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Prospective culture of the Cortez oyster Crassostrea corteziensis from northwestern Mexico: growth, gametogenic activity, and condition index.

ABSTRACT This study examined growth, gametogenic activity, condition index, as well as the relationship of the life cycle to environmental parameters of the Cortez oyster Crassostrea corteziensis, which was cultured for 25 mo in the lagoon of Las Guasimas (Sonora, Mexico). We used oocyte diameter and cytological characteristics of the gonad to determine reproductive stages in females and males. The condition index was used to describe the oyster's physiological health. Temperature, salinity, seston, and chlorophyll a, b, and c were recorded at the study site. The Cortez oyster had isometric shell growth, reaching 103.2 [+ or -] 1.82 mm height and 150.3 + 4.98 g total weight. Data were adjusted to the von Bertalanffy growth equation ([L.sub.[infinity]] = 132.2 mm and K = 1.08 [y.sup.-1]), and survival was about 70%. This native species exhibited a distinctive gametogenic cycle, with the beginning and end of the cycle controlled by seawater temperature fluctuation (15-33[degrees]C), which once started, is continuous over a 9-mo period (March to November). Elevated temperature (>25[degrees]C) produced high gametogenic activity, exhibiting primary, growing, and mature oocytes, and partial spawning in April, September, and November. The peak spawning event occurred in August, when seawater reached peak temperatures of 31[degrees]C to 33[degrees]C, which was followed by a significant reduction of the condition index. During winter, storage of nutrients took place, and this appears to be used in the following season for gametogenesis. In general, the condition index was high throughout the study period. Energy for growth and reproduction came from phytoplankton blooms in summer and high concentration throughout the year of nonchlorophyll particulate organic matter. Observations show that this oyster is a protandrous species. High survival, elevated yields, and a long, continuous gametogenic cycle indicate that C. corteziensis has importance in aquaculture in Gulf of California.

KEY WORDS: Crassostrea corteziensis, oyster, growth, gametogenesis, oocyte size, condition index, yon Bertalanffy

INTRODUCTION

Currently, bivalve aquaculture in northwestern Mexico is based on the cultivation of the introduced Pacific oyster Crassostrea gigas, with production of 2,900 tons in 2003 (SAGARPA 2003). However, serious loses have been reported by producers at the culture sites in 1997. Massive die-offs have been recorded each year in several areas and time intervals, affecting spat, juveniles, and adults. Producers demand solutions to this widespread problem or alternatives that use other bivalves. However, there is limited information on the causes of massive die-offs in this area and no measures or remedies have emerged to reduce this serious loss. Concerning other bivalve species, there is limited ecological and biological information, but previous studies of the native oyster Crassostrea corteziensis (Hertlein 1951) suggested that cultivation of this species in the coastal lagoons had potential (Sevilla 1959, Stuardo et al. 1973, Stuardo & Martinez 1975). The native species may represent an alternative to balance the losses of C. gigas farms, but more studies on the biology of C. corteziensis are essential for implementing aquaculture activities.

Crassostrea corteziensis is distributed from the Gulf of California to Peru (Fisher et al. 1995) and is usually associated with the roots of red mangrove (Rhizophora mangle) (Paez-Osuna et al. 1993). Extraction of the Cortez oyster peaked in 1970 on the Pacific coast of Mexico (Cuevas-Guevara & Martinez-Guerrero 1979). However, intensive exploitation and reduction of freshwater into lagoons resulted in severe reduction of natural beds and near-disappearance of the species in northwestern Mexico. Most of the studies of this species have focused on describing occurrence and seasonal variation of trace and heavy metals and biochemical composition of oysters (Osuna-Lopez et al. 1990, Paez-Osuna et al. 1993, Osuna-Lopez et al. 1999, Rivero-Rodriguez et al. 2007). Given the problems occurring with the introduced species, C. gigas, there is increasing interest in the commercial potential of farming the native species.

