Reproduction of the lion's paw scallop Nodipecten subnodosus sowerby, 1835 (bivalvia: pectinidae) from Laguna Ojo de Liebre, B.C.S., Mexico.

ABSTRACT Knowledge of the reproductive cycle of marine invertebrates of economic importance is essential for management of natural stocks and to initiate aquaculture activities. The reproductive biology of Nodipecten subnodosus from Laguna Ojo de Liebre, B.C.S., Mexico, was studied during a period of 25 mo. N. subnodosus is a functional hermaphrodite in which the follicles contain gametes of only one sex and remain separated from those containing the gametes of the other sex, with female follicles being dominant. Histologic evidence revealed that the lion's-paw scallop may remature at least once during the reproductive season. The temperature, analyzed as a single factor, could be important in the initiation of gametogenesis and/or as a spawning stimulus. The reproductive cycle shows a clear seasonality related to the water temperature, which is supported by the temporal variation of the oocyte diameter and by a significant positive correlation between GSI and temperature. The inactive period occurs from December to March, with low water temperature (16[degrees]C to 17.5[degrees]C). The gametogenesis started when the water temperature reached 18[degrees]C (April). The maximum maturation (90% to 100% of organisms) was reached in August when the temperature was highest (23.5[degrees]C). Spawning occurred in September when water temperature decreased. A slight reproductive activity during the cooler months (December to March) was observed. But, during 2002 the reproductive activity in that period was more pronounced and the slight spawning activity was extended to May. This behavior was in accordance with temperature anomalies that occurred in 2002. Then, N. subnodosus is potentially capable of spawning throughout the year if the environmental conditions are favorable. The length at first maturity obtained for N. subnodosus was 135-mmSL.

KEY WORDS: reproductive cycle, scallop, gonadosomatic index, histology, Nodipecten

INTRODUCTION

There are over 30 species of pectinids at the Mexican Pacific littoral (Keen 1971). However only three are considered as commercially important: the Pacific calico scallop Argopecten ventricosus, the Vogde's scallop Euvola vogdesi, and the Lion's paw scallop Nodipecten subnodosus. The lion's paw N. subnodosus inhabits shallow coastal channels with strong currents from Laguna Ojo de Liebre and the Gulf of California to Peru, (Keen 1971). It is one of the most important fisheries in the region, but indiscriminate harvesting has resulted in the depletion of most natural beds, and nowadays the exploitation is based solely on a natural population located in Laguna Ojo de Liebre B.C.S., Mexico. Several institutions are now studying the natural history and developing technologic alternatives for this species (Morales-Hernandez & Cacerez-Martinez 1996, Barrios-Ruiz et al. 2003, Racotta et al. 2003, Arellano-Martinez et al. 2004).

The knowledge of the reproductive cycle of marine invertebrates of economic importance is essential for management of will populations and to initiate aquaculture activities. Documentation on the reproductive biology of N. subnodosus is scarce. Reinecke-Reyes (1996) reported the spawning season and reproductive cycle on the basis of a 10-month study in Laguna Ojo de Liebre, B.C.S. and using lion's paw scallops from the same locality, Gutierrez-Villasenor & Chi-Barragan (1997) made a laboratory experiment of reproductive conditioning. Recently, Racotta et al. (2003) studied the biochemical composition, growth, and length of first reproduction of cultured lion's paw scallops in Bahia Magdalena, B.C.S., and Arellano-Martinez et al. (2004), studied the relationships between the nutrient storage cycle, reproductive activity, and available food of the same species in Laguna Ojo de Liebre, B.C.S.

We document here a detailed description of the gonad developmental stages of N. subnodosus and the reproductive cycle and its relation with temperature over 2 years in Laguna Ojo de Liebre, B.C.S., Mexico. Additionally, the length at first maturity was determined.

MATERIALS AND METHODS

From December 2000 to December 2002, 18 to 48 specimens per month of lion's paw scallop N. subnodosus were randomly collected by semiautonomous diving at 4-10 m depth from a wild population in the Laguna Ojo de Liebre, B.C.S., Mexico (27[degrees]35'N and 27[degrees]55'N and 113[degrees]50'W and 114[degrees]20'W). At the same time, bottom water temperature was recorded.

From each scallop the shell length was measured with a caliper at l-ram resolution. The organisms were dissected and the total soft body and gonad wet weight to the nearest 0.1 g were registered. Gonad tissue was fixed in a buffered 10% formaldehyde solution for 24 h. A standard cross section of approximately 0.5 cm was cut in the middle part of the gonad, where both ovary and testis were included. Gonad samples were then dehydrated using a series of ethanol solution of increasing concentration, cleared in Hemo-De, and embedded in paraplast. Sections of 7-[micro]m thickness were cut on a rotary microtome and placed on slides. Then, tissue was processed using a series of decreasing ethanol solution and stained with hematoxylin and contrasted with eosin (Humason 1979).

