Annual reproductive effort of Pacific winged pearl oyster Pteria sterna and its relation with the timing for planning pearl seeding operations.
Article Type: Report
Subject: Crassostrea (Physiological aspects)
Oysters (Physiological aspects)
Bioenergetics (Research)
Energy metabolism (Research)
Oyster-culture (Research)
Calorimetry (Methods)
Authors: Caceres-Puig, Jorge I.
Caceres-Martinez, Carlos
Saucedo, Pedro E.
Pub Date: 08/01/2009
Publication: Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2009 National Shellfisheries Association, Inc. ISSN: 0730-8000
Issue: Date: August, 2009 Source Volume: 28 Source Issue: 3
Topic: Event Code: 310 Science & research
Product: Product Code: 0913050 Oysters NAICS Code: 114112 Shellfish Fishing SIC Code: 0913 Shellfish
Geographic: Geographic Scope: Mexico Geographic Code: 1MEX Mexico
Accession Number: 206172575
Full Text: ABSTRACT Using a combination of stereological and calorimetric methods, we studied reproductive effort of Pacific winged pearl oyster Pteria sterna during ah annual cycle in Bahia de La Paz, B.C.S., Mexico. The relationship between changes in the volumetric fraction of germinal and somatic tissues (gonad, digestive gland, adductor muscle, and mantle tissue) and changes in their energy content was analyzed. These data were also correlated with changes in water temperature and availability of food (seston). Because P. sterna spawns several times a year, reproductive effort was estimated ~400% in terms of energy increase from early development in October 2006 to the spawning occurring in January to February 2007. During this period, when water temperature was decreasing and seston concentration was increasing, P. sterna followed a conservative strategy for allocating energy from reserves previously stored in somatic tissues. In contrast, when productivity dropped in spring, the species followed an opportunistic strategy for sustaining gametogenesis from food energy. In decreasing order, total energy channeled for reproduction came from the digestive gland (23 kJ [g.sup.-1]), adductor muscle (19 kJ [g.sup.-1]), and mantle tissue (16 kJ [g.sup.-1]). Based on these results, we recommend that commercial pearl culture practices be conducted from mid-autumn (October) through early spring (April), when P. sterna is energetically more resistant to manipulation. An additional recommendation is to avoid grafting during the summer (June through September), when the species is energetically exhausted and highly vulnerable to manipulation.

KEY WORDS: Pteria sterna, reproductive effort, stereology, bioenergetics

INTRODUCTION

In temperate and subtropical areas, marine bivalves can only assimilate limited amounts of energy from the environment, so that somatic growth and reproduction are separated in time to maximize survival (Ziolko & Kozlowski 1983, MacDonald & Thompson 1985, Paulet & Boucher 1991, Duinker 2002). Acquired energy is usually stored in somatic tissues during periods of high food supply and subsequently mobilized to the gonad during times of food scarcity or high energy demand (Bayne 1976, Epp et al. 1988, Saucedo & Southgate 2008). From the total of energy incorporated to somatic tissues (total production), that allocated specifically to reproduction is defined as reproductive effort (Lucas 1992, Ramirez-Llodra 2002). Although this trait has important implications for reproductive output (fecundity) and success of marine bivalves, it has only been studied in species such as Argopecten irradians concentricus (Barber & Blake 1986), Pinctada margaritifera (Gangnery 1997) and Atrina maura (Barrios-Ruiz 2005).

Different from reproductive cycles, which are usually studied with conventional histological and/or biochemical methods, reproductive effort can only be determined with techniques involving other approaches, such as stereology and calorimetry. When combined, these techniques provide information of total production, reproductive effort, and changes in the volumetric fraction of a particular tissue in relation to its total energy content (not only per grato tissue). This knowledge is important because reproductive effort varies between species and populations of the same species, and influences the intrinsic value of each somatic tissue for acquiring and allocating available energy to the gonad. Among the Pectinidae, available energy used for gonad build-up comes entirely from the adductor muscle (Chantler 2006), whereas Mytilidae, Ostreidae, and Veneridae take up energy, not only from the digestive gland, muscle, and mantle tissue, but from other kind of nongerminal nourishing cells, such as VCT cells and ADG cells (Mathieu & Lubet 1993). In contrast, there is a significant lack of knowledge about the strategies for energy allocation during reproduction of the Pteriidae. In Pi. mazatlanica, the energy used to fuel gametogenesis comes firstly from adductor muscle and secondly from the digestive gland; muscle proteins are mobilized to the gonad only from February through May, whereas muscle carbohydrates are used only from June through October (Saucedo et al. 2002). In Pteria sterna (Gould, 1851), the energy devoted for gametogenesis comes mainly from the digestive gland and then from the adductor muscle; only proteins from these tissues are channeled to the gonad, because carbohydrates are stored despite the progress of gametogenesis (Vite-Garcia & Saucedo 2008).

