Thermal Tolerance of Intertidal Gastropods in the Western Arabian Gulf

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Journal of Sea Research 197 (2024) 102470

Available online 16 January 2024

Thermal tolerance of intertidal gastropods in the Western Arabian Gulf

Sinatrya D. Prayudi , Asmaa Korin , Michael A. Kaminski

^*

Geosciences Department, King Fahd University of Petroleum & Minerals, PO Box 5070, Dhahran 31261, Saudi Arabia

A R T I C L E I N F O Keywords:

Gastropoda Bahrain Saudi Arabia Thermal limit Global warming

A B S T R A C T

Laboratory experiments were conducted to determine the thermal tolerance of the living shallow-water and intertidal gastropods from lagoons in Bahrain and Saudi Arabia, in the western Arabian Gulf. Our experimental trials, run in duplicate using a semi-controlled thermal incubator, quantify the thermal limits of two species of gastropods, the tropical periwinkle Planaxis sulcatus (Born, 1778) and the mud creeper Pirenella conica (Blain- ville, 1829), which are commonly found in the region. The two species display different thermal tolerances to heat exposure during this study. In the case of Planaxis sulcatus, we observe that half of the test specimens that are fully exposed to the air enter an inactive state or become comatose at about 39 ^◦C, while half of specimens that are fully immersed in sea water become immobile around 42 ^◦C. For Pirenella conica half of test specimens that are fully exposed enter become inactive at about 37.5 ^◦C, while for specimens that are fully immersed in sea water this temperature is around 45 ^◦C. At 60 ^◦C total mortality is observed with no indication of recovery. These observations have implications for climate change predictions in the western Gulf region, as water temperatures in the lagoon already reach 42 ^◦C in summer, while the substrate temperatures on mud flats exposed during low tide exceed the lethal limit of the gastropods during the summer months.

1. Introduction

Globally, the summer and autumn of 2023 were the warmest on record, with significantly higher sea and land surface temperatures than in previous years (www.ncei.noaa.gov). Numerous reports of record- breaking high temperatures for this year in comparison to the pre- industrial period have been published in various media and Press Releasess (e.g., climate.copernicus.eu), in addition to reports by Dessler (2023) and Hausfather (2023) in www.climatebrink.com. Moreover, the pace of global warming has accelerated markedly in recent years, especially in the six months of 2023, which set groundbreaking records in a global perspective, in comparison with the previous five years (Lindsey and Dahlman, 2023; Meijer, 2023).

Despite the multitude of future climate change (Randall et al., 2007;

Knutti, 2018; Zhou et al., 2023) and global warming models (Hansen et al., 2000; Zeng and Geil, 2016; Cheng et al., 2022) depicting the inevitable fate of the global terrestrial and marine realms, along with endeavors to evaluate the vulnerability of their biotas in each model (Pinsky et al., 2019), there remains a significant gap in exploring the impact of unusually high summer temperatures over short periods on the communities inhabiting these realms. While recent publications have addressed temperature impacts on flora (Liu et al., 2021; Li et al.,

2023; Sklena´ˇr et al., 2023) and fauna (Scarponi et al., 2022; Khaliq et al., 2023; Rangaswami et al., 2023) in line with concerns about future global warming, some regions lack comprehensive coverage or are un- derrepresented compared to others (Moore et al., 2023). Furthermore, greater attention needs to be given to the biota inhabiting transitional areas like intertidal and coastal zones (Bernhardt et al., 2020), where the effects of global warming are likely to be felt with more immediate effect. There is an urgent need to expand our efforts to investigate the resilience of shallow marine biocalcifying organisms to future warming.

Considered as an example of an extreme habitat for marine animals, the Arabian Gulf, or simply “the Gulf”, experiences ecological conditions that are almost incomparable globally, compounded by its geographical features that present a challenge to survival of its marine biota (Price et al., 1993; Sheppard et al., 2010). Geographically, it is characterized as restricted basin, receiving minimal freshwater input, resulting in higher salinity compared with the Indian Ocean (Vaughan et al., 2018; Amao et al., 2022). Additional natural stressors, such as elevated water temperatures and intense solar exposure during the summer months, exac- erbate thermal challenges within the Gulf (Patlakas et al., 2019; Alosairi et al., 2020). Moreover, human activities contribute to the basin’s current conditions, exemplified by discharge from desalination plants enriched with heavy metals and highly saturated brine (Sharifinia et al.,

* Corresponding author.

