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The reproductive cycle of the flame scallop, Ctenoides scaber (born 1778), from the lower Florida Keys and its relationship with environmental conditions.

ABSTRACT The reproductive cycle, sex distribution, and gonadal characteristics of the flame scallop, Ctenoides scaber, formerly Lima scabra scabra (Born 1778), collected from Boca Chica Key, FL, were investigated over the 21-mo period from January 1998 through September 1999. Gametogenic cycles were examined using qualitative and quantitative methods, and the relationships between those observations and environmental conditions (e.g., water temperature, salinity and phytoplankton concentrations) were analyzed. The relationships between sex, gonad color and shell height were also examined. Gamete development in both sexes was initiated in winter and was associated with small oocytes and follicles, cool water temperatures and moderate concentrations of food. Growth of gametes occurred throughout spring, as temperature and chlorophyll-a concentrations increased. A partial synchronous spawn occurred in early summer but did not seem to be related to environmental conditions. Maximum gamete ripeness and size occurred in late summer, when water temperatures were at maximum values and food densities were increasing. Decreases in female gamete and follicle sizes and increases in occurrence of partially spawned, spent and early growth gonads in autumn were suggestive of synchronous spawning, which coincided with a rapid decrease in water temperature and maximum measured chlorophyll-a concentrations. Decreases in oocyte size in February coincided with annual water temperature minimums and may represent the conversion of energy from reproduction to survival, and not spawning. The presence throughout the year of juveniles, ripe and partially spawned flame scallops and chlorophyll-a concentrations sufficient to support gamete development suggest a reproductive strategy of continuous spawning, common in tropical marine invertebrates. No relationship was detected between salinity and gonad condition. Flame scallops collected for this study ranged in size from 21-68 mm shell height (SH) and those >25 mm SH had gamete development. The smallest animals were found principally in summer, which suggests a massive synchronous spawning event. Analyzing sex distribution by SH showed that flame scallops are protandric sequential hermaphrodites. Flame scallops <40 mm SH were predominantly male (83%), those [greater than or equal to] 40 mm SH were mostly female (71%), and 4% were in sexual transition near 40 mm SH. The sex ratio for the sampled population was 0.63M:1F. Histologic examination of fresh gonadal tissues revealed that female gonads were predominantly purple (96%) and male gonads were predominantly cream-colored (91%). Other gonad colors observed were not reliable indicators of sex nor was there a clearly defined association between color and those animals in sexual transition. Documenting the reproductive cycle of Ctenoides scaber in the existing Florida fishery is the first logical step to understanding its life history. Because flame scallops are important to the marine aquarium industry in the United States and are a potential food source for humans, it is important that we understand the reproductive cycle of this species to ensure proper management policies. This study provides basic information applicable to mariculture of flame scallops for commercial production to supplement the harvest of wild stock for the marine aquarium industry.

KEY WORDS: flame scallop, reproduction, sex ratio, Ctenoides scaber, spawning, environmental conditions, gonad color

INTRODUCTION

Tropical flame scallops, Ctenoides scaber, are commercially important for the marine aquarium trade in the United States and support a small-scale fishery in the Caribbean Basin (Gomez et al. 1990), but little research has been done on their life history. Because there has been no research on gametogenesis in Florida flame scallop populations, we used quantitative and qualitative methods to examine Ctenoides scaber's sex distribution and reproductive development over time as related to environmental conditions. We also examined the relationships between sex, gonad color (GC), and shell height (SH).

Ctenoides scaber range from North Carolina southward to Brazil (Abbott 1974). They are commonly found attached by byssal threads to rocks and coral rubble (Abbott 1974). The reproductive cycles of C. scaber have been studied in Venezuelan waters. These studies include those by Gomez et al. (1990, 1995), which examined the relationships between sex, SH, and biomass and their effects on flame scallop reproduction during March, May and July 1994. Another study by Lodeiros and Himmelman (1999) examined the relationship between C. scaber reproduction and environmental conditions. Animals collected in those studies ranged from 12.8-81.5 mm SH. The largest animals were collected in March, and the smallest in July (Gomez et al. 1995). Flame scallops are protandric, sequential hermaphrodites and sexual transition occurs as the animal nears 40-mm SH (Gomez et al. 1990, Gomez et al. 1995). Lodeiros and Himmelman (1999) calculated the sex ratio 1M:0.84F, which was not significantly different from the expected 1M:1F.

