Morphological ontogeny of the gonad of three plectropomid species through sex differentiation and transition

The gonadal ontogeny through sex differentiation and transition of three protogynous coral trout species, Plectropomus leopardus , P. maculatus and P. laevis was described, based on anatomical and germinal differences along the length of the reproductive tract. Gonads of immature and mature females, sex changing individuals (transitionals) and males were examined. Specific anatomical features that were compared between sexual phases included the presence and structure of sperm sinuses, gonadal musculature and germinal cell types. All three coral trout species first differentiated as an immature female. The sexual pattern of P. leopardus and P. maculatus was concluded to be diandric protogynous hermaphroditism (males were derived from the juvenile phase as well as through sex change of mature females). Plectropomus laevis was found to be monandric as males were only derived through sex change in mature females. Structural changes did not occur concomitantly with the germinal changes associated with sex change in these Plectropomus species, which is atypical for protogynous species described to date. Precursory sperm sinuses in the dorso-medial region of the gonad were present, although non-functional, in a proportion of immature and mature females of all three species. These proportions, however, varied between species depending on the sexual pattern. The structural and germinal changes observed were hypothesized as anatomical adaptations that aid in minimizing time spent in the (non-reproductive) sexual transition phase and maximizing flexibility in male development in the diandric species.     

Sexual development and reproductive seasonality of hogfish (Labridae: Lachnolaimus maximus), an hermaphroditic reef fish

The seasonality, size, age, colour phases and sexual dimorphism of 13 reproductive classes of hogfish Lachnolaimus maximus are described. Analysis of histological sections of gonads ( n = 1662) confirmed earlier conclusions that L. maximus is a monandric, protogynous hermaphrodite. Sex change was initiated at the end of the spawning season and over a broad range of sizes and ages. It occurred after a functional female phase (postmaturation) and proceeded more slowly (months) than previously believed. Eventually all individuals changed sex to a terminal male phase. Females were batch spawners, spawning as often as every day during winter and spring. There was no evidence of precocious sperm crypts in active females, sperm competition or other alternative male sexual strategies. Mating has been reported elsewhere to be haremic. The sexual development of L. maximus appears to be adaptive in terms of Ghiselin's size-advantage model, which links monandric protogyny and polygyny. The slow rate of sex change, however, poses problems when fishing pressure is high because harvest of a single male has the potential to reduce the reproductive output of an entire harem.     

Sexual development and sexuality in the Nassau grouper

Hermaphroditic sexual patterns are widespread among teleosts and are especially characteristic of certain perciform families. Among the most diverse groups of hermaphroditic species are the groupers, hamlets and sea basses of the family Serranidae. Like other groupers, the epinepheline serranid, Epinephelus striatus , the Nassau grouper, has long been assumed to exhibit monandric protogyny (a form of hermaphroditism in which all males derive from adult females by sex change). Histological and demographic data, however, indicate that the sexual pattern of this species is not monandric, and that, unlike other group species, the juveniles pass through a bisexual stage of gonadal development. Sexuality in the Nassau grouper is essentially gonochoristic, with potential for sex change. The combination of bisexuality and gonochorism is previously undescribed in the serranids.     

Geographic variability in the gonadal development and sexual ontogeny of Hemigymnus,Cheilinus and Oxycheilinus wrasses among Indo-Pacific coral reefs