In most pearl oyster species, the method for inducing pearl formation is related to their reproductive status, so that pearl beds are usually seeded when the gonads are empty (Haws 2002, Taylor & Strack 2008). At this moment, however, the oysters are exhausted from the very large loss of energy after spawning, becoming thus highly vulnerable to manipulation and grafting (Caceres-Martinez et al. 2006). Because of this, determining the content and variations of energy contained in the gonad and somatic tissues during gametogenesis may help identify moments of suitability for performing surgical grafting in commercial pearl farms.

This study of annual reproductive effort of Pacific winged pearl oyster P. sterna at Bahia de La Paz, Mexico used stereological and calorimetric methods to correlate changes in volume and energy values of germinal and somatic tissues with changes in water temperature and availability of food (seston). This is the first study analyzing reproductive effort in any Pteria species and is valuable because the genus has commercial value relating to pearl production in countries that include Australia (Beer 1999), Thailand (Arjarasirikoon et al. 2004), and Mexico (Kiefert et al. 2004).

MATERIALS AND METHODS

Collection of Specimens and Data for Field Analysis

Twenty adult P. sterna (73.1 [+ or -] 5.2-mm shell height) were collected monthly from a pearl farm in Bahia de La Paz, Baja California Sur, Mexico (24[degrees]16'N, 110[degrees]19'W) from May 2006 through April 2007. During each sampling, specimens were cleaned of fouling, measured for shell height and length to the nearest 0.1 mm, weighed to the nearest 0.1 g, and divided into two groups of 10 specimens each, which were used for stereological and calorimetric analyses, respectively. Water temperature ([+ or -]0.1[degrees]C) at the site was recorded with a digital thermograph, and mean monthly values were plotted along with maximum and minimum temperatures. Additionally, 1-L samples of water were collected in triplicate each month for determining total availability of food, as described by Luna-Gonzalez et al. (2000). Briefly, water samples were filtered in Whatman glass microfiber filters (Sigma # Z242330), rinsed with ammonium formate, dried at 100[degrees]C for 48 h, burned at 450[degrees]C, and weighed to 0.001 g. This value was used for estimating total seston, and by extrapolation, the organic (POM) and inorganic seston (PIM) fractions.

Stereological Analysis

Once registered data of size and weight of the first 10 specimens, their entire body tissues were excised, fixated in 10% formaldehyde solution (prepared with seawater to act as a buffer) for 48 h, and then transferred to 70% ethanol solution for proper preservation for stereology (Morvan & Ansell 1988). The visceral mass was cut into four equal sections, labeled LI, L2, L3, and L4 (Fig. 1). A zone labeled Le represented the area of union between sections L2 and L3 and was also the center of the axis cut of the visceral mass. Each section was measured to 0.1 mm and scanned at 1,200 dpi. The images were archived and analyzed with Image Pro Plus (v. 5.1; Media Cybernetics, Bethesda, MD) to obtain the surface of the gonad and each somatic tissue (digestive gland, adductor muscle, and mantle tissue). Data of mean surfaces of all tissues were used to estimate their total volume, adopting the principle of Cavalieri, which is based on the formula:

Volumetric fraction (VF)= ([S.sub.1] x [L.sub.2]/2 + [S.sub.2] x [L.sub.2]/2) + ([S.sub.2] x [L.sub.3]/2 + [S.sub.3] x [L.sub.3]/2),

where [S.sup.1] is the surface measured for section LI for tissue x; [S.sub.2] is the surface measured for zone Lc for tissue x; [S.sub.3] is the surface measured for section L4 for tissue x; [L.sub.2] is the width of section L2 from the first cut to the Le zone; [L.sub.3] is the width of section L3 from the Le zone to the last cut. The formula estimates the volume of the gonad and each somatic tissue in relation to the volume of the entire visceral mass. The estimates were expressed as percent values.

