El Nino and La Nina effects on reproductive cycle of the pearl oyster Pinctada mazatlanica (Hanley, 1856) (Pteriidae) at Isla Espiritu Santo in the Gulf of California.

ABSTRACT The impact of El Nino (1997-1998) and La Nina (1998-1999) on the reproductive cycle of the pearl oyster Pinctada mazatlanica was studied by histologic observation of gonads, determination of the conditioning index, and oocyte monthly mean diameter, which are related to sea surface temperature and availability of food. Available food was determined by comparison between seasonal and a standard concentration of chlorophyll a. Oyster specimens were collected from Isla Espiritu Santo in the Gulf of California from May 1997 to November 1999. A direct relationship of spawning to temperature was observed from July to October. Concentrations of chlorophyll a were related to the stage of gonad development. The reproductive process was related to the conditioned index. Reproductive activity during El Nino was longer, with spawning in July to November 1997 and July to October 1998, and more intensive (in terms of population spawning frequency) than that during the La Nina event, when the spawning occurred during August to November 1999.

KEY WORDS: El Nino, La Nina, pearl oyster. Pinctada mazatlanica, reproduction

INTRODUCTION

The pearl oyster Pinctada mazatlanica is distributed from the west coast of the Baja California Peninsula south to Peru, including the southern part of the Gulf of California and islands around the Peninsula (Keen 1971, Martinez 1983). During the past century, the quality of the pearls produced by this species supported an important pearl fishery in the Gulf of California, which was the incentive for colonization of Baja California Sur (Carino & Caceres-Martinez 1990, Monteforte & Carino 1992). The fishery was closed by the Mexican government in 1938 because of overfishing (Keen 1971, Monteforte 1990, Sevilla 1969).

The pearl oyster P. mazatlanica is considered a potential and feasible resource to be developed by mariculture (Monteforte 1990). Thus, its reproductive biology is a relevant study subject. In Mexico, some studies have been performed on cultured specimens (Diaz 1972, Garcia-Gasca 1992, Gaytan et al. 1993, Saucedo-Lastra & Monteforte 1997) and on wild populations (Monteforte 1991, Moreno & Moreno 1994, Wrigth 1997). Studies of reproduction in wild populations from Bahia de La Paz were performed by Sevilla (1969) and Garcia-Dominguez et al. (1996); from Guaymas, Sonora, by Arizmendi-Castillo (1996); and from the Golfo de Nicoya, Costa Rica, by Solano-Lopez et al. (1997). In these works, there were no reported relationships and effects on reproduction in P. mazatlanica by El Nino and La Nina events. This study describes the effects on the reproductive cycle of P. mazatlanica through changes in sea surface temperature and availability of food due to the El Nino and La Nina climatic events.

MATERIALS AND METHODS

Specimens were collected monthly and randomly from May 1997 to November 1999 (except January 1999) in a wild population located near isla Espiritu Santo, B.C.S. (Fig. 1), from a depth of 4 to 6 m by personnel using scuba gear. A total of 523 organisms were collected, ranging from 20.4 to 228.3 mm shell length (mean, 119.7; SD, 27.6) and 21.2 to 167 mm shell height (mean, 113.9; SD, 23). Before dissection, the shell length and height were measured with calipers (0.01 mm resolution); subsequently, the wet weight was obtained by electronic scales (0.01 g resolution). The visceral mass (including the gonad) was fixed in a solution of 10% formalin prepared with seawater, dehydrated in an alcohol series dilution, and embedded in paraffin (Luna 1968). Sections, in a frontal and dorsal plane, 5- to 6-[micro]m thick, were made and stained with Harris hematoxylin and eosin (Luna 1968).

[FIGURE 1 OMITTED]

The diameter of at least 100 oocytes was measured using digitalized images from the histologic preparations (Sigma Scan Pro4 software program), in each of seven females per month selected randomly. The measurements were made along the longest axis in the oocytes sectioned through the nucleus containing clearly visible nucleoli. From this data, mean size and standard deviation were obtained. The specimens with few measurable oocytes and extensive phagocytosis were not considered, following the criteria of Grant and Tyler (1983a, 1983b).

Sex was determined by microscopic analysis, and the percentage of each sex was obtained. The sex ratio was determined and examined for deviation from the expected ratio of 1:1 by chi-square ([chi square]) analyses. Condition index (CI), using the formula proposed by Ricker (quoted by Bolger & Connolly 1989), was selected because it takes into account those cases in which growth is not isometric, as occurs in P. mazatlanica, and could describe in the best way the general condition variations and their relationship with the reproductive event:

CI = (PH/[L.sup.b]) x 1000

where CI was determined by dividing the visceral mass wet weight (PH) by the anteroposterior length (mm) and powered by b (value from the slope, which resulted from the power correlation from both variables). We obtained CI means for each monthly sampling.

