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Article

Population Biology of the Non-Indigenous Rayed Pearl Oyster (Pinctada radiata) in the South Evoikos Gulf, Greece

by
Dimitris Pafras
1,
Alexandros Theocharis
1,
Gerasimos Kondylatos
1,2,
Alexis Conides
3 and
Dimitris Klaoudatos
1,*
1
Department of Ichthyology and Aquatic Environment (DIAE), School of Agricultural Sciences, University of Thessaly (UTh), Fytokou Street, 38446 Volos, Greece
2
Hydrobiological Station of Rhodes, Hellenic Centre for Marine Research, Enydreiou Sq., 85131 Rhodes, Greece
3
Institute of Marine Biological Resources & Inland Waters, Hellenic Centre for Marine Research, 19013 Attika, Greece
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(8), 460; https://doi.org/10.3390/d16080460
Submission received: 3 July 2024 / Revised: 24 July 2024 / Accepted: 29 July 2024 / Published: 1 August 2024
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Abstract

:
The Atlantic pearl oyster Pinctada radiata (Leach, 1814), the first documented Lessepsian bivalve species to enter the Mediterranean basin, is present in various coastal areas in Greece, and constitutes, almost exclusively, a domestic commercial bivalve resource. The present study aimed to contribute to the limited information available on P. radiata population structure and dynamics in Hellenic waters, especially following the recent enforcement of legislation for regulation of its fishery. A total of 703 individuals were collected using scuba diving from the South Evoikos Gulf. The male-to-female ratio (1:1.70) significantly departed from 1:1. A higher probability for female prevalence was exhibited for shell heights over 50.77 mm. Significant differences were exhibited in the shell height–total weight relationship between the sexes. The fourth-year class was the dominant cohort, comprising 50.09% of the population, out of the seven age classes identified. Asymptotic length was estimated at 109.1 mm and growth index at 3.35, respectively. Longevity was estimated at 15.7 years, with natural mortality (M) at 0.39 and total mortality (Z) at 0.76. The probability of capture (LC50) was estimated at 50.72 mm at 2.8 years. Biological reference points FMSY and EMSY were higher than the fishing mortality and current exploitation rate, respectively, indicating the potential for further population exploitation.

1. Introduction

The Mediterranean Sea, home to approximately 17,000 marine species (which represent about 7.5% of the global marine biota), is a biodiversity hotspot [1]. It is also facing an increasing number of threats from invasive alien species (IAS) which are known to be able to negatively impact biodiversity and alter ecosystem structure and function [2]. The sub-tropical rayed pearl oyster Pinctada radiata (Leach, 1814), also known as the “Atlantic pearl oyster”, is prevalent in the shallow waters of tropical and subtropical continental shelves, especially in the Indo-Pacific Ocean [3,4,5]. Despite the confusion regarding the taxonomic status of the species, its currently accepted name is P. radiata [5,6,7,8,9].
In the Mediterranean Sea, the species was first reported in Alexandria, Egypt, in 1874 as Meleagrina sp., constituting the first documented Lessepsian bivalve to have entered the basin via the Suez Canal [10]. Ever since, it has successfully spread throughout the basin, and is reported as particularly abundant in the eastern parts [9] (Levantine Sea), France, Greece, Libya, Malta, Syria, Tunisia, and Turkey [11,12,13,14,15,16,17,18,19,20,21], and is currently considered among the 100 most invasive species in the Mediterranean Sea [22]. In Greece, P. radiata was deliberately introduced for mariculture in the mid-1950s [11,23] but has gained only a limited commercial interest, and constitutes, almost exclusively, a domestic commercial bivalve resource [24,25]. The rayed pearl oyster is present in various coastal areas of Greece, such as the South Evoikos Gulf. This is a gulf of rather limited bathymetry, located in central Greece between the mainland and the island of Evvoia [26]. It is characterized by a hydrodynamic circulation where the wind and tides are the most important driving forces in the movement and mixing of the water [27]. In regards to aquaculture and fisheries, it is known as a promising area [28,29], but studies on the marine biota of the area are scarce.
Pinctada radiata is a protandrous hermaphrodite bivalve [4,30], which initially maturates as a male and transitions to female after several male reproductive cycles [30,31]. This sex change is reversible and can occur multiple times throughout an individual’s life [30]. Various environmental factors, particularly stress and food availability, influence this process. Each individual can only exhibit one sexual function at a time, making the sex change transitional rather than functional [4,30]. With continuous spawning under optimal water temperature conditions, each individual can potentially function as both male and female across many spawning seasons [32].
For those pearl oyster species that occur in deeper waters, as deep as 100 m [33,34], growth rates are poor due to the lower temperatures and the limited phytoplankton availability [35] in the surrounding water environment. In general, P. radiata is a non-selective filter feeder, extracting and ingesting a variety of organic and inorganic materials, including significant amounts of mud, bivalve eggs, and larvae, from the water column [4,30,36]. Additionally, the various environmental factors, such as depth, temperature, and light, are very important as they directly influence the quality and color of the forming pearls [37].
Currently, pearl oyster fisheries and aquaculture hold significant potential to enhance the economic status of various stakeholders such as fishers, aquaculture producers, cooperatives, and international companies [4,30]. They offer lucrative markets with relatively low capital investment [4]. In addition to producing pearls for the jewelry industry, there is growing commercial interest in the edible flesh of pearl oysters for local consumption and in their shells for export revenue [4,36,38]. Pearl shells, used for buttons and jewelry, are considered high-value export commodities because they are non-perishable and inexpensive to ship [4]. At present, no nucleated pearls are produced in Greece.
To date, various studies have been conducted on P. radiata within its natural geographic range [15]. However, there are few relevant studies from the Mediterranean [12,17,39,40,41,42,43,44,45,46,47,48]. Gaps in our knowledge of the biology and population dynamics of IAS pose challenges when concerted actions to control their transmission and dominance are put in place. Understanding the population structure and dynamics of this alien, edible pearl oyster is valuable for scientists, producers, and fishers engaged in its collection and fishery activities. The aim of the present study was therefore to improve on the limited information currently available on P. radiata population structure and dynamics in Hellenic waters [40], especially in the light of a recent amendment to Hellenic national legislation by Presidential Decree (Á14/29.01.2024) implemented to regulate the P. radiata fishery and prevent its illegal fishing and trafficking as a substitute for native oysters.

