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.     

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 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 of an odacine labrid, Odax pullus

The sexual ontogeny of butterfish Odax pullus was examined in the Hauraki Gulf of New Zealand through histological analysis of gonad material, size and age information and seasonal patterns of sexual maturation. The patterns of gonad development and schedules of male recruitment were established and sexual ontogeny of O. pullus was diagnosed as monandric protogyny, with all males developing from mature females after female-to-male sex reversal. All individuals underwent an immature female phase before maturing as functional females at 228·7-264·8 mm fork length (L(F) ) and at 1·1-1·5 years of age, and there was no evidence of a juvenile bisexual phase. Degenerating mature oogenic elements were found in the gonad lumen of individuals with developing spermatogenic tissue, providing histological evidence for functional protogyny. Sex change was estimated to occur at 359-379 mm L(F) and 2-3 years of age. The diagnosis of monandric protogyny for O. pullus coincided with the pattern of sexual ontogeny seen in the majority of labrids, particularly those of the same clade (tribe Hypsigenyini) and contrasted with that seen in a number of other temperate labrids. This study suggests that the protogynous mode of sexual development in O. pullus is likely to be lineage-specific, i.e. associated with the phylogeny of labrid sexual development, and is not constrained by environmental effects on the evolution of sex change in temperate regions.     

Reproductive cycle and sex inversion in razor fish, a protogynous labrid in the southern Mediterranean Sea

The reproductive biology of the Mediterranean razor fish Xyrichthys novacula was investigated by demographic data and histological analysis of the female, intersexual and male gonads. Specimens were collected by bottom trawl on a monthly basis between June 2000 and July 2001 in a sandy bay in southern Thyrrenian. Gonad histology confirmed that the Mediterranean razor fish is a monandric, protogynous hermaphrodite. Females reached first sexual maturity at 100 mm ( L _T) and the estimated mean L _T at first maturity ( L ₅₀) was 125 mm. Females exhibited asynchronous ovarian development and multiple ovulations occurred over the spawning period. Vitellogenesis started in early May and spawning occurred from late May until late September. Sexual transition involved a large‐scale atresia of all oocyte stages and a massive degeneration of ovarian tissue followed by primordial germ cells proliferation. Sex change began at spawning time (June) but transitional individuals tended to cluster at the end of the reproductive period (September). They accounted for 17·1% of the population sampled and were found in a broad size range (105–150 mm L _T).     

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.     

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.     

Sex-specific spawning behavior and its consequences in an external fertilizer

Identifying the target of sexual selection in externally fertilizing taxa has been problematic because species in these taxa often lack sexual dimorphism. However, these species often show sex differences in spawning behavior; males spawn before females. I investigated the consequences of spawning order and time intervals between male and female spawning in two field experiments. The first involved releasing one female sea urchin's eggs and one or two males' sperm in discrete puffs from syringes; the second involved inducing males to spawn at different intervals in situ within a population of spawning females. In both, fertilization success was measured as the fraction of eggs fertilized and the paternity share of each male. The results indicate that spawning after females imposes a cost on males but only during sperm competition. Further, the optimal interval between the initiations of male and female spawning depends on degree of sperm competition, distance between males and females, and water velocity. The results show that sex differences in spawning timing of marine invertebrates can be explained on the basis of the differential costs and benefits of spawning out of synchrony with the other sex and that the result of sexual selection on external fertilizers may be behavioral rather than morphological differentiation of the sexes.     

Secondary sexual characters and sperm traits in coho salmon Oncorhynchus kisutch

A study was undertaken to examine secondary sexual characters (spawning colouration and overall body size) in relation to sperm metrics in one alternative reproductive tactic of coho salmon Oncorhynchus kisutch : large hooknose males that spawn in dominance-based hierarchies. Males with less intense red spawning colouration had higher sperm velocities than males with darker red spawning colouration. There was no relationship between male body size and sperm metrics. These results suggest that within an alternative reproductive tactic, variation in sperm competition intensity may select for a trade-off between investment in sexual colouration and sperm quality.     