Gonadosomatic indices (GSIs) indicated that reproduction in Venezuelan flame scallops was highly variable throughout the year (Lodeiros & Himmelman 1999). Spawning events were characterized by a reduction of GSIs below 5%, and animals of all sizes were reproductively active (Lodeiros & Himmelman 1999). Gamete development was initiated in winter (GSIs were 2% to ~5%) during seasonal low water temperatures (23[degrees]C) and elevated chlorophyll-a (chl-a) concentrations (~0.5 to ~7.5 [micro]g/L) and increased steadily through early summer as water temperature increased and phytoplankton levels decreased (Lodeiros & Himmelman 1999). GSIs decreased sharply throughout June and early July and coincided with a 4[degrees]C decrease in water temperature and an increase in chl-a from ~0 to 3.0 [micro]g/L, which may have been evidence of a partial spawning event. Gomez et al. (1995) also detected reduced GSIs in May and June (6% to 8%). GSIs reached maximum annual values (~15%) in August (temperature 26[degrees]C; chl-a ~1 [micro]g/L). Two years of data showed marked decreases of GSIs to <5% in autumn, which also corresponded with temperature decreases and chl-a increases and indicated a synchronized spawning event (Lodeiros & Himmelman 1999). Only chl-a concentrations were statistically related to reproduction in Venezuelan flame scallops, which may suggest that C. scaber gamete development is stimulated by elevated chl-a, as is seen in other bivalves (Sastry 1979, Barber & Blake 1991). The increased recruitment of juveniles into the population in summer supports the hypothesis that massive synchronous spawning may have occurred (Gomez et al. 1995). In addition, highly variable developmental stages throughout the year suggest continuous spawning or partial synchronous spawning may contribute to the reproductive strategies of C. scaber (Lodeiros & Himmelman 1999).

In Florida, Ctenoides scaber are found on the east coast and in the Florida Keys (Abbott 1974). A decreasing trend in Florida landings (Florida saltwater products license trip ticket data, Florida Fish and Wildlife Conservation Commission, unpublished data) since 1995 suggests that flame scallop populations might be dwindling. One possible reason for this decline is the harvest associated with the aquarium trade. For the past decade, Americans have had more disposable income than in the previous decades, and this, coupled with a stable economy, encouraged the growth of the ornamental marine aquarium industry and increased the demand for marine species. In the United States, more than 4% of homes have marine aquariums, a 4-fold increase over 1982 (Chapman et al. 1997). Most marine species are collected from the wild, not cultured, with domestic collections being made in Florida and Hawaii (Chapman et al. 1997). Wild populations of marine ornamental species are being quickly diminished as sport divers and commercial collectors harvest more animals each year than are naturally replenished (Malachowski 1988).

Species that grow rapidly, reproduce often, have large numbers of offspring and have short life spans typically have highly fluctuating recruitment (Rhodes 1991). Annual landings of flame scallops are variable and recent reductions may not be solely due to over-harvesting. However, other factors, including a decline in habitat availability (Arnold 1990) and in water quality, both of which could be related to human activities (Blake 1993), may also be contributing to the reduction of wild populations. Although commercial landings data show that flame scallops are harvested regularly in Florida, no quantitative study has assessed reproduction in this population. Documentation of Florida's Ctenoides scaber reproductive cycle would aid in better management of this natural resource and would provide baseline data useful in developing technology and procedures for culturing flame scallops for both commercial purposes and restocking efforts.

MATERIALS AND METHODS

Approximately every 5 wk from January 1998 through September 1999, Ctenoides scaber were harvested from the third channel in the submarine pits, a man-made canal system on the northwest tip of Boca Chica Key in the lower Florida Keys (Fig. 1). Flame scallops were harvested by hand from crevices in the limestone habitat by SCUBA divers at depths of 0.5-7.0 m. Samples were held in aerated water collected from the site and monitored for evidence of stress and spawning during transport to the laboratory in St. Petersburg, FL. Substantial efforts were made to keep the temperature and salinity the same as was measured at the time of collection.

