Ocean Acidification and Sea Temperature Rise Affect the Queen Scallop Aequipecten opercularis (Linnaeus, 1758) in Captivity

Abstract

Climate change poses risks to bivalves; thus, searching for resilient alternative species is crucial for sustainable fisheries. This study examines the impact of reduced pH and elevated temperature and their combined effects on the queen scallop Aequipecten opercularis in captivity. The results indicated that a low pH reduced its growth rates in both weight (0.03 ± 0.05 g/day) and length (0.06 ± 0.16 mm/day), as well as leading to decreases in meat yield (20.75 ± 2.75%) and the condition index (44.21 ± 7.19%). Conversely, elevated temperature resulted in an increased growth in length (0.07 ± 0.23 g/day), meat yield (21.57 ± 4.82%), and condition index (45.42 ± 7.35%). Combined stressors initially promoted growth but ultimately produced unsustainable outcomes, resulting in a reduced meat yield (18.28 ± 2.60%) and condition index (38.92 ± 8.23%), along with a peak mortality rate of 27%. These findings indicate that while A. opercularis can withstand individual stressors, exposure to simultaneous stressors may compromise its long-term viability in aquaculture systems.

1. Introduction

Bivalves are farmed and produced for consumption in various European countries, North America, China, and Chile. The most significant bivalve species for international trade are scallops, clams, oysters, and mussels [1]. Shellfish production in the Mediterranean is essential, contributing significantly to the local economy and food supply [2]. This region is known for its diverse range of shellfish, including mussels, oysters, and scallops. The Mediterranean’s warm waters and rich marine biodiversity create ideal conditions for shellfish cultivation, with countries like Spain, Italy, and Greece being prominent producers. Scallop farming is notable in this region, though it is less dominant than mussel and oyster farming. Globally, scallop production is more concentrated in the North Atlantic and the North Pacific, with China, Japan, and the United States leading this industry [3,4,5,6]. Although shellfish farming is significant across most European countries, scallop production is primarily concentrated in the United Kingdom, northern France, Spain, and Norway. Queen scallop farms tend to be smaller and more artisanal, in sheltered, shallow bays (30–40 m) and inlets adjacent to rocky shores. The shellfish culture system in European countries is oriented towards bottom cages or suspension cages in pearl nets and lantern nets, focusing on high-quality, locally consumed products [7]. One of the challenges for queen scallop production is the competition with great Mediterranean scallops, which are often valuable due to their higher meat content [8,9].

Nevertheless, great Mediterranean scallops are prized for their taste and freshness, thus maintaining a niche in the market. Aequipecten opercularis is one of the key species in local fisheries and marine ecosystems along the eastern Adriatic coast, with its role expected to remain crucial even under projected climate change conditions [10,11]. By integrating the sclerochronological approach through detailed shell measurements with climatological data from advanced climate model projections, Zemunik Selak et al. [12] showed a robust strategy for forecasting future trends in A. opercularis growth.

Ocean acidification and sea warming are major climate change drivers that significantly affect shellfish physiology and the quality of seafood [13,14,15,16,17,18,19]. Ocean acidification, caused by increased CO₂ absorption, lowers the pH of seawater [20], affecting the ability of shellfish to form and maintain their calcium carbonate shells [21,22,23]. This results in weaker shells and higher mortality rates, particularly in the larval and juvenile stages [15]. Sea surface warming causes an increase in the temperatures throughout the water column, altering the metabolic rates and stress levels in shellfish, which can further lead to reduced growth rates and compromised immune systems, thus altering the growing period [12,16,17,18,19,21,22,23,24,25,26]. These factors (lower pH and higher T) can cause physiological stress, making shellfish more susceptible to diseases and reducing their overall health and market quality [26]. The condition index and meat yield in bivalves are crucial economic indices affected by environmental changes [10,11,27,28,29]. Studies have shown that shellfish exposed to acidified and warmer waters often have a reduced meat content due to these combined stressors affecting their energy allocation [15]. This can lead to smaller, less nutritious shellfish, negatively impacting market value and consumer satisfaction [23,30]. Changes in shellfish physiology due to acidification and warming also affect the nutritional content of seafood, potentially reducing levels of essential nutrients such as omega-3 fatty acids [23,31,32]. Moreover, these environmental stressors can change shellfish behavior and reproduction [33,34,35,36,37], further impacting population dynamics and availability [26].