Reproductive biology and implications for management of the orange-spotted grouper Epinephelus coioides in the southern Arabian Gulf

The reproductive biology of Epinephelus coioides was determined from the examination of 1455 individuals collected between July 2005 and June 2007 in the southern Arabian Gulf. Histological preparations of gonads indicated that males were either derived from a juvenile phase or the transition of postspawning females, confirming a diandric protogynous sexual pattern. The spawning season was well defined, occurring once a year during April and early May. Peaks in spawning occurred after the full and new moons and was completed within a single lunar cycle. The presence of mature males over the entire size and age range and the absence of inactive mature females during the spawning season suggested that the population was not constrained by sperm limitation. While specimens undergoing sexual transition were only observed in size and age ranges of 335–685 mm total length ( L _T) and 5–6 years, patterns in the proportion of males in size and age classes suggested that sex change occurred at a relatively constant rate after female maturation up to the maximum size (1002 mm L _T) and age (11 years). Relationships between reproductive output and capacity with size and age indicated that conventional regulations that equate the mean size at first capture to sexual maturation are unsuitable for the management of E. coioides . The maximum age, small size and young age at sexual maturation ( L _min= 320 mm L _T, 2 years, for females and 242 mm L _T, 1 year, for males) conflict with the general pattern for large epinepheline groupers and may be a direct result of the intensive demersal fishery 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.     

未产卵雌性黄鳝的性转变

为探讨产卵是否为雌性黄鳝(Monopterus albus Zuiew)性转变的必经过程,研究分析了实验室内从受精卵或幼苗开始养殖至不同时间段的黄鳝性腺组织学状况,采用性腺活检技术跟踪了34月龄雌性黄鳝性腺发育变化,并以免疫组织化学方法探讨了黄鳝不同发育状态性腺中增殖细胞核抗原(PCNA)的分布.在养殖过程中,实验黄鳝...     

Sperm competition and sex change: a comparative analysis across fishes

Current theory to explain the adaptive significance of sex change over gonochorism predicts that female-first sex change could be adaptive when relative reproductive success increases at a faster rate with body size for males than for females. A faster rate of reproductive gain with body size can occur if larger males are more effective in controlling females and excluding competitors from fertilizations. The most simple consequence of this theoretical scenario, based on sexual allocation theory, is that natural breeding sex ratios are expected to be female biased in female-first sex changers, because average male fecundity will exceed that of females. A second prediction is that the intensity of sperm competition is expected to be lower in female-first sex-changing species because larger males should be able to more completely monopolize females and therefore reduce male-male competition during spawning. Relative testis size has been shown to be an indicator of the level of sperm competition, so we use this metric to examine evolutionary responses to selection from postcopulatory male-male competition. We used data from 116 comparable female-first sex-changing and nonhermaphroditic (gonochoristic) fish species to test these two predictions. In addition to cross-species analyses we also controlled for potential phylogenetic nonindependence by analyzing independent contrasts. As expected, breeding sex ratios were significantly more female biased in female-first sex-changing than nonhermaphroditic taxa. In addition, males in female-first sex changers had significantly smaller relative testis sizes that were one-fifth the size of those of nonhermaphroditic species, revealing a new evolutionary correlate of female-first sex change. These results, which are based on data from a wide range of taxa and across the same body-size range for either mode of reproduction, provide direct empirical support for current evolutionary theories regarding the benefits of female-first sex change.     

Gonadal development and associated changes in liver size and sexual steroids during the reproductive cycle of captive male and female Atlantic cod (Gadus morhua L.)

Gametogenesis in female and male Atlantic cod (Gadus morhua L.) was investigated by sampling blood plasma and gonadal tissue from 19 to 33-month-old fish. The reproductive cycles of both female and male Atlantic cod are characterized by distinct annual variations in gonadal size and developmental stage and these are associated with changes in sex steroids and liver size. I(H) did not change during early gonadal development, but both spent females and males had lower I(H) than late maturing females and spermiating males, respectively. In females I(G) was correlated to plasma E2 levels and they were highest in spawning females. The lowest levels during the reproductive cycle were observed in spent females. Plasma T levels were low throughout ovarian development, and were at a minimum in spent females. 11-ketotestosterone in plasma of males increased rapidly during spermiation, while T increased at earlier testicular stages and reached maximum during spermiation. High plasma levels of steroids in male and female cod during spawning serve to promote further development and growth of less advanced stages of germ cells.     