To analyze the reproductive process, gonad preparations were microscopically examined and assigned to a developmental stage following categories used previously for the same species (Reinecke-Reyes 1996): undifferentiated, developing, ripe, spawning, and spent. The description of each stage of gonad development was complemented with our own observations. As a tool for the description of the reproductive cycle, the monthly relative frequencies of all gonad developmental stages were calculated.

The reproductive condition of specimens analyzed through histologic study was further examined by calculating a gonadosomatic index (GSI), as a ratio of the gonad wet weight to the total soft body wet weight (Sastry 1970). To determine the reproductive cycle and the GSI variation, only adult scallops (51-181 mm of shell length) were considered.

Additionally, the diameters of at least 100 oocytes per scallop were measured, using the SCAN PRO software (Version 5.0, Systat Software, Inc., Richmon, CA) and digitalized images of histologic sections. Only oocytes sectioned through the nucleus and with visible nucleolus were individually traced with the pointer and the major and minor axis lengths were automatically measured by the software. Then an average of both dimensions was calculated and it was considered the estimated mean diameter, which was calculated monthly. According to the criteria of Grant & Tyler (1983) individuals with few measurable oocytes and extensive phagocytosis ("spent" specimens) were not considered.

To assess the length at first maturity the cumulative relative frequencies of all mature scallops, excluding the undifferentiated, were calculated by shell length interval (5 mm). The length interval with 50% of mature scallops was considered as the length of first maturity (length at which lion's paw reach the maturity by first time) in the population (Somerton 1980).

One-way ANOVA followed by mean comparisons post-hoc Tukey test were made to assess significant differences in GSI and oocyte diameter between months. The differences in GSI between the same months of different years were evaluated by a t-test. A Spearman-rank correlation analysis was used to investigate the relationship among reproductive activity (GSI) and water temperature. Because GSI values are percentages, before applying the analysis they were arcsine transformed (Zar 1996) to reduce the dependence of the sample variance on the mean and to normalize the data distribution. STATISTICA for Windows (V. 6.0) was used for all analyses. The level of significance ([alpha]) was preset at 0.05.

RESULTS

Gonadic Structure

The lion's paw N. subnodosus is a functional hermaphrodite, in which both male and female gametes become ripe at the same time, although not necessarily they spawn at the same time. The gonad is not embedded in the visceral mass, and it is possible to differentiate the male from the female gonadic tissue from the outside. Macroscopically, the ovary portion has color ranges from a pale cream to dark orange, whereas the testis portion goes from creamy to beige, both varying with the degree of ripeness. The ovary portion, occupies the largest proportion of the gonad ([approximately equal to]60%). The testis is located at the margin of the gonad from its origin (in the digestive gland) running anteriorly to the tip of the gonad.

Microscopically, the male and female tissues are organized in separated follicles and in different regions. However, the separation is incomplete, with small masses of spermatic tissue among the ovarian follicles or some ovarian follicles in the spermatic portion of the gonad.

Gonadal Developmental Stages

The histologic development of the gonad was simplified into 7 stages and their characteristics are as follows:

Undifferentiated

Scallops with little or no follicular material present and total absence of gametes. Connective tissue is abundant, containing different types of granulocytes and phagocytes. Externally the gonad is small and pale cream colored.

Early Development

This is the stage of gamete proliferation, characterized by the expansion of follicles, which are irregular in shape and contain oogonia (between 13 and 22 [micro]m in diameter) or spermatogonia attached to the follicle wall. Interfollicular connective tissue decreases at this stage. A central lumen is present in each follicle. Externally, the gonad acquires a pale orange (ovary) and cream (testis) colors.

Late Development

A reduction of gonias and an increase of mature gametes occur in both sexes. As development proceeds, spherical vitellogenic oocytes (45 [micro]m average diameter) and spermatozoids are more numerous. Spermatocytes and spermatids are restricted to lining the follicular walls, which have become increasingly thinner. Some ripe gametes appear in the central lumen. Externally, the gonad acquires more consistency and the female orange color and male cream color are darker as the ripeness proceeds.

Ripe

Female follicles are distended and densely packed with mainly polygon-shaped oocytes. The oocytes reach their maximum size (51 [micro]m average diameter). In male follicles dense masses of spermatozoids are located in the central lumen. In this stage, connective tissue is almost absent. Externally, the gonad is turgescent and the ovary portion acquires the characteristic dark orange color, whereas the testis portion is beige.