E-mail address: [email protected] (M.A. Kaminski).

Contents lists available at ScienceDirect

Journal of Sea Research

journal homepage: www.elsevier.com/locate/seares

https://doi.org/10.1016/j.seares.2024.102470

Received 7 November 2023; Received in revised form 29 December 2023; Accepted 9 January 2024

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Journal of Sea Research 197 (2024) 102470

2019; Saeed et al., 2019; Omerspahic et al., 2022), which potentially impacts the marine biota.

The section of the Arabian Gulf between Qatar and the Coast of Saudi Arabia in particular has been identified as the area that is most likely to be affected by climate warming (Pal and Eltahir, 2016). Climate models for the second half of the 21st century predict several degrees of warming, with sea-surface temperatures approaching 44 ^◦C and wet- bulb temperatures exceeding 35 ^◦C in the area by the middle part of the century (Pal and Eltahir, 2016; Safieddine et al., 2022). A recent report by Kaminski et al. (2023) revealed substrate temperatures above 60 ^◦C for the seasonally exposed intertidal areas and above 40 ^◦C water temperature in a small lagoon that contains living biota such gastropods and juvenile fish. Such high temperatures are predicted to have a devastating effect for eukaryotic organisms, especially if we consider the thermal tolerances of marine ectotherms based on the comprehensive review of Sunday et al. (2011, 2012).

We place emphasis on enhancing our understanding of the effects of global crises like anthropogenic climate change, since few studies have addressed this issue in the Gulf region, especially in terms of future warming trends. We ask the question: “given the current place of warming in the Gulf, at what point does increasing temperature become a threat to marine organisms? The intertidal zones at both studied localities (eastern coast of Saudi Arabia and Bahrain) have been reported

as kill zones owing to elevated temperatures during summer (Kaminski et al., 2021, 2023). Although laboratory investigations have established the thermal limits of shallow marine organisms from other regions of the world (e.g., Stirling, 1982; Williams and Morritt, 1995; Han et al., 2019;

Davenport and Davenport, 2007; Li and Dong, 2020), no such studies have yet been performed on intertidal benthic organisms in the Gulf region. The only comparable studies that outlining the impact of thermal stressors on the biota of the Arabian Gulf, mostly concern the coral reef and the adjacent communities (Coles and Riegl, 2013; Bouwmeester et al., 2020; D’Agostino et al., 2020).

To address this research gap, we conducted thermal tolerance experiments on selected intertidal organisms that are abundant enough for practical experimentation in the Gulf, utilizing various thermal exposure scenarios. Initially, we examined a salinity-tolerant intertidal ostracod belonging to the genus Cyprideis, demonstrating high thermal resilience exceeding 50 ^◦C before reaching its upper lethal limit (Prayudi et al., 2024). However, studies that outline the impact of thermal stressors across different ecological conditions, such as varying water levels, are lacking. Our prior ostracod research only considered a single scenario due to their preference for an underwater habitat. Consequently, we incorporated two gastropod species for this study, each inhabiting distinct ecological condition based on direct field observations by Kaminski and Garrison (2020) and Kaminski et al. (2021). Furthermore, Fig. 1. Sampling localities for both gastropod species.

S.D. Prayudi et al.

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we observed an uneven distribution of both targeted species in relatively close proximity, suggesting a potential influence of temperature-related factors on their spatial distribution pattern.

2. Materials and methods 2.1. Study locality selection

Our study areas are in the western Arabian Gulf, particularly Saudi Arabia and Bahrain. Two sites were chosen, Half Moon Bay or specifically in Zabnah Beach Lagoon, Saudi Arabia (26.000877, 49.997965) and a lagoon on the east coast of Bahrain known in the literature as

“Murray’s Pool” (26.044355, 50.623077), both of which are areas with little human disturbance and a rich intertidal ecosystem (Fig. 1). A number of studies (El-Sorogy et al., 2019; Amao et al., 2016; Arslan et al., 2017; Kaminski and Garrison, 2020; Kaminski et al., 2021; Joydas et al., 2013; Prayudi et al., 2024) discussed the benthic marine communities that occur in the area, including mollusks (gastropods and bi- valves), arthropods (crabs and ostracods), annelids (nematodes), and benthic foraminifera. Additionally, we consider both study localities to be among the last natural refuges for intertidal marine communities living within the vicinity, owing to the fast pace of human development along the coastlines of Bahrain and the Saudi Arabian sector of the Gulf.