2. Materials and Methods

2.1. Study Area and Sampling Methodology

A total of 703 individuals were collected using scuba diving between February 2023 and June 2024 from the southwest part of Evia Island (Eastern Mediterranean) (Figure 1) at depths of between 1.5 and 4 m and at distances of between 25 and 40 m from the shore. Sample collection was performed by a random placement of 20 quadrats (50 × 50 cm metal frame) covering each time a sampling area of 0.25 m2. From the sampled population, 119 individuals were sexually identified microscopically and macroscopically.
Following sample collection, individuals were cleaned, and a range of morphometric parameters from the left shell that included shell height (SH), shell width (SWI), and hinge length (HL) were recorded (0.01 mm accuracy) using vernier calipers (Figure 2). Additionally, total weight (TW), shell weight (SW), and flesh weight (FW) were recorded using a digital scale (0.1 g accuracy) (Table S1).

2.2. Statistical Analysis

The null hypothesis of no significant temporal differences in biometric characters was tested with the Kruskal–Wallis test. Data quality, normal distribution, and homoscedasticity were assessed with Kolmogorov–Smirnov (normality) and Levene’s test (homoscedasticity). Dwass–Steel–Critchlow–Flinger post hoc test was further employed for further statistical comparisons [49].
The Pearson correlation coefficient (PCC) was employed to measure the strength of the association between all biometric characters measured [49] (Figure 2).
To evaluate the effect of seasonality on flesh weight, a General Linear Model (GLM) was employed, allowing for a comprehensive assessment of seasonal differences in flesh weight.
The chi-square goodness-of-fit test was used to evaluate the null hypothesis of equal proportions in the male-to-female ratio and to compare our results with the published literature [50]. A nominal logistic curve was fitted to identify the shell height threshold for sex differentiation in the adult population [51].
The shell height vs. total weight relationship was determined independently for males and females, and for the total population (sex-combined) by fitting the exponential curve to the data according to [52] (Equation (1)).
T W = a × S H b
where SH is shell height (cm), TW is total weight (g), “a” is the intercept (growth factor), and “b” is the slope of the relationship (allometry coefficient).
To evaluate the allometric relationships (significant departure of the slope from 1 or 3), the one-sample t-test was used. The two-sample t-test was employed to compare non-linear regression equations.
The exponential curve was further employed to identify morphometric relationships between total weight (TW), flesh weight (FW), shell weight (SW), shell height (SH), shell width (SWI), and hinge length (HL) for the total population.