Sea surface temperature (SST) values were obtained by Coastal Zone Color Scanner (CZCS) from NOAA and chlorophyll a concentrations from the SeaWiFS Project, NASA/Goddard Space Flight Center and ORBIMAGE. Anomalies were estimated as departures from the averaged monthly cycle; on this basis, we defined the periods influenced by El Nino (May 1997 to October 1998, positive anomalies) and by La Nina (November 1998 to November 1999, negative anomalies).

The condition of the gonad was determined by microscopic analysis. Each specimen was assigned a specific stage of gametogenic development. Stages were assigned on the basis of the classification described for P. mazatlanica by Sevilla (1969) and Garcia-Dominguez et al. (1996). This classification divides the gametogenic cycle into five stages: indifferentiated, developing, ripe, partially spawned, and spent. The relative frequency of each gonad phase was determined. The reproductive period was considered at spawning stage.

RESULTS

Gonad Developmental Stages

The microscopic anatomy from each gonad stage of P. mazatlanica did not differ from those described by Sevilla (1969), Garcia-Dominguez et al. (1996), and Saucedo-Lastra and Monteforte (1997).

Reproductive Cycle

The reproductive cycle is shown in Figure 2. We observed that during the El Nino, spawning occurred from July to November 1997 and July to October 1998 (maximum peaks in July to September 1997, and July and August 1998). This period was characterized by the constant appearance of gametogenic activity in developed and ripe stages and relatively poor inactive (indifferentiated stage). The population spawning frequency was 69% mean and 90% maximum. During the La Nina, spawning took place from August to October 1999 (maximum peaks on August to October), predominated by the developed stage and more presence of the inactive stage. The population spawning frequency was 45.6% mean and 70% maximum. In both periods, the spawn occurred between 27 and 30[degrees]C and was suspended at temperatures under 25[degrees]C.

[FIGURE 2 OMITTED]

Sex Ratio

Out of 523 specimens sampled, 250 (47.8%) were males, 205 (39.2%) were females, 12 (2.3%) were hermaphroditic, and 56 (10.8%) were undifferentiated. The sex ratio (1.22 male: 1 female) did not differ significantly (P < 0.05, n = 455) from an expected 1:1 ratio.

Analysis of Oocyte Size

Mean oocyte diameters are shown in Figure 3. Maxims were observed during May and June 1997, June 1998, and July 1999. From September to December 1998 and February to March 1999, there were specimens with few or no measurable oocytes. The highest mean oocyte diameter values during El Nino corresponded to the ripe stage (May to June 1997, and April to May 1998), and the lowest mean values corresponded to the spent stage (September to November 1997 and August to October 1998). This relationship did not occur during La Nina.

[FIGURE 3 OMITTED]

Condition Index

To validate the CI determination, the height and visceral weight variables were compared. Using a power correlation, we obtained a value of r = 0.88 and slope b = 2.77 (P < 0.05, n = 523). The CI values fluctuated between 8-16% and were related to the species reproductive stages, maximum values coinciding with the development stage, and the minimum values with the spawn stage (Fig. 4).

[FIGURE 4 OMITTED]

Temperature and Anomalies

During the study, the SST varied from 19 to 30.8[degrees]C. During El Nino, SSTs varied from 21.6 to 30.8[degrees]C, with a maximum anomaly of +2.82[degrees]C (January 1998), and during La Nina, from 19 to 28.2[degrees]C, with a maximum anomaly of -1.36[degrees]C (February 1999). The SSTs and anomalies are recorded in Figure 5.

[FIGURE 5 OMITTED]

The relationship between the SST and the relative frequency of spawning are shown in Figure 6. Spawning occurred between the 27 to 30[degrees]C interval and was suspended when colder than 25[degrees]C. During the El Nino, the highest percentage of population spawned coincided with the highest temperature recordings in August 1997 and August 1998; during La Nina spawning occurred in August 1999, while the highest temperature recorded was during September of 1999.

[FIGURE 6 OMITTED]

Photosynthetic Pigment Concentration

Chlorophyll a concentrations varied during El Nino from 0.096 to 1.2 mg/[m.sup.3] and during La Nina from 0.28 to 3.6 mg/[m.sup.3]. In both periods, pigment concentrations were inversely related to the temperature, with the highest concentrations during the winter seasons and the lowest during the spring-summer seasons.

