Numbers of follicles and oocytes in mammalian ovaries and their allometric relationships

The numbers of ovarian follicles present in the reserve pool of non-growing ('primordial') stages at the commencement of adult life in 19 species varied allometrically with both body weight ( M , in kg) and with maximum life expectation (L, in years), the mathematical expressions being 27700 M ^0.47 and 820 M ^1.58, respectively. These allometric relationships, which could not be accounted for by differences in reproductive behaviour patterns or ovulation rates, indicate that species differences in the size of the follicular store, perhaps accompanied by more parsimonious utilization, could be a life strategy which guarantees fecundity throughout most of the lifespan. The number of follicles in humans at menarcheal age is commensurate with body size, and follicular deficiency at menopause in mid-life may have therefore arisen adventitiously with lifespan extension.     

Can birds count eggs in their nests?

Sensory mechanisms controlling avian clutch size have diversified into distinct types, according to the nature of the input that is used to disrupt the growth of ovarian follicles and hence halt egg‐laying. In an article on brood parasitism, Lyon (2003) claimed that female American Coots Fulica americana can reduce their clutch size on the basis of visual cues in response to eggs laid in their nests by other females; in this species, therefore, egg counting would be used to control clutch size. After a close examination of the physiological determination of clutch size in American Coots, I show that seven of 17 parasitized clutches were smaller than the range controlled through the mechanism using an input to disrupt follicular growth (7–10 eggs per clutch). My reanalysis suggests that American Coots are incapable of adjusting clutch size via counting and re‐asserts that a species that can count eggs has yet to be found among birds that rely upon their own body heat for incubation.     

Ultrasound imaging of reproductive organs and eggs in Galapagos tortoises,Geochelone elephantopus spp

This study demonstrates the efficacy of using ultrasound to determine the presence of ovarian developing, preovulatory, and atretic follicular structures and oviductal eggs in the Galapagos tortoise, Geochelone elephantopus spp. Ultrasound was effective in locating both right and left ovarian structures in 92% (n = 100 ovaries) of the trials. Developing and preovulatory follicles and oviductal eggs were echogenically visualized and had measurements ranging from 18 to 44 mm (n = 93) and 55 to 68 mm (n = 9), respectively. Atretic follicles ranged in size from 10 to 38 mm (n = 10). In one trial with four G. elephantopus, ultrasound observations were validated with the use of laparoscopy. All procedures were accomplished without general anesthesia on a specifically designed restraining table. Ultrasound provides an effective, safe modality for determining the reproductive status of adult female tortoises.     

Reproductive biology of Philodryas patagoniensis (Snakes: Dipsadidae) in south Brazil: Female reproductive cycle

In this study, we describe the female reproductive cycle of Philodryas patagoniensis in south Brazil, which was described through morpho‐anatomical and histological analyses. The peak of secondary vitellogenesis occurred during winter–spring (July–December), ovulation in spring (October–December), mating and fertilization in spring–summer (October–February), oviposition in spring–autumn (October–May) and births from late spring to autumn (December–July). The diameter of vitellogenic follicles/eggs was larger in winter–spring than in other seasons. The diameter of the shell glands was also larger in winter–spring. In spite of the clear reproductive peak, gonads only showed reduced activity in the autumn. Therefore, at the individual level, females have a discontinuous cyclical reproduction; in the populational level, the reproductive cycle is seasonal semisynchronous. We support the hypothesis that P. patagoniensis have the ability to produce multiple clutches with long‐term stored sperm. Sexual dimorphism in body size was evident, and females are significantly larger and heavier than males. Larger females were able to produce follicles and eggs in larger amount and size. The maternal body size was positively related to the reproductive effort and fecundity. To conclude, we deliberated about the proximal and distal causes that influence the reproductive traits and patterns of P. patagoniensis.     