Several studies have found that under certain conditions, such as limited food availability and oxygen saturation, an increase in temperature has a more pronounced negative impact on shell integrity in bivalves than ocean acidification [19,22,23,36]. Furthermore, temperature increases can alter many metabolic processes in bivalves [23,31,32] and affect their strength and intensity of behaviour in the marine environment. In particular, the swimming behavior of some bivalves changes depending on the water temperature [38,39]. Findings from Tomasetti et al. [19] emphasize that the most pressing threat facing coastal molluscs, as well as the fisheries, aquaculture industries, and local communities that rely on them, stems from the rapid warming of coastal waters and the increasing occurrence of hypoxia, rather than ocean acidification. According to many studies [17,20,23,24,26,39,40], addressing these challenges should be a top priority for both researchers and resource managers in the present and for the foreseeable future, as the impacts of coastal warming and oxygen depletion are likely to intensify in upcoming decades.

To the best of our knowledge, there is currently no information in the literature regarding alternative species for farming in the Mediterranean Sea region under climate change conditions. Therefore, the current study aimed to evaluate the impact of decreased pH and increased temperature and their combined effects on the queen scallop A. opercularis. This was assessed by measuring its growth rates (length and weight) and changes in commercial indices (condition index and meat yield) and somatic indices. Our study demonstrates that the queen scallop (Aequipecten opercularis) is a promising alternative for shellfish farming in the context of climate change due to its rapid growth rates and wide environmental tolerance. This study provides the first available data on the growth rates and performance indices for the queen scallop under simulated climate change conditions in captivity.

2. Materials and Methods

2.1. Scallop Processing

In February 2022, 120 specimens of the queen scallop A. opercularis (Linnaeus, 1758) were procured from a site located two nautical miles southeast of the Albanež shoal, situated within the E2 fishing zone in the Municipality of Medulin, Croatia (Figure 1). Local fishermen harvested the scallops using a bottom-trawling net from a fishing vessel at a depth of approximately 50 m.

Following their collection, the scallops were transported to the Aquarium Pula facility and housed in a circular basin with a capacity of 1900 L. The basin had a flow-through seawater system, maintained at a rate of 200 L per hour. The scallops underwent a one-week acclimatization period in this environment (dissolved oxygen = 76.33 ± 10.22%; salinity = 38.25 ± 0.24).

For this study, 90 individual scallops were randomly selected from the 1900 L tank (Figure 2a). These scallops had an average shell length of 51.4 ± 3.0 mm and an average shell width of 48.5 ± 2.2 mm.

Throughout the acclimatization and experimental period, two replicate tanks per control or treatment were maintained, where the scallops received daily nourishment following the methodology outlined by Čanak et al. [10]. Briefly, the scallops were fed with a mixture of algae cultures consisting of Tetraselmis spp. (Chlorophyta; 5 × 10⁵ cells/mL), Nannochloropsis spp. (Eustigmatophyceae; 30 × 10⁵ cells/mL), and Phaeodactylum spp. (Bacillariophceae; 12 × 10⁵ cells/mL).

2.2. Climate Change Estimation

Following a one-week acclimatization period, the scallops were divided into three groups, with each containing 30 individuals. The scallops were then transferred into closed-system tanks 190 L in volume and holding a working volume of 160 L. A single aeration stone was used to aerate the tanks. The duration of the experiment was 30 days. Continuous seawater filtration within the tanks was conducted via mechanical aquarium filters, except during the designated feeding hours, which occurred daily from 9 AM to 3 PM. Every second day, 20% of the seawater was replaced with fresh seawater to ensure water quality. The photoperiod was controlled to maintain a 12 h light and 12 h dark cycle. Throughout the experimental period, the control tank (Figure 2b) was maintained under natural seawater conditions typical of the Northern Adriatic Sea for April 2022, with stable temperature and pH levels (Figure 3). The scallops in this control tank were fed solely with algae cultures. In the first experimental tank (ΔpH), the scallops were subjected to a pH reduction of 0.2 (~pH 7.6), and in the second experimental tank (ΔT), they experienced a temperature increase of approximately 2 °C (~17 °C). In the third experimental tank (ΔpHT), the combined effect of a temperature increase and a pH decrease was applied to the scallops (Figure 2c). These climate change conditions were simulated based on predictions by Salgado-García et al. [39]. A pH controller was used to regulate and lower the pH in the experimental tanks to achieve the desired environmental conditions. The controller was designed with a spiral system to ensure the slow dissolution of the gas bubbles into the water without them rising to the surface and escaping into the atmosphere. Temperature elevation was achieved using an aquarium heater installed in the two experimental tanks (ΔT and ΔpHT). Adjustments to the algae concentration for feeding were made based on the survival rate of the scallop population. Throughout the experimental period, temperature, pH, salinity, and dissolved oxygen levels were monitored daily using a Hanna HI98193 multiparameter probe.