[FIGURE 1 OMITTED]

Calorimetric Analysis

The 10 specimens from the second group were dissected and the gonad and all somatic tissues were carefully removed. Once separated, they were wet weighed to 0.01 g and stored in plastic vials at -80[degrees]C. Tissue samples were lyophilized, dry weighed, and pulverized for preparing small pellets (0.2-1 g) that were burned in an adiabatic calorimeter to measure total energy from each tissue. Data of energy values were first expressed in calorie units and then transformed to kJ [g.sup.-1] using standard coefficients described by Lucas (1992).

Statistical Analysis

Data of size and weight of each specimen, as well as volume and energy of each tissue were first compared using the Kolmogorov-Smirnov test and then assessed with one-way ANOVA for significant differences over time. When necessary, post hoc multiple-range mean comparisons with the Tukey test were included (Sokal & Rohlf 1981). A linear regression analysis was performed for volume (mL) and weight (g) relations of each tissue to obtain a coefficient of the volume per weight unit (mL [g.sup.-1]), as well as volume data estimated for each tissue fraction. These values were transformed into wet weight units. Additionally for each tissue, we subtracted dry-lyophilized weights from individual wet weights for estimating dry weight values per each tissue fraction. These values were correlated with those of energy content and then expressed as dry weight for each tissue (kJ [g.sup.-l]). Significance was set at P < 0.05 for all tests.

RESULTS

Stereological Analysis

Temporal changes in the volume of the gonad and somatic tissues are shown in Figure 2. For all tissues, changes followed a clear seasonal trend, with a peak in October 2006 (2.3-3.8 mL) and a minimum in January 2007 (1.2-2.0 mL). These changes were significant over timer and included, in decreasing order, the digestive hl 8.91), adductor muscle (F = 8.39), gonad (F = 5.91), and mantle tissue (F = 4.94).

Calorimetric Analysis

Energy content did not vary markedly during the annual cycle (Fig. 3); values ranged from 15-20 kJ [g.sup.-1] for all tissues. The exception occurred in the digestive gland, where the content of energy varied seasonally and showed a maximum in September 2006 (25.4 kJ [g.sup.-1]) and a minimum in January 2007 (18.8 kJ [g.sup.-1]). The gonad did not undergo significant changes in energy content (F = 1.67), whereas changes were more significant for the digestive gland (F = 14.78), adductor muscle (F = 4.55), and mantle tissue (F- 4.38).

The relationship between volume and weight of each tissue was significantly fit to a linear model (r = 0.98), which indicated a robust relationship between the weight of the entire visceral mass and its volume, as it was the estimation of the volumetric coefficient of the visceral mass expressed per weight unit.

Variations in total energy of the gonad and somatic tissues (expressed in dry weight units) followed an inverse relation over time (Fig. 4). The digestive gland, adductor muscle, and mantle tissue contained the least store of energy in May 2006 (7.0, 5.9 and 8.6 kJ [g.sup.-1], respectively) and January 2007 (5.6, 5.8, and 6.9 kJ [g.sup.-1], respectively) and the highest store of energy in October 2006 (~13.2 kJ [g.sup.-1]) and April 2007 (14, 14.4, and 18 kJ [g.sup.-1] respectively).

Field Analysis

Annual variations of water temperature and POM of seston (Fig. 5) were compared with those of volume (Fig. 2) and energy (Figs. 4) of germinal and somatic tissues. Temperature decreased from October 2006 through January 2007 and was accompanied by maximum energy within the gonad and minimum energy within the digestive gland, adductor muscle, and mantle tissue. In contrast, the lowest energy level in the gonad occurred in September 2006, when water temperature was highest. From January through April, no clear relationship between water temperature and energy contained in the gonad and somatic tissues was observed.