2.3. Age and Growth

Pooled annual data grouped by intervals of length frequency distributions (LFDs) were employed to discriminate among normal distributions, with each mode assumed to represent a cohort from the overall size–frequency distribution [53] using the NORMSEP method in the FiSAT II program (FAO, Rome, Italy) (version 1.2.2) [54]. The modal progression analysis (MPA) was used to decompose the composite LFDs by application of the maximum likelihood concept to the separation of normally distributed components of size-frequency samples [55]. The separation index among different cohorts was employed to determine statistically acceptable cohorts.
The ELEFAN system (Electronic Length Frequency Analysis) on monthly LFDs for one year was used to provide quantitative information [56] on the growth of P. radiata using a seasonally oscillating version of the von Bertalanffy Growth Formula (VBGF).
Growth was described by the von Bertalanffy [57] growth equation (Equation (2)).
L t = L ∞ × 1 − e − K × t   −   t 0
where K (growth coefficient) is the rate at which the asymptotic length (L∞), is approached, t is the age in years, and t0 is the hypothetical age at which the individual has zero length.
The growth performance index was derived using the von Bertalanffy parameters [52] (Equation (3)).
φ ′ = l o g K + 2 × l o g L ∞
The maximum lifespan was estimated according to [58] (Equation (4)).
t m a x = 3 K

2.4. Mortality and Exploitation Rate

Natural mortality (M) was calculated using the updated Hoenignls estimator according to [59] (Equation (5)).
M = 4.899 × t m a x − 0.916
Total mortality (Z) was calculated using the length-converted catch curve [60].
The annual fishing mortality rate (F) was obtained by subtracting natural from Z, according to [61] (Equation (6)).
F = Z – M
The exploitation rate (E), a measure of the number of fish that are caught from a population each year, was calculated as the ratio of F to Z [60] (Equation (7)).
E = F / Z
The length class at which the fish population can achieve its maximum sustainable yield (MSY) (eumetric length) (Le) was calculated according to [58,62] (Equation (8)):
L e = 3 × L ∞ 3 + M K
The length of first capture (Lc) was the length at initial capture (smallest individual captured). The probability of capture was estimated at 25%, 50%, and 75% levels by the linear regression derived from the ascending data points of the selectivity curve [63].

2.5. Relative Y/R and B/R Analysis: Knife-Edge Selection

The knife-edge method [64] was used to evaluate the relative yield-per-recruit (Y′/R), the maximum exploitation rate (Emax), and the optimal exploitation rate (Eopt). The Beverton and Holt yield per recruit (Y/R) model was employed as a tool to evaluate the impact of different fishing strategies on the population’s long-term sustainability. This model accounts for age-specific growth and mortality, providing insights into the best age at which to begin harvesting to maximize yield. The Y/R model is particularly valuable for managing fisheries, as it helps to predict the outcomes of different fishing pressures and can inform regulations to prevent overfishing and ensure the continued health of the fish population.
Further biological reference points were calculated in accordance with [65] and [66,67], including FMSY (the fishing mortality at the maximum sustainable yield), EMSY (the exploitation rate at the maximum sustainable yield), BMSY (the biomass per recruit at the maximum sustainable yield), optimal length (Lopt), optimal fishing mortality (Fopt), fishing mortality limit (Flim), and optimal exploitation rate (Eopt).

3. Results

3.1. Population Structure

The frequency distribution of biometric characters for the P. radiata population from the South Evoikos Gulf is shown in Figure 3.
No significant difference was observed in shell height and total weight between the sexes (shell height p = 0.614; total weight p = 0.695).
The Pearson correlation coefficient and associated probability exhibited a highly significant correlation (p < 0.001) among all biometric characters measured (SL, SH, HL, FW, SWI, and TW) (Figure 4).
Only flesh weight exhibited significant temporal variation for the P. radiata population from the coastal waters of the South Evoikos Gulf (Table 1).
Analysis using a General Linear Model (GLM) further indicated a highly significant temporal effect on P. radiata flesh weight (Table 2). The model employed indicated that spring had a significant positive impact on flesh weight, whereas autumn and summer had a significant negative effect on flesh weight (Table 2). The effect of winter on flesh weight was positive but not significant.
A comparative densities plot with smoothed distribution of P. radiata flesh weight across each season throughout the year (Figure 5) further illustrated the results of the GLM with a significant positive impact of spring, a significant negative impact of autumn and summer, and a minor positive effect of winter on the flesh weight of the P. radiata population from the coastal waters of the South Evoikos Gulf.

3.2. Sex Ratio

Of the 119 individuals that were sexually identified microscopically and macroscopically, 75 were female (63%) and 44 were male (37%) at an M: F ratio of 1:1.70, exhibiting a significant departure from a 1:1 ratio (X2 = 8.08, p < 0.01).
Nominal logistic regression indicated that, for individuals with a shell height of over 50.77 mm, there was a higher probability of female prevalence in the study population (Figure 6).