Bahrain and Saudi Arabia’s intertidal areas share several characteristics. Kaminski et al. (2023), documented a distinct temperature gradient across the intertidal area from the foreshore to the lagoon.

According to our field measurements, this gradient is present in both in winter and summer. The intertidal area experiences temperatures as low as 17 ^◦C during winter (December to February) and in excess of 60 ^◦C during summer (May to August). Additionally, salinity values in Bahrain are significantly lower than those at the Zabnah Beach Lagoon (approximately 45 to 47.5 PSU versus 70 PSU), which contribute to the physio-chemical differences between the two areas.

In summer, the gastropods avoid areas of the mudflat that exceed temperatures of 40 ^◦C (Kaminski and Garrison, 2020). The living marine organisms that live there, either above or below the substrate, are subjected to differing exposure times, determined by the tides and wave heights, as well as temperature constraints resulting from seasonal solar insolation. Periodic breaking waves and high tides bring water into the lagoons, but later these lagoons may dry up partially or entirely, leaving the stranded marine organisms to suffer the effects of the increased warmth in shrinking pools of water. The benthic organisms inhabiting such an environment ought to be able to adapt to and survive three possible scenarios: (a) totally exposed during low tide or when there is no water in the lagoon or pools (full exposure or FE), (b) partially exposed when the water begins to recede (partial exposure or PE), and Fig. 2. Different types of thermal exposure observed towards the gastropod specimens in the field from both localities: A) full direct exposure of heat in Murray’s pools; B) partial exposure and full water coverage inside a small pond in Murray’s pools; C) direct exposure in the Zabnah beach lagoon; and D) all three thermal scenarios in the Zabnah beach lagoon, observable across the sight of view, as we move towards the water. All photograph were taken between December 26th to 27th, 2023.

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(c) completely submerged during high tides (full coverage or FC).

Representative composite images to address the three type of scenario where our intertidal gastropod encounter during the daily basis are observable in the Fig. 2 below.

2.2. Species selection for experiment

We selected two species to test each of the three scenarios in the intertidal habitat, in light of the fact that certain organisms must adjust to temperature constraints under various conditions. The tropical periwinkle Planaxis sulcatus (Born, 1778) and the mud creeper Pirenella conica (Blainville, 1829) were selected as representative intertidal gastropod species for our study. Both species exhibit unique body and shell shapes as well as ecological preferences (Smythe, 1982). The common periwinkle, Litorrina scabra (Linnaeus, 1758), and the tropical periwinkle both have a smooth shell surface, a large body whorl that increases rapidly in diameter with ontogeny, and a low trochospirally coiled shell. The mud creeper, on the other hand, has shells that are longer and narrower (over 30 mm for an adult), with a twisted columella and spiral beaded rows. In Murray’s Pool, where tropical periwinkles are abundant alongside mud creepers, they tend to cluster together and either cling to a rock or develop pyramidal structures as part of their seasonal thermoregulatory behavior (Kaminski and Garrison, 2020), which is not apparent in the case of the mud creeper. On the other hand, there have been no recent findings of tropical periwinkles in the Half Moon Bay area.

2.3. Sample collection

We sampled lagoonal water, sediment from the lagoon’s edge, and live snails from the Half Moon Bay and Murray’s Pools localities. The specimens removed from the study locations were first observed in the field in order to confirm that they were alive by noting their movement before being placed into the sample container. Before continuing with the experiment, the specimens were stored in a plastic container

approximately 30 ×75 cm in size. To reproduce a comparable substrate for the specimens to graze on within the container, a 0.5 cm thick block of surficial sediment from the lagoons was collected using a metal spatula, and placed in the sample container as the substrate for the snails. This provided a substrate that preserved the environmental characteristics of the lagoon to the maximum extent possible during transport.

We also collected water from the lagoons with in-situ measured salinity at 70 PSU for the Half Moon Bay locality and 44 PSU for the Murray’s Pool in order to best reproduce the environment of the snail’s natural habitat and to spare the specimens any additional physical and chemical stress. About 100 ml of lagoon water or 0.5 cm of sediment, measured from the surface of the water to the bottom of the sediment, was included in the specimen container. We observed that the majority of active specimens are found in shallow water (between 5 and 10 mm).