2.3. Analysis of Scallop Growth and Indices

The 90 individuals randomly chosen from the 1900 L plastic tank were scallops that had been acclimatized. These individuals were carefully cleaned of macroscopic fouling to ensure accurate subsequent measurements. Following the cleaning, each scallop was uniquely marked with an identification number to facilitate individual tracking before and after the experiment. Before and after (initial and final) a month of cultivation, the scallops underwent measurement of various morphometric parameters, using a digital steel calliper with an accuracy of 0.1 mm, and weight parameters, using a digital balance to the nearest 0.1 g, as outlined in Schmidt et al. [41].

The growth rates for length (GRl) and weight (GRw), specific weight growth rate (SGR w), the food conversion ratio (FCR), and the protein efficiency ratio (PER) were calculated using the following formulae [42,43]:

$$GRl=\left[finallength\right(\mathrm{m}\mathrm{m})-initiallength(\mathrm{m}\mathrm{m}\left)\right]/experimentaltime\left(\mathrm{days}\right)\times 100$$

(1)

$$GRw=\left[finalweight\right(\mathrm{m}\mathrm{m})-initialweight(\mathrm{m}\mathrm{m}\left)\right]/experimentaltime\left(\mathrm{days}\right)\times 100$$

(2)

$$SGRw(\%)=\left[log\right(finalweight\left(\mathrm{g}\right))-initialweight(\mathrm{g}\left)\right]/experimentaltime\left(\mathrm{days}\right)\times 100$$

(3)

$$FCR=Feedintake\left(\mathrm{g}\right)/Weightgain\left(\mathrm{g}\right)$$

(4)

$$PER=Weightgain\left(\mathrm{g}\right)/Proteinconsumed\left(\mathrm{g}\right)$$

(5)

To assess the condition index (CI), meat yield (MY), adductor muscle index (AI), gonadosomatic index (GSI), and hepatosomatic index (HPI), the scallop’s body was dissected after 30 days, and the adductor, gonads, and hepatopancreas were separated from the remaining soft tissue. The formulas for calculating CI and MY; AI; GSI; and HPI were described in Schmidt et al. [41]:

$$CI(\%)=\left[meatwetweight\right(\mathrm{g})/shellwetweight(\mathrm{g}\left)\right]\times 100$$

(6)

$$MY(\%)=\left[meatwetweight\right(\mathrm{g})/totalwetweight(\mathrm{g}\left)\right]\times 100$$

(7)

$$AI(\%)=\left[musclewetweight\right(\mathrm{g})/wetbodyweight(\mathrm{g}\left)\right]\times 100$$

(8)

$$GSI(\%)=\left[gonadwetweight\right(\mathrm{g})/adductorweight(\mathrm{g}\left)\right]\times 100$$

(9)

$$HPI(\%)=\left[hepatopancreaswetweight\right(\mathrm{g})/wetbodyweight(\mathrm{g}\left)\right]\times 100.$$

(10)

A standard formula was used to assess the survival rate:

$$Survivalrate(\%)=(finalnumberofscallops/initialnumberofscallops)\times 100.$$

(11)

2.4. Data Analyses

All the data are reported as means ± standard deviation (SD). Growth rates for length and weight, specific growth rates, the feed conversion ratio, the protein efficiency ratio, the condition index, meat yield, and somatic indices underwent a nonparametric Kruskal–Wallis test to examine the impact of the climate change conditions. In cases of significant differences, the mean values underwent a post hoc analysis using the Mann–Whitney test (p < 0.05). All the analyses were conducted using Statistica 9.0 software (StatSoft Inc., Tulsa, OK, USA).

3. Results

The variation in seawater pH and temperature in the control tank and the three experimental tanks is shown in Figure 3.

A slight increase in water temperature was observed in the control tank and the tank with a decreased pH (ΔpH), from a minimum of 12.2 °C to a maximum of 13.9 °C. In the tank with an elevated temperature (ΔT) and the tank with a combined effect of temperature and pH change (ΔpHT), the temperatures were recorded to be 15.78 ± 0.17 °C and 15.76 ± 0.15 °C, respectively. The mean pH values measured in the control tank and the tank with an increase in water temperature (ΔT) were 7.97 ± 0.10 and 7.97 ± 0.08, while in the decreased pH (ΔpH) tank and the tank with a combined effect of temperature and pH changes (ΔpHT), they were noted to be 7.75 ± 0.12 and 7.76 ± 0.11, respectively.

