The reproductive biology of seals is fascinating in many aspects. As in most mammals, the time of onset of puberty in seals is variable. Once sexually mature, most but not all seals are seasonally mono-oestrous, with highly synchronized breeding seasons. They have evolved as either terrestrial or aquatic copulators, although a few species mate in a variety of habitats. Their mating strategies are diverse, ranging from serial monogamy to extreme polygyny. Gestation in seals is characterized by an embryonic diapause, which is obligate in most species. Reactivation of the blastocyst is followed by a placental gestation. All species of seal require a terrestrial (including ice floes) habitat for parturition. Lactation differs between the two seal families: phocid seals have an intense period of maternal investment, during which the mothers fast; otariid seals have a prolonged lactation during which intense bouts of suckling are interspersed by days of separation from their pups while the mother forages at sea. Although the anatomy and functional morphology of seals has been well described, less is known of the endocrinology of reproduction. This is due mainly to the logistical difficulties that researchers experience in collecting serial samples from a species that is relatively difficult to handle. This article reviews the basic anatomy and physiology, and our current understanding of the comparative aspects of reproduction in seals. Reproductive behaviours as well as the influences of environmental factors, such as photoperiod, nutrition and xenobiotics, are also discussed.
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S. Atkinson and P. Williamson
Summary. Southdown ewes in mid-seasonal anoestrus were exposed to rams for 0 h (control group), 2 h, 24 h, 40 h, 3 days, 10 days or 20 days. Serial blood samples were then taken to determine LH and FSH levels. Ewes with >24 h ram exposure were ovariectomized immediately after bleeding, and all follicles >1 mm diameter were dissected from the ovaries and measured. LH basal concentrations and pulse frequency increased significantly within 2 h of ram introduction, but by 24 h fell, and then remained low. FSH concentrations fell within 2 h of ram introduction and remained low. Control group ewes (isolated) had no follicles >4 mm diameter, whereas all ewes exposed to rams had large follicles, with CL or preovulatory follicles present at 40 h after ram introduction. Ram introduction was also associated with follicle recruitment (antrum formation to <2 mm). Follicular recruitment and development to the large follicle stage therefore occurred during a period of low plasma gonadotrophin levels and suppressed LH pulsing.
S. Atkinson and W. G. Gilmarti
Summary. Blood samples from four captive male Hawaiian monk seals were collected at intervals of one month for one year for testosterone assay. Plasma testosterone concentrations, measured by radioimmunoassay, revealed a clear seasonal pattern. The lowest mean testosterone concentration (0·09 ± 0·04 ng ml−1) occurred in January, and the highest (1·78 ± 0·40 ng ml−1) in June. The seasonal occurrence of births and of injuries related to mating in wild populations of Hawaiian monk seals showed a distinct association with the period of high testosterone. This study supports other data that indicate that the Hawaiian monk seal is a seasonal breeder and is reproductively active for longer than monachine seals that live in higher latitudes.
Keywords: Hawaiian monk seal; testosterone; seasonal breeding
S. Atkinson, P. Williamson, C. L. Kang, and R. S. Carson
Summary. The introduction of rams to a group of previously isolated anoestrous ewes has been shown to stimulate ovarian follicular development and ovulation. The present experiment was carried out to determine the ability of follicles arising from this ram stimulus to produce steroids and bind hCG. Seasonally anoestrous Southdown ewes were exposed to rams for 24 h, 40 h, 3 days, 10 days or 20 days before ovariectomy. Steroid production and the concentration of hCG binding sites in follicles dissected from the ovaries were measured in vitro. The presence of a ram caused ovulation and enhanced oestradiol production by follicles, but had little effect on total androgen production or the number of hCG binding sites present in the follicles when compared to follicles from anoestrous ewes. The oestradiol concentrations in large follicles were not as high as in preovulatory follicles from cyclic ewes reported in other studies. Follicles continued to develop through the ram contact period and when incubated after 40 h and 10 days of ram contact produced high levels of progesterone, indicating partial luteinization, although the corpora lutea (CL) resulting from the induced ovulations regressed prematurely. We suggest that the lack of hCG binding sites in ram-induced follicles may be the cause of poor luteinization and suboptimal development of luteal tissue after induced ovulation in ewes during seasonal anoestrus.