Patterns of reproductive ontogeny in four species of coral reef wrasses (F: Labridae) Hemigymnus melapterus, Hemigymnus fasciatus, Cheilinus fasciatus and Oxycheilinus digramma were investigated. Populations of each species were sampled from two island groups of the central Great Barrier Reef (GBR), Australia, and from coral reefs in the central Philippines. These three sampling locations span 30° of latitude. The GBR and Philippine reefs experience biologically significant differences in water temperature, geography and human activity. The studied wrasses are effectively unfished in Australia but heavily fished in the Philippines. Gonad weights, histology and demographic data were obtained across the entire size and age range of H. melapterus, C. fasciatus and O. digramma from all locations. Analysis identified three processes of male recruitment: functional gonochorism and both forms of protogynous hermaphroditism, monandry and diandry. The expression of these distinct sexual ontogenies was locality dependent. Populations of H. melapterus, H. fasciatus, C. fasciatus and O. digramma on the GBR showed consistently uniform patterns of sexual ontogeny, with all species being exclusively monandric. H. melapterus, C. fasciatus and O. digramma in the Philippines displayed complex sexual ontogenies, with all species showing histological evidence of both diandry and functional gonochorism. Reproductive investment in gonadal tissue, and population sex structure, also differed between GBR and Philippine coral reefs. Philippine populations had substantially lower gonado-somatic indices than populations on the GBR. Nonetheless, Philippine populations matured more rapidly and displayed a protracted timing of sex change over a large size and age range. Thus, mature females appeared earlier and persisted later into ontogeny in the Philippines than on GBR reefs. Protracted timing of sex change on Philippine reefs is likely linked to the presence of primary males in the population, which is known to reduce the strength of selection for mature females to undergo sex change and become male. Hypotheses based on social structure of fish populations, environmental factors and evolutionary history were developed to account for the different patterns of sexual ontogeny in the focal wrasses.     

Reproductive life history of the introduced peacock grouper Cephalopholis argus in Hawaii

This research investigated the reproductive biology (sex ratio, hermaphroditic pattern, size and age at maturity) of Cephalopholis argus, known locally in Hawaii by its Tahitian name roi. The results suggest that C. argus exhibits monandric protogyny (female gonad differentiation with female to male sex change) with females reaching sexual maturity at 1.2 years (95% c.i .: 0.6, 1.6) and 20.0 cm total length (L_T; 95% c.i .: 19.6, 21.2). The female to male sex ratio was 3.9:1. The average age and L_T at sex change was 11.5 years (95% c.i .: 11.1, 12.9) and 39.9 cm (95% c.i .: 39.5, 41.2), respectively. Current information on spawning seasonality of this species is incomplete, but based on the occurrence of spawning capable and actively spawning females, spawning probably takes place from May to October. Evidence of lunar spawning periodicity was found, with an increased proportion of spawning capable and actively spawning females, and an increased female gonado‐somatic index during first quarter and full‐moon phases. This information fills a valuable information gap in Hawaii and across the species' native range.     

Reproductive biology and implications for management of the spangled emperor Lethrinus nebulosus in the southern Arabian Gulf

The reproductive biology of the spangled emperor Lethrinus nebulosus in the southern Arabian Gulf was determined from the examination of 781 individuals collected between September 2008 and August 2009. There was no histological evidence of adult sex change, and sex ratios did not differ significantly from unity across all size and age classes. Testes had an ovarian structure and a remnant lumen which was not used for sperm transport; furthermore, residual oocytes were observed in the testes of some immature, resting and developing males. A dramatic change in the sex ratio of the smallest and youngest size and age classes suggested that juvenile female to male sex change occurred between 21·0 cm fork length (L(F)) and 24·0 cm L(F) at 1 year of age. The combination of histological evidence with the sexual composition of the size and age structures suggests a non-functional protogynous hermaphroditic sexual pattern, which is analogous to functional gonochorism. The spawning season was well defined, occurring once a year during March, April and early May. Peaks in spawning occurred after full moons, there was a cessation in spawning activity after new moons and spawning was completed within three lunar cycles. The distribution of males over the entire size and age ranges and the absence of inactive mature females during the spawning season suggested that the population was not constrained by sperm limitation. Size-specific and age-specific reproductive potential indicated that conventional regulations that equate the mean size at first capture to sexual maturation are unsuitable for the management of L. nebulosus. The maximum recorded age (11 years), small mean size and young age at sexual maturation (L(m50) = 26·7 cm L(F), 2·1 years, for females and 19·4 cm L(F), 0·5 years, for males) may be a direct result of intensive demersal fishing in the southern Arabian Gulf.     

