throughout life. In large, old (>14 years) males, the baculum averaged 20.7 cm in length, 2.1 g/cm in density, and 44.4 g in mass. Bacular length increased relative to body length until seals were about 5 years of age, after which it averaged 8.2%. Testicular growth continued until the seals were about 12 years of age. Testes from breeding males >12 years old averaged 11.2 cm in length, 4.6 cm in width, and 138 g in mass; length averaged 4.9% of body length. In males 2-5 years of age, bacular and testicular sizes were positively allometric relative to body length; in older males, bacular mass and density were positively allometric, and bacular length and testicular size isometric, relative to body length. Bacular size was mostly positively allometric relative to testicular size (bacular length exhibited some isometry). Compared with that of the related and ecologically similar harp seal (Pagophilus groenlandicus), which is presumed to have a promiscuous mating system, the baculum of the hooded seal was structurally simpler and grew more quickly but reached a relatively smaller size in adults (8.2 vs. 9.9% of body length). Relative testicular length was also smaller (4.9 vs. 5.7% of body length) and bacular density lower (2.1 vs. 2.8 g/cm) than in the harp seal. These observations suggest that intra- or inter-sexual competition via copulation is weaker in the hooded seal.
... It is thought that males of all seasonally breeding pinnipeds experience periods of fertility and infertility (Boyd, 1991). However, dif®culties in obtaining reproductive material outside the breeding season have generally restricted longitudinal seasonal studies that might con®rm this theory (see Hamilton, 1939;Bertram, 1940;Harrison et al., 1952;Harrison, 1960;Bigg, 1969). Seasonal breeding, in which periods of sexual quiescence alternate with periods of sexual activity, has been documented in several species of phocids (Laws, 1956;McLaren, 1958;Carrick, Csordas, Ingham & Keith, 1962;Boulva & McLaren, 1979;Grif®ths, 1984a, b;Ryg, Smith & Oritsland, 1991), and two species of otariids ± C. ursinus (Kenyon et al., 1954;Ashchepkova & Fedoseev, 1988) and A. tropicalis (Bester, 1990). ...
Seasonal changes in the reproductive anatomy and histology of the male Cape fur seal Arctocephalus
pusillus
pusillus were examined. Studies were based on 99 specimens collected between Algoa Bay on the south-east coast of South Africa, and Cape Frio, Namibia, during 1974 to 1990. Reproductive organs are briefly described. The presence of sperm in the seminiferous and epididymal tubules indicates that males attain puberty between 3 and 4 years of age. Quantitative measurements of testis weight, testis volume, and the diameter of the seminiferous and epididymal tubules were analysed on a monthly basis and spermatogenesis documented. Although some males may remain in breeding condition until March, the absence of spermatozoa in the epididymis during February to June, when mean testis mass and mean tubule diameter reached a minimum, clearly showed reproductive quiescence following the rut. Four stages of spermatogenesis were observed: (1) inactive (February/March–June); (2) early spermatogenesis (July); (3) late spermatogenesis (July/August–December/January); and (4) epithelial regression (February–June). Individual variation between males, possibly differences in social status and body condition, may influence the duration of spermatogenesis, hence the overlap in duration between epithelial regression and inactivity. It appears that photoperiod may act as an obligatory proximate factor initiating spermatogenesis 3–4 months before the relatively short breeding season from November to December.
... Anatomically, the chorio-allantoic placenta of pinnipeds is comparable to many other carnivores (Harrison et al., 1952). For example , canids and pinnipeds have zonary, endothelio-chorial placentation (Craig, 1964; Miglino et al., 2006). ...
The primary objectives of this study were to validate a canine relaxin RIA for use in otariids and phocids and consider practical applications. For 6 captive Northern fur seal females, serum samples were grouped and examined according to pregnancy (n=13), post-partum (n=8) and non-pregnancy (n=6), and, for 2 captive Northern fur seal males, serum samples were grouped and examined together regardless of age (2 mo-15 yrs, n=6). Placental tissue was available for examination from one Northern fur seal, Steller sea lion and harbor seal. The validation process involved several steps using an acid-acetone extraction process to isolate a relaxin-containing fraction in pools of serum from each group of fur seals and placental tissue from each seal species. A relaxin-like substance was detected in extracts of pregnant, non-pregnant and male serum and placental tissue in a dose-responsive manner as increasing volumes of respective extracts or amounts of canine relaxin were introduced into the assay. In raw serum samples, mean immuno-reactive relaxin concentrations were higher (P<0.05) during pregnancy than post-partum and non-pregnancy, and lower (P<0.05) in male than female fur seals. During pregnancy, mean serum concentrations of relaxin progressively increased (P<0.05) over Months 4-10 and, in serial samples collected from the same fur seals before and after parturition, mean concentrations were higher (P<0.06) pre-partum than post-partum. In conclusion, validation of a homologous canine relaxin RIA for use in otariids and phocids resulted in the discovery of a relaxin-like substance in extracted and raw serum and placental tissue from Northern fur seals, a Steller sea lion and harbor seal. Distinctly higher immuno-reactive concentrations during pregnancy indicated the potential for relaxin to serve as a hormonal marker to differentiate between pregnant and non-pregnant or pseudopregnant pinnipeds.
