Combating mass extinctions: Discovering new Pinna nobilis populations in the Sea of Marmara

doi:10.21203/rs.3.rs-3328896/v1

Download PDF

Research Article

Combating mass extinctions: Discovering new Pinna nobilis populations in the Sea of Marmara

https://doi.org/10.21203/rs.3.rs-3328896/v1

This work is licensed under a CC BY 4.0 License

Journal Publication

published 08 Mar, 2024

Read the published version in Marine Biology →

You are reading this latest preprint version

Pinna nobilis is one of the largest bivalve species in the Mediterranean Sea. The situation of the species is critical as it faces widespread mass extinctions in various parts of the Mediterranean Sea. The Sea of Marmara offers a unique environment for fan mussel populations, with some areas hosting alive communities. This study aims to discover new populations of P. nobilis in the Sea of Marmara that are known to be not affected by mass extinctions. An area of 28,200 m² at 47 stations along the 105 km coastline in the southern part of the Sea of Marmara was scanned by underwater visual counting method. A total of 544 alive fan mussels were recorded during the underwater surveys, ranging in shell height from 11.8 to 31.4 cm. The mean density was estimated as 5.3 ind·100 m^− 2, and recorded very high densities which reached 18.8 ind·100 m^− 2 among the stations. The hotspots of the population were distributed from the shoreline to a 10 m depth range and 100 m distance from the shoreline in sandy and seagrass meadow habitats. The presence of juveniles provided evidence of successful recruitment and settlement. The distribution pattern and recorded mortalities were attributed to hydrodynamic factors and intense human activities. This study provides key insights into the mechanisms of resilience and survival among fan mussels' mass death events and offers valuable guidance for potential conservation strategies in other affected regions.

Population density

Demographic structure

Spatial distribution

Fan mussel

Critically endangered species

Sea of Marmara

Pinna nobilis, commonly known as the fan mussel, belongs to the family Pinnidae and is one of the largest bivalve species in the Mediterranean Sea (Vicente 1990). This species native to the Mediterranean Sea has a wide distribution from Spain to the Sea of Marmara (Butler et al. 1993; Vázquez-Luis et al. 2017). With a slow growth rate, individuals can reach an impressive shell height of 120 cm and live up to 50 years (Zavodnik et al. 1991; Rouanet et al. 2015). Fan mussels exhibit a diverse distribution, thriving in various habitats such as sandy, gravelly, and rocky environments, as well as in rhodolith beds (Katsanevakis 2006; Kersting and García-March 2017; Karadurmuş & Sarı 2022a), where they often coexist with oxygen-rich seagrass meadows (Basso et al. 2015). Abundant along the coastal zone, fan mussels are found at depths of up to 60 meters (Kersting and García-March 2017). They prefer areas with good environmental factors and gentle currents (Vázquez-Luis et al. 2017). An essential ecological role of the fan mussel is its filtering capacity, with each individual capable of processing approximately six liters of seawater per hour (Vafidis et al. 2014), effectively removing suspended particles and contributing to the clarification of the surrounding environment (Basso et al. 2015). Additionally, the fan mussel provides an attachment surface for sessile organisms, promoting biodiversity (Rabaoui et al. 2009). The diet of P. nobilis mainly consists of detritus, phytoplankton, zooplankton, and pollen dust (Davenport et al. 2011; Alomar et al. 2015).