Reproductive biology of a large, aggregation-spawning serranid, Epinephelus fuscoguttatus (Forsskål): management implications

The reproductive biology of Great Barrier Reef populations of the long-lived grouper Epinephelus fuscoguttatus (brown-marbled grouper or flowery cod) was investigated using histological analyses. Evidence provided by gonad morphology and age-based demographics suggested monandric protogynous hermaphroditism. Younger age groups contained only immature and mature females, and all males were above the size and age of 100% female maturity, consistent with secondary males derived from mature females by adult sex change. Fishing records confirmed that spawning aggregations of this species and the co-occurring Epinephelus polyphekadion (camouflage grouper) are sometimes targeted on the Great Barrier Reef. Sampling data revealed strong spawning seasonality for E. fuscoguttatus , with a relatively narrow annual spawning period (November to January). The temporal pattern of reproductive activity within the spawning period, based on occurrence of near spawning ovaries (containing hydrated oocytes), indicated spawning events may occur throughout much of the lunar cycle and only partly coincide with seasonal fishing closure periods on the Great Barrier Reef. The results indicate that protection would be enhanced by a longer seasonal closure.     

Reproduction of the inshore coral trout Plectropomus maculates (Perciformes: Serranidae) from the Central Great Barrier Reef, Australia

The reproductive biology of the serranid fish Plectropomus maculatus sampled from inshore waters of the Central Great Barrier Reef was studied based on histological analyses of gonad material. This species was shown to be a monandric protogynous hermaphrodite. The process of sex change foliowed the spawning period observed during September through November. Plectropomus: maculatus showed multiple spawning during this period. Sex change followed the usual protogynous mode with degeneration of ovarian germinal tissue accompanied by proliferation of male germinal tissue in the gonad. The sex structure of the sampled population was analysed based on age and size information. The size and age of first reproduction for females was 30.0cm s. L. and 2 years of age. The size and age of sex-transition was 35.4 cm s. L. and 4.4 years of age. The sex/size and sex/age relationships indicated that sex-change can occur over a broad range of sizes and ages. The sizes and age distributions of males and females P. maculates overlapped over 38% of the length range and over 42% of the maximum age observed.     

Reproductive biology and implications for management of the painted sweetlips Diagramma pictum in the southern Arabian Gulf

The reproductive biology of the painted sweetlips Diagramma pictum was determined from 487 individuals collected between January and December 2010 in the southern Arabian Gulf. There was no evidence of sex change and the combination of histological results with the sex composition of the size and age structures indicated a gonochoristic sexual pattern. There were peaks in gonado-somatic indices for females in March and October with spawning occurring during two seasons (April to May and November). The mean size and age at sexual maturity (L(m50) and A(m50) ) were 35·7 cm fork length (L(F) ) and 2·9 years for females and 26·7 cm L(F) and 0·5 years for males. The maximum recorded age (11 years) and small mean size and young age at sexual maturity for males may be a direct result of intensive demersal fishing in the southern Arabian Gulf. There was an exponential increase in the cumulative reproductive potential with size and a linear increase with age for both sexes. The mean L(F) (L(c50) ) at which D. pictum became vulnerable to capture was 33·3 cm, which corresponded to only 3 and 7% of the cumulative reproductive potential of males and females, respectively. Size-specific and age-specific reproductive potential indicated that conventional regulations that equate the mean size at first capture to sexual maturation are unsuitable for the management of D. pictum.     

Reproductive biology of the Panama graysby Cephalopholis panamensis (Teleostei: Epinephelidae)

The reproductive biology of the Panama graysby Cephalopholis panamensis was studied from collections and behavioural observations made in the Gulf of California from 2001 to 2006. Histological examinations, particularly the identification of gonads undergoing sexual transition, confirmed a protogynous hermaphroditic sexual pattern. The population structure and mating behaviour provided further support for protogyny. Size and age distributions by sex were bimodal, with males larger and older than females and sex ratios biased towards females. Mating groups consisted of a large male and several smaller females, and courtship occurred in pairs during the evening. Results on spawning periodicity and seasonality were incomplete, but histological data, monthly gonado‐somatic indices (I_G) and behavioural observations suggest that adults spawned around the full moon from May to September. Certain aspects of their reproductive biology (e.g. protogyny and low egg production) indicate that C. panamensis is particularly vulnerable to fishing and would benefit from a management policy in Mexico.     