Certain parameters, such as a reduced pH or an increased temperature, did not individually affect mortality in the queen scallops, while a combination of these parameters negatively impacted the scallops’ survival (Figure 4). The survival rate of the queen scallops, measured in the control tank and that exposed to a temperature increase and a pH decrease, remained above 97% over one month. In the tank with the combined effect of temperature and pH changes, the survival rate was noted to be under 90% at the end of the first week of the experiment. The mortality of the queen scallops during the second week of the experiment in the tank with the combined effect of temperature and pH was 17%, while in the third week, it increased to 23%, reaching 27% by the end of the experiment.

A significant effect of the climate change conditions on weight growth rate was observed, while the effect on length growth was not significant (Kruskal–Wallis test,

Table 1. Statistical results of the Kruskal–Wallis test calculated for weight growth rate (GRw), length growth rate (GRl), specific weight growth rate for weight (SGRw), feed conversion ratio (FCR), and protein efficiency ratio (PER) for scallops during the experiment.

	H	df	p
GRw	10.15	3	0.01
GRl	5.11	3	0.16
SGRw	3.02	3	0.38
FCR	11.93	3	0.007
PER	10.92	3	0.006

). A reduced pH or an increased temperature did not individually affect the growth rates of the queen scallops, while a combination of these parameters positively impacted the scallops’ growth rates (Mann–Whitney U test, Figure 5). A decrease in the weight growth rate was observed in the queen scallops from the tanks with the individual effects of pH, with a value of 0.031 ± 0.057 g/day, and temperature, of 0.052 ± 0.166 g/day, while control queen scallops avereged with 0.067 ± 0.114 g/day. An increase in the weight growth rate of queen scallops was observed in the tank with the combined effect of pH and temperature, with a value of 0.167 ± 0.195 g/day, and was noted to be statistically different from that of the control (Mann–Whitney U test, p < 0.05).

The length growth rate of the queen scallops in the control tank was 0.077 ± 0.229 mm/day. For the queen scallops, the minimal shell growth rate in terms of length was recorded to be 0.060 ± 0.167 mm/day in the tank with a decreased pH, while the maximal weight growth rate was 0.267 ± 0.369 mm/day in the tank with a changed pH and T and was statistically different from that of the control (Mann–Whitney U Test, p = 0.01). The weight growth rate of the queen scallops in the tank with a temperature increase was 0.076 ± 0.167 g/day.

The effect of the climate change conditions on the specific weight growth rate was not significant (Kruskal–Wallis test, Table 1). Under controlled conditions (Con), the scallops had an average specific growth rate of 1.089 ± 0.084% (Figure 6). When exposed to a decreased pH and increased temperature, the scallops exhibited higher specific growth rate values of 1.128 ± 0.087 and 1.100 ± 0.080%, respectively. In the tank with combined changes in both temperature and pH, the average specific growth rate of the scallops was 1.098 ± 0.086%.

A significant effect of the climate change conditions on the feed conversion ratio and the protein efficiency ratio was observed (Kruskal–Wallis test, Table 1). The feed conversion ratio of the queen scallops in the control tank was 1.363 ± 1.527 (Figure 7). Reduced pH or increased temperature, at values of 1.437 ± 1.679 and 1.028 ± 1.516, did not individually affect the growth rates of the queen scallops, while a combination of these parameters caused an increase in the scallops’ feed conversion ratio, reaching the value of 2.288 ± 1.872 (Mann–Whitney U test, p = 0.004). The protein efficiency ratio of the queen scallops in the control tank was 3.195 ± 2.467. Reduced pH caused a significant decrease in the protein efficiency ratio of the queen scallops, with a value of 1.038 ± 1.930 (Mann–Whitney U test, p = 0.01), while increased temperature caused a decrease, with a value of 2.466 ± 1.813, without a significant difference. A combination of these parameters caused an increase in the scallops’ protein efficiency ratio, reaching the value of 5.488 ± 1.696 (Mann–Whitney U test, p = 0.001).

A significant effect of the climate change conditions on meat yield was observed, while the condition index was not affected (Kruskal–Wallis test,

Table 2. Statistical results of the Kruskal–Wallis test calculated for the condition index (CI), meat yield (MY), adductor index (AI), gonadosomatic index (GSI), and hepatosomatic index (HPI) of the queen scallops during the experiment.