[FIGURE 1 OMITTED]

Water temperatures were collected on each sampling date at ~1.5 m below the surface, and water quality parameters were measured immediately. Temperature was measured with a handheld thermometer, and salinity was measured with a refractometer. Additionally, regional sea surface temperature data were obtained from AVHRR satellite images acquired by the Remote Sensing Laboratory at the University of South Florida. Chlorophyll-a concentration data were obtained from R. Jones and J. Boyer (FKNMS Water Quality Monitoring Project, EPA Agreement #X994621-94-0). These four water quality parameters were compared with qualitative staging data of gamete development and tested using the Kolmogorov-Smirnov Normality Test (K-S test). Significant relationships between the four water quality parameters and the four quantitative measures of female gonads were then analyzed using Pearson Product Moment Correlation or Spearman Rank Order Correlation, depending on the results of the normality tests.

During laboratory analysis, shell height (SH, maximum distance from the hinge to the ventral valve edge) was measured to the nearest millimeter using vernier calipers. To detect trends in SHs, we tested those of collected animals for normality (K-S test) and then plotted them by time and sex. A Kruskal-Wallis (K-W) ANOVA on ranks was used to identify collection months in which SHs were significantly different.

In flame scallops, the gonad is situated in the mantle cavity posterior and ventral to the foot. It is attached to the adductor muscle on the dorsal side and forms a protruding kidney-shaped bulge when ripening. Gonad tissue is also found throughout the digestive gland. The gonad varies greatly in size and color during the year. In this study, only the kidney-shaped portion of the gonad was excised from the adductor muscle and analyzed. For each animal, gonad color (GC) in fresh tissue was recorded as purple, cream, tan, clear, gray or brown; later the sex of each of these animals was determined through histologic examination. The gonads were removed from [less than or equal to] 20 animals per collection date and processed using histologic techniques. Each gonad was placed into cassettes in Helly fixative for 24 h (Yevich & Barszcz 1977). Larger tissues (>1 cm) were removed from the cassette after 4 h, scored with a scalpel and returned to the fixative to ensure preservation of the interior portion. After fixation, the gonads were washed in fresh water for 18-24 h and stored in Tissue Dry dehydrant (Barber 1980). Further processing included six changes of Tissue Dry dehydrant and three changes of Tissue Clear clearing agent (Technicon Instruments Corporation) before the gonads were embedded in Paraplast following procedures outlined in Barber and Blake (1983). Tissues were sectioned at 6-[micro]m thickness, placed on glass slides, stained with hematoxylin and eosin and covered with glass coverslips (Yevich & Barszcz 1977).

The sex of each animal was determined by microscopic examination of histologically prepared slides of gonad tissue. The sex distribution of the sample population was analyzed for normal distribution using the K-S test (Zar 1996). The expected 1:1 sex ratio was tested against the observed sex ratio using [chi square] analysis. Correlations were then made between sex, gonad stage, SH, and GC.

Sectioned gonads were qualitatively analyzed and placed into one of these distinct reproductive categories based on Ropes and Stickney (1965): undifferentiated, early growth, late growth, ripe, partially spawned and spent. The stages are described in Table 1 and depicted in Figures 2 and 3. Trends in spermatogenesis and oogenesis were evaluated over time, and we attempted to correlate observed changes with existing environmental conditions.

[FIGURES 2-3 OMITTED]

We quantitatively assessed female gonads by using an Olympus compound microscope and the Optimas system of Media Cybernetics to measure oocyte diameters, oocyte areas and follicle areas of histologically prepared ovaries. Images were captured using a digital camera and measurements were made using a computer mouse and the automatic measuring feature of the Optimas system. Measurements were based on the microscope objective used, which was calibrated with a stage micrometer. Data were exported to an Excel spreadsheet. Total magnification was calculated using microscope objective and camera tube magnifications.