... The significance of such connections is difficult to establish. Bulging of the epithelium into the interior of the cortex has been observed by: Harrison et al. (1952) in the seal (Pinnipedia) and by Perry (1953) in the elephant (Proboscidea). Harrison & Matthews (1951) state that the covering epithelium is often drawn into the middle of the ovary in the direction of the membrana albuginea lying beneath it, in the form of small curves, cavities or crypts below the surface. ...
Zbadano 79 norek amerykanskich, w tym osobniki 1-10 dniowe, 3-6 tygodniowe, 7-7,5 i 10 miesieczne oraz 11 miesieczne (tylko samice). Uzyskane wyniki wskazują, ze proces rozwoju gonad nie jest zakonczony w momencie urodzenia sie norek i trwa jeszcze u 10-11 miesiecznych zwierząt.
We investigated quantitative relationships of bacular size to age, length of body, and testicular size in the harp seal (Pagophilus groenlandicus), based on collections made in the northwestern Atlantic from 1985 to 1992. Bacular growth was faster than growth in length of body except in old seals (>9 years of age), in which relative growth was isometric. A pubertal spurt in growth in bacular size occurred between 3 and 4 years of age when length increased by 48.3%, mass by 331%, and density by 185%. Concurrently, length of body showed a spurt in growth of 7.2%. Bacular length reached 90% of its asymptotic size of 17.4 cm at ca. 9 years of age, and bacular mass reached that point relative to its asymptote (49.6 g) later at ca. 20 years. In contrast, length of body reached 90% of asymptotic size (176 cm) at only 5–6 years of age. In old seals, bacular length was correlated positively with length of body and age independently. It averaged 9.9% of length of body in old seals. Bacular size was variable: CV = 8.3% for bacular length and 32.8% for bacular mass in old seals. Testicular size peaked in February and March. For young seals (≤9 years old), growth in bacular length was isometric, and growth in bacular mass was positively allo-metric relative to testicular length and mass. In contrast, testicular length and mass of breeding old seals were not correlated significantly with bacular size, length of body, or age. In breeding old seals, testes averaged 10.1 cm in length (range = 7.4–13.2 cm, CV = 10.9%) and 128 g in mass (range = 60.6–204 g, CV = 24.9%), and testicular length averaged 5.7% of length of body. Variation in bacular and testicular size suggests that males have variable reproductive strategies. Comparative analyses on phocid species with known mating systems are needed to test this interpretation.
Beginning in the 1960s, seminal studies characterizing circulating concentrations of immunoreactive relaxin in companion dogs and evaluating the differences in concentrations among pregnant, non-pregnant, and pseudopregnant bitches indicated the potential for relaxin to be applied clinically as a diagnostic aid to detect pregnancy status in wild animal species. A brief historical overview of the nature of relaxin and early work to develop and validate immunological methods to analyze relaxin in the blood of rodents and pigs is initially discussed, which is followed by a summary of the development and validation of relaxin immunoassays to diagnose pregnancy in companion dogs and cats. Thereafter, observation of the pregnancy-specific increase in circulating concentrations of relaxin in laboratory, companion, and farm animal species leads to discussion on the application of radioimmunoassays (RIAs), enzyme immunoassays (EIA) and a rapid immuno-migration (RIM™) assay to diagnose pregnancy in wild terrestrial (e.g., wolves, lions, elephants, rhinoceros, panda) and marine (e.g., seals, dolphins) mammal species. A reference table is included with a comprehensive list of numerous species and essential reagents that have been used in various in-house and commercial immunoassays to successfully analyze relaxin quantitatively and qualitatively in blood (serum or plasma) and to some extent in urine. While the detection of relaxin concentrations has the potential to aid in the diagnosis of pregnancy in many wild animal species, there are challenges in other species. Future efforts should focus on validation of non-radiolabeled relaxin immunoassays for broader application among species and improving techniques (e.g., extraction, purification) to analyze relaxin in samples other than blood (e.g., urine, feces, saliva, blow, skin, blubber) that can be collected in a less invasive or stressful manner and processed accordingly for basic and applied purposes, especially with application towards conservation of threatened or endangered species.