	H	df	p
CI	5.08	3	0.16
MY	7.04	3	0.05
AI	17.44	3	0.0006
HPI	3.85	3	0.27
GSI	9.86	3	0.01

). The increase in temperature produced the highest values for both the condition index and meat yield, while the combined effect of temperature and pH changes resulted in the lowest values for both parameters (Figure 8). The condition index of the control queen scallops averaged 43.69 ± 9.55%. The average condition index of the queen scallops exposed to a decreased pH was slightly higher, with a value of 44.21 ± 7.19%. The highest condition index of 45.42 ± 7.35% was observed in the queen scallops exposed to a temperature increase, while the pH decrease resulted in the lowest condition index value of 38.92 ± 8.23% in the queen scallops tested. The average meat yield of the control queen scallops was 20.11 ± 3.20%. A reduction in pH induced an increase in the meat yield of the queen scallops, resulting in a value of 20.75 ± 2.75%, while an increased temperature resulted in the highest value, averaging 21.57 ± 4.82% with a statistically significant difference, when compared to the control (Mann–Whitney test, p < 0.05). The lowest meat yield was observed in the queen scallops exposed to the combined effect of temperature and pH changes, with a value of 18.28 ± 2.60%.

The results of the statistical analysis (Kruskal–Wallis test, Table 2) showed significant differences in the adductor index and the gonadosomatic index across the climate change conditions, indicating strong evidence of variation in these indices (Table 2). The p-values suggested no significant differences between groups in terms of the hepatosomatic index.

The adductor index was recorded to be the highest in the scallops kept in the tank under a temperature increase and was statistically different from that of the control (Mann–Whitney U test, p = 0.01), while the lowest adductor index was observed in the scallops kept under the combined effect of temperature and pH changes (Figure 9). For the queen scallops in the control tank, their adductor index was 10.25 ± 3.01%. Under the decreased pH conditions, the average adductor index increased to 12.67 ± 2.81%, and for the increased temperature conditions, the adductor index was higher, averaging 12.74 ± 2.48%, with both differing statistically from the control (Mann–Whitney U test, p < 0.05). Ultimately, in the tank with a combined effect of temperature and pH changes, the adductor index of the scallops dropped to 9.10 ± 3.11%.

In the control tank, the average gonadosomatic index of the queen scallops was 4.04 ± 2.14%. The highest gonadosomatic index was observed in the scallops under the temperature increase, reaching the highest value, at 5.40 ± 1.93%, and differing statistically from that of the control group (Mann–Whitney U test, p < 0.05), while the lowest value was found under the combined effect of temperature and pH changes, with an average of 3.77 ± 1.88. In the tank with a decreased pH value, the gonadosomatic index of the queen scallops was measured to be 4.48 ± 1.63%.

The hepatosomatic index of the queen scallops was relatively stable in all the experimental conditions tested compared to that in the control tank. Nevertheless, under the temperature increase, again, the highest values for the hepatosomatic index of the queen scallops were exhibited, averaging 10.18 ± 1.60%. The control scallops had an average hepatosomatic index of 10.01 ± 4.23%. In the tank with a pH decrease, the average hepatosomatic index of the scallops was slightly lower, at 9.71 ± 1.87%, while the combined effect of temperature and pH changes resulted in the lowest hepatosomatic index of 9.00 ± 1.83%.

4. Discussion

By the end of this century, climate models predict an increase in average sea surface temperatures by up to 3 °C, accompanied by a significant drop in ocean pH of approximately 0.31 units [44]. These changes in ocean conditions are anticipated to profoundly impact marine organisms, especially affecting the growth and physiology of bivalves [17,19,23,24,25,26]. Consequently, this study investigated the effects of an increase in sea temperature by 2 °C, a reduced pH of 0.2 units, and a combination of both, as projected under near-future climate change scenarios, on the growth, survival, and physiological indices of the queen scallop A. opercularis.

The survival rate of the queen scallops in the experimental tanks can be compared with the results of the study with a reduced pH (7.65) in Mytilus galloprovincialis Lamarck 1819 and Xenostrobus securis Lamarck 1819 [25]. The two organisms share the same habitat along the shores in the inner part of the Galician Rias Baixas (NW Spain). In the aforementioned study, the mortality of the mussels was recorded to be only 6.52 ± 0.95%, and the same low mortality was also noted in this study. While ocean acidification has been shown to cause mortality in bivalves [31,42], lethal effects are not universally observed [21]. Mortality typically occurs after prolonged exposure to severely reduced pH levels [13]. However, even when their survival is not immediately threatened, acidification frequently disrupts physiological processes, leading to suppressed metabolic activity, impaired ion regulation, and diminished protein synthesis. These physiological disruptions can significantly slow the growth rates of bivalves due to reduced energy availability, which hampers the organisms’ ability to maintain their normal growth functions [24,25,44].