Figure 7 shows the relationship of the reproductive cycle to the pigment concentrations. The highest pigment concentration values were significantly related with the development stage (untransformed data) (r = 0.75, P < 0.05, n = 30) and minimum pigment concentrations values with ripe and spawn stages.

[FIGURE 7 OMITTED]

DISCUSSION

The description of gonadic cycle stages and their corresponding microscopic anatomy did not differ from those performed for P. mazatlanica by diverse authors (Garcia-Dominguez et al. 1996, Saucedo-Lastra & Monteforte 1997, Sevilla 1969).

There were differences related to the gonadic cycle among El Nino and La Nina events. During El Nino, the developing and ripe stages were constants and in equilibrium along the study period whereas the spawning stage was continuous and longer on lime duration and more intensive (related to population spawning frequency); the indifferentiated stage was present in low frequency. In contrast, during La Nina the developed stage was predominant along the study period with intermittent and short ripe stage and the reproductive stage was of minor duration and intensity.

Studies performed on P. mazatlanica reproduction (Garcia-Dominguez et al. 1996) at Isla Espiritu Santo revealed spawn occurrence during June, July, and October 1992 and April 1993, with 30% mean and 33.3% maximum population spawning frequency whereas Sevilla (1969) in Bahia de La Paz found maximum spawning peaks in August and September 1963, with 30.5% mean and 50% maximum population spawning frequency. On cultured population from Bahia de La Paz, Saucedo-Lastra and Monteforte (1997) found only one maximum spawning peak during September 1992 and 30% maximum population spawning frequency. In Guaymas, Sonora, Mexico, P. mazatlanica was reported with a maximum spawning peak in June 1994 and 67% maximum population spawning frequency (Arizmendi-Castillo 1996), and from the Golfo de Nicoya, Costa Rica, two maximum spawning peaks in October 1993 and June 1994, with 31.5% mean population spawning frequency were reported (Solano-Lopez et al. 1997). The differences pointed out by the results in the current study proved that in both climatic events, there was real impact on the reproductive stages, suggesting that in the El Nino event, the environmental conditions were most favorable and that this caused intervals among the reproductive stage to be shortened and the gonads to recuperate rapidly, accelerating the ripe stage. Similar results were found by Arntz et al. (1988) and Wolf (1988) during El Nino 1982-1983, in Argopecten purpuratus (Pectinidae) at the Peruvian coast, where they observed especially high intensity on spawn.

The sex ratio in both periods did not differ from the expected 1M:1F ratio--this result coincides with those of Saucedo-Lastra and Monteforte (1997) and Solano-Lopez et al. (1997), 1M:0.38F and 1.6M:1F ratios, respectively--but differs from those reported by Garcia-Dominguez et al. (1996) where the females predominated (1.33F:1M). The hermaphroditic frequency in the current study was higher than those reported by Garcia-Dominguez et al. (1996) and Saucedo-Lastra and Monteforte (1997), 0.64% and 0.6%, respectively. In both periods, the highest hermaphroditic frequency was present during the main season of reproductive activity, while males predominated, coinciding with Sevilla (1969) and Saucedo-Lastra and Monteforte (1997) in P. maztlanica and by Behzadi et al. (1997) in P. funcata. The results in the current study and others obtained by several authors confirm the protandric condition of P. mazatlanica (Garcia-Dominguez et al. 1996, Saucedo-Lastra & Monteforte 1997, Sevilla 1969), as occurs in other Pinctada species (Behzadi et al. 1997 and Tranter 1959 in P. funcata; Tranter 1958a in P. albina; Tranter 1958b in P. margaritifera; and Rose et al. 1990 in P. maxima).

During the El Nino, the occurrence of highest mean values of oocyte diameter corresponding to ripe stage and the lowest mean values corresponding to the spawn and spent stages allow us to infer that greater oocyte size were liberated to the external environment. This relationship between oocyte diameter and gonadal stages of P. mazatlanica reflects the gametogenic cycle, as clearly occurs in other bivalve species studied in normal environmental conditions: Glycymeris gigantea (Villalejo-Fuerte et al. 1995), Spondylus leucacanthus (Villalejo-Fuerte & Garcia-Dominguez 1998), and Periglypta multicostata (Garcia-Dominguez et al. 1998). This relationship did not occur in the La Nina event.

The maximum and minimum CI values and their fluctuation tendency, in both periods, were similar. This relationship between CIs to the reproductive process suggests a strong influence of the gonad weight over the general organism condition, as was reported for P. mazatlanica by Solano-Lopez et al. (1997) in the Gulf of Nicoya, Costa Rica, and also reported for another bivalve species by Ochoa-Baez (1985) for Modiolux capax and by Villalejo-Fuerte and Ceballos-Vazquez (1996) for Argopecten circularis. These CI fluctuations are associated with the nutritional and reproductive condition of mollusks (Searcy-Bernal 1984), and for this reason we can consider CI a general condition indicator to the specimens that conform P. mazatlanica reproductive population and also as the general reproductive process.