Numerous mammalian taxa exhibit reproductive delays, pauses in reproduction that occur between mating and fertilization, between fertilization and implantation of the embryo, or after an embryo has implanted. Of the 27 mammalian orders, 9 are known to exhibit reproductive delays, including Diptrotodontia, Dasyuromorphia, Eulipotyphyta, Cingulata, Carnivora, Rodentia, Chiroptera, Lagomorpha and Cetartiodactyla. Most researchers interested in delays have focused on their evolutionary origins. However, the consequences of these delays have not been considered fully. Given the lengthening of the period over which reproduction occurs, it is possible that this unique aspect of reproduction facilitates post-copulatory sexual selection. When considered in the context of sexual selection, delays may allow sperm competition and female manipulation of fertilization (cryptic female choice) as well as other post-copulatory processes. We investigate the potential for reproductive delays to facilitate post-copulatory sexual selection and suggest avenues for research that may further our knowledge of sexual selection. We also provide a general review of reproductive delays in mammals.
Bacular development is described for the Weddell seal, Leptonychotes weddelli, based on specimens from 1 to 18 years of age. The bacular apex, cross-sectional configuration of the shaft, base, and other aspects are described and compared with other genera of phocids. The anterior dorsal aspect of the baculum of Leptonychotes is unique among phocids in development of a pronounced crest as an adult.
Reproductive tracts were collected on the eastern coast of Canada from adult female grey seals (Halichoerus grypus) during gestation and postparturition, and from adult female harp seals (Phoca groenlandica) during delayed implantation and postparturition. Reproductive tracts were fixed in 10% buffered formalin for light microscopy. The placental site and adjacent tissue were preserved in 2% glutaraldehyde – 1% paraformaldehyde for scanning electron microscopy. During the delay of blastocyst implantation, the endometria of the gravid and nongravid uterine horns were similar in microscopic appearance. During gestation, maternal septa were often surrounded by maternal epithelium deep into the placental labyrinth except distally, where the maternal cells were replaced by syncytium. Marginal hematomas increased in size and complexity throughout placentation. Following parturition, uterine regression occurred earlier in harp seals (10 days postpartum) than in grey seals (21–25 days postpartum). Postpartum changes were most pronounced in the placental site where the blood vessels underwent extensive reorganization. In some specimens, the extensively vascularized placental site of the previous pregnancy was still apparent 12 months later. Epithelial replacement in the uterus was complete in grey seals 21–25 days postpartum and sooner in harp seals. Cervical and vaginal stratification occurred in both phocids following parturition and increased towards estrus. A recently ovulated grey seal was obtained between 21 and 25 days postpartum. The vaginal stratification and the presence of sperm in their uterine horns indicated that grey seals began estrus about 12–17 days postpartum. In harp seals, estrus appeared to occur towards the end of the lactational period, about 10–12 days postpartum.
A review of literature and personal correspondence on the harbour seal suggests that large regional variations and clines occur in the timing of its pupping season. The pupping season, which generally lasts from to 2 months in any one area, extends from late January to October over the range of the species. Along the east coast of Asia, young tend to be born later as one goes northeastward. In North America, they tend to be born later going southeast from Alaska to Washington, earlier south from Washington to Mexico, and later north from New England to Baffin Island. Clines cannot be demonstrated for Europe. No reasons are apparent at this time to explain the regional variations or clines.
A bstract
Growth and reproductive biology of New Zealand fur seals ( Arctocephalus forsteri ) were studied by examining 127 seals (57 females, 64 males) killed incidentally in fishing gear in New Zealand waters in 1996. Tooth sections were used to age the animals, and male and female reproductive organs were examined macroscopically and histologically. The maximum age observed was 22 yr for females and 12 yr for males. Males were significantly larger than females, but growth was similar up to 5 yr. Males reached sexual maturity between 5 and 9 yr of age, whereas females did so between 4 and 6 yr. The mean pregnancy rate in females was 0.69 (95% CI = 0.54–0.81).
Published accounts of twinning in seals are reviewed briefly and details are given of new records of twins in the Common and Grey seals in Scotland.