Reproduction in the greenback grey mullet, Liza subviridis (Valenciennes, 1836)

This paper presents data on the reproductive biology of Liza subviridis , a little studied mullet species. The fish is heterosexual, exhibiting external fertilization. Six maturity stages can be macroscopically identified in the testes and seven in the ovaries. The macroscopic changes in the gonads are manifestations of histological changes occurring in the development of sperm cells and oocytes. First sexual maturity is attained in the length ranges of 9.5–11.5 cm and 10.5–11.5 cm in male and female fish respectively. The fecundity for fish measuring 10.3–13.9 cm in standard length ranged from 40 000–145 000 eggs. The relationship between fecundity ( F ) and length ( L ) can be represented as: F = 1.9044 L ^4.2998. The spawning duration in L. subviridis is restricted to a short and definite period, with all ripe ova being released within a single spawning act. A pronounced spawning season can be detected to extend from June to November. However, during off-seasons, some spawning also occurs. The correlations between spawning, rainfall and air temperature is discussed.     

Melatonin is Involved in Sex Change of the Ricefield Eel, Monopterus albus Zuiew

The ricefield eel (Monopterus albus Zuiew), a burrowing eel-like synbranchoid teleost, undergoes a natural sex change from female to male during its life history. Since the teleost pineal gland and its melatoninergic output have been suggested as regulators in seasonal reproduction and sexual maturation in many fish species, it is reasonable to postulate that melatonin may play important roles in the ricefield eel’s sex-change process. This hypothesis was tested by examining secretional characteristics and reproductive effects of melatonin in the ricefield eel. Results indicate that serum melatonin (mainly secreted from the pineal complex, retinae and gastrointestinal tract) is involved in sex change of this species. It seems that, within a reproductive cycle, relatively lower mid-night serum melatonin (MNSM) levels are necessary for natural spawning, but relatively higher MNSM levels after spawning permit initiation of the sex-change process. A putative model is presented to clarify the involvement of melatonin in natural sex change of the ricefield eel, although the precise mechanisms are still under further investigation.     

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.     

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.     

Aromatase immunoreactivity and the role of enzymes in steroid pathways for inducing sex change in the hermaphrodite gobiid fish Trimma okinawae

The role of aromatase (Arom) in the process of bi-directional sex change in the gobiid fish Trimma okinawae was investigated by immunohistochemical methods. Irrespective of sexual phase, gonads comprised both ovarian and testicular tissues. In each sexual phase of females, the 2nd (2DF-M) and 4th (4DF-M) days after initiation of sex change to male, males, and the 2nd (2DM-F), 4th (4DM-F) and 6th (6DM-F) days after the initiation of reversion from male to female, ovarian and testicular histological observations were made. During the female, 2DF-M, 4DF-M and 6DM-F phases, the ovary contained vitellogenic and previtellogenic oocytes, compared with previtellogenic oocytes in the other phases. Although sperm was found in the testis in every phase, sperm ducts were apparent in the male phase, but not the female phase. Arom immunoreactivity was detected in the interstitial cells between the oocytes in all phases. On the other hand, it was localized in the thecal and granulosa cells of the follicular layer enclosing the oocytes in the female, 2DF-M, 4DF-M and 6DM-F phases. Activity of Arom in the thecal and granulosa cells is thought to be important for the development of oocytes and subsequent sex change.     

The breeding ecology of Cancer gracilis (Crustacea: Decapoda: Cancridae) and the mating systems of cancrid crabs

Brachyuran crabs in the family Cancridae are found in a variety of habitats, ranging from 'open' sandy or muddy grounds to 'structured' rocky bottoms rich in refuge space. Cancer gracilis Dana inhabits shallow open habitats in the north-east Pacific Ocean. Females in all reproductive conditions aggregate in relatively small areas, where mating activity appears most intense. Maximum mating activity was observed towards the end of the spawning/hatching season (August). Females play an active role in mating, often initiating interactions with the prospective male partner. Mating in the field was non-assortative with respect to size. There was no indication of direct mate choice by either males or females; resolution of male-male competitive interactions was size-based. Males below minimum mating size (77 mm carapace width) had spermatophores in the vas deferens but did not react to receptive females.
Sperm competition is likely because sperm can be retained across moults and multiple copulations are possible within a receptive period. Female spermathecae are of the 'ventral' type (contrary to what has been indicated for cancrids), and during intercourse are beyond the reach of male gonopods. Mechanisms to exclude competing sperm include male-produced sperm plugs and post-copulatory mate guarding.
Results are discussed in the context of the 'structured-to-open' habitat gradient, which may underlay much of the diversity in cancrid reproductive ecology. We argue that, by comparison with C. magister (a larger size sympatric species also found in open habitats), (1) reproductive asynchrony and female gregariousness in C. gracilis increase the environmental potential for polygyny, resulting in a female defence polygynous mating system, and (2) reproductive asynchrony inflates the operational sex ratio, leading to stronger sexual selection.