Partially Spawned

Variable quantities of follicles are partially or totally empty, depending on the degree of advance of the spawning. In some cases, very small previtellogenic oocytes or spermatocytes are embedded in the follicle wall at the periphery of empty follicles. Externally, the color is similar to the ripe stage but the turgescence is lost. Gonads in a state of rematuration can be also assigned to this stage. These gonads are entering a new breeding cycle after their main spawning (Fig. 1a).

[FIGURE 1 OMITTED]

Spent

Gonad with ruptured follicles. Few residual oocytes and spermatozoa being phagocytized. There is no evidence of active oogenesis or spermatogenesis. The external appearance of the gonad is flaccid and pale orange or cream colored.

Reabsorption 

This stage was observed in gonads with the micro and macroscopic characteristics of the late development stage, but with large quantities of vitellogenic oocytes or spermatozoids in reabsorption process (Fig. 1b,c). Numerous phagocytes were observed (macrophage hemocytes) between and within the follicles.

Reproductive Cycle

The reproductive cycle of N. subnodosus is shown in Figure 2. In December of all years, most scallops (between 82% to 100%) were inactive (undifferentiated and spent stages). This reproductive quiescence was extended from January to March in 2001, but not in 2002 when gonads in re-absorption were observed for both sexes. In addition, some scallops presented female ripe gonads and partially spawned male gonads. Early development began in April as shown by the increase in numbers of discernible oogonia and small oocytes in the ovary region and the occurrence of spermatocytes or even spermatids in testis region. The late development stage proportion increased from April to July during both years, although the proportion of scallops in this stage was in general higher in April to May 2001 (60% to 90%) than for the same months during 2002 (25% to 55%). During the first year, ripe scallops were first observed from May (10%), reached a maximum proportion in August (near 100%), which progressively decreased thereafter to minimum values by December (5%). In the second year, in addition to the occurrence of reproductive activity in January and February previously described, the general pattern was delayed and shortened compared with 2001: initiation in June (22% to 40%), same peak in August (near 100%) and then almost no ripe scallops by November (5%). A massive spawning period was observed from September to November (25% to 75% of the population) in both years. In addition, a small proportion of partially spawned scallops were found in February to March 2001 (6.5%). As previously indicated a higher reproductive activity during these months was observed in 2002: ripe and partially spawned scallops were observed in January and their proportion in February to March (7% to 40%) was higher than in 2001.

[FIGURE 2 OMITTED]

Oocyte Diameter

The mean oocyte diameter (Fig. 3) showed significant differences among months (one-way ANOVA, P < 0.01) with a clear seasonality (post hoc Tukey test) during both years, with the largest oocytes from June to August. In 2002 the seasonality was not so clear: in addition of the largest oocytes found from June to August, large oocytes were also observed in January and March. The minimum mean oocyte diameter (23.5 [micro]m) was observed in January 2001, and the maximum (51 [micro]m) was observed in August 2001. In December 2000, March 2001, and in December 2002 the scallops were spent or undifferentiated and thus oocyte diameter was not estimated, but very low values would be obtained in these months.

[FIGURE 3 OMITTED]

Gonadosomatic Index

GSI showed a marked seasonal pattern with significant differences (one-way ANOVA, P < 0.01) throughout the study period (Fig. 4). The GSI values were low from January to March of the first year (5.7% to 7.7%); and from January to May of the second year (5.9% to 8.3%). Values of the GSI increased gradually from April of the first year and from June of the second year. GSI reached the maximum value in August of both years (27.0% and 27.7% respectively), being significantly different from the other months. From September of both years, the GSI values decreased until the lowest values were reached in December (7.0%). Comparing the GSI values of each month between years, significantly lower values were obtained in 2001 than in 2002 for February, March, June, and July, whereas significantly higher values were obtained in 2001 than in 2002 for May and September (P < 0.05, t-test, Zar 1996).

[FIGURE 4 OMITTED]

Seawater Temperature

Seawater temperature varied seasonally, with its minimum values in January to February (15.9[degrees]C) (see Fig. 4). Temperature increased gradually from March 2001 and from February 2002, reaching its maximum values in August (23.5[degrees]C) of both years. Temperature values started to decrease in September in both years. Interannual variations of water temperature were registered (Table 1). The period of January to March 2002 was warmer and the periods of May to July and October to December 2002 were cooler than the same periods in 2001. A significant correlation between the GSI and seawater temperature (R = 0.89, P = 0.000) was found.

Length at First Maturity

The range in scallops shell length was 51-mm to 174-mm (130.3-mm average, 18.8-mm standard deviation). A logistic model was fitted to data on shell length versus maturity. Although some specimens may start their gonad development as small as 51-mm SL, the length at first maturity in N. subnodosus was found at 135-mm SL (Fig. 5).