During late foetal life and at birth the gonads of both Grey and Common seals are enlarged, and there are indications of stimulation in the rest of the reproductive tract. The enlargement of the gonads is due mainly to the presence of very large numbers of cells resembling interstitial cells. The presence of groups of small round cells resembling lymphocytes and of cells intermediate between them and fully developed interstitial cells suggests that the small round cells may be the precursors of the latter. Whether these cells are lymphocytes or primitive mesenchymal cells cannot be stated with certainty. The ovaries of foetal Common and Grey seals contain no follicles beyond the stage where oocytes are ensheathed in a single layer of epithelial cells, but more marked follicular development was present in the ovaries of a still‐born Californian sea lion. No evidence of spermatogenesis was seen in the testes of any foetal or neonatal male seal. Regression occurs rapidly after birth and is nearly complete at the age of two weeks. The interstitial cells disappear by a process similar to fatty degeneration. Retrogression is accompanied by a remarkable obliteration of many blood vessels supplying the outer part of the medulla and the cortex of the ovary. The stimulus responsible for the precocious enlargement of the foetal gonads is removed with the birth of the young. The rapid decrease of endocrine influence after birth suggests that the placenta may be implicated.
In the adult Common and Grey seal the corpus luteum persists until the end of pregnancy and begins to degenerate a few days after parturition. Follicular development occurs in the maternal ovaries towards the end of pregnancy and in the immediate post‐parturient period. The maternal ovaries are probably a source of oestrogens, both before, during, and after parturition, and such oestrogens could cross the placenta and affect foetal tissues.
The prostate of all male foetuses of both species towards the end of pregnancy and immediately after birth is markedly enlarged. There is proliferation and hypertrophy of the prostatic alveoli, dilation of the tubules, and an increase in the size of the epithelial cells. A week after birth the weight of the gland is reduced by more than one‐half. Persistence and hyperplasia of the uterus masculinus occurs in some foetal and newborn pups of the Common seal, but no similar enlargement was seen in the Grey seal.
The thyroid in the late foetal and neonatal Common and Grey seals showed wide differences in their histological appearances. The thyroid glands from an adult lactating seal of each species were widely different. In the Grey seal it was almost completely atropic but in the Common seal it appeared to be intensely active.
The amount of medulla present in the adrenal of foetal seals is small by comparison with that of the cortex. A large number of cortical islands packed with lipid is present in the medulla, often containing more lipid than the cortex itself. The capsule of the adrenal varies considerably in thickness in different parts of the gland and in individuals of similar age. It is relatively thick in the glands of young animals and becomes much thinner in those of older individuals. In some specimens the capsule contains islands of cells containing transitional stages between capsular and glomerular cells. This supports the conception of a capsular origin of the cortical cells. The adrenal in seals is lobulated and folded, particularly in the adults. Large connective tissue trabeculae extend into the medulla from the capsule, accompanied by folds of the zona glomerulosa. The zona glomerulosa is very well‐developed and the large size of this zone may be associated with the seal's marine habitat. Pigment occurs in the cortex of a number of seal adrenals, more frequently in Grey than in Common seals, and appears to bear no relation to age or sex.
The pituitaries from five Common seals were examined, and evidence was found that the neurosecretory material present in the hypothalamus and pituitary was considerably more conspicuous than in, for example, the dog. This may be correlated with the elaboration of posterior pituitary principle, and perhaps of antidiuretic hormone. It is possible that the capacity of the seal to secrete these principles is already well‐developed at birth and might be expected in the offspring of an aquatic mammal. In the adenohypophysis the maturity of the pars distalis at birth is striking, and the pars tuberalis and the pars intermedia are relatively large as compared, for example, with those of the dog. The α‐ and ß‐cells in the pars distalis of a newborn seal are comparatively mature. It is not, however, thought that the foetal and neonatal pituitary can alone be the cause of the gonadal hypertrophy, since the hypertrophy subsides rapidly after birth. It must therefore be concluded that the stimulus causing the hypertrophy before birth is derived primarily from an extra‐foetal source, but that a part may possibly be played by the foetal pituitary cannot be completely excluded. Anatomically, histologically, and behaviourally, the young seal is born in a remarkably mature state, probably more advanced comparatively than in most other mammals. It may thus well be that the endocrine system is so developed in the late foetal and neotal seal that it is particularly sensitive to the hormonal influences from the maternal side of the placenta, or originating in the placenta itself, or perhaps passing to the foetus from both sources.
The internal growth rings of the teeth of the crabeater seal (Lobodon carcinophagus) are described and the annual pattern established.
By examination of near term foetuses, recently weaned pups, half‐year‐old, one‐year‐old and older animals the probable pattern of dentine deposition in the first year is established. The neonatal line is conspicuous; a line marking the time of weaning is present and also a line which probably represents the pup moult. The rate of dentine deposition is discussed and it is suggested that lactation extends over about five weeks.
