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.     

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.     

A preliminary test of the transitional growth spurt hypothesis using the protogynous coral trout Plectropomus maculatus

Estimates of back-calculated size at age provided no evidence of a growth spurt following sexual transition in the protogynous serranid Plectropomus maculatus. The results suggested that mature females that had a large size at age early in life changed sex to male.     

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.     

Gonadal development and an indication of functional protogyny in the Indian damselfish (Dascyllus carneus)

The objective of this study was to determine the sexual pattern of the Indian dascyllus Dascyllus carneus . After an initially undifferentiated state, gonads of D. carneus developed an ovarian lumen and primary growth stage oocytes, and subsequently cortical-alveolus stage oocytes. From ovaries with cortical-alveolus stage oocytes and from more developed ovaries, some gonads redifferentiated into testes. From a sample of 163 individuals, two had a gonad containing degenerating vitellogenic oocytes and proliferating spermatogenic tissue, nine had a gonad containing degenerating cortical-alveolus stage oocytes and spermatogenic tissue, and five had a gonad with degenerating primary growth stage oocytes and spermatogenic tissue. The size of these individuals overlapped greatly with the size range of mature females, suggesting that at least in some individuals, redifferentiation toward a testis occurred after spawning as females. This indicates that D. carneus is a functional, diandric protogynous hermaphrodite. Removal of a dominant male(s) did not induce a sex change in any of the ranking females in the laboratory and field groups. There was no difference in the number of chases and signal jumps performed by the ranking female between control and experimental field groups, or before and after removal of the male. However, the sizes of the ranking females were at or beyond the size range of individuals with a mixed-stage gonad, suggesting that the developmental window for female-to-male sex change may not be open ended. In 41 of 43 field groups, in which sex of fish was determined histologically or by the shape of the urogenital papilla, one to several highest size ranks were occupied by males, followed by one to several females. Mature males, however, were not limited to the highest ranks and occurred at various lower size ranks within groups. Individuals with a mixed-stage gonad also occupied various size ranks within groups.     

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.     

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.     

Seasonal cycles of gonadal development and plasma sex steroid levels in Epinephelus morio, a protogynous grouper in the eastern Gulf of Mexico

In a field population of the protogynous red grouper Epinephelus morio in the eastern Gulf of Mexico, females with oocytes at all stages of development were collected during the spawning season suggesting that several batches of oocytes may be released over the spawning period. Plasma oestradiol (E₂) levels were highest in ripe females whose gonads contained both cortical alveoli and vitellogenic oocytes during the breeding season. Males were still spermiating as late as August, although levels of androgens 11-ketotestosterone (11-KT) and testosterone (T) had declined from their peaks in March. A few red grouper with either perinucleolar or cortical alveoli stage oocytes were undergoing sex change both during and after the spawning period. Low levels of E₂, T and 11-KT were detected in transitionals. Proliferation of male tissue was not restricted to any specific area of the gonad but occurred in pockets within the ovarian lumen. The sequence of an increase in gonial cells along the periphery of the lamellae, increase in interstitial tissue, degradation of female elements, and formation of a sperm duct seemed to be concurrent with spermatocyte proliferation and the process of preparing the gonad to function as a testis.     

Reproductive biology of squaretail coralgrouper Plectropomus areolatus using age‐based techniques

The squaretail coralgrouper Plectropomus areolatus was identified as a fast‐growing, early maturing and relatively short‐lived aggregation‐spawning epinephelid. Examinations of sectioned otoliths found females and males first maturing at 2 and 3 years, respectively, suggesting protogynous hermaphroditism; however, no transitionals were observed in samples. Age distribution for the two sexes was similar and both were represented in the oldest age class; however, significant sex‐specific differences in size‐at‐age were identified. Both sexes fully recruit into the fishery at age 4 years and reach 90% of asymptotic length by age 3 years. Underwater visual assessments, combined with the gonado‐somatic indices, revealed a 5 month reproductive season, with interannual variability observed in the month of highest density within the spawning aggregation. Catch restrictions on adults during spawning times and at reproductive sites, combined with gear‐based management and enhanced enforcement, are recommended to maintain spawning stocks. Based on the available evidence, the sexual pattern for this species is unresolved.     

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.     

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.     

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.     

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.     

