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Growth and survival of the winged pearl oyster sterna (Gould, 1851) in suspended culture in the tropical Eastern Pacific: Influence of environmental factors

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ORIGINAL ARTICLE

Growth and survival of the winged pearl oyster Pteria sterna (Gould, 1851) in suspended culture in the tropical Eastern Pacific: Influence of environmental factors

Cesar Lodeiros1,2 | Daniel Rodrıguez-Pesantes1 | Adrian Marquez 1 | Jormil Revilla1 | Luis Freites2,3 | Carla Lodeiros-Chacon 4 | Stanislaus Sonnenholzner1

1Escuela Superior Politecnica del Litoral, ESPOL, Centro Nacional de Acuicultura e Abstract Investigaciones Marinas, CENAIM, The growth, survival and influence of environmental factors were analysed in two Guayaquil, Ecuador cohorts of cultured Pteria sterna in Ayangue Bay, Province of Santa Elena, Ecuador 2Instituto Oceanografico de Venezuela, Universidad de Oriente, Cumana, Venezuela (tropical Eastern Pacific). Juveniles representing cohorts I and II (8.4 0.54 and 3Universidad Estatal Penınsula de Santa 5.0 0.17 mm in dorso-ventral axis) were deployed in November 2015 and Febru- Elena (UPSE), Santa Elena, Ecuador ary 2016, and grown in pearl nets suspended in a long line for 12 and 10 months 4Master Interuniversitario en Acuicultura, Universidades de Santiago de Compostela, respectively. The stocking density was monthly and bi-monthly reduced during sam- ~ ~ La Coruna, Espana pling of individuals to determine growth in dorso-ventral shell axis, dry mass of

Correspondence shell, soft tissues and dry mass of fouling on shell. Water temperature, salinity, total Cesar Lodeiros, Escuela Superior Politecnica seston and phytoplankton biomass (chlorophyll a) were determined at the culture del Litoral, ESPOL, Centro Nacional de Acuicultura e Investigaciones Marinas, site. Results showed that P. sterna reached ~100 mm in length during the first year CENAIM, Guayaquil, Ecuador. of culture. Although little negative influence of environmental factors was detected, Email: [email protected] high temperatures during the reproduction period can be the most negative influen- tial trait. The highest tissue mass (6 g), which occurred at the 10th month of cultiva- tion, as well as a high availability of spat by artificial collectors in the coastal waters, showed that the species can be considered a good candidate for aquaculture in the tropical eastern Pacific.

KEYWORDS American Pacific, aquaculture, growth, pearl oyster, tropics

1 | INTRODUCTION regions, including tropical areas, are suitable for the cultivation of pearl oysters, particularly for P. sterna (Serna-Gallo et al., 2014). In In the tropical and subtropical American Pacific, there are several equatorial waters, it has been observed a high, although periodic, species of bivalve mollusks with potential to produce pearls, but only availability of P. sterna spat through natural catch using artificial col- two (the mother pearl oyster and the winged lectors (up to 4–5 juveniles of 10 mm in 5 cm2 of sardine fishing net pearl oyster Pteria sterna) produce an iridescent nacre suitable for -personal observation), which could support a growing industry, with quality pearls (Kishore, Southgate, Seeto & Hunter, 2015; Southgate interest in the production of pearls and/or food, as well as byprod- et al., 2008). Although some pearl production trials have been con- ucts that can be made with its shell. ducted in the American Pacific, only Mexico has promoted a low- Although P. sterna has a distribution from Morro Santo Domingo, scale pearl industry in the subtropical zone of Baja California Sur in Baja California (28.2°N), to Ancon, Lima, Peru (11.8°S) (Coan & and Sonora, and certain information has been produced on this sub- Valentich-Scott, 2012), and has commercial importance, there are ject (Lodeiros, 2014; Monteforte, 2013; Saucedo, Castillo-Domınguez few studies on its aquaculture feasibility in tropical areas. Only & Melgar-Valdes, 2015; Southgate et al., 2008). However, many Serna-Gallo et al. (2014) demonstrates the feasibility of P. sterna