Measurements of 50 oocyte diameters and 50 oocyte areas were made for each female at a magnification at x721. Oocytes were selected randomly from the gonad section and were restricted to those in which nucleoli were clearly visible in the nuclei; because we assumed that the cut was near the center of the oocyte if the nucleoli were visible (Arnold pers. comm.). Area measurements of 30 randomly selected follicles from each female were made at a magnification x355, and all oocytes within each measured follicle were counted. Oocyte density was then computed for each follicle measured. The distributions of all measured gonad parameters were tested for normality using the K-S test (Zar 1996). A K-W ANOVA on ranks analyzed temporal variation in each parameter. If a significant difference existed, Dunn Test was used to differentiate between months (Zar 1996). Testes were not quantitatively analyzed.

RESULTS

A total of 454 flame scallops were collected, from which 333 gonads were prepared using histologic techniques. Monthly sample size was 9 to 66 live flame scallops. The sample population consisted of 194 females, 124 males, 14 flame scallops in sexual transition and 1 sexually undifferentiated animal. The sex ratio was 0.63M:1F, which was significantly different from the expected 1:1 ratio ([chi square], P = 0.05).

Qualitative Analysis

The percentages of females (Fig. 4a) and males (Fig. 4b) in each gonad development category for each collection month are shown. No females were observed in the early growth category, so to more easily compare the numbers of each sex in the reproductive categories, males in early and late growth categories were combined. Observed reproductive trends for both males and females indicated that gamete initiation and early growth occurred primarily in winter (December to February), although no females were observed in these stages in winter 1998 (Fig. 4a). The number of ripe individuals increased steadily throughout spring (March to May) and summer (June to August), with peak ripeness occurring in late summer (Fig. 4). Although partially spawned animals were seen throughout the year, the greatest proportion was observed in late summer (August) and autumn (September to November) (Fig. 4). No samples were taken in September 1998 because of the passage of a hurricane through the collection area. The majority of flame scallops with spent gonads were seen in November. Multiple stages of development were observed in late autumn and early winter (Fig. 4). Small gametes were present near the follicle periphery during and immediately after spawning indicating that flame scallop gonads do not have a resting period between gametogenic cycles. Annual, seasonal and sexual variations were observed.

[FIGURE 4 OMITTED]

Examination of histologically preserved gonad tissues indicates that Florida flame scallops are protandric, sequential hermaphrodites, with 4% of the population in sexual transition. Those in transition have both male and female gametes occurring concurrently in follicles (Fig. 5). Male gametes were more mature than female gametes and were seen in the central portions of the follicles; the female gametes were near the follicle periphery (Fig. 5).

[FIGURE 5 OMITTED]

Quantitative Analysis

Figure 6a summarizes 4 quantitative measures of female gonad condition: oocyte diameter, oocyte area, follicle area and oocyte density. Table 2 summarizes the statistical analysis for each parameter. Data were not normally distributed (K-S: P < 0.001) for any of these parameters, so nonparametric statistical methods and median values were used in further analyses.

[FIGURE 6 OMITTED]

The median oocyte diameters and areas were small in the winter and increased in size throughout the spring. In June of each year, slight decreases were observed (Fig. 6a). Maximum gamete sizes were measured in late summer (August) and were statistically similar among years (Table 2). Rapid decreases in oocyte sizes were seen in autumn (Fig. 6a). Measurements of oocyte sizes made in early winter (December) were at annual minimums. Within the annual cycles, gamete size peaks (solid vertical lines in Fig. 6a) occurred in January and August of both years and in May 1999. These size peaks were immediately followed by noticeable size decreases (dashed vertical lines). Also, noticeable decreases in oocyte sizes occurred in February of each year (Fig. 6a). Median oocyte diameters measured in December were significantly different (P < 0.001) from those in all other months. In November and December median oocyte areas were significantly different (P < 0.001; Table 2). Median oocyte diameters and areas from February, October and November 1998 and February 1999 were statistically similar.