N. R. Adams, S. Atkinson, and M. R. Sanders
Summary. In a series of 5 experiments, ewes were treated with implants releasing oestradiol-17β and the effects on ovulation rate were observed. Large doses of oestradiol-17β (> 20 μg/day) produced anovulation while smaller amounts only reduced the proportion of twin ovulations. Amounts of exogenous oestradiol comparable to ovarian production rate in the luteal phase (< 1 μg/day) produced a significant (P < 0·01) suppression in ovulation rate. Treatment during the follicular phase of the oestrous cycle was most effective, but treatment during the luteal phase alone also appeared to suppress ovulation rate. Furthermore, in 2 of 3 experiments ewes treated with low amounts of oestradiol during the first half of the luteal phase were less likely to have multiple ovulations at the subsequent oestrous period. The results support the hypothesis that oestrogen is involved in the physiological control of ovulation rate in the ewe, but this action is probably not restricted to the assertion of dominance by a maturing follicle during the follicular phase.
Keywords: oestrogen; ovulation rate; sheep
S. Atkinson, W. G. Gilmartin, and B. L. Lasley
Adult male Hawaiian monk seals were administered a gonadotrophin-releasing hormone (GnRH) agonist to determine its effectiveness in reducing the testicular production of testosterone. Blood samples were collected from four treated seals and two control seals at weekly intervals for 10 weeks and again at the beginning of the following breeding season. The GnRH-agonist had an initial, brief, stimulating effect on circulating testosterone, but this was followed by an inhibitory effect that lasted for 7 to 8 weeks. The plasma concentrations of testosterone were within normal ranges by the following spring. These results demonstrate a reversible form of long-term androgen suppression, which may have applicability in a variety of wildlife management programmes.
S. Atkinson, N. R. Adams, and G. B. Martin
Summary. In two experiments, mature Merino ewes were fitted with subcutaneous implants containing oestradiol-17β or empty implants (control). Peripheral concentrations of LH and FSH were measured during luteal and follicular phases, which were synchronized by means of intravaginal progestagen-impregnated sponges. The ovulation rates of the ewes were determined by laparoscopy, 1 week after luteolysis. In Exp. 1, small implants (3 mm) decreased the LH pulse frequency before luteolysis. In the ewes with oestradiol implants, the amplitude of the preovulatory surge of LH was reduced and the onsets of the LH and FSH surges were delayed. There was no effect of oestradiol on LH baseline, LH pulse amplitude or in the concentration of FSH during the luteal or follicular phases. In Exp. 2, larger implants (10 mm) were inserted for the luteal, follicular, or luteal + follicular phases. The control ewes had empty implants. In the ewes with oestradiol implants, LH pulse frequencies were decreased during the luteal phase. This decrease persisted throughout the follicular phase, even though the oestradiol implants had been removed. There were no differences in the other measures of LH or FSH in the luteal or follicular phases. Ovulation rates were not affected by oestradiol treatment in either experiment, indicating that the regulation of LH pulse frequency is not a critical factor in the determination of ovulation rate in ewes. This was supported by retrospective analysis of the gonadotrophin profiles of single and twin-ovulating ewes, in which all measures of LH were similar between the two groups. However, twin-bearing ewes had slightly higher circulating concentrations of FSH during the luteal phase. As the difference in FSH was not large (13%), and it disappeared after luteolysis, it is difficult to postulate that FSH plays a major role in the final selection of the preovulatory follicle(s) in the ewe.
Keywords: ovulation rate; LH; FSH; oestradiol; sheep
S. Atkinson, B. L. Becker, T. C. Johanos, J. R. Pietraszek, and B. C. S. Kuhn
Female Hawaiian monk seals at Laysan Island in the Northwestern Hawaiian Islands seasonally risk aggressive mating attempts by groups of adult male monk seals. These attacks, which also target immature female and male seals at a lower frequency, result in injuries that are often fatal and are termed mobbings. This study was undertaken to assess the reproductive status of nine female seals that died after mobbing attacks and to obtain basic morphological data of reproductive tracts from ten females. Reproductive morphology of the seals indicated that the lengths of the uterine body and both uterine horns were significantly shorter in nulliparous than in parous seals. Seven of the nine seals were periovulatory, on the basis of gross morphology of the ovaries at death. The ovaries of the other two seals possessed immature follicles. Histological studies of the vagina and uterus confirmed the reproductive status of the seals. When the reproductive status at the time of first injury was estimated, all seals were in the follicular phase of the oestrous cycle. At least four of these seals were estimated to be in oestrus at the time of their first injury, and seven of the seals sustained at least one injury during the estimated period of oestrus (2–6 days). These results support the hypothesis that most adult female Hawaiian monk seals that die following an attack by male monk seals are periovulatory, and that the majority of the attacks occur during oestrus.