Reproduction in the dusky grouper from the southern Mediterranean

Demographic data and gonad histology confirmed that the dusky grouper Epinephelus marginatus is a protogynous hermaphrodite that follows a monandric pathway to sexual development. Females reached first sexual maturity at 36·7 cm L_s and estimated mean length at first maturity (L₅₀) was 43·8 cm L_s for females and 81·3 cm L_s for males. Adult sex ratios during the reproductive period were c. 3·5: 1 females to males. Females exhibited group-synchronous ovarian development and multiple ovulation occurred over the spawning period. Gonads were ripe from early May and spawning occurred from June until early September. The size of ripe testes (0·6% W )indicated strong oligospermy and suggested a mating system with no sperm competition. Sexual transition was protogynous involving regression of ovarian tissue and proliferation of testicular tissue in the gonads. Transitional individuals occurred from May through November and accounted for 9% of sampled adult population. Sex change occurred in fish 69–93 cm (L_s) long and the size distributions of males and females overlapped over 27% of the L_s range. Special zones were recognized as gathering areas for sexually mature dusky groupers during the reproductive period.     

Juvenile bisexuality in the red sea bream,Pagrus major

The histology of the gonad of the red sea bream,Pagrus major, was examined in order to study the early gonadal development, sexual maturation and sex ratio in a natural population. A total of 1,117 fish between the ages of 4 months and 8 years were examined. Gonads of 4-month-old fish were either sexually undifferentiated with a central cavity, or ovarian in form. Gonads of 12- and 18-month-old fish were ovaries or bisexual gonads, while those of 2-year-old fish were ovaries, bisexual gonads or testes. Fish aged between 3 and 8 years had ovaries or testes, except for a few bisexual gonads found in 3- and 4-year-old fish. The chronological appearance of females, hermaphrodites and males in that order, and histological evidence, suggested that the testis originates from the ovary via a bisexual gonad in the juvenile stage. The sex ratio of females to males at the age of 2 years and over was about 1:1, suggesting that hermaphroditic red sea bream appear in about 50% of the juvenile population. The sexual pattern in this species, therefore, is concluded to be gonochorism with a bisexual juvenile stage.     

Gonadal development and diandric protogyny in two populations of Dascyllus reticulatus from Madang, Papua New Guinea

Two Dascyllus reticulatus populations from Madang, Papua New Guinea exhibited diandric protogyny. In both populations, gonads began as undifferentiated, and then developed oocytes in the primary growth stage and an ovarian lumen. From this ovarian state or from more developed ovaries containing oocytes beyond the primary‐growth stage, some gonads developed into testes. The first sign of testicular development was degeneration of oocytes, degeneration of oocytes in the primary growth stage in ovarian gonads and degeneration of oocytes of all growth stages present including the primary growth stage in ovaries, which was then followed by development of spermatogenic tissue. In both populations, most of the fish that had gonads with degenerating oocytes were smaller than the smallest mature females, indicating that development towards testes was mostly initiated in immature gonads containing only pre‐vitellogenic oocytes. On some occasions, however, females as large as other mature females also had gonads with degenerating oocytes, suggesting that development towards testes may have occurred in mature ovaries as well. This latter notion is further strengthened by the discovery of a fish having a gonad that contained both degenerating vitellogenic oocytes and developing spermatogenic tissue. Taken together, these results suggest that D. reticulatus can exhibit diandric protogyny, because testes in D. reticulatus developed from juvenile gonads as well as from mature ovaries.     