The results of this study demonstrate a significant impact of a pH decrease on the growth and physiological indices of queen scallops. The decreased pH conditions led to a decrease in weight growth rate and length growth rate, highlighting the detrimental effects of acidification on shell formation. This finding aligns with previous studies indicating that a lower pH disrupts calcification processes in marine organisms, leading to reduced shell growth [22,23,45]. Furthermore, these results can be compared with the growth rates of the mussels from the Galician Rias Baixas (NW Spain). Gestoso et al. [15] found a significant effect of pH on the growth rates of M. galloprovincialis, with a 50% reduction in growth under reduced pH (7.65) treatments, whereas no effect of the experimental conditions was detected on the growth rates of the invader Xenostrobus securis. Furthermore, the condition index of M. galloprovincialis was noted to be higher with an increase in acidity (pH of 7.65) at 16 °C, as was noted in this study. The enhanced somatic growth observed under hypercapnic conditions, characterized by elevated CO₂ levels, may be attributed to these organisms’ ability to prioritize tissue development over shell formation. Under these acidic conditions, soft tissue growth tends to be less affected than shell accretion, which becomes more challenging as pH decreases [15]. Similar patterns have been reported in other marine species, such as the keystone sea star, where researchers found that reduced pH levels stimulated its somatic growth [33,34,35,36,37], while its calcification processes were significantly inhibited [22,23]. This suggests that marine organisms may redirect energy towards maintaining body tissue when external shell formation is compromised by ocean acidification [36,46].

The increased meat yield of the queen scallops maintained in the tanks with a reduced pH and an elevated temperature may be attributed to their successful acclimation, as observed in X. securis in experiments with acidity and high temperatures [15]. Earlier research has emphasized the remarkable ability of mussels to safeguard their soft tissues from the harmful effects of ocean acidification. Beesley et al. [47] demonstrated that despite the challenges posed by reduced pH levels, mussels exhibit physiological mechanisms that enable them to maintain the integrity of their soft tissues. This resilience likely stems from adaptive responses that allow mussels to allocate resources more efficiently, ensuring tissue preservation even under the stressful environmental conditions caused by acidified waters.

Interestingly, while the growth rates of the queen scallops in this study were inhibited, an increase in their adductor muscle index was observed, indicating a possible compensatory mechanism to maintain functionality under stress. The higher adductor and gonadosomatic indices under decreased pH conditions suggest that their energy allocation may have shifted towards muscle and reproductive tissue development, potentially at the expense of shell growth. However, the lower gonadosomatic index compared to that in the control group could reflect a trade-off between energy demands, where reproduction is maintained but not fully optimized [33,35]. These findings contribute to a broader understanding that environmental stressors, such as ocean acidification, significantly affect marine bivalves through alterations in their energy allocation and physiological responses [23,36,37]. While earlier studies on bay scallops primarily concentrated on the detrimental impacts of ocean acidification as a significant climate change threat [17], mounting evidence suggests that rising ocean temperatures pose an even greater challenge. Heat stress appears to be the more immediate and critical factor affecting scallop survival, with scallops likely to experience mortality due to elevated temperatures well before the effects of acidification become fatal. The abovementioned research underscores that warming, rather than acidification, may be the primary driver of stress in these organisms as global temperature rise.

The results from this study indicate that elevated temperature had a notable impact on the growth and physiological indices of the queen scallops. Specifically, an increase in temperature resulted in a decreased weight growth rate and length growth rate in the scallops, suggesting that while their overall biomass accumulation slowed, their linear shell growth was enhanced. This pattern may reflect a reallocation of energy resources, where scallops prioritize shell extension over mass gain in response to thermal stress [48]. The shift toward higher optimal growth temperatures with increased food availability occurs because bivalves can tolerate higher temperatures better when ample food is available. Kamermans and Saurel [23] investigated the combined effects of temperature and food availability on the growth of mussels (Mytilus edulis and M. galloprovincialis) and oysters (Crassostrea gigas and Ostrea edulis), highlighting how temperature effects are strongly influenced by food conditions. Said study demonstrated a clear relationship between food availability and growth rates in mussels. Under conditions of a low food supply, the maximum shell growth rate of the mussels was measured at 0.0283 ± 0.0060 mm/day, but this rate significantly increased to 0.1703 ± 0.0297 mm/day when food levels were abundant. Similarly, their maximal specific growth rate surged from 0.2651 ± 0.0191 mm/day at low food concentrations to a remarkable 1.7697 ± 0.2177 mm/day with a higher food availability. Oysters followed a similar growth pattern, with their shell growth rate increasing from 0.0616 ± 0.0115 mm/day under limited food conditions to 0.2548 ± 0.0279 mm/day when food was plentiful. The specific growth rate for oysters also showed a substantial rise, ranging from 0.5608 ± 0.0856 mm/day at low food levels to 2.2855 ± 0.2169 mm/day under the optimal feeding conditions. These findings highlight the crucial role of food availability in enhancing the growth rates of mussels and oysters. Moreover, these findings underscore the importance of food availability in mediating the impact of temperature on the growth of these bivalves, with higher food levels significantly enhancing the growth rates in both species.