Along with the snail samples, some 500 g of sediment are also taken from the Murray’s Pool and Zabnah Beach Lagoon for future use, particularly for simulating the environmental conditions needed for the snails to carry out their activities.

Live snail specimens were sampled on separate two occasions (up to 100 specimens of each species in each sample). The first set of samples was collected in May and June 2022, with the mud creeper as our primary objective. The second round of samples were collected in late spring to early summer, 2023 (March to May). We conducted experimental trials in the Micropaleontology Laboratory at King Fahd Uni- versity of Petroleum & Minerals (KFUPM), in Dhahran, Saudi Arabia. As a necessary component of an ecological experiment, additional sampling was performed in order to conduct replicate trials (see: Hairston, 1989).

2.4. Heat exposure experiment and specimen recovery observation Specimens were gathered in the morning, placed a plastic container, and immediately transported back to the KFUPM Laboratory of Micro- paleontology in order to set up the experiment’s next stage. Six specimens were randomly chosen from among the numerous previously Fig. 3. Configuration of the thermal limit experiment of gastropods: A) top-view of each petri dish containing sediment and noting each type of scenario on the lid of petri dish; B) side-view of each petri dish to show the sediment thickness and water height for each scenario; C) placement of petri dishes inside the incubator; and D) specimen placing within each petri dish before the start of experiment.

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collected specimens and placed inside a 100 mm diameter petri dish with a top cover to preserve moisture. Three different scenarios were set up in order to mimic the typical substrate and environmental characteristics in their natural habitat. It is further revealed that in these particular scenarios, the snails are capable of interacting with the substrate through grazing or feeding. The scenarios comprised (a) complete immersion in lagoon water within a specific depth range, (b) partial exposure in lagoon water, and (c) full body exposure on wet mud.

Following separation into three groups, a total of 18 snail specimens were used for each experimental trial (around 200 specimens were used in total).

We attempted to replicate the three natural scenarios in the petri dishes. In the first scenario, which entails total exposure on wet mud, local sediment about 3 mm deep was provided as the substrate inside the petri dish. The previously compacted silt was then topped with around 10 cc of lagoon water to simulate the damp, moist mud. For the second and third scenarios, the same amount of sediment was placed into the petri dish, but different amounts of water were added. For the second scenario, about 25 ml of lagoon water was added which extended as high as 0.3 cm above the sediment. For the third scenario, 50 ml of water was added to the third petri dish with the 0.3 cm thick sediment, with approximately 0.6 cm of water above the sediment. Fig. 3 illustrates the layout of the petri dish for the experiment, while Fig. 4 illustrates the

layout of the petri dish for the placement of the snails and monitoring of their movement. Overall, we conducted our experiment using a different methodology compared with previous studies of thermal limits first developed by Evans (1948), and then revived with similar methodolo- gies in the studies of Stirling (1982), Han et al. (2019), and Li and Dong (2020). Davenport and Davenport (2007) and Williams and Morritt (1995) conducted their experiments using methodology closest to ours, which included a range of settings and heat exposures in gastropod species.

The snails were heated using a confined heat source within an oven with a viewing window, a suitable heat capacity, and a simple temperature control. We used the semi-controlled thermal incubator (Memmert Universal Oven U Incubator I UN 30, Memmert, Germany) for this experiment. In the heating experiment, several specimens were placed in petri dishes that attempted to simulate the natural substrate and exposure conditions, and subjected to five different temperature exposures—40 ^◦C, 45 ^◦C, 50 ^◦C, 55 ^◦C, and 60 ^◦C—along with one replicate trial to confirm the consistency of results.

Three sets of petri dishes were simultaneously placed into the oven in a certain order to reflect the first, second, and third environmental scenarios. Prior to commencing the experiment, the temperature of the substrate in the petri dishes and the initial placement of the specimens were measured and recorded to serve as a starting point and a Fig. 4. Placement of snails in petri dishes and their movement in the three scenarios (partial exposure, full exposure, full coverage). At the beginning of the experiment snails were placed at 2, 4, 6, 8, 10, and 12 o’clock positions in the petri dish.