Natural spat collection of C. corteziensis is not possible; therefore, hatchery production is the only feasible approach for supplying juveniles. Our center (CIBNOR) produces spat of the Cortez oyster under controlled conditions (Mazon-Suastegui et al. 2002). More recently, juvenile oysters were raised in an experimental culture area in the State of Sonora, using plastic containers suspended from long-lines (Chavez-Villalba et al. 2005). In this study, we report data of growth rates and survival of the Cortez oyster. However, information about the gametogenic cycle of the species is still limited. Whereas contributions to the study of reproduction have been made (Cuevas-Guevara & Martinez-Guerrero 1979, Ruiz-Dura 1980, Frias-Espericueta et al. 1997) to determine the aquaculture potential of C. corteziensis, it is necessary to have a more complete understanding of its reproductive biology and life history. Sustainable aquaculture relies on the timing of gametogenic development and spawning events so potential broodstock can be collected at the appropriate time (Aragon-Noriega et al. 2007). We need detailed knowledge of the reproduction process, condition indices, growth rates, and basic environmental conditions. For instance, there are no reports concerning the variations of the condition index through an annual cycle, with the exception of a gonad index determined by Frias-Espericueta et al. (1999).

This study was designed to determine the aquaculture potential of Crassostrea corteziensis in a coastal lagoon of Sonora, Mexico by documenting growth and survival of the Cortez oysters in a suspension system, measure gametogenic activity and variations in its condition index, and determine how environmental parameters affect growth and reproduction of this oyster.

MATERIALS AND METHODS

Spat Production

A batch of 200 adult oysters (80-100 mm) was collected in Bahia Ceuta, Sinaloa. The specimens were placed in thermal-insulated containers and transported by airplane to facilities at CIBNOR in La Paz, B.C.S. Broodstock management, spawning, larval culture, setting of eyed larvae, and nursery procedures were performed following methods described in previous studies (Mazon-Suastegui et al. 2002, Chavez-Villalba et al. 2005). When the spat reached an average length of 2-3 mm, approximately two months after fertilization, about 5,000 spat (height 2.66 [+ or -] 0.1 mm; n = 30) was taken from the growing tanks and transported from La Paz to Guaymas to initiate experimental cultivation.

Culture

The cultivation experiment was carried out in a lagoon (27[degrees]33'N, 110[degrees]38.5'W) adjacent to Bahia Guasimas, located about 40 km southeast of Guaymas, Sonora (Fig. 1). The experiment was performed with assistance of personnel at the Palapas de Belem Cooperative that cultures C. gigas. The same practices and maintenance activities used for the Pacific oyster were used for raising the Cortez oyster. The standard practice is to place spat in 2-mm mesh plastic bags (~1,000 juveniles per bag) on plastic trays attached to a long-line. Juveniles (30 mm height) were placed directly on the plastic trays. Maintenance is performed each month by cleaning or replacing trays and reducing the density to 60-80 oysters per tray when they reach ~80 mm height. Empty shells were recovered and counted at each sampling to estimate mortality.

[FIGURE 1 OMITTED]

Sampling

Samples of 30 oysters were taken each month throughout the 25-mo experiment, starting in July 2003 and ending in September 2005. No samples were collected in June and October 2004. Specimens were transported to the laboratory for cleaning and measuring height, length, width, and dry weight. Three principal dimension complexes of oyster valves (Carriker 1996); height, distance between umbones, and posterior margins of the valves; length, maximal distance between ventral and dorsal margins parallel to the hinge axis; and width, maximal distance between the outside surface of closed valves measured at right angles to the plane of closure of the valves. Only height was measured in July, the beginning of the experiment; all other dimensions were recorded monthly from August 2003 to the end of the study. After recording these data, the oysters were opened. The tissues and shells of 10 specimens were used to calculate the condition index (CI) described by Walne & Mann (1975). The soft tissues were dried in an oven for 48 h at 80[degrees]C and dry weight then determined. The CI was calculated as: CI = (P1 x 1,000)/P2, where P1 is the dry weight of soft tissue (g) and P2 is the dry weight of the shell (g). Measurements of total weight and estimates of CI started in October 2003. Another 10 oysters were used for histological studies of their gonads.

