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BYSSUS GROWTH IN WINGED PEARL OYSTER PTERIA PENGUIN (RODING, 1798).

INTRODUCTION

Byssi are secreted by pearl oysters to anchor them to various substrates (Wada & Temkin 2008), and the duration of byssal attachment may vary among species. Pinctada margaritifera and Pinctada fucata, for example, continue active byssus secretion throughout their lives (Gervis & Sims 1992), whereas Pinctada maxima cease byssal secretion once large and heavy enough to withstand agitation or dislodgement caused by ocean currents (Taylor et al. 1997). Byssus growth in pearl oysters is influenced by many factors including water temperature, pH (Welladsen et al. 2011), salinity (O'Connor & Lawler 2004), and local currents (Taylor et al. 1997). The impact of the age of individuals, however, has been much less thoroughly investigated, and the only report existing demonstrated that the number of byssal threads produced diminished as P. maxima aged (Taylor et al. 1997).

Oysters can deliberately shed their byssus by first ejecting the existing threads, and afterward, secreting new threads. In some cases, attachment was observed even before the old byssus threads had been entirely cast off (Dharmaraj et al. 1987). The occurrence of adult individuals without byssus in lantern-cultured Pteria penguin has been reported (Vasquez et al. 2017), and, occasionally, when the byssus has been completely shed, oysters do not exhibit byssus regeneration (Wang unpublished data). Vasquez et al. (2017) reported that the length and diameter of the byssus was closely related to the weight of the animal rather than the size of the shell in young oysters. But, as individuals continued gaining weight, no further increase in the byssus diameter (BD) was measured, suggesting the existence of a threshold for the BD in heavier and older oysters.

Historically, cultivation of Pteria penguin in China has been carried out mainly for the production of mabe pearls (Zhifeng et al. 2013). Experimentation in free round pearl production has not been capable of yielding a successful harvest. The predominant reason for failure was that the oyster rapidly rejected most of the newly inserted nuclei. In Pinctada margaritifera, the presence of the byssal organ in close proximity to the developing pearl-sac has the potential to impact pearl-sac formation and the resulting pearl quality (Kishore & Southgate 2016). On this basis, it becomes essential to accurately describe byssogenesis in P. penguin, considering the byssus is remarkably strong (Rao 1960, Morton 1995, Wada & Temkin 2008). To assist in optimizing cultivation practices for cultured P. penguin, this study augments the available data to include a more precise and discriminating description of the byssogenesis in oysters at different sample dates during the first year of cultivation in the sea.

MATERIALS AND METHODS

Broodstoek and Larval Culture

Pearl oysters Pteria penguin were obtained through larviculture carried out at the Wuzhizhou Island Marine Mollusks Laboratory, Hainan University. Briefly, a number of 3-y-old stock were collected from a commercial farm at Wuzhizhou Island (18[degrees] 19' 1 "N, 109[degrees]45'43"E). Oysters were transported to the laboratory, where they were cleaned and further divided into males and females by using gonad biopsy. Twenty female and 20 male oysters were induced to spawn using the protocols for Pinctada fucata martensii (Zhifeng et al. 2011). After 12-15 days postfertilization, competent larvae were set on polyethylene rope-type collectors.

Cultivation Method and Site

Once seed reached a shell length of 2-3 mm, the collectors, together with the seed, were taken from the hatchery and placed into 1-mm mesh sleeves, and hung from long-lines at a depth of 3 m at a pearl oyster farm located near Wuzhizhou Island, Hainan, P. R. China. Later, seed were carefully detached from the collectors and transferred to lantern nets at a regular spacing of 1 m on the long line.

Biometry

Monthly between 50 and 300 oysters were collected and kept moist in cool boxes for transport to the laboratory for analysis within 48 h of collection. Shell height (SH) measurements ([+ or -]0.1 mm) were conducted from June 2016 to June 2017, whereas the measurement of total wet weight (TW; [+ or -]0.1 g) and BD (0.1 mm) began on September 2016 when oysters were heavy enough to allow for a reliable weight measurement.