Additionally, the highest condition index and meat yield in the queen scallops were observed under an increased temperature, indicating an overall improvement in their physiological condition and tissue development despite the reduced weight gain. The elevated adductor, gonadosomatic, and hepatosomatic indices further suggest that thermal conditions favor the development of key tissues, such as muscle and reproductive organs. This may be due to enhanced metabolic activity at higher temperatures, which can accelerate physiological processes and promote energy allocation to critical functions like reproduction and muscle maintenance [17,33,36,49]. However, the long-term sustainability of these benefits under continued thermal stress requires further investigation, as prolonged exposure to elevated temperatures may lead to metabolic imbalances or exhaustion of energy reserves [23,31,32]. These findings are consistent with prior research showing that moderate temperature increases can enhance physiological performance in marine bivalves within a certain thermal threshold. Conversely, in another study conducted on two species of mussels (Mytilus edulis and M. galloprovincialis) and oysters (Crassostrea gigas and Ostrea edulis), it was noticed that the condition index was higher when the food concentrations were increased and decreased with increasing temperature [23]. Furthermore, Kamerman’s 2022 study demonstrated that mussels and oysters exhibited high survival rates when they were exposed to elevated temperatures ranging from 3 to 19 °C, with survival rates from 93 to 100%. Additionally, Tomasetti et al. [18] conducted a notable study investigating how a rise in temperature may have contributed to the dramatic decline in bay scallop (Argopecten irradians) harvests in the Cape Cod region of northeastern USA, where catches plummeted by 98% between 2019 and 2021. This comprehensive study utilized a combination of fishery data, environmental monitoring, and both field and laboratory experiments to uncover the effects of climate-driven coastal warming in Nantucket Harbour and Nantucket Sound, where temperatures increased by 2.48 and 3.42 °C between 2003 and 2020, respectively. These researchers found that the interaction of warming and hypoxia, rather than hypoxia alone, led to significant scallop mortality. Laboratory simulations mimicking these environmental conditions confirmed the field data, revealing that a combination of warming and low oxygen was 9.4 times more lethal to scallops than hypoxia, 57.4 times more lethal than elevated temperatures, and 119.7 times more deadly than conditions with normal oxygen levels and no warming.

Overall, these results underscore the severe biological impacts of warming and hypoxia on marine molluscs, as both factors disrupt the energy availability necessary for growth and reproduction, ultimately leading to high mortality rates [31]. Considering these findings, queen scallops emerge as a promising alternative for aquaculture under climate change pressures given their faster growth rates and broader environmental tolerance compared to mussels and oysters. Queen scallops can adapt to warmer and cooler waters, thus being more resilient to the temperature fluctuations associated with global warming [31]. Moreover, their rapid reproductive cycles and less demanding habitat requirements make them sustainable bivalves for mitigating the risks of changing marine ecosystems [24,25].