Gonadal development and non-functional protogyny in a coral-reef damselfish, Dascyllus albisella Gill

All gonads of the Hawaiian dascyllus Dascyllus albisella , irrespective of the final sex of individuals, developed an ovarian lumen and primary-growth-stage oocytes after an initially undifferentiated state. From this ovarian state or from more differentiated ovaries, some gonads redifferentiated into testes. None of 117 individuals examined had a gonad containing degenerating vitellogenic oocytes and proliferating spermatogenic tissue. Eleven individuals had gonads containing degenerating cortical-alveolus-stage oocytes and developing spermatogenic tissue. The size of these individuals overlapped with the female size range in which the majority of the females were still in the middle of the maturation process. They were absent from the larger size range where the majority of females had vitellogenic oocytes. This indicated that the transition toward maleness is likely to have occurred after the onset of cortical-alveolus stage, but before final oocyte maturation and spawning as females. Therefore the protogynous pattern of gonadal development was non-functional. There was no dimorphism in the sperm duct configuration, and all the testes were secondary testes reported for diandric, protogynous species with undelimited gonads. Very early development of an ovarian lumen appeared to have resulted in a secondary-male configuration in all testes, although redifferentiation into males appeared to have occurred before sexual maturity and spawning as females.     

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).     

Reproductive characteristics of Spondyliosoma cantharus (Linnaeus, 1758) in the Gulf of Tunis

The reproductive features of Spondyliosoma cantharus were studied in the Gulf of Tunis to contribute to better fisheries management on a regional scale and to broaden knowledge on whether there are actual performance differences compared to others areas. A total of 369 fish were caught by trammel and gill nets in the Gulf of Tunis from January 2005 to June 2006. Sex‐ratio, gonad maturation, size and age at maturity, sexual cycle, condition and reproductive strategy were determined. The male : female ratio was initially skewed in favour of females, with males predominating in larger sizes. Length of females at first maturity was 17.8 cm TL (n = 141), which corresponds to 4 years of age. A recommendation is made to increase the length at capture. Spawning season extends from January to May, with a peak in March–April correlated to the lowest sea surface temperatures (14.8–15.6°C); during this period, a dichromatism arises between males and females. The hepatosomatic index and the condition factor present significant monthly changes in relation to the breeding activity. The bimodal size frequency distribution, the biased sex ratio, and the presence of bisexual gonads outline a protogynous hermaphroditism; diandry should be confirmed.     

Reproductive biology of the East African lungfish (Protopterus aethiopicus) in Mwanza Gulf, Lake Victoria

The population of lungfish (Protopterus aethiopicus (Heckel)) was sampled by bottom trawling for 12 months from June 1984 to May 1985. A total of 576 lungfish were investigated. The sex ratio in the population was 1 male : 1 -98 females. Average size at maturity was found to be 960cm total length (TL) but the smallest matured male measured 72-9 cm and the female 840 cm TL. It was not possible to establish spawning times and reproductive activity trends either from the variation in relative condition factor ‘kn’ or from gonadosomatic index (GSI). Whereas male lungfish seem to show no further increase in GSI after gonadal maturity stage III, females exhibit GSI values that vary directly with oocyte maturation and ovarian weights. Fat deposited along the gonads was found to be a better basis for assessing maturation and spawning in lungfish. The potential spawning period was found to be from September to May. Absence of lungfish with spent gonads over the 12-month period and the presence of different egg sizes in ovaries, suggest that the fish is a multiple spawner. Fecundity was found to range from 705 eggs (in 84-cm TL fish) to 14,922 eggs (in 130-cm TL Fish).     

Anatomical changes to the gonad during protogynous sex change in the half-moon grouper Epinephelus rivulatus (Valenciennes)

Anatomical changes to the gonad during sex change in the protogynous grouper Epinephelus rivulatus are described from histological observations. A decrease in ovarian mass occurred soon after the onset of sex change as oocytes atrophied and were removed from the gonad. Blood supply and abundance of unidentified somatic cells increased at this time as proliferation of sperm tissue commenced. As the gonad was cleared of ovarian tissue, the rate of spermatogenesis increased and the lamellae soon became dominated by sperm and connective tissue. Putative Leydig cells, the probable sites of male steroid production, appeared in transitional gonads and were most abundant in the testes of immature males. Peripheral sperm sinuses subsequently formed within basal tissue layers of the tunica and expanded as they filled with spermatids. The process of sex change, occurring as a result of experimental manipulation of wild populations at the start of the spawning season, took c. 3 weeks. This appears rapid compared to other hermaphroditic species and may reduce the impacts of fishing on reproductive output by E. rivulatus populations.     

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.