3.3. Allometric Relationships

The relationships between shell height and total weight for the total population and for each sex are shown in Figure 7.
Significant negative allometry was indicated for the total population and for each sex for the relationship of shell height vs. total weight. Furthermore, a significant difference was exhibited for the shell height–total weight relationship among sexes, with a highly significant difference among slopes (p < 0.001) and a significant difference among intercepts (p < 0.05). This difference indicates that in individuals of similar total weight, the males exhibit longer shell height compared to the females.
The allometric relationships between the morphological characteristics of P. radiata from the coastal waters of the South Evoikos Gulf are shown in Table 3.

3.4. Age Composition

Seven age classes were identified. The dominant cohort was the fourth-year class, comprising 50.09% of the population, followed by the third (25.35% of the population) and the fifth (19.92% of the population) year classes, respectively (Figure 8).

3.5. Growth, Mortality, and Exploitation Rate

Asymptotic length L∞ was estimated at 109.1 mm, and the growth index (Φ′) was 3.35 for the total population, indicating a fast growth rate. Longevity was estimated at 15.7 years for the total population. Natural mortality (M) was estimated at 0.39, total mortality (Z) at 0.76, and fishing mortality (F) at 0.37. The exploitation rate (E) was estimated at 0.48, indicating an underexploited population in the study area, and the eumetric length (Le) was estimated at 64.7 mm.
The seasonally oscillating VBGF was fitted to the monthly length-frequency data (Figure 9). The plot displays the seasonally oscillating growth curve of Pinctada radiata shell height based on monthly length-frequency data from South Evoikos Gulf. Black bars represent the frequency of shell heights observed each month, while the red lines are fitted growth curves showing seasonal growth patterns. Information is crucial in our understanding of the seasonal growth dynamics of Pinctada radiata and its effective population management.

3.6. Probability of Capture—Lopt

The probability of capture was estimated at 25% (LC25), 50% (LC50), and 75% (LC75) levels as 49.11, 50.72, and 52.37 mm, respectively (Figure 10). The age at which there is a 50% probability of capture (t50) was estimated at 2.8 years.

3.7. Relative Y/R and B/R Analysis: Knife-Edge Selection

The Beverton and Holt yield per recruit (Y/R) model with fishing mortality (F) and exploitation rate (E) fitted against Y/R, and the indicated biological reference points are shown in Figure 11 and Figure 12, respectively. The results of the yield-per-recruit analysis and biological reference points are shown in Table 4.