Byssus Diameter Measurement

A group of 50-100 oysters were kept in a freezer at -20[degrees]C for at least 24 h and later thawed to facilitate removal of the byssus from the oyster body. After each byssus was removed, BD ([+ or -]0.1 mm) at the proximal section was measured as described in Vasquez et al. (2017) utilizing a Mustcam USB digital microscope (5M pixels image sensor and magnification 10X to 300X).

Statistical Analysis

Absolute growth rate (AGR) of SH, TW, and BD was calculated using the following equation:

AGR = y/t, (1)

where y was SH, TW, or BD, and t the age in days.

Before any statistical analysis, any outliers were identified and removed using the boxplot.stats function that applies the Tukey's method of identifying outliers ranging more than and less than the 1.5 interquartile range approach. All data groups were first checked to avoid violation of the linearity and homoscedastic assumptions of simple linear regression by interpreting residual plots and histograms of residuals constructed using residPlot from the Fisheries Stock Assessment package (Ogle 2016) and Shapiro--Wilk's test assessed normality.

Post hoc Tukey honest significant difference multiple comparison test was conducted to assess differences in the BD growth among sampling dates.

All biometric relationships were determined as previously described in Vasquez et al. (2017) and were performed at 68, 183, and 366 days of cultivation. Briefly, the degree of association between the relations SH-BD and TW-BD were calculated by the determination coefficient ([r.sup.2]), and its level of significance was then determined using one-way analysis of variance (ANOVA). Relations were considered significant at P < 0.05. Curve fitting and plotting were conducted using the ggplot package (Wickham 2009). All statistical analyses were assessed in R (R Development Core Team 2016).

RESULTS

The means values for SH, TW, and BD in the pearl oyster Pteria penguin are shown in Figure 1. The highest mean values for SH and TW were 55.0 [+ or -] 9.5 mm and 18.3 [+ or -]8.1 g, respectively, and were observed at the end of the experiment. Byssus exhibited steady growth up to day 257 of cultivation when BD reached the highest mean value of 2.3 [+ or -] 1.1 mm however, byssus growth halted hereafter to the conclusion of the experiment (Tukey honest significant difference test, P > 0.05).

The AGR of SH, TW, and BD in the pearl oyster Pteria penguin is shown in Figure 2. The AGR for SH fluctuated from 0.12 to 0.16 mm [day.sup.-1], with a mean value of 0.15 mm [day.sup.-1] throughout the experiment (Fig. 2A). Absolute growth rate for TW increased gradually as the oysters aged, exhibiting the highest AGR (0.05 g [day.sup.-1]) at 366 days of cultivation (Fig. 2B). Byssus AGR increased gradually from 0.002 mm [day.sup.-1] at the beginning of the experiment to 0.01 mm [day.sup.-1] at the 183rd day of cultivation only to gradually decrease thereafter (Fig. 2C).

Mean ratios of BD/TW for Pteria penguin are shown in Figure 3. Initially, and again at the end of the experiment, oysters exhibited small BD/SH and BD/TW ratios. The ratio BD/SH increased steadily, then leveled off for a period of 3 months, and then was observed to return to its initial level. Conversely, the tendency in the BD/TW ratio abruptly increased during the early stages of the experiment but gradually declined as oysters aged.

The relations SH-BD and TW-BD in oyster Pteria penguin at 68, 183, and 366 days of cultivation are shown in Figure 4. In general, the relations SH-BD and TW-BD at day 68 were not significant over the period of the study (P > 0.05). At day 183, significant [r.sup.2] values for SH-BD and TW-BD were 0.25 and 0.28, respectively (P < 0.05). At day 366 of cultivation, despite both relations exhibiting lower [r.sup.2] values than on day 183, they were still observed to be statistically significant (ANOVA, P < 0.05), and the [r.sup.2] value in TW-BD remained comparatively higher than in SH BD.

