The Impact of Increasing Seawater Temperatures over the Last 30 Years on the Reproductive Cycle of the Pearl Oyster Pinctada radiata (Leach, 1814) in the Arabian Gulf

Abstract

The pearl oyster Pinctada radiata (Leach, 1814), a crucial ecosystem builder in the Arabian Gulf, has experienced a significant decline, mainly attributed to anthropogenic pressures. This study aimed to characterize the reproductive cycle of P. radiata in Qatar and compare the current data with historical records in the region obtained between 1992 and 1993. From May 2020 to April 2022, we found a well-defined seasonal reproductive pattern, with a narrow peak spawning period in April. This observation stands out strongly from the previous recordings of 1992–1993 for the region, where spawning extended from May to August. The observed shift in the reproductive cycle coincides with a notable increase in the maximum sea surface temperature (SST), rising from 34 °C in August (1992–1993) to 37 °C in July (2020–2022), while the minimum SST remained stable at 15–16 °C in January during both periods. Furthermore, a contraction in the duration of the main spawning period was observed, with spawning now confined to an earlier and shorter timeframe. We propose that climate change, in addition to other environmental stressors, must have played a key role in modifying the reproductive cycle of the pearl oyster P. radiata in the Arabian Gulf. These findings highlight the importance of further monitoring reproductive dynamics in the context of climate change.

1. Introduction

The increasing temperature of seawater presents a significant challenge for the future of our planet [1], and the Arabian Gulf is today the world’s hottest sea. It exhibits typical summer sea surface temperatures (SSTs) exceeding 35 °C [2]. In the Gulf, the pearl oyster Pinctada radiata (Leach, 1814) is an iconic ecosystem builder forming the oyster reefs, one of the larger seascapes in this semi-enclosed sea. Historically, the pearl oyster formed massive oyster beds on the western side of the Arabian Gulf, with its larger density extending from Kuwait to the UAE [3]. For centuries, the economy of Qatar was based on the pearl oyster industry and fishing activity on the historically abundant oyster bed resources [3,4]. Notwithstanding its economic and social importance, the pearl oyster was not immune to environmental pressures, linked mainly to the rapid industrial and urban growth of the Gulf countries in recent decades, and a significant decline has been observed in the historical P. radiata oyster beds of Qatar [5]. The collapse of the pearl oyster ecosystem in Qatar and the Arabian Gulf threatens long-term biological and economic functionality in this shallow marine environment. Oysters are vital ecosystem engineers, providing essential services such as natural water filtration, and the loss of this function poses significant environmental risks [6,7].

The risk extends beyond oyster beds to encompass the entire marine biodiversity and ecosystems of the Gulf, which are currently under significant threat from multiple local anthropogenic stressors. These include inputs from domestic sewage, eutrophication, overfishing, and extensive coastal construction. Additionally, these impacts are further compounded by the effects of climate change [8], particularly due to the Gulf’s shallow depth [9] and its location within an arid region that frequently experiences severe atmospheric events. Globally, sea surface temperatures have risen by approximately 0.6 °C since 1900 [10]. However, the Gulf has been warming at an accelerated rate, with a trend of 0.6 °C per decade from 1982 to 2022 [11]; ref. [12] also reported an even more rapid increase of 0.7 °C per decade between 2003 and 2018 on the western side of the Gulf, far exceeding the global average rate of ocean warming since 1900.

In Qatar, the restoration of oyster beds through initiatives like aquaculture-based restocking could help recover marine biodiversity while also preserving the country’s maritime heritage. However, the successful cultivation and rearing of P. radiata require (i) a comprehensive understanding of its reproductive cycle, which remains poorly characterized for Qatari populations, and (ii) more knowledge of its recent life history in the context of rapid local warming. Although studies on the gonadal development and spawning period of Pinctada species have been conducted since the 1950s, detailed research on P. radiata in Qatar has been limited. Previous studies on Pinctada species were performed in Australia, Japan, Kenya, Korea, and Iran (e.g., [13,14,15,16,17]) and on P. radiata in Tunisia, Turkey, Greece (e.g., [18,19,20]), and Bahrain in the early 1990s [21]. Most of these previous studies showed a main spawning period in the summer months, mainly from June to August/September, with some presenting a second minor autumn peak (e.g., [18,19,20,21,22]). However, numerous authors are evidencing that populations of the same species from different regions can have significant reproductive differences, which will be crucial for hatchery production (e.g., [23,24]).