4. Discussion

The main outcomes of our research provide significant insights into the population dynamics of P. radiata in the South Evoikos Gulf, highlighting critical spatial and temporal variations. The findings reveal that the flesh weight of the species shows substantial seasonal fluctuations, peaking in spring and dipping in autumn, likely due to reproductive cycles. Comparatively, our study recorded higher mean morphometric values in spring than previous studies in Malta, suggesting richer nutrient availability and environmental protection in the Evoikos Gulf. The study also documented the highest mean shell height values within the Mediterranean, underscoring the unique ecological conditions of the study area that promote greater growth. These results not only enhance the understanding of P. radiata’s biology but also provide a baseline for effective management and conservation strategies.
Soon after the Suez Canal opening, the influx of non-indigenous (NIS) marine species became the focus of attention of many scientists [68]. The phenomenon has been intensified since the beginning of the 2000s and drastic measures are needed for population control of all IAS [22,69]. To guide that process, the collection of biological data for all the species that present broad distribution and large populations within the basin is crucial. Pinctada radiata exhibits these characteristics, and its population control is most likely achievable through commercial exploitation [70].
The present study presented new information on the rayed pearl oyster population structure, growth, mortality, exploitation rate, and recruitment pattern in the South Evoikos Gulf. Our results demonstrated significant spatial and temporal differences in the FW of P. radiata, with the highest values recorded during spring and the lowest during autumn. Temporally, these differences could be attributed to the reproductive cycle of the species, as analyzed in [71]. It is worth mentioning that for spring, the mean values of morphometrics were higher in our study than those in Malta [14]. These differences are the direct result of either the higher nutrient richness in the coastal waters of the South Evoikos Gulf compared to Maltese waters [72], the protection from wave action characteristic of the Evian coasts, or a combination of both factors.
The mean SH values (64.5 ± 11 mm) of the individuals studied here were greater than those of individuals studied elsewhere in the Mediterranean, including those from the Gulf of Antalya, Turkey (highest mean SH 23.9 ± 3.7 mm) [73], Southern Tunisian waters (60.98 ± 0.68 mm) [47], Linosa, Italy (61.3 ± 12.7 mm) [16], Malta (39.6 ± 6.2 mm) [14], Tivat, Montenegro (38.3 ± 6.1 mm) [39], and the Saronikos Gulf, Greece (58.96 ± 13.24 mm) [40]. On the other hand, they are very close to the values obtained from the North Evoikos Gulf (64.21 ± 14.91 mm) in a recent study by [40]. This resemblance can be attributed to the proximity of the two gulfs, North and South Evoikos, along with the higher concentrations of nutrients and chlorophyll a ([40] and references herein). Notably, the mean values of morphometrics in the latter study are somewhat lower than those in our study. For example, the TW of our individuals was 49.1 ± 18.2 mm, whereas the TW in [40] was 30.2 ± 17.7 mm. In both studies, the depth range of the collection zone was almost identical; however, their TW refers to a fracture of the total individuals collected from both the Saronikos Gulf and the Evoikos Gulf.
Nevertheless, the maximum SH value we recorded was 101.1 mm, clearly higher than the respective morphometric value from other regions within the Mediterranean: 85.0 mm from El Bibane Lagoon, Tunisia, [74], 64.0 mm from Egypt [44], 96.0 mm from the Gulf of Gabès, Tunisia [47], 78.7 mm from Linosa [16], and 48.0 mm from Malta [14]. Closer to our results were the findings from Bizerta Lagoon, Tunisia (100.5 mm) [12,42], whereas the results from Hammamet, Tunisia (104.3 mm) were higher [48]. This 101.1 mm individual is the largest reported from the northern coastlines of the basin and from the Red Sea (93.2 mm) [36,44].
Regarding the overall M: F ratio of 1:1.70, which is in favor of females, it does not agree with the 1:0.89 reported from the Gulf of Gabès, Tunisia [75]. However, our M: F ratio presents no significant difference (X2 = 1.82, p > 0.05) with findings from Izmir Bay, Turkey [76], where the ratio was calculated as 1:1.32. According to our results (Figure 5) the M: F ratio tends toward the 1:1 within the length range of 40.00–60.00 mm with a threshold value of the effect of SH on the sex ratio at 50.77 mm. Very close to the size range for the 1:1 sex ratio is that reported by [75]. These authors concluded that the SH range of 60.00–70.00 mm comprised equal numbers of male and female individuals. Reductively, the threshold value is the missing point in the statement that the “sex ratio of pearl oysters in the wild approaches 1:1” ([32,77] and references herein). Nevertheless, we cannot exclude the possibility of bias in the sampling procedure.
Because the sex of the rayed pearl oyster is related to size, a common method to depict such relations is the grouping of collected individuals into size classes [75]. Ref. [47] concluded that the dominant size class for the individuals collected within the depth range of 0–1 m was 25.00–50.00 mm, and a few years later [78] reported that the majority (75.76%) of total individuals collected from the shallower waters (0–1 m) belonged to the size classes 35–55 mm. In the present study, 50.09% of the collected individuals belonged to the SH 67.13 ± 4.89 mm, followed by 25.35% of the SH 54.64± 7.34 mm.
The size and age of the rayed pearl oyster are important parameters in terms of their relation to the pearl size. An increase in the occurrence of pearls in larger rayed pearl oysters has been demonstrated (>58 mm HL in [79]). Such knowledge is valuable for the development of managerial guidelines in fisheries where the harvest of oysters greater than a certain size could be promoted.
In the present study, we identified seven cohorts with mean SHs of 27.1, 36.16, 54.64, 67.13, 75.79, 85.29, and 97.32 mm. The only study that has reported results closer to ours is that of [36] from the Red Sea, who identified six cohorts with mean SHs of 20.3, 47.9, 66.4, 78.8, 87.0, and 91.7 mm, where the first represents the 0 age group. Other studies from the Mediterranean and elsewhere have identified four or five age groups [40,44,80]. Longevity was estimated at 15.7 years which is higher than the estimations from Japan (10-year lifespan [81]), the Red Sea (7.69 years [36]), and Greece (5 years [40]).
All the allometric equations presented negative allometry. Similarly to our study, [78] reported a negative allometric growth pattern from the Gulf of Gabès, as well as [40] from central Greece, indicating a slower gain in SH than in TW of the species in these areas, although in the latter study, the SW showed positive allometry with respect to SH, in contrast to our results.
On the other hand, the L∞ (109.1 mm) and Φ′ (3.35) indicated a fast growth rate for the species in the South Evoikos Gulf. The respective values from various regions demonstrate variability and have been summarized by [40]. L∞ and Φ′ range from 69.20 to 132.00 mm and from 3.43 to 4.04, respectively. Our results are closer to those of [44,82] and for the L∞ and Φ′, respectively. The differentiation in the growth parameters of the rayed pearl oyster could be attributed to respective differences in the ecosystems where the individuals of each study were collected from, and to the responses of species to environmental gradients [78]. Differences in the L∞ have been attributed to the collection depth, with L∞ being smaller in the coastal waters in contrast to the deeper waters of Tunisia [79].
Understanding the mortality estimates associated with growth parameters is important in order to comprehend the population dynamics of a certain species [83]. In the South Evoikos Gulf, our results show that F, M, and Z (0.37, 0.76, and 0.39, respectively) suggest an exploitation rate lower than 0.50 (E = 0.48). The estimated Fopt and Flim as 0.39 and 0.26, respectively, indicate the potential for further increase in F if the case is to commercially exploit the species. The difference between the Eopt and E (0.50 and 0.48, respectively) further supports the indication of further exploitation. Thus, P. radiata has the potential to expand its market, provided that a sustainable fishery will be implemented. The estimated exploitation rate in our study is lower than or similar to those calculated elsewhere in the basin [40,78], suggesting a sustainable population with long-term viability.