832 | © 2017 John Wiley & Sons Ltd wileyonlinelibrary.com/journal/are Aquaculture Research. 2018;49:832–838. LODEIROS ET AL. | 833 cultivation in the Bay of Acapulco, Mexico (16°N), but dependent on 2.3 | Fouling and environmental factors spat production in the laboratory. Some preliminary studies (Jara, Gregori & Freites, 2016; Trevino~ & Figueroa, 2009) show high In order to estimate the impact of environmental factors (including growth rate in equatorial waters (0° and 2°S). At this moment, more fouling) on the growth of the pearl oyster, water samples (in triplicate) studies are necessary to examine growth and survival in tropical were collected weekly between 0.5 and 1 m of sea surface with 12 L waters to determine the feasibility of P. sterna cultivation. These plastic bottles. Sub-samples of water were obtained for the determina- studies must be accompanied by records of environmental factors, tion of salinity (with a refractometer, 0.1 of precision), as well as seston to estimate, from an integrated eco-physiological point, the possible and phytoplankton biomass. For the latter, water samples previously causes that could influence the growth and survival, in order to filtered with 153-lm pore size mesh to eliminate macroplankton, were establish cultivation strategies. For instance, food availability and transferred to dark plastic bottles (2 L) to be transported to the labora- temperature should be considered, since it has been determined that tory, in order to estimate the phytoplankton biomass by the concen- they are the main factors controlling the growth and reproduction of tration of chlorophyll a, and total seston. These analyses were tropical pearl oysters (Freites et al., 2017; Pouvreau, Bacher & Heral, performed by retaining the sample particles in Whatman GF/C filters 2000; Pouvreau & Prasil, 2001; Serna-Gallo et al., 2014; Tomaru, (1.2 lm pore diameter) using Millipore vacuum filtration equipment. Kumataba, Kawabata & Nakano, 2002). For the determination of chlorophyll a the spectrophotometric method The present study evaluates the growth and survival of two was used and the seston method was performed using gravimetric P. sterna cohorts under suspended cultivation conditions and the techniques following Strickland and Parsons (1972). The temperature influence of environmental factors associated to equatorial waters of was continuously recorded every 30 min or 1 hr using an electronic the Eastern Tropical Pacific Ocean. thermograph (Hobo, Onset, MA, USA). Shell fouling (organisms and material deposited on shell) was scraped and its weight determined as dry mass with an analytical 2 | MATERIALS AND METHODS balance (0.001 g of precision), after a dehydration process by heat treatment (60°C until reaching constant weight). The fouling index 2.1 | Experimental culture was estimated as the % in dry mass of fouling in relation to the dry The study was carried out in Ayangue Bay, Province of Santa Elena, mass of shell. Ecuador (1°5901.59″S; 80°45035.15″W). Two lots of juveniles that recruited on sardine fishing net collectors at two time periods of the 2.4 | Statistical analysis year, were suspended (2–4 m in depth) from an experimental long line, and identified as cohort I to those juveniles for which the The contrasts of the means of each growth variables between succes- experimental culture started in November 2014, and cohort II in sive samples in each cohort, or between cohorts in a particular sample, February 2015. The juveniles measured 8.4 0.54 mm (cohort I) were made by Student’s t-test at a probability of .05. To evaluate the and 5.0 0.17 mm (cohort II) in dorso-ventral length. The juveniles effect of environmental factors on growth of the pearl oyster, we exam- (>2,000 in each cohort) were confined in several pearl nets (initially ined the relationship of changes in body components to environmental 3 mm mesh size, increasing it as the crop evolved) maintaining a factors using a stepwise multiple regression procedure applied to Log density equivalent to 25%–30% coverage of the basket base. (X + 15) transformed data, following Hair, Black, Babin and Anderson Monthly or bi-monthly samplings were made on the pearl nets, (2014). The probability of entry of the variables in the models was .05. decreasing the number of individuals per basket according to the cri- The regression analysis was performed between the daily specific teria established. Lots of four to six baskets were protected with a changes in shell (length and mass) and in the mass of soft tissues with cover bag made of sardine fishing net (10 mm mesh size), in order the mean of each environmental factor corresponding to the same per- to avoid the incidence of predators, mainly fish of the family Balisti- iod. The daily specific change was the mean daily change between two dae (Sonnenlhozner, Marquez & Lodeiros, 2017). The cultivation subsequent sampling dates divided by pearl oyster size mass or length periods of cohort I and II were 12 and 10 months respectively. at the earlier sampling date. All environmental variables were used except salinity, due to its high correlation with the other environmental variables and possible collinearity effects. It was also considered that 2.2 | Growth parameters and survival the maximum range of variability in salinity was only 4, and did not During each sampling, five individuals were taken from each of three appear to influence any physiological process in the pearl oyster. culture replicates and alive pearl oysters were counted. The remain- ing baskets were kept under the same conditions for replacement 3 | RESULTS purposes. The dorso-ventral length was determined with a digital caliper (0.01 mm of precision), as well as the dry mass of the soft 3.1 | Growth body and shell with an analytical balance (0.001 g of precision), after a dehydration process by heat treatment (60°C until reaching con- Both cohorts showed a growth curve in length with a generally lin- stant weight). ear trend (Figure 1a) and reached over 90 mm at the end of the 834 | LODEIROS ET AL.