The objective of this study was to gain a deeper understanding of the reproductive cycle of P. radiata from a historical perspective, covering the last few decades. The goal was to determine whether global warming may be linked to significant changes that have previously gone unnoticed.

We aimed to (1) characterize the reproductive cycle of the current pearl oyster populations in Qatar and analyze the water’s physico-chemical properties and (2) determine the timing of the present spawning period and reproductive cycle and compare it with local historical data (Bahrain, [21]).

2. Material and Methods

2.1. Study Area and Field Sampling

Figure 1 shows the coastal study area of Simaisma, located on the east coast of Qatar (N 25°32.779/E 51°30.580), and a comparison site in the north of Bahrain, studied by [21] during 1992–1993. The two sites are approximately 100 km apart, with depths ranging from 3 to 5 m at both locations and similar distances from the shore. Pearl oysters were hand-collected by scuba diving from a local oyster bed at a depth of approximately 4 m, during monthly sampling from May 2020 to April 2022. Each month, 35 oysters were randomly collected for histological analysis and an additional 10 individuals were collected to determine the condition index. Water samples (four 500 mL dark high-density polyethylene HDPE bottles) were also collected at each sampling time for chlorophyll-a (Chl-a) determination and stored in an ice-filled cooler during transport. At the site, a multiparameter probe (YSI-Model 6050000) was used to measure temperature, conductivity/salinity, dissolved oxygen (DO), pH, and total dissolved solids (TDS).

2.2. Water Analysis

Chlorophyll-a

Chlorophyll-a (Chl-a) concentration was determined using the spectrophotometric method described by [25]. Water samples were filtered through nitrocellulose filter paper (Millipore 0.45 μm pore size). Chl-a was then extracted by adding 10 mL of 90% acetone to the filter and leaving it for 24 h at 4 °C. After the extraction period, samples were centrifuged at 4000 rpm for 10 min. To account for phaeopigments, a first absorbance reading was taken at 665 and 750 nm. The samples were then acidified with diluted hydrochloric acid (1:1) and the absorbance was measured again at the same wavelengths.

2.3. Pearl Oyster Analysis

2.3.1. Histology

Thirty-five individuals were analyzed monthly throughout the study period, except for June 2021 due to logistical limitations. Measurement of length (L), width (W), and height (H) were determined for each oyster using a digital caliper (Vernier caliper 0–200, precision 0.01 mm) and weight (shell included) was determined on a scale (Mettler Toledo (model XS403S, max weight = 410 g)).

To assess the gametogenic stages in both sexes, a 5 mm section of the visceral mass near the pericardial region was dissected and fixed in Davidson’s solution for 48 h and then transferred to 70% ethyl alcohol for storage. The tissue samples were then processed using a tissue processor (Thermo Scientific REVOS, Waltham, MA, USA) where they were dehydrated in ascending ethanol solutions, cleared with xylene, and embedded in paraffin wax. For embedding, samples were transferred to molten wax using an embedding machine (Thermo Scientific HistoStar). Thin sections of 6 μm were cut using a microtome (Thermo Scientific HM355S), mounted on glass slides, and stained with Harris Hematoxylin and Eosin [26] using an automated stainer (Gemini AS). The slides were mounted using a DPX mounting medium. The stained sections were screened and analyzed using an OLYMPUS BX62 light microscope (Tokyo, Japan) at 10× and 20× magnifications, attached to an OLYMPUS DP73 digital camera and supported by OpenLab software (OLYMPUS CellSense Entry). The gametogenic stages in both sexes were classified following the six-stage scale of [27], as adapted by [28]. A brief description and illustration of the stages are provided in Figure 2a,b. When multiple development stages were present within a single individual, the stage observed in the majority of the section was used for classification.