Semi-Quantitative Histology

A 1-[cm.sup.3] section of the visceral mass above the pericardium was fixed in Davidson's solution for 48 h (Howard & Smith 1983). Samples were then placed in 70% alcohol where they were stored. For dehydration, samples were passed through a series of increasing ethanol concentrations, cleared in xylene, and then embedded in paraffin, following standard histological techniques (Howard and Smith, 1983). Sections (~5-6 [micro]m) were mounted on glass slides and stained with Harris hematoxylin and eosine Y/floxine B procedure. The histological preparations were examined using an optical microscope (Zeiss) connected to a digital camera (Canon PowerShot G5). For female specimens, 5-10 photos were taken on a random basis to record at least 100 oocytes from each specimen. Sigma Scan Pro 5.0 software was used for image analysis, and a calibration of the program used a microruler of 1,000 [micro]m mounted on a slide before measuring the oocytes. After calibration, measuring methods were established, based on the description by Lango-Reynoso et al. (2000). The surface of each oocyte that presented a well-defined germinal vesicle was measured by drawing its perimeter on the computer screen to calculate an area (in pixels) that was transformed into a theoretical diameter (in [micro]m), using the relationship: [D.sub.theoretical] = [square root of (4S/[pi])] (Lango-Reynoso et al. 2000).

To assess the reproductive phase of female Cortez oysters, we used the classification used for C. gigas (Lango-Reynoso et al. 2000), which is based on oocyte diameter and cytological features of the gonad (Table 1). For males, we used the classification of Chavez-Villalba et al. (2002), which is based on the percentage of spermatids and sperm in the follicles (Table 2). Gonads in undifferentiated oysters were mostly connective tissue without sexual cells.

Environmental Parameters

Seawater surface temperature and salinity were recorded at each sampling event with a laboratory thermometer and refractometer. At the same time, 4 L seawater was collected to measure concentrations of chlorophyll a, b, and c, and seston. The concentration of chlorophyll was determined by the method described by Contreras-Espinosa (1984). In brief, one liter of seawater was passed through A/E Gelman filters. The filters were placed in conical tubes where they were crushed with 10-mL 90% acetone, the conical tubes were covered with aluminum foil and stored in the dark at 4[degrees]C for 24 h; samples were centrifuged at 1,300g for 10 min; spectrophotometric readings were made at 630, 647, 664, and 750 nm. For seston determinations, we used the technique described in Chavez-Villalba et al. (2005). Two liters of seawater is passed through 4.7-cm diameter GF/C Whatman filters. The filters with samples were placed in an oven at 80[degrees]C for 24 h, then weighed, and then placed in a muffle furnace at 450[degrees]C for 4 h. The filters were weighed again to obtain the organic seston as the difference of the previous weight, so that the total seston was the sum of the inorganic seston and the organic seston.

Data Analysis

Shell measurements (height, length, and width) and weight of oysters were used to determine isometric and allometric relationships among variables. For isometric relationships, we used linear regression tests to obtain descriptive equations; allometric growth was estimated using potential regression. In both cases, goodness-of-fit was described by the [r.sup.2] correlation coefficient (Sokal & Rohlf 1969). The nonparametric test of Kruskal-Wallis was used to determine differences in the condition index. Statistical significance was set at P < 0.05.

Daily growth rate (height; in mm) was calculated as:

DWR = ([t.sub.1] - [t.sub.0])/d,

where [t.sub.1] = height at time 1, [t.sub.0] = height at time 0, and d = day. Growth was adjusted to the von Bertalanffy model, with height as the variable (Pauly 1987):

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII],

where [H.sub.[infinity]] is the asymptotic height (mm), K is the growth constant per year, t is the age (in years) and to is the age at zero height. The parameters of the model were calculated using the FAO-ICLARM Stock Assessment Tools software (FiSAT; Gayanilo et al. 1995).