[FIGURE 5 OMITTED]

DISCUSSION

The sexuality of pectinids ranges from strictly gonochorists to functional hermaphrodites (Coe 1945, Reddiah 1962), and there are 2 types of follicular structure in hermaphroditic specimens (Coe 1945, Reddiah 1962, Gaspar-Soria et al. 2002). In the type 1 the follicles contain gametes of only one sex, and remain separated from those containing the gametes of the other sex, whereas in the type 2 the male and female gametes are present in the same follicle. According to the earlier mentioned facts, the histologic analysis confirmed that N. subnodosus is a type 1 functional hermaphrodite, with female follicles being dominant. The most common form of hermaphroditism in pelecypods is the type 1 (Sastry 1979), although the occurrence of type 2 is frequent (Rose et al. 1990, Villalejo-Fuerte et al. 1996, Ceballos-Vazquez et al. 2000, Gaspar-Soria et al. 2002). However, the hermaphroditism is very complex in pectinids. For example, Placopecten magellanicus is considered to be a gonochoric species (Parsons et al. 1992), although some cases of type 2 hermaphroditism with dominance of male gametes have been reported from this species (Giguere et al. 1994). This indicates that pectinids may have individual variations in the expression of sexuality and probably different reproductive strategies.

Although the gonad of hermaphrodite scallops can produce both types of sexual cells at the same time, they are not usually discharged simultaneously, to avoid self-fertilization. Morales-Hernandez and Cacerez-Martinez (1996) mentioned that the hermaphrodite scallops, first release the sperm and subsequently release the oocytes. In this study, we found gonads with the testis partially spawn or spent, together with a ripe ovary also suggesting that the sperm was released before the eggs. This behavior was observed during spawning induction for N. subnodosus under laboratory conditions although it depends on the method of induction (Ibarra personal communication, CIBNOR, La Paz, Mexico). Additionally, the histologic evidence revealed that N. subnodosus may remature at least once and possibly more, during the reproductive season because we frequently observed individuals in which one sex was in an advance developmental stage whereas the other sex was in an early development stage. Therefore scallops avoid the spent stage and they go directly to a new development after the first spawning to start on another breeding cycle. It is important to clarify that all of these scallops were found only after the main spawning period (when the rematuration of testis and ovary is asynchronous as a consequence of the alternate spawning by sex), and never at the start or end of the reproductive activity period. The presence of rematuration has been also reported for Pinctada mazatlanica (Sevilla 1969, Saucedo & Monteforte 1994) and Argopecten ventricosus (Villalejo-Fuerte & Ochoa-Baez 1993).

Gametogenic cycles are generally ruled by external environmental factors (i.e. temperature, photoperiod, food availability) that may trigger and synchronize the "timing" of the different stages (Lubet 1983, Gallardo 1989). It is well established that temperature is one of the most important environmental factors influencing the regulation of gametogenic cycle of mollusks (Giese 1959, Mann 1979, Sastry 1975, Giese & Kanatani 1987, Wada et al. 1995). In some scallops likely Chlamys islandica sudden increases in water temperature seem to be the final cue for stimulating maturation and spawning (Skreslet & Brun 1969, Giguere et al. 1994), or in other scallops such as N. nodosus a specific temperature (17.5[degrees]C) seems to increase sexual maturity and synchronize the reproductive behavior (Rupp et al. 1997). However, the effects of temperature on gametogenesis and spawning cycles of bivalves are complex, and depend on the overall reproductive strategy and the environmental temperature range (Marsden 1999). In this study, the reproductive cycle of N. subnodosus shows a clear seasonality related with the water temperature, which is supported by the temporal variation of the oocyte diameter and by the significant positive correlation between GSI and temperature. In a general context, the inactive period (undifferentiated and spent stages) occurs from December to March, with low values of water temperature (16[degrees]C to 17.5[degrees]C) and GSI (5.4-8.2). Gametogenesis started in April when the water temperature reached 18[degrees]C and continued during the warmer months. The maximum maturation (90% to 100% of organisms) was reached in August when the temperature was (23.5[degrees]C) and GSI (27.0 in 2001 and 27.7 in 2002) were highest.

On the other hand, the spawning of N. subnodosus occurred in September when water temperature and GSI decreases, and continued through November. This is in agreement with the highest spat concentration found within this period by Garcia-Dominguez et al. (1992). The general reproductive pattern also agrees with previous studies in this species at the same locality (Reinecke-Reyes 1996, Arellano-Martinez et al. 2004) and at a southern locality (Racotta et al. 2003).