The monthly mean gonadal index (GI) was also calculated as per the below [29] with a scale adaptation:

$$GI=\left[{\displaystyle \frac{\left(\sum \mathrm{i}\mathrm{n}\mathrm{d}.\mathrm{e}\mathrm{a}\mathrm{c}\mathrm{h}\mathrm{s}\mathrm{t}\mathrm{a}\mathrm{g}\mathrm{e}\times \mathrm{s}\mathrm{t}\mathrm{a}\mathrm{g}\mathrm{e}\mathrm{r}\mathrm{a}\mathrm{n}\mathrm{k}\mathrm{i}\mathrm{n}\mathrm{g}\right)}{\mathrm{t}\mathrm{o}\mathrm{t}\mathrm{a}\mathrm{l}\mathrm{i}\mathrm{n}\mathrm{d}.\mathrm{e}\mathrm{a}\mathrm{c}\mathrm{h}\mathrm{m}\mathrm{o}\mathrm{n}\mathrm{t}\mathrm{h}}}\right]$$

A numerical ranking was assigned in this study for each of the development stages as follows: inactive stage (0), development stage 1 (I), development stage 2 (II), ripe stage 3 (III), spawning stage 4 (IV), spent stage 5 (V). The GI ranged from 0 (with all individuals in the rest stage) to 5 (all individuals in the spent stage).

Oocyte diameter measurements were conducted using the equation provided by [30]. For each female oyster, five randomly selected oocytes were measured by outlining their perimeters in ImageJ software v1.51 to obtain the area in pixels. This pixel-based area was then converted to a theoretical diameter using the equation D = √(4S/π), where S represents the measured area.

2.3.2. Condition Index

From each monthly sampling, the condition index (CI) was calculated for the 10 pearl oysters as previously mentioned, according to [31]:

$$CI=\left[{\displaystyle \frac{\mathrm{a}\mathrm{s}\mathrm{h}\mathrm{f}\mathrm{r}\mathrm{e}\mathrm{e}\mathrm{d}\mathrm{r}\mathrm{y}\mathrm{m}\mathrm{e}\mathrm{a}\mathrm{t}\mathrm{w}\mathrm{e}\mathrm{i}\mathrm{g}\mathrm{h}\mathrm{t}\left(\mathrm{g}\right)}{\mathrm{d}\mathrm{r}\mathrm{y}\mathrm{s}\mathrm{h}\mathrm{e}\mathrm{l}\mathrm{l}\mathrm{w}\mathrm{e}\mathrm{i}\mathrm{g}\mathrm{h}\mathrm{t}\left(\mathrm{g}\right)}}\right]\times 100$$

Dry meat and shell weight were determined after oven drying at 80 °C for 24 h. Dry meat samples were ashed at 450 °C in a muffle furnace for ash weight determination and ash-free dry meat weight calculation.

2.3.3. Statistical Analysis

To assess the differences between sampling months for all estimated descriptors and evaluate the relationships among the studied parameters, a principal component analysis (PCA) was conducted using MATLAB^® 7.1. The PCA allowed for the identification of key patterns and variability within the dataset. Correlation coefficients and their associated probabilities between the various studied parameters were derived from the PCA scores to further explore the interdependencies among the variables.