[FIGURE 2 OMITTED]

RESULTS

Environmental Parameters

Similar patterns were observed in the concentrations of chlorophyll a, b, and c (Fig. 2). In 2005, peaks occurred (in [micro]g [L.sup.-1]) in July (a = 28.8, b = 47.5, and c = 55.1) and August (a = 21.3, b = 35.3, and c = 40.9). Low concentrations occurred in spring 2004 and 2005, but also in July 2003 and March, June, and September 2005; concentrations in these months were lower than 0.3 [micro]g [L.sup.-1]. Particulate inorganic material (PIM) was higher than particulate organic material (POM) at most samplings and both followed a similar changing pattern at different scales; varying slightly at a low concentration prior to February 2004 and present at a high concentration after July 2004, except in March, April, and May 2004 when PIM was lower than POM (Fig. 2). Highest concentration of PIM (298 mg [L.sup.-1]) and POM (62 mg [L.sup.-1]) occurred in July 2004 and the lowest PIM occurred in April 2004 (0.5 mg [L.sup.-1]) and the lowest POM in December 2003 (7 mg [L.sup.-l]). Temperature patterns were similar on an annual basis, with highest temperature in July 2003 (33[degrees]C), August 2004 (33[degrees]C), and August 2005 (30.5[degrees]C) and the lowest in December 2003 (15[degrees]C) and December 2004 (16[degrees]C) (Fig. 2). A clear pattern in salinity was not evident, with highest salinity of 42 in December 2004 and April to May 2004 and lowest salinity of 33 in September 2004 (Fig. 2).

Growth

Growth of oysters after 25 mo of cultivation was: height = 103.2 [+ or -] 1.82 mm, length = 63.4 [+ or -] 0.74 mm, width = 31.9 [+ or -] 0.78 mm and 150.3 [+ or -] 4.98 g total weight (Fig. 3). Isometric and allometric growth relationships are shown in Table 2. The daily growth rate (height) was 0.218 mm during the first year and 0.127 mm over the entire experiment. Analysis of height used von Bertalanffy growth model. The results for the model were; [H.sub.[infinity]] = 132.2 mm (height); K = 1.08 [y.sup.-1], and [t.sub.0] = -0.18. The growth model, using height (H), is H = 132.2 {1 - [e.sup.[-108 (t+0.18)]]}. Finally, survival at the end of the experiment averaged more than 70% and no massive die-offs occurred during the study period.

Reproduction

From histological preparations, we confirmed the four reproductive stages (early gametogenesis, growing, mature, and degenerating) (Fig. 4A, B, C, and D) for female oysters described by Lango-Reynoso et al. (2000) and found cytological features of hermaphrodite oysters (Fig. 4E). We confirmed the three stages (early gametogenesis, growing, and mature) for male oysters (Fig. 4F, G, and H) described by Chavez-Villalba et al. (2002).

Assessment of reproductive activity started in October 2003 on very young oysters (6 mo old). The annual gametogenic cycle began in March 2004 and April 2005 with high activity until November in both years (Fig. 5). Elevated proportions of vitellogenic oocytes (70-83.2%) were detected from May through November 2004 and from July through September 2005 (62.5-77.2%). Maximum reproductive activity (seasonal peaks, defined by percent of mature oocytes) occurred in October 2003 (66%), April 2004 (66%), and June 2005 (61.3%). Although degenerating oocytes were uncommon in the histological slides, these provided evidence of partial spawning in November 2003 and April, August, and September 2004. Higher proportions of mature males were observed from March through December 2004, reaching 100% of the examined specimens in July and August 2004 (Fig. 5). In 2005, high proportions of males in the growing stage occurred from March through May and September with a peak of mature oysters (75%) in July.

[FIGURE 3 OMITTED]

By measuring oocyte diameter, gametogenesis began in March 2004 and April 2005 with growing oocytes measuring 24.9 [+ or -] 8.5 [micro]m and 20.6 [+ or -] 11.4 [micro]m, respectively (Fig. 6). Growing stage prevailed from May to November 2004 and May to September 2005. Significant declines in oocyte diameter from October to November in 2003 and from April to May in 2004 and 2005 indicated the presence of spawning events. The end of the gametogenesis cycle was clearly identified by oocytes in early gametogenesis in December 2004 and no females in December 2005. Although linear regression analysis showed [R.sup.2] = 0.39, oocyte diameter was related (P < 0.05) to seawater temperature. During the study, oocytes ranged from 2.5-46.1 [micro]m.