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benchmark for the following phase. In each petri dish, a specimen is placed in one of six locations, with the anterior canal pointing roughly towards the center and the shell’s apex either touching or very close to the dish’s rim. We measured the substrate temperature within the petri dish using a TAYLOR RA44069 806GW Digital Thermometer by inserting the tip of the instrument into the substrate surface. Three images of each petri dish depicting the specimens’ current position and condition as well as a real-time measurement of the substrate temperature were captured for each step.

During the thermal exposure experiment, along with the three hours of exposure, three procedures were carried out during the experiment:

two pre-exposure (Fig. 5) and one post-exposure procedure. No direct observation during thermal exposure was possible due to limitation of the equipment, therefore we checked the specimens after each abovementioned interval. As the petri dish containing the specimens and the

water-sediment mixture is placed in the oven, the first operation, initial placement, is carried out. The second procedure, the initial heating, was initiated in between the recorded temperature during initial placement and up to the desired air exposure within the system. Heating interval constrained by 10 ^◦C below the desired exposure temperature, for example 40 ^◦C exposure was initiated at an inside air temperature of 30 ^◦C. Temperature measurements were conducted during the initial step and each specimen observation session, to compare between the previous and current temperature difference.

Further on, the primary heat exposure technique, was carried out twice over the course of two distinct durations when the air temperature reaches the desired target. During a one-hour experiment, the first interval is used, with five minutes between each observation, documen- tation, and recording. The following round of primary experiments lasts for a total of two hours, with a 10-min gap between each data collection.

Fig. 5. Example of substrate and air temperature fluctuation during the main thermal experiment on Pirenella conica specimens. During the exposure session, substrate temperature never crossed into the air temperature, possibly due to the heat capacity of damp substrate and water being used in our experiment.

Simultaneously, early part of heating shows that air temperature was exceeding the targeted temperature, but slowly stabilized as the experiment progressed. Notes for abbreviations: TE =Thermal Exposure, MIN =Minimum/lowest air temperature displayed in the recording, MAX =Maximum/highest air temperature displayed in the recording, S1 =First scenario/full exposure, S2 =Second scenario/partial coverage or exposure, S3 =Third scenario/full coverage.

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In either the first or second batch experiment, a total of 27 data re- cordings, 27 sets of photographs for each petri dish (81 in total), and 27 measurements of substrate temperature for each substrate inside the dishes (81 in total) were made. These measurements were made once for each recording of the three different scenarios, and later the whole experiment was repeated for the replicate trial.

The third step involved allowing the specimens to recover in a new petri dish filled with fresh water once they were taken out of the experimental petri dish. The time required for each specimen to recover or reawaken following the experiment was documented during the recovery observation in order to record how long each specimen remains in a heat coma following the stress exerted on them during the final stage of the experiment.

2.5. Behavioral observation and heat-induced status determination During the experiment, we observed the typical behavior of our specimens during the heat exposure intersession, and recorded their current status. For each image made during each intersession, we compared the snails’ previous positions to their current positions, to ensure that specimens were still alive at the observation and recording time (Fig. 3).

In addition, to estimate at which temperature our specimens entered a comma, whether partially or completely, we recorded all their status changes along with the temperature measurement. We determined the heat comma temperature (HCT) to represent when at least one of our specimens from each scenario became immobile. Furthermore, we also determine at which temperature half of our specimens become inactive or comatose, which is known as the median coma thermal limit (CT50),

as well as upper coma thermal limit (CT100), the temperature at which all specimens become inactive.

2.6. Data visualization

All of the acquired data, i.e., substrate temperature records, number of specimens that show status change, as well as temperature fluctuations during the experiment, were processed using Spyder (Anaconda3).

Data visualization was made using matplotlib.pyplot for line graphs and seaborn for boxplots. Graphs were arranged into one figure using the subplot option from matplotlib.pyplot.