3. Results

3.1. Environmental Parameters and Chlorophyll-a at Simaisma in 2020–2022

Seawater temperature ranged from 28 to 37.3 °C from May to August (summer period) and from 16.1 to 23 °C from December to February (winter period), with an annual average of 27.2 ± 6.4 °C. The highest temperature during the 24-month period was recorded in July 2020 (37.3 °C) and the lowest was recorded in January 2021 (16.1 °C). Salinity showed only slight monthly variations, with an average of 36.24 ± 1.95, with the exception of the months of May, June, and July 2020, which presented higher values, with the highest value of 42.8 psu being recorded in June 2020. Chlorophyll-a values on the other hand showed a wide range, varying from 0.53 μg/L in March 2021 to a peak value of 4.72 μg/L in December 2020, with an average of 2.62 ± 2.03 μg/L. Dissolved oxygen presented an average air saturation value over the two-year study of 93.3 ±18.4%; however, a different pattern was observed in both studied years, especially during the summer months, with the highest value observed in the first sampling year in August 2020 (128.6%) and the lowest in August and September 2021 of the second sampling year (55.5%). The values for conductivity in both years presented a similar pattern, with a mean value of 56.3 ± 7.1 mS/cm, with the highest values observed in the summer months (highest value 65.9 mS/cm in August 2021) and the lowest in the winter months (lowest value of 43.7 mS/cm in January 2022). Finally, TDS remained relatively stable throughout the monitoring period, with an average value of 35.4 ± 7.1 g/L, with the highest value of 41.4 g/L observed in June 2020 and the lowest value of 33.1 g/L observed in November 2020.

3.2. Gametogenic Cycle

Across all P. radiata collected over the two-year study, the overall sex ratio (F:M) was 1.25:1, with males prevalent in smaller individuals (shell height less than 65 mm). Hermaphroditism was observed in only two individuals (Figure 3), one in September and one in December 2021, with a weight of 50.32 g, length of 66.3 mm, width of 61 mm, and height 26 of mm and weight of 51.93 g, length of 65.6 mm, width of 60.4 mm, and height of 24.9 mm, respectively. Pearls, with an average diameter size of 0.26 mm, were found during six of the sampling months. Typically, only one pearl per individual was observed, and no more than one individual per monthly sample exhibited a pearl, except in May 2021, when 12 pearls were found in a single oyster.

The monthly frequency of each stage of gonadal maturation of P. radiata from May 2020 to April 2022 is presented in Figure 4a. A general synchronism in the gonadal development of males and females was observed throughout the 24 months (Figure 4b,c), and there was a seasonal pattern in the reproductive cycle of species. In November and December 2020, the majority of individuals were in the earlier stages of development, with 56% and 44% in stage 0—sexual rest, respectively, and 24% and 34% in development stage 1, which corresponded to the lowest gonadal index (GI), in both November and December of 2020, with a value of 0.91 (Figure 5). Although starting slightly earlier, a similar pattern for both sexes (Figure 4a) was observed the following year in September and October 2021, dominated by the sexual rest (stage 0), with 48% and 54% (GI: S = 1.9, O = 1.77), respectively. In the spring season, the oysters reached their highest spawning peak, with 97% in April and 41% in May 2021, and 40% and 3% were in ripe stage 3, also represented by the highest GI values of 3.96 and 3.97, respectively. The following year, oysters also showed a spawning peak in April 2022, with 80% in stage 4 (i.e., spawning stage) and a GI of 3.85. In both sampling years, gonads underwent a very rapid evolution to ripe and spawning stages starting in January and lasting until May, with both sexes presenting a spawning peak in April. Condition index was a fairly good indicator of the gonadal cycle mainly in the first sampling year, with the higher values observed between January and April 2021, with a peak in March 2021 (13.78), and between December and March 2022. The lowest values were observed from August to November in both years.

To better understand the factors influencing the reproductive cycle, a principal component analysis (PCA) was performed. The PCA biplot (Figure 6) shows that PC1 and PC2 together explained over 78% of the total variance, with PC1 accounting for 54.21% and PC2 for 23.96%. This high percentage indicates that the key environmental and biological factors affecting pearl oyster development were well represented in these two dimensions.