The P. mazatlanica reproductive cycle showed a seasonable relation to SST. The minimum gonadic activity (indifferent stage) occurred during autumn at El Nino and in winter at La Nina; the highest developing frequency during summer at El Nino and in winter at La Nina; and the ripe stage in the close of spring at El Nino and in middle summer at La Nina. In both periods, when the temperature reached 27[degrees]C (middle summer at El Nino, close of summer at La Nina), spawning began and was maintained during all the lime (months) while the temperatures were about 30[degrees]C (late autumn during El Nino and early autumn during La Nina), and spawning in both periods was suspended at temperatures under 25[degrees]C. This crucial interval could be considered as optimum for P. mazatlanica spawning and is similar to those reported in the same species by Sevilla (1969), Tripp-Quezada (1991), Arizmendi-Castillo (1996), Garcia-Dominguez et al. (1996), and Saucedo-Lastra and Monteforte (1997). The difference in both periods was that the reproductive event in El Nino was longer in time and more intensive on population spawning frequency, and all this explained was happened to P. mazatlanica by Garcia-Dominguez et al. (1996) on "El Nino" 1991-1992, at Isla Espiritu Santo, B.C.S., Mexico, where spawning activity occurred throughout the study period (June 1992 to August 1993). In La Nina, the spawning activity was shorter in time length and began until the 27[degrees]C temperature was reached (August 1999). For both periods, temperature was inversely related to CI, and CI was closely related to condition of specimens and they, on lowest temperature periods (winter season), were in indifferent and developing stages having the highest condition values. During the highest temperature periods (summer season), spawning was present and hence the minus CI values.

The oocyte mean diameter during El Nino was related to the ripe and spawning stage and CI, all of them influenced by temperature variations, as pointed out above. During La Nina, this relationship did not occur at all.

Pigment concentration in both periods presented similar seasonal fluctuations. The difference between both periods was that during El Nino, the mean, maximum, and minimum pigment concentrations were smaller than those during La Nina. In P. mazatlanica, for both periods, gametogenic production (developing stage) started during winter, coinciding with highest photosynthetic pigment concentration. During ripe and spawning stages, no relationship was found in both periods with pigment concentration, and we assume that these events were realized at the expense of organism nutrient reserves. There are observations in many bivalves that gametogenic process takes place at the expense of conjunctive reserve tissue (Galtsoff 1964, Mathieu and Lubet 1993), as the case in the mussel Perumytilus purpuratus (Lozada and Reyes 1981) during spawning and in P. mazatlanica (Garcia-Gasca 1992) during gamete formation.

During El Nino, pigment concentration was related to CI, but not during La Nina, in this case the fluctuations of CI could be attributed to the irregular gonadic process, as occurred during the developing and ripe stages presented by the specimens during this period. The monthly mean oocyte diameter, in both periods, was not related to pigment concentration, as the maximum monthly mean diameters occurred in summer.

Finally, it may be concluded that temperature was the main factor regulating the spawning time during the El Nino and the La Nina, and that food availability was not related to the pearl oyster spawning.

ACKNOWLEDGMENTS

This study was conducted as part of an Institutional Program of the Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN, Mexico), which is funded by Consejo Nacional de Ciencia y Tecnologia (CONACYT-Mexico) and Consejo Nacional de Educacion Tecnologica (COSNET-Mexico). Our gratitude to Manuel Zamarron and Ciro Arista for their help in collecting samples, Fidel Camacho and Jorge Lopez for their work on histologic processing, and the CIBNOR editorial staff for review of the English text. Daniel Lluch-Belda and Federico Garcia-Dominguez received a grant from the Comision de Operacion y Fomento de Actividades Academicas of the Instituto Politecnico Nacional.

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J. ANGEL GARCIA-CUELLAR, (1,2), * FEDERICO GARCIA-DOMINGUEZ, (1) DANIEL LLUCH-BELDA, (1) AND SERGIO HERNANDEZ-VAZQUEZ (2) (1) Centro Interdisciplinario de Ciencias Marinas (CICIMAR), Instituto Politecnico Nacional, La Paz, B.C.S. 23000, Mexico; (2) Centro de Investigaciones Biologicas del Noroeste (CIBNOR), La Paz, B.C.S. 23000, Mexico

* Corresponding author. E-mail: [e-mail]