Median follicle area trends were similar to those of oocyte diameters and areas. In 1998, median follicle areas varied only slightly in winter and spring (Fig. 6a). Annual maximum follicle areas occurred in early summer and decreased sharply throughout late summer and autumn. Annual minimum follicle areas occurred in November (Fig. 6a). Similar trends were observed in 1999; however, annual maximum follicle areas were observed in late spring (May). No noticeable decrease in follicle size was noticed in February, as was seen in oocyte diameters and areas (Fig. 6a). Although no collection months were significantly different (P > 0.05) from all others, mean follicle sizes throughout autumn were statistically similar (Table 2).

Median oocyte densities have an inverse relationship to the other parameters and are less variable over the study period. Oocyte densities were greatest in winter and decreased steadily throughout spring and summer as oocyte size increased (Fig. 6a). Annual minimum densities occurred in late summer, when oocytes were at maximum size, and a less well-defined decrease in oocyte density occurred in May 1999 (Fig. 6a). Although median oocyte densities increased in autumn, no annual maximum occurred in late autumn or early winter as in the other parameters. Only slight changes in densities were observed in February and June. No collection dates were found to be significantly different (P > 0.05).

Similar trends were observed in several measures of female gonad condition, but only oocyte diameters and oocyte areas had a high correlation coefficient (r = 0.92; P < 0.001). Oocyte area and density were inversely related, but the relationship was not as strong (r = -0.51, P < 0.03).

Environmental Conditions

Temperature and salinity measurements taken at the sample site, regional temperature measurements from AVHRR satellite technology, and chlorophyll-a concentrations from Boca Chica Channel are shown in Figure 6b. Temperatures ranged from 20[degrees]C to 33[degrees]C, with yearly lows in winter and maximum temperatures in summer. Local (collection site) and regional (AVHRR) temperature measurements followed similar trends over the study period except in autumn 1998, when regional temperatures dropped quickly after August. Temperatures at the collection site remained elevated until November, when a 7[degrees]C decrease was measured.

Strong relationships exist between AVHRR regional temperature data and oocyte diameter (r = 0.71), area (r = 0.76), and density data (r = -0.77; P < 0.001 for all).

Salinity measurements ranged from 32-44 ppt during the study period but were usually between 38-40 ppt (Fig. 6b). The lowest salinity measurements occurred in late winter and autumn 1998 (following the hurricane), and the greatest salinity measurements were made in late spring 1999. Seasonal trends were not forthcoming, though annual maximum salinity measurements were seen in summer (Fig. 6b). No statistical relationships between salinity and female gonad parameters were found.

Surface chlorophyll-a concentrations from Boca Chica Channel ranged from 0.1 to 1.1 [micro]g/L. The lowest concentrations were measured in winter. Concentrations increased throughout spring and summer. The greatest measured values occurred in late summer and early autumn (Fig. 6b). No significant relationships were observed between chl-a and female gonad parameters.

The sampling period coincided with an El Nino/La Nina event that began in late 1997 and persisted through 1998. Rainfall in southern Florida increased by 88% in spring and summer 1998, and mean temperatures decreased by 2.1[degrees]C in winter 1998 (Anonymous 1997). Few effects from E1 Nino/La Nina were felt in south Florida during the remainder of 1998 (Schmidt et al. 2001).

Shell Height

Shell heights ranged from 24-68 mm, with mean SH ranging from 35-50 mm (Fig. 7). No significant differences in SHs between months were detected throughout the study period except in July 1998 (K-W ANOVA; P < 0.05), although great variability in SHs was observed for most sampling months (Fig. 7). Small animals (<30-mm SH) were collected throughout the year but were most common in summer. Each summer featured shell height minima (primarily in July). Most (83%) of the flame scallops measuring <40 mm SH were male, whereas 71% of those in larger size classes were females (Fig. 8). Flame scallops in sexual transition measured 35-54 mm SH. One flame scallop (24-mm SH) was sexually undifferentiated.

[FIGURES 7-8 OMITTED]

Gonad Color

A strong relationship was seen between GC and sex for cream-colored (91% male) and purple (96% female) gonads. No obvious relationships were seen between sex and clear, gray, tan or brown gonads (Fig. 9). Flame scallops in sexual transition were found in all GC categories.