Using ages determined from the growth rings in the canine teeth, an average growth curve for body length has been constructed and is compared with earlier estimates of the rate of growth in the first few years.
Evidence is given which suggests that the average neonatal length is 45 in. The sizes subsequently attained by the two sexes are similar, though the largest females tend to be slightly larger than the largest males. The mean body length of animals over twelve years old is 89 $2–36 in.
The question of the age at sexual maturity is re‐examined and it is concluded that in the female sexual maturity is usually attained at an age of a few months over two years.
The age distribution of the two samples of crabeater seals is discussed. The oldest animals in the material were 19 years old on the basis of dentine rings.
The venous system has been examined by dissection and by making Marco resin casts of the vascular system of young and adult specimens of Phoca vitulina, Halichoerus grypus, Hydrurga leptonyx, Mirounga leonina and Phocaena phocaena. Embryos and foetuses of the above species and of Leptonychotes weddelli, Lobodon carcinophagus, Zalophus californianus, Delphinus delphis, Globiocephala melaena, Balaenoptera physalus and Megaptera novaeangliae have been dissected, injected with coloured gelatin or serially sectioned.
A duplicated abdominal posterior vena cava, thin‐walled and of large size, was found in all species examined. A well‐defined sphincter supplied by the right phrenic nerve was found surrounding the posterior vena cava anterior to the diaphragm in all species of Pinnipedia; the sphincter generally consisted of circular bundles of striated muscle, separated from the diaphragm by a fibrous ring. In the Zalophus foetus there was a thin caval sphincter composed of two slips of diaphragmatic muscle. A sphincter‐like “sling” of diaphragmatic muscle was found in Phocaena.
A large hepatic sinus was present in all the Pinnipedia examined except Zalophus, but was absent in the Cetacea.
A marked stellate plexus of veins on the surfaces of the kidney was present in all species of Pinnipedia. No renal vein emerges from the hilum and the stellate plexus drains by several large vessels into the corresponding limb of the posterior vena cava. The stellate plexus has numerous communications, particularly with an extradural intravertebral vein. A superficial plexus is present, though less marked, in Cetacea, and the main drainage is by one or more renal veins emerging from the mesial slit.
The extradural intravertebral venous system is well‐developed in all specimens of Pinnipedia and is present in all adult and foetal Cetacea examined. In Phoca it is in the form of a large vein lying dorsal to the cord, which communicates posteriorly with the stellate renal plexus and the pelvic plexuses, and anteriorly with the intracranial venous sinuses. In Phocaena there is a large vein placed ventral to the cord, but its main communication is with the anterior vena cava. In the Balaenoptera foetus there are two small veins lying ventral to the cord, which communicate with the anterior vena cava via the dorsal thoracic veins. In the latter two species the vertebral canal anterior to the thorax is filled with retial tissue surrounding the cord.
In all specimens examined there is only a poorly developed jugular venous system. The intracranial venous drainage would appear to be almost entirely via veins, sinuses or retial tissue in the vertebral canal.
The Pinnipedia have a well‐developed azygos system; the Cetacea either a poorly developed one or none at all.
All specimens of Pinnipedia, except Zalophus, and those Cetacea examined show a venous plexus or a single vein encircling the pericardium and projecting into the pleural cavity and draining into the thoracic posterior vena cava.
Certain experiments carried out on anaesthetized seals are described. Stimulation of the right phrenic nerve in Phoca caused contraction of the caval sphincter, which was recorded manometrically and also by X‐rays after intravenous injection of radio‐opaque substances. A fibre count was made of the phrenic nerve and its terminal branches.
Estimations of blood volume (117 ml. per kg. body weight in a Common Seal pup) and of other blood constants are recorded.
The possible function of the peculiarities of the venous system in Pinnipedia and Cetacea is discussed.
. 1May to September observations on a colony of c. 400 Phoca vitulina in Shetland. The limiting factors of the habitat are described.2Daily 8 a.m. counts showed that numbers hauled out depended chiefly on swell or human disturbance (both erratic), to a lesser degree on the state of the tide and little, if at all, on rain and sun.3Relations with other species include: practically no overlap with Halichoerus grypus, indications that sea-birds may be taken as food, and man as a long-established enemy, mainly in the pupping season, when almost an entire generation may be wiped out.4In May and early June there was a great deal of play, apparently sexual, with “pairs” rolling together in the water. First pups appeared on June 14th when the play period ceased. The pupping season extended over three weeks.5Breeding behaviour proved largely aquatic. Pups may be born on tidal rocks or apparently even in the water. They found great difficulty in landing at first and spent most of their time at sea. Mothers guarded them closely for about three weeks and suckled them either in the shallows or ashore. Lactation lasted four weeks.6After the pups became independent, adults began to moult. Sexual play was not resumed and no coition was seen during this post-pupping season.7Of the seals present at the beginning of the season c. 15 per cent were yearlings and possibly only 70 per cent. were adult. The number of pups born was c. 18 per cent of the total population. Comparisons are made with a colony in Orkney.