Condition Index

Values derived from the Walne-Mann condition index (CI) are shown as three curves with higher values in December 2003 (66.7%), April 2004 (69.4%), and June 2005 (72%) (Fig. 6). Significant reduction (P < 0.05) of CI occurred from July through August in 2004 and 2005 and lowest CI occurred in September, evidence of a major spawning event. Nevertheless, the other spawning periods, detected by histological observations, did not reflect significant changes in CI.

Sex Ratio Related to Size

Of the oysters specimens we observed histologically, 50.9% were females, 35% were males, 12.7% were undifferentiated, and 1.4% were hermaphrodites. Frequency distribution based on size classes of females, males, hermaphrodites, and undifferentiated oysters showed that females were most abundant (67.5-90.5%) in the middle size classes (70-80 mm) and less abundant in the small and large size classes (Fig. 7). Males were present in higher proportions in the small (70%) and largest size classes (50%) and less in the middle size class (9.5%; 70-75 mm). When oysters grew larger than 95 mm in height, their sexual ratio became close to equal. No oysters were found to determine sex ratio in the 85-90 mm size class. Mature males were found in oysters six months old (45-50 mm), indicating that gonads became functional in young, small specimens.

DISCUSSION

Environmental Parameters

Research has demonstrated that growth in bivalves is influenced by variations in the quantity of the seston (Toro et al. 1999). The concentration of POM was relatively constant throughout the experiment, but seston was less concentrated from July 2003 to April 2004, compared with May 2004 to the end of the study in 2005. Changes in seston load were not related to significant variations in shell growth. However, a significant increase in total weight was detected during the change from low to high concentrations of seston in May 2004. Paterson et al. (2003) demonstrated that POM is a controlling factor in the growth of the Sydney rock oyster Saccostrea glomerata. The oysters in our study were cultivated in parallel with other batch of oysters in a different lagoon (Chavez-Villalba et al. 2005). In the lagoon at Las Guasimas, weight gain after cultivation for 13 mo reached 59.9 g under average POM concentrations of 31 mg [1.sup.-1]; weight gain at the other location was 30.1 g under average POM concentrations of 9.7 mg [1.sup.-1]. This suggests that the concentration of POM influences weight gain, but ecophysiological experiments are needed to confirm this. We believe that Cortez oysters adjust their feeding behavior to different food conditions and exploit POM under great variations in PIM.

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[FIGURE 5 OMITTED]

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[FIGURE 7 OMITTED]

In coastal habitats, POM consists of bacteria, detritus, nanozooplankton, but phytoplankton is the main source of nutrition for bivalve filter feeders (Dame 1996). Phytoplankton biomass at Las Guasimas, expressed as chlorophyll a concentration, increased during spring and the highest values occurred during the summers of 2003, 2004, and 2005. The range observed in this study coincided with the annual cycle of chlorophyll reported by Arreola-Lizarraga (2003) for this same coastal lagoon. Normally, seasonal abundance of phytoplankton (chlorophyll a) is strongly related to temperature (Toro 1996). This was the case in Las Guasimas, where phytoplankton blooms occurred during the summer and low concentrations of microalgae were associated with low temperatures during winter. Moreover, high chlorophyll levels in summer seem to be fueled by additional nutrients coming from freshwater runoff from summer rainstorms and shrimp farming activities within the lagoon. More nutrients from phytoplankton and algae have been associated with aquaculture activities (Toro et al. 1999). Similarly, Castillo-Duran (2007) found a significant increase of nutrients during farm operations from April to October. In terms of potentialities for oyster aquaculture in this coastal lagoon, the author reported a succession of phytoplankton communities during summer and winter associated with changes in the water masses; for example, summer was characterized by 68% diatoms (Coscinodiscus concinnus, Lioloma delicatulum, and Paralia sulfata) with a diversity index of H' = 6356 bits [cell.sup.-1] and winter by 44% diatoms (Actinocyclus curvatulus, Paralia sulfata, and Thalassionema nitzschioides nitzschiodes) with a diversity index of H' = 1,686 bits [cell.sup.-1].

