McDonough et al.: Sexual differentiation and gonad development in Mugil cephalus 



617 



The presence of developing females indicated repro- 

 ductive activity through April: however numbers were 

 small (McDonough et al., 2003). Most of the specimens 

 collected in March and April were either immature or 

 inactive. It has also been demonstrated that striped 

 mullet in closed freshwater systems, such as impound- 

 ments, can begin reproductive development. However, 

 unless artificially manipulated, spawning did not oc- 

 cur in freshwater and the fish resorbed the developed 

 gametes (Shireman, 1975; Tamaru et al., 1994). The 

 re-absorption of gametes would undoubtedly have a 

 positive effect on growth rates and may contribute to 

 some of the variation in size at age. Reproductively 

 inactive (but mature) females present every month 

 could indicate that mature mullet do not spawn every 

 year or that fish that remain in the estuary do not 

 migrate offshore to spawn. The most likely possibility 

 would be that inactive females found in the early part 

 of the spawning season may not spawn until much 

 later. However, the presence of developing oocytes be- 

 ginning in August would indicate that a few months 

 were required for complete recrudescence. It has been 

 shown that striped mullet undergoing the spawning 

 migration between the Black Sea and the Sea of Azov 

 required two months for full ovarian development (Ape- 

 kin and Vilenskaya, 1978). Also, inactive females from 

 the mid to late spawning season could have spawned 

 early, returned to the estuary, and their ovaries could 

 have regressed. We found no ripe female mullet in 

 the estuaries during the entire study; their absence 

 was likely due to their migration from coastal waters. 

 Evidence of striped mullet spawning (through the back 

 calculation of birthdates from daily growth increments 

 from juveniles) has also shown that the spawning sea- 

 son extends from October through April (McDonough 

 and Wenner, 2003). 



Sexual development 



It is not known what cue initiates gametogenesis in 

 striped mullet, but it is generally accepted that changes 

 in temperature and photoperiod help regulate the sea- 

 sonal reproductive cycle (Anderson, 1958; Kuo et al., 

 1973; Greeley et al., 1987; Kelly et al., 1991; Render 

 et al., 1995). It has been shown that although striped 

 mullet can mature in a range of salinities, the best pro- 

 duction is reached when their gonads develop in salini- 

 ties of 13 to 35 ppt (Brusle, 1981; Tamaru et al., 1994). 

 Previous studies of striped mullet (Kuo et al., 1974) 

 and other fall spawning fishes that migrate offshore 

 to spawn (de Vlaming, 1974; McQuarrie et al., 1978; 

 Whitehead et al., 1978) have indicated that a shortening 

 day length was the key stimulus for annual reproduc- 

 tive development and migration. Dindo and MacGregor 

 (1981) demonstrated a high correlation between the 

 levels of serum gonadal steroids and the gonadosomatic 

 index in striped mullet during the reproductive cycle; 

 a shortening photoperiod was suggested as the major 

 factor in stimulating reproductive activity. In our study 

 the most reproductively advanced specimens (late recru- 



descence) in freshwater were captured in October and no 

 other specimens of similar development were captured 

 during the rest of the spawning season in freshwater. 

 In contrast, the majority of the specimens undergoing 

 vitellogenesis were captured in the lower portions of the 

 estuaries during November and December in salinities 

 greater than 15 ppt. This finding indicated movement 

 of these developing fish from the freshwater portions of 

 the estuary toward the ocean for the spawning migra- 

 tion. This migration time-period also coincided with a 

 mean monthly temperature decrease in temperature 

 (from 21.8° to 13.6°C) and in photoperiod in both the 

 freshwater and brackish portions of the estuaries. 



The ovarian atretic process in female striped mullet 

 was characterized by four distinct stages that followed a 

 very similar progression to that described for the north- 

 ern anchovy (Hunter and Macewicz, 1985). Our study is 

 the first to describe the atretic process in striped mullet 

 ovaries in detail and to apply the classification system 

 developed by Hunter and Macewicz (1985). Knowledge 

 of ovarian atresia is useful for the timing of spawning. 

 However, the lack of immediate atretic-stage fish, with 

 indicators such as postovulatory follicles, prevented us 

 from determining the temporal duration of the different 

 atretic stages. The detailed morphological descriptions 

 of ovarian atresia presented in our study would be of 

 value for future studies to determine the specific timing 

 of the atretic process. 



The histological descriptions for male and female 

 developmental stages in association with both size and 

 age data provide a clear picture of these parameters at 

 differentiation and maturity in South Carolina striped 

 mullet. Previous studies of striped mullet reproduction 

 concentrated on just one sex or used cultured fish exten- 

 sively and may have considered size or age but not both 

 in a single study. Because of the length of the undiffer- 

 entiated gonad stage in juvenile striped mullet, previous 

 studies have proposed the possibility of protandric her- 

 maphrodism in this species. However, the results of our 

 study indicated that striped mullet are gonochoristic but 

 capable of nonfunctional hermaphroditic characteristics 

 in differentiated mature gonads. It is hoped that the 

 descriptions of developmental morphological features 

 presented in the present study will be useful for future 

 studies by providing a key to reproductive ontogeny that 

 relates directly to somatic growth and age in striped 

 mullet. In particular, the morphological characteristics 

 of sexual differentiation could enable more precise de- 

 terminations of sex in immature mullet, which, in turn, 

 would indicate the sex ratio of males and females in a 

 given population and allow the development of better 

 management strategies. 



Acknowledgments 



This study would not have been possible without the 

 assistance of everyone, past and present, at the Inshore 

 Fisheries group at the Marine Resources Research 

 Institute of the South Carolina Department of Natural 