The structure of the seminiferous tubules in neonate harp seals, Pagophilus groenlandicus, was essentially similar in one-, five- and ten-day old animals. The tubules were small in diameter, devoid of lumina and contained predominantly supportive cells. The interstitial cells in the neonates were large, numerous and highly vacuolated. They became smaller and appeared less active in the ten-day old animals compared with the one-day old seals, although they were still considerably more numerous and vacuolated than in testes taken from adult harp seals.
Ultrastructural study of the Leydig cells of nonbreeding crabeater, leopard and Ross seals showed that three types of cells could be distinguished. Type I cells possessed the cytological features typical of steroid-secreting cells. Type II cells exhibited various features of degeneration, e.g. accumulation of large amounts of lipofuscin granules (residual bodies), lipid droplets, secondary lysosomes, rectangular crystalloids, and previously undescribed 'peculiar bodies'. These cellular inclusions and debris were released into the interstitium to be phagocytosed by macrophages and/or resorbed by the lymphatics. Type III Leydig cells contained large amounts of lipid droplets, sparse cytoplasmic organelles and essentially became lipid storage cells.
Ovaries were collected from 26 Ross seals shot in the King Haakon VII Sea south of the 60 degrees latitude during 3 periods, between 12 January and 2 February 1980-1982. The structure of the ovaries resembled that of other pinnipeds. A corpus luteum was found in 18 of 26 females, which therefore were regarded as reproductive. However, no females were lactating or visibly pregnant (presence of fetus in the uterus). Of the remaining 8 females (non-reproductive), 3 had neither a corpus luteum nor a corpus albicans. Ovulation did not alternate between ovaries in 4 of 10 females. Ovarian weight was greater in reproductive females than in non-reproductive females, and was also correlated with presence of a corpus luteum. Follicular development was more advanced in reproductive females than in non-reproductive females, and it was also more pronounced in the ovary containing a corpus luteum. The finding of a high percentage of females with a corpus luteum, but with no fetus in the uterus, together with histological characteristics of the ovarian structures in the present study, and earlier published data on mating, pupping and moulting, provide circumstantial evidence for delayed implantation in Ross seals.
Chorionic gonadotrophin activity in extracts of the term placenta of a dolphin, a sea lion and a grey seal was measured by its effectiveness in increasing uterine weight in the mouse and by solid-phase RIA using hCG as immunogen and labelled antigen. Bioreactive (B) gonadotrophin was found in these placentae and, compared to the human term placenta, the concentration of CG in the dolphin was higher, in the sea lion similar and in the grey seal lower. The biological activity in each species was neutralized with a rabbit anti-hCG serum. All placental extracts contained material active in the hCG immunoassay (I). The ratio B/I was significantly higher for the CG in the placental extracts of the marine mammals compared with that of the human term placenta. Results of in-vivo bioassay, RIA, electrophoretic and gel-chromatographic studies indicate structural similarities between CG in the placentae of the marine mammals and human CG.
Segments of the taenia coli from guinea-pig were transplanted into the anterior chamber of the eye. Depending on such factors as the total volume of the transplant and the presence or absence of ganglion cells degeneration was either very extensive (90% or more of the total number of muscle cells) or localized (alternating regions of degenerating and normal structure). During days 1–2 muscle cells lost their plasma membranes so that their cytoplasmic contents were dispersed into the intercellular spaces. Many cells produced numerous small processes which were pinched off and dispersed in a similar manner. Following a period of intense mitotic activity (3–8 days) numerous cells with the characteristics of embryonic smooth muscle cells were evident. Within 10–14 days these differentiating cells produced bulbous protrusions and assumed more irregular outlines than at 3–8 days. The protrusions formed close contacts (50–100Å intercellular space) and tight junctions between adjacent muscle cells. Aggregation of muscle cells into bundles was under way between 14–28 days. At approximately 4–6 weeks these developing muscle groups were invaded by nerve fiber bundles. The pattern of the innervation and the form and size of the muscle bundles simulated the normal. These findings are discussed in relation to the possible functions of the intercellular contacts and cellular protrusions which characterise various periods of regeneration.