The separation of months along PC1 and PC2 highlighted distinct seasonal patterns, with variables like temperature, condition index, and oocyte sizes contributing significantly to the observed distribution. For instance, months with higher temperatures clustered in the third PCA quadrant of the biplot, demonstrating the strong seasonal influence on the oysters’ biological cycles. In the biplot, month numbers (1 through 12) represent the centroids for each respective month across the two sampled years. These centroids were calculated as the average position of the same month in 2020 and 2021, reflecting the central tendency and showcasing the strong seasonal consistency in the data. The cyclic arrangement of these centroids emphasizes the annual cyclicity of the environmental and biological variables. For example, months occurring in similar seasons (e.g., winter or summer) are positioned closely together, indicating that similar environmental conditions and biological responses are repeated annually. This consistency suggests that factors like temperature and chlorophyll-a follow a predictable annual cycle, which, in turn, influences the reliability of the observed gametogenic stages and other biological processes.

The clustering of the same months across two consecutive years in the biplot highlights a consistent and reproducible seasonal pattern, suggesting that the environmental conditions and biological responses of the pearl oysters remained stable during the study period. This consistency reinforces the reliability of the observed gametogenic cycle and environmental conditions.

The red vectors in the biplot represent the original variables (temperature, chlorophyll-a, condition index, gametogenic index, and oocyte size). The direction and length of these vectors indicate the degree to which each variable influenced the principal components. For instance, a long vector for temperature implies a strong impact on PC2, while the angle between the vector and the axes reflects its correlation with the principal components.

The biplot also shows the association between certain variables, such as gametogenic index and oocyte size, which are closely aligned with specific months, particularly April in both years. This alignment reflects the timing of key biological processes, i.e., spawning. The positioning of these months in relation to the vectors indicates that these biological processes are likely driven by environmental factors, such as temperature and nutrient availability, as suggested by chlorophyll-a levels.

The global warming of seawater is recognized as a major driver of reproductive changes, though direct in situ quantifications are still needed [32]. In the Western Arabian Gulf, the reproductive cycle of P. radiata was previously studied in 1992–1993 in Bahrain [21]. We compared these historical data with our present findings from the period 2020–2022. Figure 7 shows the temperature profile changes between these two periods and the corresponding shifts in spawning stage patterns throughout the year. It shows that in 2020–2022, the peak of spawning (stage 4) was reached in early April, followed by a rapid drop, whereas, in the previous study with data from the period 1992–1993, the gonads underwent a rapid transition to the spawning stage only in May/June, maintaining a nearly 100% spawning stage until July 1992. Interestingly, Figure 7 also shows that in both periods, the onset of the spawning stage coincided with water temperatures of 24–25 °C. However, the sudden decline in stage 4 observed in 2020–2021 data aligned with temperatures exceeding 30 °C, rising up to 33 °C. This suggests that increasing seawater temperatures may be limiting the duration of the spawning period, causing a more rapid shift in reproductive patterns compared to the earlier study.

Note that the stage 4 value of January 2021, that appears as an outlier at this season, should be associated with the exceptional peak of chlorophyll-a up to 4.72 μg/L we measured in December 2020.

4. Discussion

In the present work, we studied the impact of the last 30 years’ rise in seawater temperature on marine life in one of the warmest seas on Earth, the western Arabian Gulf. We compared the current reproductive cycle of the pearl oyster P. radiata sampled from 2020 to 2022 in Qatar at the Simaisma coastal site with past data measured in 1992–1993, approximately 100 km away in northern Bahrain [21]. While the two sampling sites in Qatar and Bahrain are approximately 100 km apart, they share similar environmental characteristics, including shallow depths (4–5 m) and coastal locations with comparable distances from the shore. This depth range was essential as it provides similar light penetration, thermal inertia, and sensitivity to temperature fluctuations, which are known to influence the reproductive cycles of bivalves. Furthermore, previous studies on larval connectivity within the Arabian Gulf suggest that populations of benthic species in this region are ecologically connected through larval transport [33]. This connectivity implies that the populations sampled in Qatar and Bahrain are not isolated but likely form part of a broader metapopulation within the Gulf. Consistent with observations in other bivalve species, such interconnected populations typically exhibit synchronized reproductive cycles in response to shared seasonal environmental cues, such as temperature and chlorophyll-a levels (e.g., the Pacific oyster, Crassostrea gigas, on the French Atlantic coast [34]). Therefore, despite the spatial separation, it is reasonable to consider these populations comparable, as they are likely responding to similar environmental drivers across the Gulf’s semi-enclosed and relatively homogeneous thermal environment.