Growth and Mortality

The oyster industry in northwestern Mexico is based on the production of Crassostrea gigas. Some experimental cultivation has been done with C. corteziensis, but the results are not available and information comes from personal communications. Recently, agencies within the State of Sonora supported studies of growth of the native oyster in different locations in the state. Unfortunately, the results of these experiments are not published, but we collected information from reports to compare our results with these findings. These unpublished reports showed daily growth from 0.222-0.253 mm over a period of 7-10 mo of cultivation in lagoons with typical marine conditions. Higher growth rates were detected (0.304 mm) in experiments carried out in discharge channels of shrimp farms with hyposaline water of ~25. Growth rates in marine locations were similar to results obtained here, when adjusting for the length of time (0.251 mm for 10 mo). In general, growth rates of the Cortez oyster are lower than for the Pacific oyster at marketable size (>80 mm or >60 g) in 7-10 mo of cultivation. Geographically, growth rate of C. gigas diminishes in southern locations (Ramirez-Filippini et al. 1990) and has slower growth than specimens described in our study. The authors obtained growth curves of suspension and bottom cultures of C. gigas oysters using von Bertalanffy-growth-function with values of [L.sub.[infinity]] (60.7 and 78.9, respectively) and K (0.0078 and 0.0057, respectively), which were lower than values we obtained with the Cortez oyster: [L.sub.[infinity]] = 132.25 mm and K = 1.08 [y.sup.-1]. In a previous study, we reported the data derived from the von Bertalanffy equation ([L.sub.[infinity]] = 114 mm and K = 1.1 [y.sup.-1]) obtained from 13 mo of cultivation of C. corteziensis at Laguna El Soldado (Chavez-Villalba et al. 2005). Growth values at Las Guasimas fitted the model we proposed earlier; we obtained a similar value for K, but the calculated [L.sub.[infinity]] was higher because the data came from a two-year experiment, where [L.sub.max] = 135 mm. We believe the model is useful for oystermen in predicting growth of Cortez oysters.

Since 1998, massive die-offs of C. gigas have regularly occurred around the end of October, March, and April at farms in northwestern Mexico. No massive die-offs occurred at Las Guasimas during the study period. Over the course of this study, survival was ~70% and was similar to survival rates obtained in the study of C. corteziensis at El Soldado, where a massive die-off occurred (Chavez-Villalba et al. 2005). Survival of the Cortez oyster at Las Guasimas was similar to reports of experimental cultures of the Pacific oyster (Ochoa-Araiza & Fimbres-Pena 1984, Ramirez-Filippini et al. 1990). However, it is essential to estimate survival rates of the native Cortez oyster at larger scales to anticipate the impacts on commercial operations.

Reproduction

Gametogenesis of the Cortez oyster involves a cycle that begins in March-April and ends in November, with temperature as the major factor affecting reproduction. Initiation and extent of gametogenesis were related to the high annual temperature variations of 15[degrees]C to 33[degrees]C. Wide seasonal fluctuations in these coastal lagoons is from water masses from the lower Gulf province (Arreola-Lizarraga 2003). The rapid change from low to high temperature activates gametogenesis and induces oocytes to pass rapidly from the early stage to the growth and maturity phase at the beginning of the cycle. This same pattern was observed at the start of reproduction of C. gigas in other coastal lagoon in this region (Chavez-Villalba et al. 2007). The presence of different oocyte phases at the same time indicated a polymodal oocyte distribution in the Pacific oyster during periods when conditions for spawning are favorable (Lango-Reynoso et al. 2006). This pattern was present during the entire gametogenic cycle of the Cortez oyster under the influence of long-term high temperatures of [approximately equal to] 25[degrees]C. This situation produced high oocyte growth rates and generated continuous production of primary oocytes, rapid oocyte growth, and accumulation of ripe oocyte before spawning. Evidence of partial spawning in the histological slides was detected in April, August, September, and November 2004, which coincides with other reports of partial spawning in C. corteziensis (Cuevas-Guevara & Martinez-Guerrero 1979, Ruiz-Dura 1980). The significant reduction of the condition index from July to August in 2004 and 2005 suggests that massive spawning occurs when temperature reached a peak. Temperature started to fall in September, but growing, mature, and reabsorbed oocytes were still present until November in 2003 and 2004. No oocyte in these phases occurred with minimum temperatures from December, which indicated the end of the gametogenic cycle, characterized by a short and rapid process of gamete reabsorption inside the gonad.