3. Results

3.1. Substrate temperature fluctuations

In three different scenarios, the substrate temperature changes and fluctuates during the experiment (Fig. 6). The third scenario (full coverage) had the lowest temperature recorded, and the same scenario also had the highest: 27.6 ^◦C and 50.9 ^◦C. The temperatures for the other two scenarios are likewise noticeably different: the partial exposure scenario’s temperature range is 32.2 ^◦C to 49.9 ^◦C, whereas the full exposure scenario temperature range is 32 ^◦C to 49.6 ^◦C. Each scenario falls within very similar ranges for the total average temperature values:

40.1, 40.9, and 41.0 ^◦C, respectively. The temperature of the substrate does not surpass or be stable within that restriction (see example in Fig. 4), despite the first (lowest) and fifth (highest) temperature setting of the incubator being set at 40 ^◦C and 60 ^◦C, respectively.

Fig. 6. Substrate temperature ranges and averages for the three scenarios used during the experiment of selected gastropod species, simultaneously from the two duplicate experiments in a single boxplot.

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3.2. Thermal limit results

The mud creeper Pirenella conica exhibits remarkable results for the overall thermal situation. The test specimens begin to show partial immobility (not moving on the sediment or clinging to the tip) and enter a comatose state in the first scenario, in which the specimens are exposed to the air during the experiment, starting at 31.6 ^◦C. As the temperature rises, we observe that at about 37.5 ^◦C, half of the specimens enter a comatose state, and at around 39 ^◦C, all individuals become motionless. Similar results were seen for the second scenario (partial coverage), but at higher temperatures: 39.1 ^◦C, 44.8 ^◦C, and 48 ^◦C, respectively, indicating the first comatose incidence, half the specimens becoming comatose, and the entire population entering the comatose state. Third scenario (full coverage): 45 ^◦C, 47.6 ^◦C, and 48.5 ^◦C shows a higher temperature window for each case when a specific number of test specimens enter a comatose state. Both the first and second scenarios (as shown in Fig. 7) show a rather slow fall in recorded activity as temperature is increased throughout the experiment, however the third scenario exhibits a sudden and dramatic decline in the activity of the test specimens. Each of the abovementioned results are based on the five different temperature exposures in two duplicate trials, and are summarized in Fig. 8.

In comparison with the mud creeper, the tropical periwinkle Planaxis sulcatus, the intertidal snail from Bahrain, exhibits overall results that are markedly different (Fig. 7). This species began to show partial immobility in the first scenario testing at a lower temperature than the mud creeper, at 30.7 ^◦C. The test specimens become increasingly immobile as the temperature rises, with half going into a comatose state

at around 39 ^◦C, and all specimens becoming immobile around 42.1 ^◦C.

In general, this species displays a trend of reduced activity for the other two situations that differ only in the temperature values. In both scenarios, the first specimen entered a comatose state between 37.6 ^◦C and 38.2 ^◦C, followed by the immobilization of half the specimens between 40.1 ^◦C and 40.9 ^◦C, and then the entire test population at 43.2 ^◦C and 44.1 ^◦C, respectively. When comparing the three scenarios for this species, it was found that the first scenario saw a relatively slow drop followed by a quick fall, but the second and third scenarios experienced abrupt declines as temperature increased. Similarly, the results for the Planaxis are also based on five different exposures and two duplicate trials, and are summarized on the boxplot in Fig. 8.

3.3. Post-experiment recovery timing

Regardless of the environment in which they find themselves during recovery, both species show a minor variation (Fig. 9). The mud creeper’s total recovery period varied from 18 s after exposure to 40 ^◦C in the FC scenario, which was the shortest timeframe, to 90 s in the FE scenario before the first specimen started moving again. The tropical periwinkle, on the other hand, exhibits somewhat longer initial specimen recovery time, with the shortest interval being roughly 42 s in the FC scenario and the longest being 102 s in the FE scenario. However, for the fourth heat increment (55 ^◦C), the mud creeper had the shortest recovery time, with the first specimen becoming mobile after 342 s, while the tropical periwinkle took 456 s to recover. Following the last heat treatment (60 ^◦C heat exposure), no specimens of either species showed any signs of recovery.

Fig. 7. Effect of substrate temperature on the observed activity of the mud creeper Pirenella conica (solid lines) and the tropical periwinkle Planaxis sulcatus (dashed lines) during the experiment.

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4. Discussion

Over the past half-century, a number of studies on the temperature tolerance of various mollusks, particularly gastropods, have been un- dertaken worldwide using a variety of analytical methods (Stirling, 1982; Mu˜noz et al., 2005; Williams and Morritt, 1995; Han et al., 2019;

Mardones et al., 2021). Only a few studies have analyzed temperature limits of the Potamididae or mud creeper family of gastropods or the tropical periwinkle (Planaxidae), which has become the focus of our concern (Egonmwa, 2006; Nonyukela et al., 2019; Li and Dong, 2020).