DISCUSSION

The reproductive cycle of Ctenoides scaber in a Florida Keys population was determined by examining the initiation of gamete development, the growth of gonad components, and spawning activity. In this study, notable variations in gonad development occurred between months, seasons, annual cycles, and sexes, but both qualitative and quantitative data suggest that gamete development was initiated in winter. Growth of gametes occurred throughout spring, and in early summer, synchronous spawning occurred in some of the population. Gametes reached maximum ripeness by August. Another more massive synchronous spawn occurred in autumn and was mostly complete by December, as indicated by the fact that the greatest number of partially spawned and spent animals were observed in November and by the significantly smaller oocyte diameters and oocyte areas measured in December. Quantitative data also identified measurable decreases in oocyte size in February of each year; however, because annual minimum temperatures occurred then, the decrease in gonad size could be representative of the conversion of energy from reproduction to survival.

Lifetime reproductive success in bivalves occurs when they respond well to annual changes in environmental conditions, have a protracted spawning period, or have synchronous spawning events (Geise & Pearse 1974). If ideal spawning conditions are not achieved, then repeated or partial spawning may occur to ensure that at least some of the larvae will find favorable conditions for survival (Langton et al. 1987). Species found in topical and subtropical latitudes may spawn continuously to ensure reproductive success (Langton et al. 1987).

Flame scallops in Florida and Venezuela appear to use several means to ensure reproductive success. Evidence suggests that decreases in GSIs, changes in female gonad components, and the appearance of juveniles in the population within a small time frame help to ensure that a massive, autumnal synchronous spawn occurs and that a partial spawn occurs in early summer. Variability in gonad stages throughout the year, no resting period after synchronous spawns, and the presence of small oogonia at the follicle periphery in both partially spawned and spent animals also indicate that continuous spawning may occur. Slight differences in the timing of the early-summer partial spawns and the lack of resting period between the Florida and Venezuelan populations may be a function of latitude or of the particular conditions of the various habitats.

Environmental conditions may play an important role in the timing of gamete development and spawning in bivalves (Sastry 1966) and may vary greatly as a function of latitude (Sastry 1970). Seasonal changes in water temperature are believed to help initiate gametogenesis, whereas short-term temperature changes may stimulate spawning (Thorson 1946, Bricelj et al. 1987). The specific critical temperature at which gamete development is initiated, can occur at different times of the year at various latitudes (Sastry 1970); as latitude decreases, water temperatures are less variable, resulting in protracted spawning periods (Geise & Pearse 1974). Because flame scallops are suspension feeders, like most bivalves, their reproductive cycle may be influenced by changes in phytoplankton biomass and species composition (Sastry 1968, Geise & Pearse 1974, Sastry 1979). Spawning in bivalves commonly occurs when food is plentiful to feed the progeny and to replenish energy lost during spawning and gamete development (Bayne 1975).

The gametogenic cycle of this Florida Keys population of Ctenoides scaber is likely related to changes in water temperature and food availability; however, no relationship with salinity was identified. Seasonal low temperatures coincided with minimum chlorophyll-a concentrations, minimum oocyte and follicle sizes and gamete initiation, and these correlations were particularly evident in males. Increases in water temperatures and food concentrations throughout spring coincided with the growth of gametes and an increase in the number of ripe gonads. Maximum gamete ripeness and size observed in late summer (August) were related to seasonal maximum water temperatures. Noticeable decreases in oocyte and follicle sizes, and increases in oocyte densities and the number of partially spawned and spent animals have been associated with rapid decreases in local and regional water temperatures in autumn and with maximum chlorophyll-a concentration. In addition, multiple stages of gonad condition were observed in late autumn and early winter. From these data we inferred that synchronous spawning occurs in autumn. Interestingly, Lodeiros and Himmelman (1999) suggested that phytoplankton abundance--not temperature--was the primary environmental factor influencing gonad growth in flame scallops and that changes in environmental parameters were related to seasonal upwelling. Statistical analysis in our study shows that changes in water temperature are strongly correlated to gonad development but that chlorophyll-a levels are not. Future studies of this population should include chl-a collection at the site to assess its impact on flame scallop reproduction. Also, food composition and concentration may be adequate year-round to support gamete formation and development and this may further support evidence of a continuous spawning strategy. Further studies will be needed to explain these results.