5. Conclusions

The present study examined the population structure, growth, mortality, and exploitation rates of the invasive rayed pearl oyster, Pinctada radiata, in the South Evoikos Gulf (Greece). Our findings revealed significant spatial and temporal differences in the flesh weight of the species. The mean shell height values observed were higher than those reported elsewhere in the Mediterranean and the Red Sea, with a maximum SH of 101.1 mm. The male-to-female ratio was similar to that in Izmir Bay, Turkey. We identified seven cohorts, with similar findings only reported from the Red Sea. Allometric equations indicated negative allometry. The growth parameters suggested a fast growth rate in this area. Biological reference points indicated the potential for increased exploitation, though sustainability must be considered. We recommend further studies on the species’ biology across the Mediterranean.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d16080460/s1, Table S1: Sample data.

Author Contributions

Conceptualization: D.P.; methodology: D.K.; software: D.K.; validation: G.K., A.C. and D.K.; formal analysis: D.P., A.T. and D.K.; investigation: A.T., G.K., A.C. and D.K.; resources: D.P.; data curation: D.P. and D.K.; writing—original draft preparation: D.P., A.T., G.K. and D.K.; writing—review and editing: D.P., A.T., G.K., A.C. and D.K.; visualization: D.K.; supervision, D.K.; project administration: D.P.; funding acquisition: D.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The datasets analyzed from the current study are available from the corresponding author upon reasonable request.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Map of the study area (red outline) and location of sampling area (black outline) (color variation indicates depth).
Figure 1. Map of the study area (red outline) and location of sampling area (black outline) (color variation indicates depth).
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Figure 2. Morphological measurements of the shell of the rayed pearl oyster of Pinctada radiata collected from the coastal waters of South Evoikos Gulf (Greece). L: left valve, R: right valve, SH: shell height, SWI: shell width, HL: hinge length, WNL: width of the nacreous part in left valve, and LNR: length of nacreous part in right valve.
Figure 2. Morphological measurements of the shell of the rayed pearl oyster of Pinctada radiata collected from the coastal waters of South Evoikos Gulf (Greece). L: left valve, R: right valve, SH: shell height, SWI: shell width, HL: hinge length, WNL: width of the nacreous part in left valve, and LNR: length of nacreous part in right valve.
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Figure 3. Frequency distributions with overlayed fitted normal distribution of biometric characters (mm and g) of Pinctada radiata collected from the coastal waters of South Evoikos Gulf (Greece). (A): Total weight; (B) Flesh weight; (C) Shell weight; (D) Shell height; (E) Hinge length; and (F) Shell width.
Figure 3. Frequency distributions with overlayed fitted normal distribution of biometric characters (mm and g) of Pinctada radiata collected from the coastal waters of South Evoikos Gulf (Greece). (A): Total weight; (B) Flesh weight; (C) Shell weight; (D) Shell height; (E) Hinge length; and (F) Shell width.
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Figure 4. Scatterplot matrix with fitted line plots (lower left triangle of the scatterplot matrix) and heat map with Pearson correlation and associated probability values (upper-right triangle of the scatterplot matrix) of Pinctada radiata biometric characters measured from the coastal waters of South Evoikos Gulf (Greece). The color of each circle represents correlation strength circle size represents correlation significance between each pair of variables (larger circle indicates a more significant relationship).
Figure 4. Scatterplot matrix with fitted line plots (lower left triangle of the scatterplot matrix) and heat map with Pearson correlation and associated probability values (upper-right triangle of the scatterplot matrix) of Pinctada radiata biometric characters measured from the coastal waters of South Evoikos Gulf (Greece). The color of each circle represents correlation strength circle size represents correlation significance between each pair of variables (larger circle indicates a more significant relationship).
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Figure 5. Temporal comparison of densities plot of flesh weight of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece).