A destructive and geographically widespread mass death event in the Mediterranean basin has affected P. nobilis populations since 2016 (Basso et al. 2015; Vázquez-Luis et al. 2017). Mortality events began with the virus-like protozoan pathogen Haplosporidium pinnae (Catanese et al. 2018), and subsequent studies have also reported that it influences mortality in bacteria such as Mycobacterium sp. or Vibrio sp (Catanese et al. 2018; Künili et al. 2021). The infection-associated deaths rapidly spread from west to east, starting in Spain and reaching the eastern Mediterranean Sea within a span of fewer than three years (Vázquez-Luis et al. 2017; Katsanevakis et al. 2019). As far as current knowledge goes, the infection extent has reached the Dardanelles Strait (Künili et al. 2021), representing a significant geographic spread. Mortality rates have reached 80–100% across the Mediterranean in most places, including Dardanelles Strait (Kersting et al. 2019; Katsanevakis et al. 2021; Scarpa et al. 2021). Several projects (LIFE PINNA, LIFE PINNARCA) are underway to monitor, conserve, restore existing fan mussel populations in these regions and to breed captives for restocking with disease-resistant individuals. While some populations in the Mediterranean Sea have managed to remain pathogen-free, they are situated in geographically isolated and environmentally specific regions (Cabanellas-Reboredo et al. 2019; Katsanevakis et al. 2021). Local-scale threats such as habitat loss, tourism, anchoring, illegal fishing, and coastal constructions primarily contribute to deaths in certain areas (Basso et al. 2015; Öndeş et al. 2020a; Karadurmuş and Sarı 2022a). However, climate change is widely attributed to the spread of pathogens and the ensuing mass mortality events. The World Union for Conservation of Nature (IUCN) has categorized the species as Critically Endangered due to the severe mass mortality and significant reduction in stock sizes. As recommended by the IUCN, high-density regions are protected, and containment measures include any impact that could cause incidental deaths (Kersting et al. 2019). Due to the high risk of extinction and the sharp decline in its global population, critical populations are drastically protected within existing marine protected areas as well as various international and national directives (Kersting et al. 2019). Turkey first provided protection to this species in 1997, and it remains on the list of forbidden species in the country (Karadurmuş and Sarı 2022a).

In contrast to the reported mass mortalities reaching up to 100% in various regions of the Mediterranean Sea, the Sea of Marmara stands out as a unique haven, still hosting thriving and high-density P. nobilis populations (Öndeş et al. 2020a; Çınar et al. 2021a, b; Acarlı et al. 2022; Karadurmuş and Sarı 2022a). This study aims to discover new fan mussel populations that are not affected by widespread mass extinctions in the Sea of Marmara and to examine their ecological aspects with a holistic approach (spatial and bathymetric distribution, abundance, mortality, population status). This study sheds light on the factors contributing to their resilience and survival of P. nobilis in the face of mass mortality events, providing valuable insights into potential conservation strategies for other affected areas.

The study area covers Bandırma Bay and a large part of Kapıdağ Peninsula located in the south of the Sea of Marmara. In the study area, diving based on underwater observation was made at randomly determined stations at every 5 km intervals along the 105 km coastline (Fig. 1). Additional stations were defined in areas that are considered ecologically important and where critical density changes are in question. Underwater visual census includes techniques based on the assessment of habitat uses of target species and the determination of the abundance of target species within the transect area (Colvocoresses and Acosta 2007; Caldwell et al. 2016). These methods allow one to make predictions about densities per unit area. Fan mussels were counted using the strip transect method in this study. This method gives more precise results since the boundaries are determined with precise strips and is frequently used in the estimation of fan mussel studies (García-March et al. 2002; Vafidis et al. 2014; Tsatiris et al. 2018; Karadurmuş and Sarı 2022a). Lead rope with a diameter of three mm and a length of 150 m, marked at intervals of five meters, was used as the transect material. The line was laid bottom vertically to the shore, starting from the shoreline. Two divers on either side of the strip used a two meters wide lead made of plastic pipe with a center mark in their hands. The divers counted along the remaining strip in the transect area. In this way, two divers at each station scanned an area of 600 m² (150 m × 4 m) in total. Divers recorded the number of individuals, living status, depth, distance from shore, and the relative habitat type between the two marks by means of an underwater board for each segment.

During the census, the divers analyzed the living status of the individuals and recorded the alive and dead mussels counted in each subsection. The alive/dead distinction is easy: alive mussels respond by quickly closing their shell on approach or touch, while dead mussels contain no tissue and are unresponsive, their shells open and not closing. In addition, buried mussels with cracked or broken shells were defined as dead. Individuals completely plucked from benthic were not included in the count as they may have been carried indiscriminately by the flows. Recordings were taken throughout the entire field, including areas absent of fan mussels. The habitat type in each segment was classified and recorded as sandy, seagrass meadow, gravelly, rocky, shellfish, and muddy (IUCN 2023). Biometric measurements were made with a long-jaw multi-caliper and depth caliper with 0.1 cm division in randomly selected individuals along the transect. Measurements were made by taking the maximum width (W), minimum width (w), and maximum length (UL) measured from the unburied part of the shell. Based on these measurements; maximum shell length (Ht) was estimated (García-March et al. 2002). The Ht was calculated using the equation Ht = UL + h, and the regression (h) 1.79w + 0.5 was used for the buried shell length.