Blood samples collected from Leopard Seals, Hydrurga leptonyx, from Heard Island and Macquarie Island were surveyed electrophoretically for allozyme variation in blood proteins. Thirty four proteins encoded by a minimum of 39 genetic loci were surveyed; six of these were found to be polymorphic, but only one could be considered polymorphic at the 95% level of significance. The mean observed heterozygosity was 0.01 I ± 0.007, which is the lowest yet recorded for a species of Antarctic seal. Hydrurga leptonyx exhibited fixed allelic differences with the Southern Elephant Seal, Mirounga leonina, at 26% of loci screened.
The ferret has been but little used for experimental laboratory work on reproduction, although its small size and marked sexual changes, together with the fact that it ovulates only after coitus, make it a very suitable species for laboratory investigations. The study of the ferret's œstrous cycle, however, formed the subject of an investigation by one of us some 25 years ago (Marshall, 1904), when it was shown that there was normally a well-marked breeding season, extending from about March to August, and an anœstrum during the rest of they year. The fact was verified that œstrus in the absence of the male may extend over a very prolonged period (as much as 6 weeks) and that it is characterised by a very well marked swelling of the vulva. Congestion of the uterus and other internal changes were also described. Futhermore, it was ascertained that ovulation in the ferret, as in the rabbit, does not occur spontaneously, but depends upon sexual intercourse, a fact which was confirmed later by Robinson (1918). It has been shown by a number of authors (Ancels and Bouin, 1910; Schil, 1912; Hammond and Marshall, 1914) that in the rabbit the condition known as pseudo-pregnancy can be induced by a sterile mating ( e. g. , the doe copulating with a vasectomised buck), the stimulus of sexual intercourse resulting in ovulation and the subsequent formation of corpora lutea, which develop as in true pregnancy up to about the 16th day, and during this time bring about a growth of the uterine musosa and an hypertrophy of the mammary glands comparable to that which occur during true pregnancy. In the present investigation experiments were carried out to determine whether pseudo-pregnancy could be induced similarly in the ferret, and a series of observations was made upon the correlated changes in the ovaries, uterus, mammary glands, and vulva in various stages and conditions during the seasons of reproductive activity.
Examination of the ovaries from 106 different species of mammals has revealed the presence in a number of them of sub-surface crypts, lined by germinal epithelium, which penetrate into, or pass through the tunica albuginea. Such crypts are differentiated from intra-ovarian clefts which simply sub-divide the ovary and from Pfluger's tubes which have no lumen. The crypts are constantly found in six species of Pinnipeds, frequently in numbers of Marsupialia, Insectivora, many fissiped Carnivora, two species of Procaviidae, Loxòdonta africana, and occasionally in Rodentia and Primates, including the human subject. In the Pinnipedia, and probably in the other species, the maximum development is at the time of oestrus and early pregnancy and the degree of development of the crypts appears to undergo changes corresponding to the degree of follicular activity and oogenesis. Experimental injection of gonadotrophins or oestrogens causes the appearance of crypts in Putorius furo, a species which does not normally show marked crypt formation.
The association of crypt formation with oogenesis is discussed and it is suggested that such crypts are possibly a vestige of the primitive pattern of ovarian structure.
In the human subject the formation of crypts is associated with the possible subsequent development of fibroadenoma or cystadenoma of the ovary.
The southern species of Elephant Seal (Mirounga leonina L.) has a circum-polar, subantarctic distribution and it is almost certain that by far the largest focus of population is found in South Georgia where there is an enormous herd.
Summary(i) Morphological studies relating to the origin and differentiation of the definitive germ cells in vertebrates have, as indicated, resulted in conflicting views. In many instances two or more competent investigators who have studied the same form have reached different conclusions. (2) Some contend that the germ cells are set aside from the soma during the early stages of embryonic development, and that these alone serve as the progenitors of the functional sex cells. (3) Others recognize an early differentiation of sex cells but hold that these are supplemented by others produced from the somatic epithelium of the gonad in late embryonic or post-embryonic stages. (4) Another group recognizes the early differentiated cells as germ cells but contend that these all degenerate and that the definitive ones are formed from the germinal epithelium. These degenerating germ cells are believed by certain authors to be a phylogenetic recapitulation of the condition in lower forms. (5) Finally, yet another group contends that the so-called primordial germ cells are not germ cells at all but are enlarged cells in some stage of mitosis or in some specific metabolic phase. This group believes that all germ cells are derived from the somatic cells of the germinal epithelium. (6) Experimental work supports the view that the primordial germ cells, which are recognized early, are the progenitors of the definitive sex cells. When these primordial germ cells are prevented from reaching the site of the developing gonad the individual fails to develop sex cells, although a sterile gonad and its associated structures may develop. (7) I suggest that the observed proliferation of germ cells from the germinal epithelium, reported by numerous investigators, can be interpreted in another way by a thorough study of the enlarged germ cells in relation to the epithelium. It seems probable that the cells of the epithelium, which form functional sex elements, are not and never were a part of the mesothelial covering, but are cells which were segregated early, and are merely stored in the epithelium.