Figure 5. Temporal comparison of densities plot of flesh weight of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece).
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Figure 6. Nominal logistic curve and threshold values (values above which there is an increasingly higher probability that sex is female) of the effect of size (shell height) on the sex ratio of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece).
Figure 6. Nominal logistic curve and threshold values (values above which there is an increasingly higher probability that sex is female) of the effect of size (shell height) on the sex ratio of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece).
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Figure 7. Shell height–total weight relationship of (A) both sexes and (B) each sex separately of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece).
Figure 7. Shell height–total weight relationship of (A) both sexes and (B) each sex separately of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece).
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Diversity 16 00460 g008
Figure 8. Characteristics of the identified age groups for all captured individuals of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece). Confidence intervals indicate the standard deviation.
Figure 8. Characteristics of the identified age groups for all captured individuals of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece). Confidence intervals indicate the standard deviation.
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Diversity 16 00460 g009
Figure 9. Seasonally oscillating growth curve fitted to monthly length-frequency data of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece).
Figure 9. Seasonally oscillating growth curve fitted to monthly length-frequency data of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece).
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Figure 10. Probability of capture for different length classes (LC25, LC50, LC75) of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece).
Figure 10. Probability of capture for different length classes (LC25, LC50, LC75) of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece).
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Figure 11. Yield per recruit (Y/R) and biomass per recruit (B/R) of Pinctada radiata collected from the coastal waters of South Evoikos Gulf (Greece), for different fishing mortalities.
Figure 11. Yield per recruit (Y/R) and biomass per recruit (B/R) of Pinctada radiata collected from the coastal waters of South Evoikos Gulf (Greece), for different fishing mortalities.
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Diversity 16 00460 g012
Figure 12. Yield per recruit (Y/R) and biomass per recruit (B/R) of Pinctada radiata collected from the coastal waters of South Evoikos Gulf (Greece), for different fishing exploitation rates.
Figure 12. Yield per recruit (Y/R) and biomass per recruit (B/R) of Pinctada radiata collected from the coastal waters of South Evoikos Gulf (Greece), for different fishing exploitation rates.
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Table 1. Temporal variation of biometric characters (mm and g) of the shell of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece). HL: hinge length, TW: total weight, FW: flesh weight, SW: shell weight, SH: shell height, SWI: shell width, WNL: width of the nacreous part in left valve, LNL: length of the nacreous part in left valve, WNR: width of the nacreous part in right valve, LNR: length of the nacreous part in right valve, represented as mean value ± standard error (SE). Seasonal average water temperature in degrees C ± standard deviation (SD).
Table 1. Temporal variation of biometric characters (mm and g) of the shell of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece). HL: hinge length, TW: total weight, FW: flesh weight, SW: shell weight, SH: shell height, SWI: shell width, WNL: width of the nacreous part in left valve, LNL: length of the nacreous part in left valve, WNR: width of the nacreous part in right valve, LNR: length of the nacreous part in right valve, represented as mean value ± standard error (SE). Seasonal average water temperature in degrees C ± standard deviation (SD).
SeasonAutumnWinterSpringSummerSignificanceTotal Population
TW ± SE47.7 ± 17.251.9 ± 18.648.9 ± 19.947.8 ± 16.6ns49.1 ± 18.2
FW ± SE9.27 ± 3.06 c11 ± 3.34 b12.6 ± 4.36 a9.76 ± 3.41 c***10.7 ± 3.79
SW ± SE38.4 ± 14.440.8 ± 15.736.3 ± 1638.1 ± 14ns38.4 ± 15.1