In addition to the general reproductive events analyzed earlier, the qualitative histologic observations revealed a slight reproductive activity during the cooler months (January to March of 2001), as indicated by the presence of reproductively active scallops in a low proportion (2.7% to 6.8%). Notwithstanding, during 2002 the reproductive activity in that period was more pronounced, with higher proportion of reproductively active scallops (3.4% to 26.9%) and in addition, the spawning was extended until May. This behavior was in concordance with the temperature anomalies occurred in 2002, which were higher than in 2001, and thus reinforces the influence of temperature on the gametogenic cycle of N. subnodosus. In this sense, Jaramillo and Navarro (1995) suggested that spawning could be induced by a combination of internal and environmental factors and that their interaction may vary seasonally, producing annual variations in onset and intensity of spawning. On the other hand, Brousseau (1987) mentioned that it is possible that some species could begin a facultative spawning if environmental conditions are favorable. An earlier, minor spawning is common in other species such as Mya arenaria (Brousseau 1987), Pecten maximus, P. magellanicus, in species of the genus Chlamys (Thompson 1977), and in the particular case of N. subnodosus (Arellano-Martinez et al. 2004). However, it is important to stand out that only in this period of possible facultative spawning (January to May 2002), gonadal regression (reabsorption stage) was found. Similarly, a thermal stress has been shown to prevent or inhibit the egg release in P. maxima (Rose et al. 1990). In this sense, the massive lysis of gametes can be caused, among other factors, by unfavorable environmental conditions, thus stopping a sexual cycle, which in favorable conditions would end with spawning (Motavkine & Varaksine 1983, Dorange & LePennec 1989). Therefore, we believe that N. subnodosus is potentially capable of spawning throughout the year if the environmental conditions are favorable.

The bivalve production of gametes is also influenced (set in a seasonal context) by food availability (Bayne 1976, MacDonald & Thompson 1985, Jaramillo et al. 1993). It has been suggested that spawning of some scallops may be triggered by changes in temperature and/or phytoplankton blooms (DiSalvo et al. 1984, Villalaz 1994, Jaramillo et al. 1993, Arsenault & Himmelman 1998, Luna-Gonzalez et al. 2000, Arellano-Martinez et al. 2004). Although in this study the food availability was not determined, the higher concentration of chlorophyll a (1.2 mg/L) in the Laguna Ojo de Liebre was found in September to October (Arellano-Martinez et al. 2004), just along with the spawning. It has been previously suggested that the spawning of N. subnodosus in Laguna Ojo de Liebre seemed to be triggered more by the phytoplankton abundance than by temperature (Arellano-Martinez et al. 2004), probably as a strategy to ensure food supply to the larvae (Newell et al. 1982). In this sense, Wolf (1988) suggests that high temperature, although favoring maturation and spawning, might be less critical for a successful spawning than food availability. From the results of this study, it is now difficult to separate between the relative influences of temperature and food availability, but probably both factors play an important role.

Finally, no data are available so far concerning the length at first maturity of N. subnodosus. Our results indicate that the individuals of this species attain their first maturity at a shell length of 135-mm. However, histologic observation showed some individuals of N. subnodosus sexually mature at 51-mm SL. Garcia-Dominguez et al. (1992) reported that this species grows 0.21 mm of shell height by day at the same locality, but in culture. This shows that this species becomes sexually mature at approximately 8 mo of age in Laguna Ojo de Liebre. Similarly, Racotta et al. (2003) reported, in culture conditions, maturing N. subnodosus scallops of 8 mo of age (55 mm SL, approximately) in Bahia Magdalena, B.C.S., Mexico, a locality about 400 miles to the south.

In conclusion, lion's paw N. subnodosus from Laguna Ojo de Liebre, Mexico, is sensitive to water temperature changes and it behaves as many temperate species, maturing during the warmer months and spawning when temperature begins to decrease, with minimum or null reproductive activity during winter (December to March). This pattern agrees with the northern pectinid Aequipecten tehuelchus (Narvarte 2001). Villalaz (1994) mentioned that the temperature probably has a greater influence on reproduction in temperate than in tropical bivalves, because in the former, thermal fluctuations are higher.

TABLE 1.

Interannual variation of water temperature.

  Month      2000    2001    2002    Difference

January              15.9    17          1.1
February             15.9    17.3        1.4
March                17.6    17.9        0.3
April                18      18
May                  19      18.5       -0.5
June                 20.5    19         -1.5
July                 22.5    21.2       -1.3
August               23.4    23.4
September            23      23
October              22.8    20         -2.8
November             20.1    19.8       -0.3
December       16    17      16         -1.0

ACKNOWLEDGMENTS

The authors thank Compania Exportadora de Sal, Sociedad Cooperativa Pescadores Unidos de Guerrero Negro, Reserva de la Biosfera El Vizcaino, and Instituto Politecnico Nacional for the grants (EDI and COFAA) and the authors. Marcial Arellano is a PhD student-fellow of CONACyT. Study supported by the following projects: CGPI-20031573, 20038005, and SEMARNAT 2002-C01-0277.