Temperature and food supply are the most influential factors on initiation and duration of the reproduction cycles of bivalves (Dinamani 1987, Ruiz et al. 1992), so gametogenesis in many tropical bivalves is normally continuous because temperature and food supply vary little during the year (Urban 2000). Among temperate species, where temperature and seston vary seasonally, gametogenesis is a cyclic pattern (Fabioux et al. 2005). The cycle in C. corteziensis is as a combination of these two patterns; the beginning and the end of the cycle is related to increasing and decreasing temperatures, and once initiated, it is continuous over nine months with several spawning periods. The timing and amplitude of the cycle correlates with seawater temperature, with annual variations based on the quality and quantity of the food supply. Energy required for gametogenesis comes from two sources, phytoplankton and nonchlorophyll-related seston. No correlation between POM and chlorophyll a suggests that when phytoplankton is low, POM is composed of other constituents (protozoa, bacteria, zooplankton, detritus, etc.). Oysters use the organic components of these constituents.

Concentrations of POM in winter were sufficient for oysters to increase energy reserves. In the absence of sexual activity during the winter of 2003 and 2004, the condition index indicates accumulation of energy and specific nutrients that will be used for initiation of the gametogenic cycle. These results indicate that nutrient accumulation over the winter is as important in the reproduction of the Cortez oyster as in other species (Ren et al. 2003). Berthelin et al. (2000) found that reserves in C. gigas accumulate during the autumn-winter and are used later for gametogenesis. Also, Chavez-Villalba et al. (2007) found the same pattern of reproduction in this same species in other coastal lagoons in this region. In general, the Cortez oyster maintained high CI throughout the study; with the exception of February and March, CI averaged 10% higher than the CI of the Pacific oyster during one year of cultivation at Laguna El Soldado (Chavez-Villalba et al. 2007). This is relevant information for future commercialization of this species.

Gamete development in terms of oocyte diameters confirmed the significant relationship of gametogenesis with temperature; large oocytes were found during periods of rising temperatures, whereas primary cells were associated with low temperatures. Ren et al. (2003) found that oocyte diameter in C. gigas was directly related to surface seawater temperature. The size of oocytes have been used to describe reproduction of C. corteziensis, but the method was based on two categories, small (maturing) or large (>50 [micro]m.) spawning oocytes (Ruiz-Dura 1980). The maximum diameter in our Cortez oysters was 46 [micro]m; we suspect that differences in cell size are related to the methods used to assess phases of gametogenesis. Nevertheless, oocyte diameter is a good quantitative descriptor of reproductive development in females.

The sex of any individual within a population is partly a function of size, which in most cases is linked to age (Deslous-Paoli & Heral 1988). In the Cortez oyster, males predominated until the oysters reached 50-55 mm height, which corresponds to an age of six month; after which, females are more abundant. Small numbers of hermaphrodites were observed before the peak in females, which occurred at 70-75 mm, but also were present in two larger size classes (75-80 and 95-100 mm). These results are similar to the proportion of each sex at each growth interval as in the Pacific oyster, where juveniles usually mature as males and change into females later in life (Baghurst & Mitchell 2002). Hermaphrodites represent an intermediate stage from male to female in the Pacific oyster (Lango-Reynoso et al. 2006); the proportions at that stage (0.35% to 1.7%) (Mann 1979, Paniagua-Chavez & Acosta Ruiz 1995, Steele 1998) are similar to our results (1.5%). These observations suggest that the Cortez oyster is a protandric, dioecious species with functional hermaphroditism.

CONCLUSION

Experiments in cultivation of the native Cortez oyster were characterized by high survival and similar or better weight gain than the Pacific oyster. Growth rates indicated that marketable size could be reached in 18 mo, which would necessitate new cultivation programs for the native species. Resistance to massive die-off events would compensate for longer grow-out.

The duration of gametogenesis activity determines the availability of spat during the year, an essential factor for the success of a developing aquaculture (Urban 2000). With a continuous gametogenic cycle over nine months, hatchery production of larvae and spat would probably occur for most of the year. However, better yields of early stages would be anticipated for August and September. This study demonstrated that the native Cortez oyster is an excellent alternative for diversifying and improving aquaculture activities in parts of the Gulf of California.