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

For the gonad, the highest energy content occurred when POM was lowest. Volume and energy content of adductor muscle gradually increased with an increase in the POM concentration in July and September 2006. Similarly, when POM dropped from October through December, volume and energy values of this tissue also dropped. The pattern of energy storage within the digestive gland and mantle tissue had no relation with changes in POM. After values peaked in September, there was an increase in the energy content of the two tissues in October 2006, followed by gradual declines in their energy and POM values until April 2007, when both indicators increased again.

DISCUSSION

The stereological and calorimetric approach to study reproductive effort of P. sterna at Bahia de La Paz (Mexico) allowed us to measure variations in the energy content per gram tissue, as well as total energy per entire tissue compartment that have involvement in the transfer of energy to the gonad for gametogenesis. Considering the value of minimum energy of each tissue as its basal level (100%), we estimated a first increase in energy in all tissues of nearly 200% at the onset of gametogenesis in October 2006. After this energy increase, almost all the energy stored in somatic tissues was used for gonad development until spawning occurred in January to February 2007. This result suggests that P. sterna followed a conservative strategy for regulating gametogenesis during this period, likely because water temperature was decreasing and seston content was increasing. There was a new and sharp increase of nearly 250% in the energy contained in somatic tissues from February through Apri12007, but these reserves were not used despite the progress of gametogenesis. In this case, the evidence indicates that P. sterna followed an opportunistic strategy to sustain gonad development during this period, fueled by the energy obtained from food. Scenarios like this, where a species combines conservative and opportunistic strategies to regulate gametogenesis seem typical of ecotones that are transitional between temperate and tropical provinces, where there are marked seasonal changes in water temperature and food productivity (MacDonald & Thompson 1985, Paulet & Boucher 1991, Duinker 2002). We identify other bivalve species from transitional areas that display similar changes from conservative to opportunistic strategies to regulate reproduction. This is true for Pecten maximus from Northwestern Spain (Pazos et al. 1997), Ar. ventricosus from Bahia de La Paz, Mexico (Luna-Gonzalez et al. 2000), Crassostrea gigas from North Korea (Kang et al. 2000), and Pi. mazatlanica from Bahia de La Paz (Saucedo & Southgate 2008).

[FIGURE 4 OMITTED]

[FIGURE 5 OMITTED]

Given the marked variations in energy content of the gonad that P. sterna experienced throughout the year, total reproductive effort was measured again from its basal level (= 100%) in October. From this value, we estimated an increase of ~400% to reach the stage of gonad ripeness, which would ensure the maximum rate of gamete release. We noted, however, that 50% of this energy (200% of the basal energy) was lost after spawning and left the next cycle with hall this value. Similarly, Barrios-Ruiz (2005) studied reproductive effort of the penshell A. maura in Laguna San Ignacio (Baja California Sur, Mexico) using a stereological approach and calculated 200% energy loss from the onset of gametogenesis to spawning. In contrast, Heral & Deslous-Paoli (1983) reported that C. gigas from the French Atlantic coast lost only 53% to 63% of its basal energy after spawning. We believe that P. sterna do not consume all of its energy reserves because it spawns multiple times over the year in most areas of the Gulf of California (Hernandez-Diaz & Buckle-Ramirez 1996, Saucedo & Monteforte 1997, Hernandez-Olalde 2007, Vite-Garcia & Saucedo, 2008). Hence, nutrients from residual gametes that remain viable within acini after a partial spawning are rapidly recycled to give rise to short breeding cycles. For example, after the main spawning season that occurred at the end of the winter, there were still low water temperatures and high seston contents (POM) that triggered a new, short breeding cycle in the early spring. In support of this finding, some authors (Besnard 1991, Paulet & Boucher 1991, Robinson 1992, Duinker 2002, Chavez-Villalba 2001, Saucedo et al. 2002) have noticed that species such as P. maximus, C. gigas, and Pi. mazatlanica can delay or skip the spent stage when field conditions, particularly water temperature and seston abundance, remain favorable after a population spawning.