LITERATURE CITED

Arellano-Martinez, M., I. S. Racotta, B. P. Ceballos-Vazquez & J. F. Elorduy-Garay. 2004. Biochemical composition, reproductive activity, and food availability of the lion's-paw scallop Nodipecten subnodosus in the Laguna Ojo de Liebre, B.C.S., Mexico. J. Shellfish Res. 23:15-23.

Arsenault, D. J. & J. H. Himmelman. 1998. Spawning of the Iceland Scallop (Chlamys islandica Muller, 1776) in the northern gulf of St. Lawrence and its relationship to temperature and phytoplankton abundance. Veliger 41:180-185.

Barrios-Ruiz, D., J. Chavez-Villalba & C. Caceres-Martinez. 2003. Growth of Nodipecten subnodosus (Bivalvia: Pectinidae) in La Paz, Bay. Aquaculture Res. 34:633-639.

Bayne, B. L. 1976. Aspects of reproduction in bivalve molluscs. In: M. L. Wiley, editor. Estuarine Processes. New York: Academic Press. pp. 432-448.

Brousseau, D. J. 1987. A comparative study of the reproductive cycle of the soft-shell clam, Mya arenaria in Long Island Sound. J. Shellfish Res. 6:7-15.

Ceballos-Vazquez, B. P., M. Arellano-Martinez, M. Villalejo-Fuerte & F. Garcia-Dominguez. 2000. Reproductive cycle of the rugose pen shell, Pinna rugosa Sowerby, 1835 (Mollusca: Bivalvia) from Bahia Concepcion, Gulf of California and its relation to temperature and photoperiod. J. Shellfish Res. 19:95-99.

Coe, W. R. 1945. Development of the reproductive system and variation in sexuality in Pecten and other Pelecypod mollusks. Trans. Conn. Acad. Arts Sci. 36:673-700.

DiSalvo, L. H., E. Alarcon, E. Martinez & E. Uribe. 1984. Progress in mass culture of Argopecten purpuratus with notes on its natural history. Rev. Chilena de Hist. Nat. 57:33-45.

Dorange, G. & M. LePenec. 1989. Ultrastructural study of oogenesis and oocytic degeneration in Pecten maximus from the Bay of St. Brieuc. Mar. Biol. 103:339-348.

Gallardo, C. 1989. Patrones de reproduccion y ciclo vital en moluscos marinos benticos; una aproximacion ecologico-evolutiva. Medio Ambiente 10:25-35.

Garcia-Dominguez, F. A. P., Castro-Moroyoqui & E. F. Frlix-Pico. 1992.

Spat settlement and early growth of Lyropecten subnodosus (Sowerby, 1835) in Laguna Ojo de Liebre, B.C. Mexico, 1989-1990. Abstracts, 1992 Triennial Meeting National Shellfisheries Association, Orlando, Florida. J. Shellfish Res. 11:195.

Gaspar-Soria, R., M. S. Pascual & V. H. Fernandez-Cartes. 2002. Reproductive cycle of the cholga paleta, Atrina seminuda Lamark, 1819 (Bivalvia: Pinnidae) from northern Patagonia, Argentina. J. Shellfish Res. 21:479-488.

Giese, A. C. 1959. Reproductive cycle of some west coast invertebrates. In: R. Withrow, editor. Photoperiodism and related phenomena in plant and animals. Washington, DC: American Association of Science, Publication No. 55, pp. 625-538.

Giese, A. C. & H. Kanatani. 1987. Maturation and Spawning. In: A. C. Giese, S. Pearce & V. B. Pearce, editors. Reproduction in Marine Invertebrates, vol. 4. General aspects: seeking unity in diversity. Palo Alto: Blackwell Scientific. pp. 251-339.

Giguere, M., G. Gliche & S. Brulotte. 1994. Reproductive cycle of the sea scallop, Placopecten magellanicus (Gmelin), and the Iceland scallop, Chlamys islandica (O. F. Muller), in Iles-de-la-Madeleine, Canada. J. Shellfish Res. 13:31-36.

Grant, A. & P. A. Tyler. 1983. The analysis of data in studies of invertebrate reproduction. II. The analysis of oocyte size/frequency data, and comparison of different types of data. International. J. Invertebr. Rep. 6:271-283.