ACKNOWLEDGMENTS

The authors thank CIBNOR technicians David Urias, and Edgar Alcantara for laboratory and field assistance. This research was supported by the International Foundation for Science, Stockholm, Sweden with a grant to Jorge Chavez-Villalba and by SAGARPA-CONACYT 2003/002-061 and CIBNOR AC 4.1 projects.

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JORGE CHAVEZ-VILLALBA, (1) * ANDRES HERNANDEZ-IBARRA, (1) MARIA R. LOPEZ-TAPIA (1) AND JOSE M. MAZON-SUASTEGUI (2)

(1) Centro de Investigaciones Biologicas del Noroeste (CIBNOR), Unidad Sonora, Apdo. Postal 349, Guaymas, Sonora 85454, Mexico; (2) Centro de Investigaciones Biologicas del Noroeste (CIBNOR), Mar Bermejo 195, Col. Playa de Santa Rita, La Paz, BCS 23090, Mexico

* Corresponding author. E-mail: jechavez04@cibnor.mx
TABLE 1.
Reproductive classification used for Crassostrea gigas to describe the
reproductive stages of C. corteziensis. Females were classified by
oocyte diameter (Lango-Reynoso et al. 2000) and males by cytologic
characteristics of the gonad (Chavez-Villalba et al. 2002).

 Stage
 Interval
Female Stages ([micro]m) Histological Description

Early gametogenesis 3.0-12.0 Follicles are elongated and often
 isolated in abundant connective
 tissue with walls consisting
 of primary oocytes of homogeneous
 size.
Growing 12.1-30.0 Start of oocyte growth. Large range
 in oocyte size at all gametogenic
 stages can be observed, including
 some free oocytes. Interfollicular
 connective tissue disappears.
Mature 30.1-41.0 Follicles of relatively homogeneous
 size completely filled with mature
 oocytes with distinct nucleus.
Degenerating 41.1-60.0 Follicles containing degenerating
 oocytes, often elongated in shape,
 sometimes broken. Obvious
 redevelopment indicated by
 increased number of primary
 oocytes.

Male stages
 Early Abundant connective tissue
 gametogenesis containing elongated follicles
 with walls consisting of germinal
 epithelium with some spermatogonia
 and spermatocytes
 Growing Connective tissue is reduced and
 follicles become larger; normal
 sequences of spermatogenesis are
 observable with spermatocytes I
 and II, spermatids and some
 spermatozoids are organized in the
 lumen
 Mature Connective tissue almost
 disappeared. Follicles filled
 with packages of spermatozoids
 oriented with tails toward
 the follicle lumen
Undifferentiated Abundant connective tissue with
 oysters no follicles. Follicles, when
 present, small and isolated
 with no detectable presence
 of sexual cells.

TABLE 2.
Isometric and allometric growth relationships of Crassostrea
corteziensis.

Relationship Equation n CC *

Height--Length y = 0.6048x + 7.1121 666 0.940
Height--Width y = 0.3558x - 4.1851 666 0.891
Length--Width y = 1.4205x + 20.2131 666 0.882
Weight--Height y = 0.00007([x.sup.3,0953]) 606 0.921
Weight--Length y = 0.004([x.sup.2,3473]) 606 0.758
Weight--Width y = 1.9561([x.sup.-1.0212]) 606 0.721

Relationship [R.sup.2] F-Ratio P-Value

Height--Length 88.39 5056.98 0.0000
Height--Width 79.38 2557.54 0.0000
Length--Width 77.77 2323.21 0.0000
Weight--Height 84.77 3697.18 0.0000
Weight--Length 57.48 897.73 0.0000
Weight--Width 51.97 718.47 0.0000

* Correlation coefficient.
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Article Details
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Author:Chavez-Villalba, Jorge; Hernandez-Ibarra, Andres; Lopez-Tapia, Maria R.; Mazon-Suastegui, Jose M.
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:1MEX
Date:Aug 1, 2008
Words:6971
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