Our findings demonstrate that in the warmer Qatari sea today, the reproductive cycle still exhibits a distinct seasonal pattern. The primary spawning period is shorter, occurs earlier in the year, and is concentrated in April. In contrast, 30 years ago in Bahrain, this period extended from May to August.

• Reproductive cycle

The reproductive cycle in bivalves encompasses a series of events, starting from the onset of gametogenesis and leading to spawning. These processes are intricately regulated by a combination of internal endocrine factors and external factors, with temperature and food availability playing pivotal roles (e.g., [28]). An unbalanced sex ratio, with female prevalence and the predominance of males in the lower size classes observed in this study, was previously observed in populations from Tunisia [18,22], Turkey [19], and Greece [20]. However, populations of P. radiata from New South Wales, Australia presented contrarily a predominance of males (56%) [35]. The low rate of hermaphroditism observed seems to be common in this species, like in populations from Turkey [19] and Tunisia [22].

The reproductive cycle in both females and males followed a well-defined seasonal pattern, with gonads going through a fast gonadal maturation to ripe and spawning stages, starting in January and being prolonged to May, with both sexes presenting a narrow spawning peak in April. The synchronized gonadal development between sexes guarantees reproductive success by enabling a synchronized release of sperm and oocytes into the water column, enhancing fertilization chances. The gonadal index fairly reproduced the gonadal cycle, with the minimum values observed in late Autumn, where individuals were mainly in stage 0 (and early development stages), and the highest values observed in spring, with the highest value in May 2021, a period during which most pearl oysters were in spawning and spent stages (respectively stages 4 and 5). Understanding this cyclicity is crucial for effective management and conservation strategies, as it highlights the predictable nature of these cycles and the potential impacts of environmental changes. The PCA biplot effectively captures the seasonal dynamics and environmental influences on pearl oysters in Qatar. The strong consistency across two years and the clear representation of key environmental variables—temperature and Chlorophyll-a—provide valuable insights into the factors driving the gametogenic cycle and related biological processes.

The condition index was also a good indicator of the gonadal cycle, generally increasing in line with the majority of individuals being at an advanced stage of gametogenesis, with decreases at the post-spawning stage associated with weight loss following gamete release. The condition index values that deviate from this trend may be attributed to the fact that the condition index reflects both somatic and gonadal tissues, with some influencing factors not directly related to the gametogenic cycle.

• The forward shift in the spawning period

Previous studies on P. radiata from other geographical locations including Bahrain, showed a main spawning period during the summer months, from June to August/September, with some presenting a second minor autumn peak (e.g., [18,19,20,21,22]).

The differences observed in the main spawning periods between the different populations of P. radiata may be attributable to different geographical locations and environmental parameters such as temperature and food availability, as previously reported for other bivalve species (e.g., [28] for the clam Ruditapes decussatus; [23] for the scallop Argopecten purpuratus).

This work, comparing two geographically proximate sites in the Arabian Gulf studied 30 years apart, demonstrates that recent increases in seawater temperature, linked to global warming, can lead to significant shifts in long-term ecological patterns.