Despite their abundance and widespread distribution across the Indian Ocean, Arabian Gulf, and throughout the entire Mediterranean (based on documented distribution in https://www.marinespecies.org/), no studies have been conducted specifically for our region of interest in the arid and hypersaline environment of the Arabian Gulf. Given the location of our study sites in the Gulf, the only information that society may be aware of is that these creatures are exposed to one of the most stressful environments on Earth, including exposure to extremely high and fluctuating temperatures, physiological stress from high salinity, and human-induced stress from oil spills and other types of pollution (Sheppard et al., 2010; Amao et al., 2019).

In order to understand the thermal limits of the common gastropods in the Gulf in practical circumstances, we devised a straightforward yet applicable experimental approach for determining the thermal limits of Gulf gastropods. We were able to determine thermal limits by considering three possible scenarios and varying the levels of heat exposure, while attempting to reproduce/mimic natural conditions in the laboratory and minimizing additional stress caused by sampling and transport of the specimens to the laboratory. A comparative example of a thermal experiment, but differing in the practical set-up was done by Li and Dong (2020), in which the authors exposed the organisms to a prolonged thermal exposure, but did not consider the different observable ecological preferences of their intertidal specimens. Considering that temperature fluctuations at our locality can vary drastically during the day, such as the recent report bu. Kaminski et al. (2023), our short-term

temperature experiment is more ecologically suitable and reflects the actual observed conditions. Additionally, one major difference from other similar thermal experiments concerns the use of an incubator rather than a thermal bath for conducting the experiment. Future experimental trials will be performed to calibrate our current findings from the incubator with data obtained by the use of a thermal bath.

Our experimental results show that both gastropod species display different thermal tolerances to heat exposure. In a logical sense, and as reported by Kaminski and Garrison (2020), when subjected to a substrate temperature above 40 ^◦C, all of the specimens of both species enter a comatose state and become immobile. In the field, there is a distinct “snail line” on the natural tidal flat during the summer months, and only dead snail shells are found in the upper reaches of the tidal flat where substrate temperature exceeds 40 ^◦C. Our FC and PE scenarios attempt to mimic these natural conditions in the laboratory. However, higher thermal tolerance is observed in the FC scenario, in which specimens are fully immersed in water. In the case of the tropical periwinkle, half of the specimens were able to remain mobile at 42 ^◦C, while the mud creeper tolerated higher temperatures, with half of the specimens becoming immobile at 47.6 ^◦C. Li and Dong (2020) found a similar tendency in their experiment using gastropods from the same family, which showed thermal limits in the range of 46 ^◦C to 48 ^◦C. In an acute lethal temperature experiment on marine gastropods, higher thermal limits were determined by Stirling (1982), focusing on specimens from Hong Kong and Tanzania, which displayed higher values of 56.5 ^◦C.

However, Sterling’s study did not consider substrate temperature as the baseline for thermal exposure, and only heat induced from a water bath was used to determine thermal limits. It is noteworthy that during the summer of 2023, we measured substrate temperatures in excess of 63 ^◦C at our study locality in Half Moon Bay – the highest temperatures ever recorded.

Meanwhile, if increasingly intense high-temperature records reported by local news (Asif, 2023; Abueish, 2023) persist and potentially escalate in the future, an ecological shift is likely to ensue. A study by Wabnitz et al. (2018) that addresses future projections of habitat Fig. 8. Substrate temperatures in comparison to the status change of the mud creeper Pirenella conica (left) and the tropical periwinkle Planaxis sulcatus (right), for all three scenarios and from both duplicate trials.

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suitability in light of the impact of climate change on marine biodiversity, anticipates local species loss and diminished habitat suitability by the year 2100. We argue that this phenomenon may already extend to the intertidal realm based on our observations: the mud creeper lives in both locations, while the tropical periwinkle is exclusive to the Bahrain area. Considering the former species’ greater thermal resilience compared to the latter, ongoing warming trends likely pose a threat to their survival. The tropical periwinkle is at higher risk and may potentially disappear from the Bahrain region first.