Observations on the female reproductive cycles of captive Asian yellow pond turtles (Mauremys mutica) with radiography and ultrasonography

The annual reproductive cycle of 27 female Mauremys mutica was observed by radiography and ultrasonography from April 2006 to August 2007. Radiography was used to monitor clutch size and ultrasonography was used to monitor changes in the ovarian follicles. The follicles started to enlarge in September and became preovulatory in January. The mean maximum follicle diameter of ovulation was 18.30±1.44 mm, and ovulation occurred from March through August. Eggs were laid between April and August. Turtles entered latent period in early August and the maximum follicular size was at a low of 13.22±2.36 mm in late September. The vitellogenesis of the next reproductive cycle began in October. The 24 adult females laid 56 clutches containing a total of 227 eggs. Average clutch size was 4.05 eggs (range 1–8) and there were 2.33 clutches (range 1–4) per female. Egg shell images were first observed on the sixth or seventh day after ovulation. The oviductal period averaged 6.9 weeks (range 2–16 weeks) on the first clutch, 3.4 weeks (range 2–8 weeks) on the second, and 2.75 weeks (range 2–6 weeks) for the third. Radiography and ultrasonography are non‐invasive and convenient methods to evaluate the reproductive cycle of female M. mutica. They should be applicable to other turtles and should greatly enhance knowledge of reproductive physiology. Zoo Biol 29:50–58, 2010. © 2009 Wiley‐Liss, Inc.     

A comparison of energy substrates and reproductive patterns of two anurans. Acris crepitans and Bufo woodhousei

The seasonal pattern of carcass, liver and ovary lipid and liver non-lipid mass was examined in the cricket frog, Acris crepitans, and Woodhouse's toad, Bufo woodhousei. Reproductive patterns were also studied. The over-winter reduction of body lipid and liver non-lipid material was attributed to metabolism in Acris crepitans. Male, but not female, Bufo woodhousei exhibited seasonal variation in lipid stores that was attributable to metabolism. Females, but not males, showed seasonal variation in liver non-lipid mass and quantified liver glycogen. Females of both species mobilized body lipid during the period of ovarian development; however, an inverse relationship between fatbody mass and ovary mass was evident for Acris, only. Female Acris crepitans depleted all ovarian follicles prior to brumation; however, Bufo woodhousei retained enlarged follicles throughout the year. Variation in metabolic substrate use between species was related to the differences in reproductive patterns exhibited by the two anurans. These variations in reproductive strategy represent adaptations that enhance the survivability of different species in dissimilar habitats.     

Ultrasonography of the female reproductive organs in farmed ostriches (Struthio camelus spp.)

The main objective of this study was to determine whether transcutaneous ultrasonography could be used as a diagnostic tool to monitor the reproductive organs of female breeding ostriches. An additional aim was to investigate whether the use of this technique could facilitate prediction of the start or end of the egg production season. A technique for on-farm ultrasound scanning is described and examples of ultrasonographic images of different ovarian structures, developing ova and eggs within the genital tract are presented. These data were obtained by scanning mature female breeding ostriches (n=8). In vivo scanning took place a day prior to slaughter, and immediately after slaughter the reproductive organs were scanned in vitro in a water bath. By comparing ultrasonographic images with post mortem ovarian morphology, it appeared that the following morphological structures can be identified using ultrasonography: ovarian follicles of different sizes (diameter (phi) 1-9 cm), atretic follicles, post-ovulatory follicles (POFs), ova at different stages of development and eggs within the genital tract. Of the number of follicles counted during post mortem investigation, 58% (95% confidence interval 0.41-0.79) had been detected during previous in vivo examination. In the second part of our study, ultrasonographic scans were made at weekly intervals in two farmed female ostriches (n=2) during the breeding season in order to determine the predictive value of the technique. By comparing the images of ovarian activity with individual egg production of these hens, preliminary evidence was obtained that scanning might be of value in predicting egg production, especially at the start and the end of the breeding season. It is concluded that transcutaneous ultrasound scanning in mature female breeding ostriches is an easy, noninvasive technique for the monitoring of ovarian (in)activity, for visualization of different functional ovarian structures, for following the development of individual ova and for visualization of an egg with calciferous shell within the oviduct, and that this technique will be a valuable tool in future research on reproductive physiology and pathology, and the development of more advanced reproductive technologies, such as artificial insemination.     