Gutierrez-Villasenor, C. E & G. Chi-Barragan. 1997. Effect of temperature and feeding ratio on the conditioning of Lyropecten subnodosus Sowerby, 1835. Book of Abstracts.Eleventh International Pectinid Workshop, La Paz, B.C.S., Mexico. pp. 73-75.

Humason, G. L. 1979. Animal tissue techniques. 4th ed. San Francisco: W. H. Freeman and Company. pp. 111-129.

Jaramillo, R., J. Winter, J. Valencia & A. Rivera. 1993. Gametogenic cycle of the chiloe Scallop (Chlamys amandi). J. Shellfish Res. 12:59-64.

Jaramillo, R. & J. Navarro. 1995. Reproductive cycle of the Chilean ribbed mussel Aulacomya ater (Molina, 1982). J. Shellfish Res. 14:165-171.

Keen, A. M. 1971. Sea shells of tropical west America. Stanford: Stanford University Press. 1064 pp.

Lubet, P. 1983. Experimental studies on the action of temperature on the reproductive activity of the mussel (Mytilus edulis L. Mollusca, Lamellibranchia). J. Mollusc. Stud. Suppl. 12A: 100-105.

Luna-Gonzalez, A., C. Caceres-Martinez, C. Zuniga-Pacheco, S. Lopez-Lopez & B. P. Ceballos-Vazquez. 2000. Reproductive cycle of Argopecten ventricosus (Sowerby II, 1842) (Bivalvia: Pectinidae) in the Rada of Puerto de Pichilingue, B.C.S., Mexico and its relation to temperature, salinity, and quality of food. J. Shellfish Res. 19:107-112.

MacDonald, B. & R. J. Thompson. 1985. Influence of temperature and food availability on ecological energetics of the giant scallop Placopecten magellanicus. I. Growth rates of shell and somatic tissue. Mar. Ecol. Prog. Ser. 25:279-294.

Mann, R. 1979. Some biochemical and physiological aspects of the growth and gametogenesis in Crassostrea gigas and Ostrea edulis grown at sustained elevated temperatures. J. Mar. Biol. Assoc. UK. 59:95-110.

Marsden, I. D. 1999. Reproductive cycles of the surf beach clam Paphies donacina (Spengler, 1793) from New Zealand. J. Shellfish Res. 18: 539-546.

Morales-Hernandez, R. & C. Cacerez-Martinez. 1996. Pesqueria de almeja mano de leon Nodipecten subnodosus. In: M. Casas-Valdez y & G. Ponce-Diaz, editors. Estudio del Potencial Pesquero y Acuicola de Baja California Sur. Mexico. La Paz, B.C.S.: SEMARNAP, Gob. de B.C.S., FAO, U.A.B.C.S., CICIMAR-IPN, CRIP La Paz, pp. 87-100.

Motavkine, P. A. & A. A. Varaksine. 1983. Histophysiologie du systeme nerveux et regulation de la reproduction chez les mollusques bivalves. Sciences. Moscu. 208 pp.

Narvarte, M. A. 2001. Biologia reproductiva, historia de vida temprana y comportamiento en cultivo de la vieira tehuelche (Aequipecten tehuelchus D' Orb., 1846) (Bivalvia, Pectinidae). Tesis doctoral, Universidad Nacional del Comahue, Argentina. 100 pp.

Newell, R. I., T. J. Hilbish, R. K. Koehn & C. J. Newell. 1982. Temporal variation in the reproductive cycle of Mytilus edulis (Bivalvia: Mytilidae) from localities on the East Coast of the United States. Biol. Bull. 162:229-310.

Parsons, G. J., S. M. C. Robinson, R. A. Chandler, L. A. Davidson, M. Lanteigne & M. J. Dadswell. 1992. Intra-annual and long-term patterns in the reproductive cycle of giant scallop Placopecten magellanicus (Bivalvia: Pectinidae) from Passamaquoddy Bay, New Brunswick, Canada. Mar. Ecol. Prog. Ser. 80:203-214.

Racotta, I. S., J. L. Ramirez, A. M. Ibarra, M. C. Rodriguez-Jaramillo, D. Carreno & E. Palacios. 2003. Growth and gametogenesis in the lionpaw scallop Nodipecten (Lyropecten) subnodosus. Aquaculture 217: 335-349.

Reddiah, K. 1962. The sexuality and spawning of Manx Pectinids. J. Mar. Biol. Assoc. UK. 42:683-703.

Reinecke-Reyes, M. A. 1996. Madurez y desove de la almeja mano de leon Lyropecten subnodosus Sowerby, 1835 (Bivalvia: Pectinidae) en la laguna Ojo de Liebre, B.C.S. Mexico. In: C. E. Castro-Aguirre, editor. Boletin Pesquero SEMARNAP/INP-CRIP-La Paz, B.C.S., Mexico. 17-20.