The examination of sex as related to shell height suggested that Florida Ctenoides scaber are protandic sequential hermaphrodites with transition occurring near 40 mm SH, which corroborates findings by Gomez et al. (1990) for C. scaber in Venezuela. Interestingly, in the Florida flame scallops in sexual transition, the male portion of the gonads appeared to be more mature than the female portions. Similar to that found by Sastry (1979), spawning did not occur in our study until both sexes reached maturity. Hermaphroditism in bivalves is not uncommon. The evolutionary mechanism for sequential hermaphroditism may be hormone release (Coe 1945), food metabolism (Orton 1920, Tranter 1958), genetic isolation (Ghiselin 1969), or the prevention of self-fertilization in broadcast spawners (Geise & Pearse 1974). Florida flame scallops live in large aggregations and hermaphroditism may enhance fertilization success. More studies are needed to clarify the evolutionary tendency to hermaphroditism in this population of flame scallops.

The sex ratio of the sampled population was calculated to be 0.6M:1F rather than the expected 1:1, and it varied considerably from the 1M:0.84F reported by Gomez et al. (1990). The sex ratio also varied with SH. Sexual differentiation may not occur until individuals reach 25 mm SH. Gomez et al. (1995) reported that smaller flame scallops lived on sandy bottoms, whereas the larger animals preferred rocky and coral habitats. They also stated that parrotfish quickly devoured the juveniles. Observations at the Florida collection site suggest that crabs also prey on flame scallop populations. Differences in the Florida sex ratio from those previously published could be explained by sampling biases such as camouflage of shells and easier detection of the larger animals predation of juveniles or because the sandy substrate was obscured by layers of Cassiopeia jellyfish during the summer months. Mean shell heights were highly variable within sample months but did not show great changes between months, with the exception of July 1998, which was significantly different from all other months. This may be explained by a small sample size due to poor visibility during collection and massive mortalities during transport.

Mean SH in June 1999, though not significantly different, was smaller than those from other collection months in that year. The presence of many small animals in one collection period may suggest that a synchronous spawning event occurred previously, and their presence throughout the study may indicate that continuous spawning is a reproductive strategy in the population.

This study suggests that gonad color (GC) may be a reliable indicator of the sex of flame scallops. Strong relationships between histologically confirmed sex and purple or cream gonad colors allow easy in vivo identification of the sex of individuals. There was no clear indicator for Ctenoides scaber in sexual transition. Strathmann (1987) said that there is little gross morphologic indication of sexual dimorphism in bivalves; however, the data reported in this study show that GC could be used to differentiate sexes in flame scallop individuals. Because the gonads are visible when the flame scallops are feeding, sex can be determined without sacrificing or greatly stressing the animals, which would be useful in mariculture applications.

The reproductive cycle of Ctenoides scaber in Florida is complex, This study indicates that environmental conditions and latitudinal influences may regulate the timing of reproduction and that a combination of reproductive strategies, including continuous reproduction, partial spawns, massive synchronous spawning events, and hermaphroditism may be used to ensure reproductive success. More life history studies are needed to further explore the effects these factors have on the reproductive cycle. In addition, further investigation of food availability, composition, and preferences; age and growth; recruitment; and fecundity would help reveal what effects these factors may have on reproductive variability in flame scallops throughout the species' range. Such information is needed for resource managers to effectively ensure a sustainable population that could support recreational and commercial fisheries. Gomez et al. (1990) reported that C. scaber could be a commercially important small-scale fishery in the Caribbean basin but that difficulties in harvesting in the coral and rock habitats make it unprofitable. Flame scallops also have a high meat-to-shell ratio as compared with other bivalves, which makes it a potentially profitable species for mariculture (Gomez et al. 1990). There will not likely be a demand for this food source in the United States principally because of aesthetic reasons. It is important to understand the reproductive cycle of flame scallops because of their importance to the marine aquarium industry and their potential as a food source for humans. Basic information will allow for proper management of the wild population and provide a basis for mariculture, which may ameliorate the effects of over-harvesting and habitat degradation by supporting stock enhancement programs and providing an alternate source of stock for the commercial trade.