A phylogenetic analysis of egg size,clutch size,spawning mode,adult body size,and latitude in reef fishes

Theoretical treatments of egg size in fishes suggest that constraints on reproductive output should create trade-offs between the size and number of eggs produced per spawn. For marine reef fishes, the observation of distinct reproductive care strategies (demersal guarding, egg scattering, and pelagic spawning) has additionally prompted speculation that these strategies reflect alternative fitness optima with selection on egg size differing by reproductive mode and perhaps latitude. Here, we aggregate data from 278 reef fish species and test whether clutch size, reproductive care, adult body size, and latitudinal bands (i.e., tropical, subtropical, and temperate) predict egg size, using a statistically unified framework that accounts for phylogenetic correlations among traits. We find no inverse relationship between species egg size and clutch size, but rather that egg size differs by reproductive mode (mean volume for demersal eggs = 1.22 mm³, scattered eggs = 0.18 mm³, pelagic eggs = 0.52 mm³) and that clutch size is strongly correlated with adult body size. Larger eggs were found in temperate species compared with tropical species in both demersal guarders and pelagic spawners, but this difference was not strong when accounting for phylogenetic correlations, suggesting that differences in species composition underlies regional differences in egg size. In summary, demersal guarders are generally small fishes with small clutch sizes that produce large eggs. Pelagic spawners and egg scatterers are variable in adult and clutch size. Although pelagic spawned eggs are variable in size, those of scatterers are consistently small.     

Female freshwater crayfish adjust egg and clutch size in relation to multiple male traits

Females may invest more in reproduction if they acquire mates of high phenotypic quality, because offspring sired by preferred partners may be fitter than offspring sired by non-preferred ones. In this study, we tested the differential maternal allocation hypothesis in the freshwater crayfish, Austropotamobius italicus, by means of a pairing experiment aimed at evaluating the effects of specific male traits (body size, chelae size and chelae asymmetry) on female primary reproductive effort. Our results showed that females laid larger but fewer eggs for relatively small-sized, large-clawed males, and smaller but more numerous eggs for relatively large-sized, small-clawed males. Chelae asymmetry had no effects on female reproductive investment. While the ultimate consequences of this pattern of female allocation remain unclear, females were nevertheless able to adjust their primary reproductive effort in relation to mate characteristics in a species where inter-male competition and sexual coercion may mask or obscure their sexual preferences. In addition, our results suggest that female allocation may differentially affect male characters, thus promoting a trade-off between the expression of different male traits.     

Gross morphology of ovarian changes during the reproductive cycle of Indian lizards (Calotes versicolor and Hemidactylus flaviviridis).

A comparative study has been made of the reproductive cycle and gross ovarian changes in two species of Indian lizards (Calotes versicolor and Hemidactylus flaviviridis), which are oviparous. They exhibit a single, short breeding season that extends over a few months. Calotes ovalutes 10 to 32 eggs per clutch (the highest number recorded so far for lizards belonging to the family Agamidae) from last week of June to the first week of September, with July through August being the months of highest reproductive potential when monsoon occurs. From October to May, there occur reduced ovaries containing small previtellogenic follicles which begin to increase in size with the approach of June when heavy yolk deposition occurs. Hemidactylus ovulates from mid-March to mid-May, with a peak in April when there occurs an appreciable increase in day length and temperature. It usually ovulates two eggs per clutch (one from each ovary). From June to the 3rd week of February, the ovaries remain small whitish bodies, each containing 3 or 4 small previtellogenic follicles of variable size which, with the approach of March, begin to increase in size by accumulating yolk. Various indirect evidences suggest that both the lizards lay more than one clutch of eggs during the breeding season.     