雅鲁藏布江黑斑原鮡繁殖生物学研究

对2004-2006年采集于雅鲁藏布江拉萨河的190尾黑斑原鮡进行了繁殖生物学研究。雄性最小性成熟(精巢Ⅳ期)个体体长141.7mm,体重45.2g,性体指数1.09%,雌性最小性成熟(卵巢Ⅳ期)个体体长146.8mm,体重66.7g性体指数11.52%,相应年龄均为5龄。初次性成熟年龄(L50):♂,170.1mm相应年龄为7龄;♀,150.2mm,相应年龄5龄。通过组织切片法和GSI的周年变化分析,繁殖时间集中在5-6月,每年繁殖一次,繁殖之后的6-8月卵巢从Ⅵ期回复到Ⅲ期,9月卵巢发育到Ⅳ期越冬。卵径频率分布显示,卵巢发育类型为分批同步型,卵巢中至少存在2批卵径,每年成熟一批卵并同时产出,产卵类型为完全同步产卵。卵黏性,成熟卵卵径在2.04-3.37mm之间,平均(2.83±0.16)mm。对19尾产卵前夕(体长为151.0-210.0mm)的标本进行统计,其绝对繁殖力范围在525-2058粒之间,平均为(1244±346)粒,相对繁殖力为(14.7±5.8)粒/g。绝对繁殖力与体长呈直线正相关,表达式为F=13.624L-1187。       

Reproductive aspects of the yellowtail snapper Ocyurus chrysurus from the southern Gulf of Mexico

In this study, sex ratio, spawning season, fork length (L(F)) at maturity (L(F50)), batch fecundity and spawning frequency were characterized for the continental population of Ocyurus chrysurus from the Campeche Bank, in the southern Gulf of Mexico. A total of 1657 specimens were collected from February 2008 to January 2009. The overall sex ratio (male:female) and sex ratios by size-class showed no significant differences from an expected 1:1 ratio. The Campeche Bank population did not conform to the reproductive seasonality pattern characteristic of a continental population. A protracted spawning season that extended from January to September with peaks occurring mainly between April and May and additionally in September was observed. The population conformed, however, to the sexual maturity pattern observed for populations and species associated with a continental margin. Fish of both sexes reached the onset of sexual maturity at a similar and small L(F) of c. 14 cm, and L(F50) (L(F) at which 50% of females and males become mature) was 21·3 and 19·4 cm. Asynchronous-type ovarian development was observed for this species and batch fecundity estimates ranged from 14,102 to 164,756 oocytes (mean ±S.D. = 43,852 ± 32,684 oocytes). The overall spawning frequency estimate was once every 8·3 days or 26 times during the 9 month spawning season.     

Reproductive traits of the freshwater oyster Etheria elliptica (Bivalvia: Etheriidae) in the Pendjari River,Benin: implications for conservation

The African freshwater oyster Etheria elliptica, which is of great economic importance throughout the continent, is facing overharvesting in many fisheries in West Africa. Its reproductive traits (sex ratio, size at sexual maturity, oocyte diameter and fecundity) were studied at four stations located along the Pendjari River, northern Benin, in April 2013. Histological techniques were implemented to identify sex and gonad development stages. Oocyte sizes were measured based on the histological images and mean oocyte diameter was 38 µm. Fecundity, estimated by counting the developing eggs, averaged 106 724 eggs and increased significantly with shell size. The average sex ratio was approximately 1:1. Hermaphrodites were rare. Males reached sexual maturity at 57.6 mm dorsoventral height, earlier than females at 64.7 mm. The majority of the oyster specimens were in ripe-spawning stages, indicating that reproductive activities partly took place towards the end of the dry season. Both mature and immature individuals were subjected to harvesting at all the investigated fishing sites. The mean size of exploited oysters was 60.6 mm, lower than the size of females at maturity. Management strategies must enforce the minimum size of 65 mm required for harvesting, particularly in open access sites where juveniles are mostly harvested.     

A field experiment on the effects of interspecific competition from roach, Rutilus rutilus (L.), on age at maturity and gonad size in perch, Percafluviatilis L.