The percentage of Pteria penguin oysters without byssus was observed to be as high as 30% in earlier samples but decreased gradually during cultivation until no oysters without byssus were found in the sample at day 366 of cultivation (Fig. 5).

Ridgeline plots for BD in Pteria penguin exhibited positively skewed distributions in younger individuals up to day 183 of cultivation (Fig. 6). Samples from day 204 to 303 showed normally distributed diameters. At day 366, oysters exhibited a skewed distribution again (P < 0.05, Shapiro-Wilk's test).

DISCUSSION

Despite oysters exhibiting continuous shell growth and weight increase over the observation period, byssal growth halted after 257 days of cultivation (Figs. 1 and 2). Moreover, calculated BD/TW ratio exhibited a steady decrease as Pteria penguin aged (Fig. 3). Taylor et al. (1997) reported similar observations in Pinctada maxima and hypothesized that a point is reached where the increased water resistance, because of greater surface area, is offset by the greater stability resulting from increased mass. Eventually, the weight of the pearl oyster becomes such that the importance of its byssal attachment as its primary means of maintaining position diminishes.

The relationships between the BD and the shell traits in younger oysters proved to be insignificant (Fig. 4), probably because the oysters were neither heavy nor large enough to exhibit the relationships, but when oysters increased in size and weight, the relations became significant. Moreover, the diameter of the byssus was found to be more closely related to the weight of the animal rather than the size of the shell, with oysters at day 183 exhibiting comparatively higher r values than oysters at day 366 of cultivation. These observations are consistent with the previous report where BD in 18-m-old Pteria penguin adults weighting 69.5 [+ or -] 19.0 g was related more closely to the weight of the oyster than to any other shell trait (Vasquez et al. 2017). Mature individuals continued to gain weight, but byssi did not increase in diameter, suggesting the existence of a threshold for the BD in larger oysters. In bigger oysters, the byssus may increase its mechanical strength by some other yet undefined mechanism other than the continued addition of individual threads to the byssus stem resulting in an increased diameter (Vasquez et al. 2017). Although, in the present investigation, byssus strength was not measured, some probability exists that byssus in larger individuals may secrete weaker byssus, as has been reported in mussels (Babarro et al. 2008).

The presence of oysters lacking byssi decreased gradually in relation to the number of days of cultivation (Fig. 5). Pearl oysters are capable, particularly during early developmental stages, of traversing short distances utilizing the foot on dislodgement of the byssus and before secreting a new one within short periods of time (Taylor et al. 1997, Wada & Temkin 2008). In some cases, a new attachment was observed even before the old byssus threads had been cast off (Dharmaraj et al. 1987). This byssal production is also noticeable in the BD distributions, which were positively skewed, mostly within the first 183 days of cultivation, suggesting increased byssogenesis at younger ages (Fig. 6).

In summary, byssus growth and the number of oysters lacking byssus was higher in juveniles of Pteria penguin compared with larger individuals under culture conditions in the sea. Furthermore, the BD was found to increase in slightly greater concordance with the weight than the size of the oyster, but when the oysters grew older, the byssus-to-weight ratios decreased gradually.

ACKNOWLEDGMENTS

Thanks are due to the Sanya Pearl Farm staff for their technical assistance. This study was funded by the National Science Foundation of P. R. China (31560717, 31772847), State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, and China Postdoctoral Science Foundation (Grant No. 170618).

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HEBERT ELY VASQUEZ, XING ZHENG, XIN ZHAN, ZHIFENG GU AND AIMIN WANG (*)

State Key Laboratory of Marine Resource Utilization in South China Sea, Ocean College, Hainan University, 58 Renmin Avenue, Haikou, Hainan 570228, P. R. China

(*) Corresponding author. E-mail: aimwang@163.com

DOI: 10.2983/035.037.0307
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Author:Vasquez, Hebert Ely; Zheng, Xing; Zhan, Xin; Gu, Zhifeng; Wang, Aimin
Publication:Journal of Shellfish Research
Article Type:Report
Date:Aug 1, 2018
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