tissues of cohort I, and 26.4 3.49 and 2.9 0.30 g for cohort II respectively. Equating the growing time to 10 months, cohort I sig- nificantly exceeded the biomass reached by cohort II.

3.2 | Survival

Survival in cohort I remained above 90% until the end of September, when it decreased to 85% (Figure 2). In contrast, survival in cohort II was >90%, except for the month of June (87.7%). At the end of the experimental period, the cumulative survival for both cohorts was >60%.

3.3 | Environmental factors

The dry mass of the fouling observed in the shells of cohort I showed an almost sustained increase from March to August 2015, when the values exceeded 4.5 g; then, the fouling mass decreased until the month of November 2015, with values smaller than 3 g (Figure 3a). Cohort II generally followed the same growth pattern of I, with exponential increases up to September when it reached 3 g, to decrease between 2.5 and 3 g at the end of the study. The per- centage of fouling with respect to shell mass followed a similar trend of the fouling mass on the shell, except in the first months of the study (Figure 3b). Values were in a range of 4%–29% and 5%–24% for cohort I and II respectively. The average daily temperature showed a sustained trend, with marked variations in small periods of 2–3 days, reaching peaks above 28°C between March and June 2015, and then decreased gradually to August. It increased again to peaks above 27°C in December 2015 (Figure 4a). Also, abrupt decreases were observed in late Jan- uary to early February 2015 and mid-March, with immediate recov- eries of the temperature level in those periods. Intraday temperature range reached more than 6°C (mid-March 2015). Higher intraday temperature variation was observed during Jan-Feb (4°C), Feb-Apr (up to 6°C), and Jun-Jul (4.3°C); variation during the rest of the study was <1°C (Figure 4b).

FIGURE 1 Growth in dorso-ventral length (a), dry mass of the shell (b) and soft tissues (c) of the Winged Pearl Oyster P. sterna under suspended culture conditions in Ayangue Bay, Santa Elena Province, Ecuador. Vertical lines show a 95% confidence interval experimental period: 97.3 2.01 mm at 12 months of culture for cohort I and 91.6 9.06 at 10 months for cohort II, without show- ing significant differences between them. The shell (Figure 1b) and soft tissue (Figure 1c) masses showed low growth during the first 3 months, and then increased signifi- cantly, expressing an exponential trend. An exception was observed towards the end of the experimental period (late September to late November 2015), when the tissue growth declined in cohort II and decreased in cohort I. In spite of this, at the end of the study period, FIGURE 2 Monthly survival of winged pearl oyster P. sterna cohort I showed significantly higher biomasses. The average bio- under suspended culture conditions in Ayangue Bay, Province of masses reached 54.3 3.84 g for shell and 6.3 0.87 g for soft Santa Elena, Ecuador. Vertical lines show a 95% confidence interval LODEIROS ET AL. | 835

FIGURE 3 Total fouling mass (a) and its percentage relative to FIGURE 4 Daily average (a) and intraday range variation (b) of the shell mass (b) of the winged pearl oyster P. sterna under temperature at the winged pearl oyster P. sterna culture site in suspended culture conditions in Ayangue Bay, Province of Santa Ayangue Bay, Santa Elena Province, Ecuador Elena, Ecuador. Vertical lines show a 95% confidence interval