N. R. Adams, S. Atkinson, G. B. Martin, J. R. Briegel, R. Boukhliq, and M. R. Sanders
During earlier studies we observed that ewes housed and sampled intensively to measure pulses of LH in plasma had a higher ovulation rate than similar ewes housed outside. In Expt 1, we pursued this observation by testing whether the increase was due to effects of housing or collection of blood samples. Ewes sampled at intervals of 4 h for 2 days before progestagen sponge removal and 2 days after sponge removal, and every 20 min for 12 h the day before sponge removal and every 10 min for 4 h on the day of sponge removal had a higher ovulation rate than ewes that were not sampled (1.72 versus 1.41; P < 0.05). The ovulation rate of the ewes housed indoors but not sampled was similar to that of ewes that remained in the paddock (1.43). In Expt 2, we studied the effects of blood sampling in three groups of 20 ewes sampled every 20 min for different periods of 24 h. Ewes from all three groups were sampled the day before sponge removal (day − 1) and, in addition, one group of ewes was sampled for the previous 48 h (i.e. days −3 to −1) and another group was sampled on day − 8. The frequency of LH pulses was lower (P < 0.05) in ewes sampled for the first time on day − 1 compared with the frequency of LH pulses in groups also sampled earlier in the cycle (day −8 or days −3 and − 2). In ewes sampled on days −3 to −1, the frequency of LH pulses was low for the first 24 h and then increased. Changes in the mean concentration of FSH followed a pattern similar to that of LH pulse frequency. The ovulation rate was increased in ewes sampled on day −8 (P < 0.01) compared with a control group of 40 unsampled ewes. We conclude that collection of blood samples from Merino ewes to measure LH pulses can change the frequency of those pulses and the mean concentration of FSH, and these changes can be accompanied by an altered ovulation rate.
J. J. Robinson, R. P. Aitken, T. Atkinson, J. M. Wallace, and A. S. McNeilly
Twelve anoestrous ewes maintained under natural photoperiod at 57°N received an oral dose of 3 mg melatonin daily at 15:00 h from 1 May. Starting 41 days later and extending from 11 June until 5 September, six of the ewes were also infused continuously with 0.8 mg thyrotrophin-releasing hormone (TRH) day−1 via subcutaneous osmotic minipumps. The remaining six ewes acted as controls. Behavioural oestrus, ovulation rate and luteal function were determined by exposure to a vasectomized ram, laparoscopy and the measurement of progesterone in peripheral plasma, respectively. TRH infusion stimulated a sustained increase (P < 0.001) in plasma concentrations of thyroxine, tri-iodothyronine and prolactin (thyroxine: 158 ± 9.3 and 65 ± 7.7 nmol l−1 for TRH-infused and control ewes, respectively; tri-iodothyronine, 2.6 ± 0.12 and 1.1± 0.19 nmol−1 and prolactin, 57±12 and 11 ± 2 μg l−1). No ewes were in oestrus before the TRH infusion and the mean number of behavioural oestrous cycles per ewe during the infusion period was 1.3 ± 0.33 and 2.5 ± 0.34 for TRH-infused and control ewes, respectively (P < 0.05). Corresponding mean intervals from 1 May to the onset of the first luteal phase (progesterone > 1 ng ml−1) were 88 ± 8.9 and 79 ± 3.5 days (not significant). TRH infusion had no effect on the mean numbers of corpora lutea (1.7 ± 0.14 and 1.6 ± 0.20 for TRH-infused and control ewes, respectively), but was associated with a lower mean incidence of normal luteal phases (1.5 ± 0.43 versus 2.7 ± 0.21, P= 0.052). Abnormalities in luteal function included delayed initial expression, extended ovarian cycles, suprabasal periovulatory progesterone concentrations and protracted periods of low progesterone secretion between successive ovarian cycles. Thus continuous TRH infusion suppressed plasma prolactin, doubled the circulating concentrations of thyroxine and tri-iodothyronine, and was associated with a wide range of abnormalities in ovarian function and endocrine status, the nature of which varied between ewes.