蓝尾石龙子杭州和宁德种群繁殖生活史特征的差异

测定处于不同纬度的浙江杭州和福建宁德的蓝尾石龙子(Eumeceselegans)种群的个体大小和繁殖特征。宁德种群的产卵时间为5月27日—6月22日,早于高纬度杭州种群(6月4日—7月12日)。宁德种群最小繁殖雌体及性成熟个体大小均显著小于杭州种群。宁德和杭州两种群的相对窝卵重无显著差异;当统计去除母体体长的影响之后,两地种群的窝卵数和窝卵重也无显著差异,但杭州种群的卵重量显著大于宁德种群。蓝尾石龙子窝卵数和卵重量呈负相关,窝卵数和卵大小的权衡存在种群间差异。特定窝卵数条件下,杭州种群的卵重量显著大于宁德种群。由此可见,蓝尾石龙子种群间的繁殖生活史特征存在显著差异,而且与母体大小的差异密切相关。推测不同纬度地区的蓝尾石龙子种群的繁殖策略存在差异。     

Reproductive allocation and reproductive ecology of seven species of Diptera

1. Variation in resource allocation to egg size and number was investigated in seven sympatric species of Piophilidae that oviposit on carcasses or discarded cervid antlers: Liopiophila varipes (Meigen), Prochyliza xanthostoma Walker, Protopiophila latipes (Meigen), Protopiophila litigata Bonduriansky, Stearibia nigriceps (Meigen), and two unidentified species of Parapiophila McAlpine. 2. Following optimal reproductive allocation theory, relatively larger, fewer eggs were expected in (1) species that oviposit on antlers, where larvae probably experience lower risk of predation and greater competition than larvae in carcasses, and (2) species with aggressive males and male-biased sex ratios on the oviposition substrate, where risk of injury during oviposition may have favoured females laying fewer eggs. 3. Variation in reproductive allocation strategies could not be explained by known differences in larval or adult environment, but congeneric species clustered by reproductive allocation patterns. The Parapiophila species produced larger, fewer eggs than the other species, and egg number increased slowly with body size. The Protopiophila species did not deviate from expected egg sizes and numbers, and egg number increased steeply with body size. 4. An interspecific egg size–egg number trade-off resulted in a tight linear scaling of ovary volume to body size, suggesting common physiological constraints on relative ovary mass. 5. Within each species, egg size was nearly constant whereas egg number increased with female body size, suggesting species-specific stabilising selection on egg size.     

Ovarian activity and reproduction in the frog, Rana esculenta

Rana esculenta specimens were collected, during the last 13 years, in well-defined areas around Naples. The annual ovarian cycle shows distinct phases of recrudescence (starting September; vitellogenesis), breeding (late March-early July; egg deposition and active oogenesis) and quiescence (July-August; no follicular growth). Previtellogenic follicles are recruited for vitellogenesis in early September and in between two successive ovulatory waves. Breeding congregations are generally formed after a heavy rain fall and eggs are laid in standing waters, temporary or permanent. A maximum of three clutches of eggs is produced during the breeding season, at roughly monthly intervals. All mature females reproduce to some extent. Ovarian weight and clutch size are positively correlated to body weight. Depending upon the body size, the potential clutch size ranges from 1000 to 3500 eggs during the first wave of ovulation and it is notably smaller in the successive wave(s) of ovulation. Egg masses and tadpoles are left unprotected and mortality is high. The life cycle from the fertilized egg to completion of metamorphosis is 2 months and oogenesis in the ovary starts in the larva before the onset of metamorphic climax. Young females hatching from the first clutch of eggs may reach sexual maturity and breed in May the following year; those hatching from the last clutch require nearly 20 months to reach sexual maturity. The importance of some endocrine and exocrine factors for the regulation of ovarian activity and reproduction is discussed.     

Reproductive strategies and body shape in the European pond turtle (Emys orbicularis) from contrasting habitats in Italy

Comparisons within and among populations offer important insights into variation in life-history traits and possible adaptive patterns to environmental conditions. We present the results of observed differences in body size, body shape and patterns of reproduction in four separate populations of the European pond turtle Emys orbicularis in central and southern Italy – coastal ( n =3) and mountainous ( n =1) sites and pond ( n =2) and canal ( n= 2) habitats – to determine whether phenotypic plasticity affects reproductive output. Although we did not find any significant latitudinal variation in body size, we observed significant differences in body shape between canal (rounded body shape) and pond (elongated body shape) systems and smaller size with rounded shape in the mountainous population. Reproductive output is similar among populations (median=5 eggs per clutch), whereas reproductive investment (relative clutch mass to maternal body mass) is higher in the mountain population (one clutch per year) than in coastal populations (two clutches per year), suggesting differential trade-offs between geographic locality, elevation and habitat type. Turtle shell shape and geographic location together affect reproductive output in E. orbicularis in Italy.     