The combination of an increased temperature and a decreased pH impacted the mortality, growth, and physiological performance of A. opercularis in this study. The mortality rates increased significantly throughout the experiment, indicating that the combined stressors of temperature and pH changes create harsh environmental conditions that hinder survival. This was also reflected in the feed conversion ratio and the protein efficiency ratio. In aquaculture, scallops generally exhibit efficient feed conversion due to their natural filter-feeding behavior. Unlike carnivorous fish, which require high-protein feeds, scallops and other bivalves derive nutrition from the organic matter in water, including phytoplankton [50]. This characteristic leads to a low feed conversion ratio, as was found in the control scallops in this study [43]. Among bivalves, scallops in captivity often achieve rapid growth without intensive feed input, making them economically viable in aquaculture systems [42,51,52]. However, variations in bivalves exist based on climate change that affect the increase in the feed conversion ratio compared to bivalves not exposed to climate change. This can be attributed to the conversion of nutrients in algae into bioavailable forms (such as ammonia, urea, and phosphate), which may support subsequent phytoplankton production. [50]. The protein efficiency ratio of scallops in captivity is generally lower compared to that of more feed-intensive species such as shrimp and tilapia, as scallops and other filter-feeding bivalves rely on naturally occurring proteins from phytoplankton and other microorganisms [52]. In scallop farming, however, improving the protein retention efficiency remains a key area of ongoing research, particularly under climate change conditions, where feed modifications can influence this parameter [53]. The combined effect of temperature and pH showed synergistic rather than additive effects, which frequently varied depending on the response variable considered [15]. Such results are consistent with those of most previous studies on shelled molluscs that suggest the prevalence of synergistic effects when ocean acidification is combined with temperature [37,39]. It has generally been suggested that a pH decrease may narrow the thermal windows of marine ectotherms [54] and thus increase their susceptibility to environmental changes.

Despite this, the maximal growth rate in weight and length was observed under the combined effect of pH and temperature changes, surpassing that of the control or the single-stressor treatments. This suggests that while growth mechanisms were stimulated by the environmental changes, these effects were unsustainable, as indicated by the lowest meat yield and condition index of the queen scallops kept in the tank with the combined effect of a changed pH and temperature. A decrease in the condition index and meat yield generally indicates a state of lower “health” [27,29], illustrating a negative effect of both temperature and pH conditions. The combination of physiological stress and possibly an insufficient food supply to meet the increased nutrition requirements of higher metabolic rates at higher temperatures could explain such patterns [23].

The reduced somatic indices, including the gonadosomatic and adductor indices, further suggest that their energy reserves were depleted, likely due to the increased metabolic costs associated with coping with both stressors simultaneously [23,31,32,53,55]. These findings align with a study on the effect of hypoxia, hypercapnia, and warming on the cellular metabolism of the great scallop Pecten maximus, showing that marine bivalves can exhibit short-term compensatory growth responses to environmental stressors, but such responses often come at the expense of their overall physiological condition and survival in the long term [31]. The increased mortality and decreased meat yield and condition index underscore the negative synergistic effects of temperature and pH stress on scallop health.

While moderate increases in temperature and acidification may initially stimulate certain physiological responses in queen scallops, their long-term impacts are unknown. These findings highlight the importance of continued research and monitoring to develop resilient aquaculture practices and inform conservation strategies as climate change affects marine ecosystems. Reducing CO₂ emissions and implementing sustainable aquaculture practices are critical steps in mitigating the detrimental effects of ocean acidification and warming on marine scallops [17].

These results further underscore the broader implications of climate change for shellfish aquaculture. The Mediterranean, known for high-quality mussel and oyster production, faces significant challenges due to ocean warming and acidification. These environmental stressors are already affecting shellfish yields in some regions, with potential consequences for food security and the livelihoods of communities dependent on the industry. Given their strong performance under experimental conditions, queen scallops could be considered an alternative bivalve species for aquaculture in the Mediterranean, particularly in the face of climate change [12]. The focus on A. opercularis alone limits conclusions about broader shellfish aquaculture under climate change. Future studies could benefit from including other potential aquaculture species for a more comprehensive understanding. Investigating the performance of A. opercularis compared to other shellfish species under similar climate stressors could further strengthen its potential as a sustainable aquaculture candidate. Further research could explore the economic feasibility of farming A. opercularis at commercial scales, including the costs, the market demand, and the species’ potential to replace or supplement traditional bivalves such as mussels and oysters in aquaculture.

5. Conclusions

In conclusion, this study reveals that decreased pH, increased temperature, and their combined effects significantly influence the growth, physiological indices, and survival of A. opercularis. While a decreased pH resulted in reduced growth rates and increased stress responses, an increase in temperature enhanced their growth in length and physiological indices, the condition index and meat yield, though at the cost of reduced weight gain. The combined effect of increased temperature and decreased pH produced the highest growth rates, feed conversion ratio, and protein efficiency ratio, but these benefits were unsustainable, as indicated by the lowest meat yield, condition index, and somatic indices, alongside high mortality rates (27% by the experiment’s end). These results suggest that although its short-term growth may be stimulated by environmental changes, the long-term health and survival of A. opercularis are severely compromised under these combined stressors. This study highlights the potential risks of climate change for marine species, particularly under simultaneous exposure to multiple stressors.