1. Published descriptions of the development of the corpus luteum show that the majority of the luteal cells are derived from the granulosa cells.
2. In the vertebrates, other than mammals, the development of a corpus luteum does not appear to be associated solely with viviparity.
3. The fate of the theca interna cells varies greatly, even in closely related species.
4. The theca interna cells may remain in groups at the periphery of the gland, or they may invade the developing corpus luteum and either: ( a ) disappear entirely a few days after ovulation, ( b ) become indistinguishable from the granulosa cells, or ( c ) possibly revert to fibroblasts.
5. The function of the theca interna or theca‐luteal cells in the mature corpus luteum is unknown. It is, however, possible that they secrete oestrogen.
6. The blood vessels of the corpus luteum are derived from the theca interna plexus of capillaries; the corpus luteum is well vascularized by the time that implantation occurs.
7. The connective tissue of the corpus luteum is believed by many authors to be derived from theca interna cells that have reverted to fibroblasts. In the Artiodactyla and in Macaca , and possibly in other animals, there is evidence that the endothelial cells give rise to the reticular framework.
8. The corpus luteum is generally fully developed by the time of implantation of the blastocyst.
9. The appearance of the vacuoles in the luteal cells of pregnant mammals is not necessarily indicative of impending cessation of function or of degeneration. Such vacuolation may mark a ‘resting period’ as in those animals in which implantation is delayed, or a ‘transition period’ during which the placenta is becoming established structurally and functionally.
10. The time of appearance of retrogressive changes in the corpus luteum of pregnancy in any species is probably related to the degree of activity of the placenta in that species and to the prolactin level in the anterior pituitary.
11. Accessory, aberrant and other atypical forms of corpora lutea have been reported in the macaque, the tree porcupine and the mare.
The interstitial The Weddell seal in the Bay of Whales The estrous cycle in the rat and its associated phenomena The early development of the ferret ; the zona granulosa Ovarian autografts in monkeys Cyclical changes in the vagina and vulva of the ferret Xatural history of the elephant seal
- J A Loxa
- Evaas H M Zona
- A M Manul
- S Zttckermas
KIXG~BURY (1914). The interstitial cells of the mamnialiari ovary : Felia domestica. dmer. J. Anat. LINDSEY, A. A. (l9X). The Weddell seal in the Bay of Whales. J. Mammal. 18, 127. Loxa, J. A., R: EVAAS. H. M. (1922). The estrous cycle in the rat and its associated phenomena,. MAINLANU. D. (1932). The early development of the ferret ; the zona granulosa, zona pellucida MANUL, A. M., & ZTTCKERMAS, S. (1949). Ovarian autografts in monkeys. J. Arut., Lond. 83, 315. MARSHALL, F. H. A. (1933). Cyclical changes in the vagina and vulva of the ferret. Quart. J. exp. Physiol. 22, 131. MATTHEWS, L. H. (1929). Xatural history of the elephant seal.
The natural history of the grey seal, including lactation Sub-surface crypts, oogenesis, and the corpus luteum in the ovaries of seals The homology of the vesicular ovarian follicles of the mammalian ovary with the coelom
- Rtriews
- L H Mattiiews
- L H Haermjk
&!rTriEws, L. H. (1950). The natural history of the grey seal, including lactation. Proc. zool. Soc. Lond. 120, 763. MATTIiEWS, L. H., & HAERMJK-, R. J. (1949). Sub-surface crypts, oogenesis, and the corpus luteum in the ovaries of seals. Nature, Lond. 164, 587. MOSSMAN, H. W. (1938). The homology of the vesicular ovarian follicles of the mammalian ovary with the coelom. Anat. Rec. 70, 643. MURIE, J. (1871). Researches upon the anatomy of the Pinnipedia. I. On the walrus (Trichechus roSrnaru8 Linn.). Trans. 2001. Soc. Lond. 7, 411. MURIE, J. (1874). Researches on the anatomy of the Pinnipedia. 111. Descriptive anatomy of the sea-lion (Otaria jubata). Trans. 2001. SOC. Lond. 8, 501.
History of North American Pinnipeds. A monograph of the Walruses Sea-lions Sea-bears and Seals of North America
- J A Allen
The walrus of the Kara Sea
- Chapsky K. K.