Scaling of follicular sizes in mammalian ovaries

The scaling of ovarian follicle and oocyte sizes according to body weight ( M , ranging from 0005–500 kg) has been analysed using data obtained from 22 mammalian species in nine orders. The diameters of non-growing (primordial) follicles were correlated significantly with body weight, the relationship being described by the allometric formula y = 0028 M ^0.10. The mean size at which growing follicles began to accumulate extracellular fluid was approximately the same in all species, 0–3 mm diameter. Graafian follicle sizes varied allometrically with body weight as a result of differences in the volumes of follicular fluid rather than those of oocytes, which were relatively similar in eutherian mammals. The statistical significance of the correlation between Graafian and body sizes was increased when the dimensions for an ovulatory quota of follicles were combined because follicles in polyovulating species were disproportionately small. The total Graafian surface areas and volumes were then predicted from body weight by 58–4 M ^0.65 and 18–5 M ^1.06, respectively. Follicular dimensions in the three species of primates were significantly greater than predicted by the allometric relationship. The exponents of these relationships show that the total volume of a set of preovulatory follicles varies approximately isometrically with body weight and, therefore, with the presumptive hormone distribution volume ( M ^1.0). The hypoallometric relationship of follicular surface area demonstrates that, during the course of the evolution of body size, the surface area for secretion has not increased to match the dilution of hormones in the body pool.     

Covariation between clutch size, egg weight and egg shape: comparative evidence for chelonians

The variation in reproductive variables is documented both within and across species of chelonians. At both the generic and family levels, egg weight and clutch size show positive, significant correlations with adult carapace length. There is a negative correlation across both genera and families between clutch size and egg weight after removing the effects of body size, suggesting an evolutionary trade-off between these two life-history characteristics. However, the trade-off is not complete, since clutch size is positively correlated with clutch weight after removing the effects of body size. Terrestrial species lay fewer and larger eggs for their size than freshwater or marine species, but this association is statistically confounded by the fact that chelonian families form ecological groups. There is no significant association between habitat and clutch weight after removing the effects of body size, nor between latitude and either egg weight or clutch size, but temperate species have a heavier clutch weight after removing the effects of body size. Larger species lay eggs that are more spherical, but after controlling for body size, egg shape is not associated with clutch size. The patterns of covariation between adult weight, egg weight and clutch size contrast with those reported for birds and mammals, and some reasons for these differences are discussed.     

Identification and tissue-specific distribution of sulfated glycosaminoglycans in the blood-sucking bug Rhodnius prolixus (Linnaeus)

We have previously characterized heparan sulfate (HS) as the major ovarian sulfated glycosaminoglycan (GAG) in females of Rhodnius prolixus, while chondroitin sulfate (CS) was the minor component. Using histochemical procedures we found that GAGs were concentrated in the ovarian tissue but not found inside the oocytes. Here, we extend our initial observations of GAG expression in R. prolixus by characterizing these molecules in other organs: the fat body, intestinal tract, and the reproductive tracts. Only HS and CS were found in the three organs analyzed, however CS was the major GAG species in these tissues. We also determined the compartmental distribution of GAGs in these organs by histochemical analysis using 1,9-dimethylmethylene blue, and evaluated the specific distribution of CS within both male and female reproductive tracts by immunohistochemistry using an anti-CS antibody. We also determined the GAG composition in eggs at days 0 and 6 of embryonic development. Only HS and CS were found in eggs at day 6, while no sulfated GAGs were detected at day 0. Our results demonstrate that HS and CS are the only sulfated GAG species expressed in the fat body and in the intestinal and reproductive tracts of Rhodnius male and female adults. Both sulfated GAGs were also identified in Rhodnius embryos. Altogether, these results show no qualitative differences in the sulfated GAG composition regarding tissue-specific or development-specific distribution.     