ACKNOWLEDGMENTS

The authors thank Jim Holmes, Melanie Parker, Sarah Peters, Lisa Hallock, Libby Tyner, Wendy Ettish and Gary Gilliland for field support; Candice Way and Chris Canning for laboratory and technical support; Ruth Reese, Ann Forstchen, Judy Leiby, and Jim Quinn for editorial comments. This work was supported by funds from The Ayelsworth Foundation, The Old Salts Fishing Club, The Sanibel Shell Club, and Sharron Fuller (president: Sturdevant National Bank).

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ANGELA K. DUKEMAN, (1,2) NORMAN J. BLAKE (1) * AND WILLIAM S. ARNOLD (2) (1) College of Marine Science, University of South Florida, 140 7th Avenue S, St. Petersburg, Florida 33701; (2) Florida Fish and Wildlife Conservation Commission, 100 8th Avenue SE, St. Petersburg, Florida 33701

* Corresponding author. E-mail: nblake@marine.usf.edu
TABLE 1. Qualitative descriptions of Ctenoides scaber gonads.

Description Male Female

Undifferentiated No gametes No gametes
 Follicles small Follicles small
 No lumen No lumen

Early Growth Narrow band of large Lumen devoid of cells
 cells Young oocytes with
 Spermatogonia/ small nuclei attached
 spermatocytes to follicle periphery
 No spermatids or
 spermatozoa
 Lumen large/no cells

Late Growth Wide band of large
 cells
 Spermatogonia/ Oocytes large,
 spermatocytes elongate, some
 Lumen non-existent attached
 Small pink streaks Several mature oocytes
 Smaller spermatozoa near Lumen incompletely
 center filled

Ripe Full of spermatocytes, Many large oocytes
 spermatids, and Lumen is filled
 spermatozoa Few still attached
 Difficult to
 differentiate cell
 types
 Follicles stained black
 to dark purple

Partially Spawned Follicles with clear Most oocytes mature
 lumen Large nuclei
 Surrounded by clusters Oocytes unattached to
 of spermatozoa follicle
 Many follicles with few
 or no mature oocytes

Spent Follicles empty Follicles mostly empty
 Large lumen space Few oocytes
 Few spermatozoan cells Blood cells present
 Blood cells present Gonads smaller
 Gonads smaller Cytolysis (darkly
 stained bodies with
 obscure nuclei)

TABLE 2.
Statistical analyses of female gonad parameters. Monthly parameter
data were analyzed using Kruskall-Wallis ANOVA on Ranks.
Significantly different months were determined by Dunn's Test.

 Statistically Months with
 Significant Statistically
 Difference Similar
Gonad Parameter Calculated Maximum Values

Oocyte Diameter Yes August 98
 August 99
 September 99

Oocyte Area Yes August 98
 September 99

Follicle Area Yes January 98
 June 98
 May 99

Oocyte Density Yes February 99
 (inversely related March 99
 to other gonad
 parameters)

 Months
 Months with Significantly
 Statistically Different
 Similar from All
Gonad Parameter Minimum Values Other Months

Oocyte Diameter February 98 December 98
 October 98
 November 98
 February 99

Oocyte Area January 98 November 98
 February 98 December 98
 October 98
 February 99

Follicle Area October 98 None
 November 98
 December 98

Oocyte Density August 98 None
 (inversely related November 98
 to other gonad August 99
 parameters) September 99

Figure 9. Comparison of observed gonad colors (GC) in whole animals
to sex determined by histologic examination of gonad tissues. Total
number in each group is indicated.

Number of Flame Scallops

Field Color Cream Purple Gray Tan Clear Brown

In Sexual Transition 5 3 1 2 1 2
Females 4 172 3 14 0 1
Males 97 4 4 14 5 0
Undifferentiated 0 0 0 1 0 0

Note: Table made from bar graph.
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Author:Arnold, William S.
Publication:Journal of Shellfish Research
Geographic Code:1U5FL
Date:Aug 1, 2005
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