SH ± SE63.3 ± 9.7866 ± 11.265.2 ± 11.763.6 ± 11.2ns64.5 ± 11
HL ± SE47.8 ± 5.3348.9 ± 6.9148.1 ± 6.8047.7 ± 6.63ns48.1 ± 6.45
SWI ± SE26.3 ± 527.4 ± 5.3727.4 ± 5.5226.6 ± 4.99ns26.9 ± 5.23
WNL ± SE41.7 ± 7.0943.7 ± 7.5342.3 ± 7.9741.7 ± 7.86ns42.3 ± 7.64
LNL ± SE47.2 ± 7.0848.8 ± 7.6048.5 ± 8.3947.3 ± 8.08ns48 ± 7.82
WNR ± SE46.8 ± 6.5248.2 ± 7.7647.2 ± 8.5846.8 ± 8.28ns47.3 ± 7.83
LNR ± SE51.9 ± 7.4953 ± 8.353.1 ± 8.9551.8 ± 8.74ns52.4 ± 8.39
Average Temperature21.5 ± 1.615.2 ± 2.015.2 ± 1.724.2 ± 1.54
(ns: non-significant, ***: p < 0.001). Means that do not share a superscript are significantly different.
Table 2. General Linear Model results of temporal effects on the flesh weight of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece).
Table 2. General Linear Model results of temporal effects on the flesh weight of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece).
TermScaled Estimate Std Errort RatioSignificance
Intercept10.6525Diversity 16 00460 i0010.14602572.95***
Autumn−1.385833Diversity 16 00460 i0020.252922−5.48***
Spring1.8988333Diversity 16 00460 i0030.2529227.51***
Summer−0.893833Diversity 16 00460 i0040.252922−3.53**
Winter0.3808333Diversity 16 00460 i0050.2529221.51ns
(ns: non-significant, **: p < 0.01, ***: p < 0.001). Means that do not share a superscript are significantly different.
Table 3. Allometric equations between total weight (TW), flesh weight (FW), shell weight (SW), shell height (SH), shell width (SWI), and hinge length (HL) of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece). R2: coefficient of determination, t-test: statistical significance of the allometric relationship, type of allometry (ns: non-significant, *** p < 0.001).
Table 3. Allometric equations between total weight (TW), flesh weight (FW), shell weight (SW), shell height (SH), shell width (SWI), and hinge length (HL) of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece). R2: coefficient of determination, t-test: statistical significance of the allometric relationship, type of allometry (ns: non-significant, *** p < 0.001).
RelationshipEquationR2t-TestAllometry
SH vs. TWTW = 0.008205 × SH 2.082484.9%***Negative
SH vs. FWFW = 0.006241 × SH 1.782170.9%***Negative
SH vs. SWISWI = 0.71535 × SH 0.8712361.4%***Negative
SH vs. SWSW = 0.00499 × SH 2.1477.7%***Negative
SH vs. HLHL = 3.6505 × SH 0.6196968.6%***Negative
HL vs. SWSW = 0.79975 × HL 0.9082541.2%nsNegative
SW vs. FWFW = 1.0617 × SW 0.6384461.9%***Negative
Table 4. Relative yield/recruit analysis (knife edge) and biological reference points of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece).
Table 4. Relative yield/recruit analysis (knife edge) and biological reference points of Pinctada radiata individuals collected from the coastal waters of South Evoikos Gulf (Greece).
EY/RB/R
0.010.0080.844
0.200.0140.699
0.300.0200.566
0.400.0240.444
0.500.0280.336
0.600.0300.241
0.700.0310.159
0.800.0300.093
0.900.0290.040
0.990.0280.003
Biological reference points
FMSY0.934
EMSY0.637
BMSY0.03295
Emax0.694
E0.10.616
E0.50.353
Fopt0.39
Flim0.26
Eopt0.50
E, the exploitation rate; Y/R, yield per recruit; B/R, biomass per recruit; FMSY the fishing mortality at the maximum sustainable yield; EMSY the exploitation rate at the maximum sustainable yield; BMSY the biomass per recruit at the maximum sustainable yield; Emax, the exploitation rate which produces the maximum yield; E0.1, the exploitation rate at which the marginal increase in relative yield per recruit is 1/10th of its value at E = 0; E0.5, value of E under which the stock has been reduced to 50% of its unexploited biomass; Fopt, the optimum fishing mortality; Flim, the fishing mortality limit; Eopt, the optimum exploitation rate.
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Pafras, D.; Theocharis, A.; Kondylatos, G.; Conides, A.; Klaoudatos, D. Population Biology of the Non-Indigenous Rayed Pearl Oyster (Pinctada radiata) in the South Evoikos Gulf, Greece. Diversity 2024, 16, 460. https://doi.org/10.3390/d16080460

AMA Style

Pafras D, Theocharis A, Kondylatos G, Conides A, Klaoudatos D. Population Biology of the Non-Indigenous Rayed Pearl Oyster (Pinctada radiata) in the South Evoikos Gulf, Greece. Diversity. 2024; 16(8):460. https://doi.org/10.3390/d16080460

Chicago/Turabian Style

Pafras, Dimitris, Alexandros Theocharis, Gerasimos Kondylatos, Alexis Conides, and Dimitris Klaoudatos. 2024. "Population Biology of the Non-Indigenous Rayed Pearl Oyster (Pinctada radiata) in the South Evoikos Gulf, Greece" Diversity 16, no. 8: 460. https://doi.org/10.3390/d16080460

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