Plasma estradiol, testosterone, and progesterone levels during the ovulatory cycle of the skate (Raja erinacea)

Amounts of estradiol, testosterone, and progesterone in plasma were measured during the reproductive cycle of female Raja erinacea. Estradiol titers correlated directly with follicle size in females undergoing ovarian recrudescence, while highest concentrations were found in females with preovulatory follicles. These data indicate that as follicles grow, their steroidogenic capacity increases. In mature, nonspawning females, titers of estradiol and testosterone varied markedly. Progesterone was not detected in peripheral plasma of skates that did not produce eggs during the observation period. In females producing eggs, estradiol and testosterone predominated during the follicular phase of each spawning cycle. While estradiol and testosterone were elevated, progesterone was not detectable in the peripheral circulation. As ovulation and formation of capsules approached, plasma estradiol and testosterone declined to near baseline levels. Circulating progesterone rose sharply two days before encapsulation of ovulated eggs and remained elevated for only two days. On the day of encapsulation, concentrations of plasma progesterone had fallen to nearly baseline levels. Progesterone titers remained low throughout egg retention and oviposition. These measurements demonstrate that progesterone titers are elevated at specific times during the reproductive cycle of the skate and clearly suggest that progesterone is critically involved in events occurring at ovulation, encapsulation, and possibly oviposition.     

Reproductive variation and adult size in two co-occurring grasshopper species

ABSTRACT. 1. Egg sizes and clutch sizes of the grasshoppers Chorthippus brunneus (Thunb.) and Myrmeleotettix maculatus (Thunb.) were compared among three years and among three sites less than 1.3 km apart. Relationships between these reproductive traits and date of egg laying, body size and body condition were sought.
2. M.maculatus , the smaller species, laid fewer but larger eggs; and only the eggs of this species showed significant differences between sites and years.
3. A negative correlation between egg size and number per clutch was evident between species and years, but generally not among sites and among individuals of a population.
4. However, a hidden negative correlation between egg size and number was uncovered within populations when the relationship was examined for females of a given mature weight.
5. Variation in the number of eggs per clutch was explained statistically by a positive relationship between female body weight and egg number. Also, both interpopulation and intrapopulation comparisons revealed that for M.maculatus , but not for C.brunneus , females with long hind femurs laid large eggs.     

Ovarian cycle and egg production of the western swamp tortoise Pseudemydura umbrina (Testudines: Chelidae) in the wild and in captivity

The reproductive organs of logn-term captive females and of wild females of the western swamp tortoise, Pseudemydura umbrina , which were taken temporarily into captivity, were studied over several years by ultra-sound scanning. Pseudemydura umbrina , a critically-endangered species, is active during winter and spring when the ephemeral swamps it inhabits contain water and aestivates during summer and autumn (November to May/June) when the swamps are dry. The vitellogenic growth of ovarian follicles commences during aestivation in summer and continues during autumn and winter. The timing of the vitellogenic cycle is remarkably similar to that of many other Australian chelids and that of many other chelonians of temperate and subtropical regions, but the patterns of energy harvest, storage and allocation to ovarian follicles is different. Ovulation occurs between late September and early November and is preceded by a feeding bout and a sharp increase in female body mass. One clutch of 3–5 eggs (exceptionally of one or two) is laid in November/December. Sub-adult females show cycles of follicular growth, followed by atresia, for several years before ovulating and laying eggs. Females taken into captivity may miss the following vitelogenic cycle, but captivity does not generally affect vitellogenic cycles. Ovulation and egg production of captive animals is easily suppressed, however, under stress or sub-optimal food intake in spring. The sensitivity of ovulation to sub-optimal conditions and the subsequent reabsorption of the yolk material may enhance survival of the reproducing individual during long dry periods in an unpredictable environment.