A dramatic and important temporal shift was indeed observed in the main spawning period when compared with records from 1992 and 1993, as depicted by the average annual cycle of spawning in both periods. The annual reproductive cycle followed a clear forward shift of the peak of the spawning period. In addition to the temporal shift in peak spawning, there has also been a notable change in the duration of the spawning period. During 1992–1993, the frequency of oysters in spawning remained above 70% from April to July, indicating a prolonged spawning season lasting approximately six months. In contrast, the 2021–2022 data show that the period of very active spawning, with stage 4 frequencies above 70%, is much shorter, spawning only from late March to late April. This contraction of the spawning window shows that the conditions favorable for spawning are now limited to a narrower timeframe, which will have deep implications for the reproductive success and population dynamics of the species.

In the previous study of 1992–1993, the higher frequency of the spawning period started when the water temperature reached ≈24–25 °C in May. Then, it was prolonged until August, peaking in June/July, indicating that the majority of the population was ready to spawn during these four months. On the contrary, currently, in 2021–2022, the peak shifted to earlier in the year, occurring in April, but again when the water temperature reached ≈24–25 °C. Then, as the temperature continued to rise rapidly up to 37.3 °C, 3–4 °C higher than in Bahrain in 1992–93, there was a sharp decline in gonadal maturity. The analysis of both studies suggests that a temperature of around 24–25 °C must be a key value for the onset of spawning in P. radiata populations of the Arabian Gulf. However, elevated temperatures, potentially due to their rapid increase, exert a significant negative impact by shortening the spawning period. Excessive sea surface temperature, driven by global climate change, could be altering or limiting the cues that trigger spawning in pearl oysters, leading to an earlier and more condensed spawning season.

In fish, studies have shown that increasing ocean temperatures can also induce earlier reproduction activity and shorten the spawning period, which leads to fewer opportunities for reproduction [36]. The authors proposed that the inhibitory effects of temperature rises in fish are mediated by the endocrine system. We suggest that gonadal maturation in bivalves is also regulated by endocrine mechanisms, albeit through pathways that differ from the well-established endocrine systems of vertebrates [37].

• Not only the temperature changed

Fluctuations in ocean surface temperatures correlated with variations in other factors, including biological indicators like Chl-a [38]. The variability pattern of Chl-a appeared less homogenous than SST variability. Chl-a was shown to be positively correlated with increases in SSTs in the Arabian Gulf by [39] but not by [40]. Indeed, the latter argued that Chl-a tends to globally decrease, whereas SST has displayed an increasing trend over the last 20 years. Unfortunately, we were unable to compare our Chl-a results with the previous study in the region, since no Chl-a determinations were presented by [21].

Shifts in nutrient availability, as indicated by changes in chlorophyll-a levels, may also play a role in modifying the timing and duration of reproductive cycles, but the shallow coastal Arabian Gulf areas, like the studied area, are not food-limited [41]. In addition to a distinct spawning period, in this study, pearl oysters exhibited a strategic reproductive approach that ensured a consistent supply of gametes during the reduced spawning season.

• Water temperature difference between near-shore and offshore sites

The state of the ocean report says that the ocean is warming twice as fast as it did 30 years ago, and 2024 is likely to be one of the warmest years. Since the end of June 2024, the maximum SST in the Arabian Gulf has been reported to oscillate between 33 and 35 °C by the NOAA Satellite and Information Service [2]. But, in the present report, at our site near the coast, we measured a maximum value of 37.3 °C, which is 2 degrees Celsius warmer. This observation illustrates the fact that global warming could well have an impact more quickly along the coast, where life is often concentrated, than offshore.

5. Conclusions

Understanding the temporal dynamics of spawning is crucial for the conservation and management of pearl oysters, particularly in light of these observed shifts. The earlier and shorter spawning period, with a shift from summer to spring, of recent years will affect larval recruitment and the overall resilience of the population. The shorter spawning period implies that the bulk of larvae are now exposed to higher seawater temperatures during their early growth period, which could have unknown consequences. While the adjustment in spawning timing may align with more suitable temperatures for adults, the larvae will encounter previously unexperienced thermal conditions. Conservation strategies must be adjusted to account for these changes, ensuring that critical spawning habitats are protected during the narrower spawning window and that any stressors exacerbating these shifts are mitigated.