In terms of reproductive effort, our results show that the digestive gland contributed nearly one quart (23 kJ [g.sup.-l]) of the total energy needed to activate and sustain gametogenesis, whereas the adductor muscle contributed 19 kJ [g.sup.-1]. Similarly, gamete production in Ar. irradians concentricus requires the catabolism of 19.9 kJ of somatic energy reserves (Barber & Blake 1986). Our results are also consistent with findings by Vite-Garcia and Saucedo (2008) that the digestive gland (first) and adductor muscle (second) are the most important energy reservoirs for overall development of the gonad in P. sterna, contributing with 17 and 13 kJ [g.sup.-1], respectively. Conversely, when comparing the volume of both tissues with their total energy values, a different scenario arises, indicating that the adductor muscle has a larger role than the digestive gland for fueling gametogenesis. This new finding, which disagrees now with that of Vite-Garcia & Saucedo (2008), may be the result of comparing data of biochemical composition expressed in mg per grato tissue versus those determined by stereology and calorimetry, which denote total energy contained per entire tissue compartment. The finding, however, is in agreement with that of Saucedo et al. (2002) showing that adductor muscle (firstly) and digestive gland (secondly) are the two somatic tissues channeling more energy for reproduction of subtropical Pi. mazatlanica in the same location (Bahia de La Paz). The result is also consistent with the intrinsic values attributed to both tissues in the Pectinidae, where adductor muscle is recognized as the most important energy storage repository for reproduction (see reviews by Chantler 2006 and Roman et al. 2002).

The role of mantle tissue was secondary for reproduction in this species, because it only contributed ~16 kJ [g.sup.-1]. Similar reports of the secondary or negligible role of mantle tissue for overall development of the gonad are reported for A. irradians irradians (Epp et al. 1988), Ar. ventricosus (Racotta et al. 1998, Racotta et al. 2003), Nodipecten nodosus (Lodeiros et al. 2001), Pi. mazatlanica (Saucedo et al. 2002), and for P. sterna (Vite-Garcia & Saucedo 2008). However, when analyzing the data of total energy content of this tissue in relation to its corresponding volumetric fraction, mantle tissue seems to be a more active participant in reproduction. In N. subnodosus from Laguna Ojo de Liebre in Mexico, Arellano-Martinez et al. (2004) also observed depletion of mantle proteins during early gonad development, together with depletion of mantle glycogen during final ripening and spawning phases. This depletion indicates an important participation of this tissue to sustain gametogenesis in this species.

For Pteriidae, it is a general observation that oysters destined for surgical grafting at pearl farms should not have much gonad development to facilitate seeding of the saibo (mantle) allograft and reduce stress (Haws 2002, Taylor & Strack 2008). This is true for the three common pearl-producing species: Pi. fucata, Pi. margaritifera, and Pi. maxima. In P. sterna, our results of measuring reproductive effort have application in commercial cultivation ofpearls, by helping to identify the moments of suitability or unsuitability for grafting. For example, the oysters are energetically more resistant to manipulation and respond favorably to stressful conditions of grafting from mid-fall (October) to early spring (April). Conversely, we recommend avoiding grafting during the summer (June through September), when availability of food declines, water temperature peaks, and the oysters ate exhausted, have very low energy reserves, and they are highly vulnerable to manipulation.

ACKNOWLEDGMENTS

This study is part of a Master's project supported by Mexican Research Council (CONACYT) as a scholarship given to the first author. This study was also done as part of a collaborative agreement between CIBNOR and the pearl oyster farm "Perlas del Cortez". The authors thank the staff, for assistance during collection of specimens; S. Rocha and F. Hernandez at CIBNOR, for technical support during sample processing; I. Fogel for a final editorial review of this manuscript, and M. Arellano-Martinez at CICIMAR for valuable comments.

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JORGE I. CACERES-PUIG, (1,2) * CARLOS CACERES-MARTINEZ (3) AND PEDRO E. SAUCEDO (1),*

(1) Centro de Investigaciones Biologicas del Noroeste (CIBNOR) Mar Bermejo 195, Col. Playa Palo de Santa Rita, La Paz, B. C. S., 23090, Mexico; (2) perlas del Cortez, S. de R.L. MI. Anuiti 4723, Col. Pericues, La Paz B.C.S., 23090, Mexico; (3) Universidad Autonoma de Baja California Sur (UABCS), Km 5.5 Carretera al Sur, La Paz, B.C.S., 23080, Mexico

* Corresponding author. E- mail: psaucedo04@cibnor.mx
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