The effects of interspecific competition from roach on gonad development in O+ and 1+ perch were studied in a pond experiment by varying the roach density between treatments. The proportion of mature O+ males first increased and, thereafter, decreased with increasing roach density and increasing somatic weight. O f females were immature and all I+ males were mature. The proportion of mature 1+ females decreased with increasing roach density and decreasing somatic weight. The gonad weight of O+ and 1+ males as well as 1+ females decreased with increasing roach density and decreasing somatic weight. For 1+ males, which were individually marked, both start weight as well as somatic end weight were positively related to gonad weight. One possibleexplanation for the hump shaped relationship between the proportion of mature O+ males and somatic weight is that behavioural interactions between O+ and I+ males in the absence of roach affected maturing in O+ males. This study supports previous suggestions that annual variation in resource availability may give rise to variance in fecundity-body size relationships.     

Sex-specific apoptosis regulates sexual dimorphism in the Drosophila embryonic gonad

Sexually dimorphic development of the gonad is essential for germ cell development and sexual reproduction. We have found that the Drosophila embryonic gonad is already sexually dimorphic at the time of initial gonad formation. Male-specific somatic gonadal precursors (msSGPs) contribute only to the testis and express a Drosophila homolog of Sox9 (Sox100B), a gene essential for testis formation in humans. The msSGPs are specified in both males and females, but are only recruited into the developing testis. In females, these cells are eliminated via programmed cell death dependent on the sex determination regulatory gene doublesex. Our work furthers the hypotheses that a conserved pathway controls gonad sexual dimorphism in diverse species and that sex-specific cell recruitment and programmed cell death are common mechanisms for creating sexual dimorphism.     

Maturation and sexual ontogeny in the spangled emperor Lethrinus nebulosus

The reproductive development and sexual ontogeny of spangled emperor Lethrinus nebulosus populations in the Ningaloo Marine Park (NMP) were investigated to obtain an improved understanding of its evolved reproductive strategy and data for fisheries management. Evidence derived from (1) analyses of histological data and sampled sex ratios with size and age, (2) the identification of residual previtellogenic oocytes in immature and mature testes sampled during the spawning season and (3) observed changes in testis internal structure with increasing fish size and age, demonstrated a non‐functional protogynous hermaphroditic strategy (or functional gonochorism). All the smallest and youngest fish sampled were female until they either changed sex to male at a mean 277·5 mm total length (L_T) and 2·3 years old or remained female and matured at a larger mean L_T (392·1 mm) and older age (3·5 years). Gonad masses were similar for males and females over the size range sampled and throughout long reproductive lives (up to a maximum estimated age of c. 31 years), which was another correlate of functional gonochorism. That the mean L_T at sex change and female maturity were below the current minimum legal size (MLS) limit (410 mm) demonstrated that the current MLS limit is effective for preventing recreational fishers in the NMP retaining at least half of the juvenile males and females in their landed catches.     

Rapid larval growth predisposes sex change and sexual size dimorphism in a protogynous hermaphrodite, Parapercis snyderi Jordan & Starks 1905

The temporal relationship between growth history, sex-specific growth divergence and sex change was investigated in the haremic sandperch Parapercis snyderi using otolith microstructure and gonad histology. Parapercis synderi was found to display rapid near-linear growth with a maximum longevity of 303 days. All individuals matured first as female and later changed sex to become male (monandric protogynous hermaphroditism). Individual age-based growth histories obtained from otolith increment widths illustrated that males were larger than females at any given age. Males were found to diverge from the female growth trajectory during two ontogenetic periods; during the larval period and during the period that sex change took place. In addition, male otoliths contained a discontinuity, or 'check mark', associated with the rapid increase in otolith growth during the sex-change period. This microstructural feature was absent from all female otoliths. Accelerated growth in male otoliths lasted up to 25 days, following check-mark formation, after which time otolith growth returned to the pre-check-mark rate. Given the isometric relationship between otolith and somatic growth in P. synderi , and the temporal relationship between the time of check-mark formation and gonad condition, these results strongly suggest that individuals accelerate somatic growth during sex change to become the largest members of the population. Moreover, evidence suggests that the factors that determine the initial growth of larvae influence which individuals will later become males and achieve the highest reproductive success.