Additionally, alongside the thermal stressor outlined in our study, another significant threat imperils the existence of locally established intertidal communities at both locations, with the Bahrain site facing particularly heightened jeopardy. Intensive inland development through coastal reclamation, sediment dredging, and land use changes are steadily diminishing the natural environment in both areas (Zainal et al., 2012; Naser, 2015, 2022). Furthermore, unregulated litter disposal in the proximity of marine and intertidal zones poses another looming threat to the natural inhabitants, specifically within these areas and across the broader scope of the Arabian Gulf (Al-Salem et al., 2020;

St¨ofen-O et al., 2022). The authors have diligently monitored both issues during extensive long-term observations in the region (Fig. 10), although they do not constitute the primary focus of this study. Ulti- mately, without future developments aimed at mitigating the impact of both natural and anthropogenic stressors on local intertidal inhabitants, their demise appears inevitable, irrespective of the primary cause behind their local disappearance.

5. Conclusions

We conclude that the shallow-water gastropods found on mudflats in Saudi Arabia and Bahrain are experiencing stress from elevated temperatures during summer, when the laboratory-determined coma temperature for exposed specimens may be exceeded by as much as 15 to 20 degrees. By using two species of intertidal gastropods from the selected localities and different exposure scenario to mimic their ecological preferences, we found that the mud creeper that occurs in both locations has a higher thermal tolerance from all scenarios in comparison to the tropical periwinkle that only occurs in Bahrain. Our laboratory experiment also reveals the coma stance or immobility of both specimens during and after the experimental session, where the recovery period increases as higher thermal exposure is subjected to the gastropod specimens. This finding that shallow-marine to intertidal biocalcifying organisms are experiencing thermal stress is in line with predictions of climate models, which concluded that portions of the Arabian Gulf will become too hot to sustain eukaryotic and macrofaunal life in the next decades. Our laboratory and field observations confirm that this is already the case for the intertidal gastropods that are found in tidal pools and mudflats.

Credit authorship contribution statement

Sinatrya D. Prayudi: Conceptualization, Methodology, Formal analysis, Writing – original draft, Sample collection. Asmaa Korin:

Laboratory Investigation, Michael A. Kaminski: Supervisor, Fig. 9. Recovery times for heat-exposed Pirenella conica and Planaxis sulcatus specimens in the three scenarios based on average results of both main and control experiments.

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Conceptualization, Sample collection, Writing – original draft, review &

editing.

CRediT authorship contribution statement

Sinatrya D. Prayudi: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Visualiza- tion, Writing – original draft, Writing – review & editing. Asmaa Korin:

Conceptualization, Data curation, Methodology. Michael A. Kaminski:

Conceptualization, Funding acquisition, Methodology, Project admin- istration, Resources, Supervision, Writing – original draft, Writing – review & editing.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. In accordance to the animal experimentation attempt, local ethical and moral requirements for the research purposes; although in the current author’s affiliation (KFUPM) not declared in more specific details, we tried to satisfy the required condition that being stated by National Committee of BioEthics:

Implementing Regulations of the Law of Ethics of Research on Living Creatures released in 2022, specifically in Chapter Twelve: Use of Ani- mals & Plants in Experiments. Despite the actual concern for the animal experimentation being outlined in the abovementioned documents are mostly for livestock and pets, but we made every effort to comply with the majority of listed requirement (Article 38).

Data availability

Data will be made available on request.

Acknowledgements

We are grateful to the Deanship of Scientific Research, KFUPM, for funding the study through grant DF191042. We also acknowledge laboratory support from the College of Petroleum & Geosciences at KFUPM.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.

org/10.1016/j.seares.2024.102470.

Fig. 10. Composite photographs illustrating the primary environmental concerns contributing to the alteration of intertidal communities in our study area are as follows: A) Murray’s pool depicted in its pristine state, albeit with scattered litter observed in the high tide zone (photograph captured on August 23rd, 2019), B) a recent depiction of Murray’s pool showcasing changes due to land use alteration into a mangrove growing area and heightened litter dumping (photographed on September 9th, 2023), C) an altered intertidal area at Zabnah beach displaying litter, (photographed on October 8th, 2021), and D) occurrences of deceased fish and living gastropods coexisting with litter in the mud creeper habitat at Zabnah beach (photograph taken on May 16th, 2022).

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