Seston showed great variability in a range generally between 5 linear length shell growth (without reaching an asymptote of maximum and 15 mg/L, with a high period (>15 mg/L) in April 2015 and a low sizes) and an exponential growth in masses of shell and soft tissues, period (<5 mg/L) between mid-September and late October (Fig- typical of bivalve molluscs (Urban, 2002). In general, this behaviour sug- ure 5a). Chlorophyll a fluctuated between 2 and 4 lg/L during most gested that organisms were not stressed physiologically. Only at the part of the experiment (Figure 4b). Peaks above 7 lg/L were end of the study period, a deceleration (Cohort I) and decrease (Cohort observed in early February 2015 and October to November 2015. II) of soft tissue growth rates were observed. Although a suitable repro- Salinity remained above 33.6 with the lowest salinity (32.5) in March ductive condition study was not performed, both full and flaccid and October (Figure 5c). gonads were visually observed in cohort I during the last 3 months of Multiple regression analyses (combining all the variability gener- culture, suggesting that gonadal developmental activity and spawning ated in cohorts I + II) yielded little explanation of the growth variability had occurred. Reproduction, as an endogenous process, and high tem- (<25%, Table 1). The variability of the percentage of accumulated foul- perature as an exogenous one in the last months (26.5–27.5°C), could ing with respect to shell mass was the only environmental variable sig- have performed an additive or synergistic action leading stress on the nificantly explaining the variability of the growth in length and tissue pearl oyster, with the consequent growth decrease and the lowest sur- masses. In the same way, only the range of intraday temperature vari- vival rate observed in the study (85%). The studies of Meza-Buendia ability could explain the shell growth variability. In attempting to con- (2016) on the influence of temperature on the physiological processes struct the models to describe the growth of each cohort, no of P. sterna support the above hypothesis, since the optimal metabo- environmental factor entered significantly into them. lism of P. sterna is found between 22 and 25°C, while the critical limit is at 28°C. This last temperature is close to the value observed towards the end of the experimental period. Similarly, Serna-Gallo et al. (2014) 4 | DISCUSSION reported an association between the decline in growth rates and the reproductive period of P. sterna at high temperatures. The winged pearl oyster P. sterna kept under suspended culture condi- On the contrary, periods of low temperature (with high food tions in the Ayangue Bay, Santa Elena Province, Ecuador, showed a availability) could lead to energy storage processes in bivalve with 836 | LODEIROS ET AL.

TABLE 1 Step wise multiple regression models to explain the growth of P. sterna in suspended culture in Ayangue Bay, Santa Elena Province, Ecuador, according to the variability of environmental factors

Growth parameter Equation R2 Length 1.175 + 0.00058% fouling 0.23 Shell mass 1.101 + 0.064 Tinter 0.24 Soft tissues mass 1.172 + 0.0041% fouling 0.18

Salinity was not included in the analyses because of its high correlation with the other environmental variables and possible collinearity effects. % Fouling = proportion of the fouling mass with respect to the shell mass. Tinter = intraday temperature range. Data analysed and expressed in Log (X + 15). Input of independent variables to the model p < .05.