Rose, R. A., R. E. Dybdahl & S. Harders. 1990. Reproductive cycle of the western Australian silver lip pearl oyster Pinctada maxima (Jamerson) (Mollusca: Pteriidae). J. Shellfish Res. 9:261-272.

Rupp, G. S., A. Velez, M. M. De Bem & C. R. Poli. 1997. Effect of temperature on conditioning and spawning of the tropical scallop Nodipecten nodosus (Linnaeus, 1758). Book of Abstracts.11th International Pectinid Workshop, La Paz, B.C.S., Mexico. pp. 132-133.

Sastry, A. N. 1970. Reproductive physiological variation in latitudinally separated populations of the bay scallop Aequipecten irradians Lamarck. Biol. Bull. 138:56-65.

Sastry, A. N. 1975. Physiology and ecology of reproduction in marine invertebrates. In: F. J. Vernberg, editor. Physiological ecology of esturine organisms. Columbia: University of South Carolina Press. pp. 279-299.

Sastry, A. N. 1979. Pelecypoda (excluding Ostreidae). In: A.C. Giese & J. S. Pearse, editors. Reproduction of marine invertebrates. New York: Academic Press, pp. 113-292.

Saucedo, P. & M. Monteforte. 1994. Breeding cycle of pearl oysters Pinctada mazatlanica and Pteria sterna (Bivalvia: Pteriidae) at Bahia de La Paz, Baja California Sur, Mexico. J. Shellfish Res. 16:103-110.

Sevilla, M. L. 1969. Contribucion al conocimiento de la madreperla Pinctada mazatlanica (Hanley, 1945). Rev. Soc. Mex. Hist. Nat. 30: 223-262.

Skreslet, S. & E. Brun. 1969. On the reproduction of Chlamys islandica (O.F. Muller) and its relation to depth and temperature. Astarte 2: 1-6.

Somerton, D. A. 1980. A computer technique for estimating the size of sexual maturity in crabs. Can. J. Fish. Aquat. Sci. 47:1488-1494.

Thompson, R. J. 1977. Blood chemistry, biochemical composition, and annual reproductive cycle of the giant scallop, Placopecten magellanicus, from southeast Newfoundland. J. Fish. Res. Board Canada 34: 2104-2116.

Villalaz, G. J. R. 1994. Laboratory study of food concentration and temperature effect on the reproductive cycle of Argopecten ventricosus. J. Shellfish Res. 13:513-519.

Villalejo-Fuerte, M. & R. I. Ochoa-Baez. 1993. El ciclo reproductivo de la almeja catarina, Argopecten circularis (Sowerby, 1835), en relacion con temperatura y fotoperiodo, en Bahia Concepcion, B.C.S., Mexico. Ciencias Marinas 19:181-202.

Villalejo-Fuerte, M., B. P. Ceballos-Vazquez & Y. F. Garcia-Dominguez. 1996. Reproductive cycle of Laevicardium elatum (Sowerby, 1833)(Bivalvia: Cardiidae) in Bahia Concepcion, Baja California Sur, Mexico. J. Shellfish Res. 15:741-745.

Wada, K. T., A. Komaru, Y. Ichamura & Y. H. Kurosaki. 1995. Spawning peak occurs during winter in the Japanese subtropical population of the pearl oyster Pinctada fucata fucata (Gould, 1850). Aquaculture 133: 207-214.

Wolf, M. 1988. Spawning and recruitment in the Peruvian scallop A. purpuratus. Mar. Ecol. Prog. Ser. 42:213-217.

Zar, J. H. 1996. Bioestatistical analysis. 3rd ed. Englewood Cliffs, NJ: Prentice Hall. 662 pp.

MARCIAL ARELLANO-MARTINEZ, (1), * BERTHA PATRICIA CEBALLOS-VAZQUEZ, (1) MARCIAL VILLALEJO-FUERTE (1), FEDERICO GARCIA-DOMINGUEZ (1), JUAN FELIX ELORDUY-GARAY, (1) AARON ESLIMAN-SALGADO (2) AND ILIE S. RACOTTA (3)

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

(1) Centro Interdisciplinario de Ciencias Marinas, Instituto Politecnico Nacional Apartado Postal 592, La Paz, B.C.S. 23000, Mexico; (2) Reserva de la Biosfera el Vizcaino, Guerrero Negro, B.C.S. Mexico; (3) Centro de Investigaciones Biologicas del Noroeste, Apdo. Postal 128, La Paz, Baja California Sur 23000, Mexico