Mazouni, 2014; Lodeiros & Garcıa, 2004; Lodeiros & Himmelman, 1996). This negative effect is more pronounced in species with hori- zontal arrangement (Lodeiros, 2002), than those with vertical arrangement such as P. sterna. Furthermore, the fouling index was <30%, suggesting that the shell ligament could support this little additional weight. However, the multiple regression analyses used to explain growth variability (length and mass) suggest an environmen- tal influence of the fouling index (percentage fouling mass with respect to shell mass). This relationship could be associated with the slower growth rate of shell mass at the beginning of the experiment. These effects, detected in multiple regression analyses with fouling, can camouflage the effect of other environmental variables on bivalves under cultivation (Lodeiros & Himmelman, 2000). Another factor that significantly contributed to the models was the intraday temperature variability. This factor (which can reach >6°C), seems to affect the growth of cultivated organisms. However, its association with growth rate was positive. The lack of evidence about the negative influence of temperature on growth, except for the possible effect of temperature together with the reproductive process (highly demanding energy to P. sterna; Vite-Garcıa & Sau- cedo, 2008) indicated above, suggests that P. sterna could be evolu- tionarily adapted to the great variability of temperature and other environmental factors that occur in the peninsular coasts of Ecuador, since it is a transition zone of the American Pacific, characterized by FIGURE 5 Total seston (a), phytoplankton biomass estimated by a remarkable spatial and temporal variability of the oceanographic chlorophyll a (b) and salinity (c) at the winged pearl oyster P. sterna conditions (Allauca, 1990). culture site in Ayangue Bay, Santa Elena Province, Ecuador Pteria sterna, in this study, reached sizes of about 100 mm in the reproductive capacity, prior to reproduction (Bayne & Newell, 1983). first year of cultivation, which is the highest growth rate so far This could explain the abrupt increase in soft tissues in cohort I (or- reported for this species under cultivation conditions. For example, ganism >70 mm), during the period from late June to late August in the northern subtropical American Pacific, Buckle-Ram€ ırez, Volto- 2015, coinciding with low sea surface water temperatures. This situ- lina, Morales and Valenzuela (1992) report maximum sizes of 94 mm ation may explain the differences in soft tissue masses between the at 14 months in the Bay of Los Angeles, Baja California, Mexico two cohorts, since individuals of cohort II during this period were (29°020N, 113°320W). Gaytan-Mondragon, Caceres-Martınez and still juveniles with no reproductive capacity (organisms <50 mm; Tobias-Sanchez (1993), in the Bay of La Paz, Baja California Sur, Saucedo & Monteforte, 1997a,b). Studies on the influence of repro- Mexico (24°160N; 110°190W) showed that P. sterna grown in differ- duction and environmental factors on the growth of P. sterna are ent systems and culture means (bottom culture and suspension, pearl necessary to elucidate this hypothesis. net, lantern nets, poket nets, cages) reaches 103–106 mm, but in The weight of the fouling on the shell can influence the growth 18 months. On the other hand, Saucedo and Monteforte (1997a,b) of several bivalves under culture conditions (Lacoste & Gaertner- observed in the same bay, that P. sterna reaches sizes close to LODEIROS ET AL. | 837

80 mm in a year under bottom culture conditions (beginning with ACKNOWLEDGMENTS juveniles of about 30 mm). The work has been carried out as a complementary part of the The sizes reached in the present study are higher than those research project “Development of domestication protocol for the reported in tropical waters of Mexico (Bahıa de Acapulco, Guerrero, sustainable use of new marine species for food consumption and 16°50 N, 99°54 W) by Cantu-Cantu (2003) of 50 mm in 7 months repopulation of natural banks, financed by SENESCYT, Ecuador”. and by Serna-Gallo et al. (2014) of 60 mm in 1 year. Preliminary Cesar Lodeiros and Luis Freites participated in the study during their studies of P. sterna cultured in equatorial waters (Jara et al., 2016; linkage with CENAIN-ESPOL and UPSE, respectively, through the Trevino~ & Figueroa, 2009) show high growth rates (7–14 mm/ Prometeo project of SENESCYT, Ecuador. month), although their experiments did not reach 100 mm sizes. This suggests that the high growth rates of P. sterna in equatorial waters CONFLICT OF INTEREST are indicative of the species’ potential to quickly obtain the minimum sizes required for induction of pearl production (70–80 mm; Sau- All authors have no conflict of interest. cedo, Monteforte & Blanc, 1998; Serna-Gallo et al., 2014), which can be achieved in about 7–8 month, according to the growth curve of cohort I. These results contrast with the 24 month projection that ORCID Gaytan-Mondragon et al. (1993) estimate to reach the appropriate Cesar Lodeiros http://orcid.org/0000-0001-9598-2235 size for nuclei implantation in this species, in the Mexican Pacific. The winged pearl oyster P. sterna may also be an emergent spe- cies suitable for food production, either for direct or processed con- REFERENCES sumption (canned, marinated with vinegar, etc.), due to the edible Allauca, S. (1990). Presencia de la corriente costanera ecuatoriana. 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