The mean fan mussel density at the stations was estimated as the individual number in per hundred square meters (ind·100 m^− 2). Density status were classified as low (< 5 ind·100 m^− 2), medium (5–10 ind·100 m^− 2), high (10–15 ind·100 m^− 2) and very high (> 15 ind·100 m^− 2) (Rabaoui et al. 2008; Karadurmuş and Sarı 2022a). All analyzes were performed separately for alive and dead individuals. The mortality rate (%) was calculated from the ratio of the number of dead individuals to the total number of individuals at each station. All density data were correlated with depth, distance from shore and habitat type in the surveyed segment. Individuals with a shell length less than 20 cm were defined as juveniles, and those larger than 20 cm as adults (Šiletić and Peharda 2003).

The data sets to be used in the study were examined in terms of suitability before the analysis. The assumptions of normality of variables and homogeneity of variances were evaluated with the Shapiro-Wilk test (Shapiro and Wilk 1965) and Levene's test (Levene 1960). In the comparison of the quantitative data between two independent groups, parametric tests were used if the assumptions were significant, and non-parametric tests were used if the assumptions were not significant. The significance level for the test statistics of the hypotheses in both the assumption controls and parameter estimations was determined as α = 0.05 (Sokal and Rohlf 1969). Descriptive statistics (mean, standard error, quartiles, percentiles) were obtained according to the distribution structure for all data obtained. Data analysis and modeling was performed with SPSS v0.26.

A total area of 28,200 m² was scanned across 47 stations, revealing the presence of fan mussel individuals in only 17 of these stations. In total, 789 individuals were recorded, providing valuable insights into the distribution and abundance of fan mussels within the scanned area. Among the recorded individuals, 544 (68.9%) were found to be alive, while 245 (31.1%) were observed in dead state. The mean alive individual density, reaching 18.8 ind·100 m^-2, was calculated as 5.3 ind·100 m^-2 across the entire study area. Notably, five stations (S37, S44, S45, S46, and S47) exhibited above-average population densities, indicating localized aggregations of fan mussels. The total area covered by patches with fan mussels accounted for only 11.3% of the scanned area. At two specific stations (S37 and S45), very high-density clustering of fan mussels was recorded, while most of the remaining stations were classified as having low densities. Stations (S9, S12, S14, and S16) located in the eastern portion of the study area were represented by a very limited number of individuals (one or two individuals in each station).

Table 1. Details on the location of scanned stations and the status of Pinna nobilis populations in the study area

Station	Coordinate		Count (n)		Density (ind·100 m^-2)		Density status^*	Mortality rate (%)
Station	Latitude	Longitude	Alive	Dead	Alive	Dead	Density status^*	Mortality rate (%)
S1	40.38686	28.12038	0	0	–	–	n/a	–
S2	40.37582	28.05474	0	0	–	–	n/a	–
S3	40.37425	28.05044	0	0	–	–	n/a	–
S4	40.36149	27.98236	0	0	–	–	n/a	–
S5	40.35705	27.96824	0	0	–	–	n/a	–
S6	40.36185	27.93083	0	0	–	–	n/a	–
S7	40.37523	27.91672	0	0	–	–	n/a	–
S8	40.38542	27.89952	0	0	–	–	n/a	–
S9	40.39847	27.90824	2	0	0.3	–	low	0
S10	40.40741	27.92021	0	0	–	–	n/a	–
S11	40.40865	27.92348	0	0	–	–	n/a	–
S12	40.41181	27.93150	1	2	0.2	0.3	low	66.7
S13	40.42306	27.95409	0	0	–	–	n/a	–
S14	40.42433	27.96836	2	1	0.3	0.2	low	33.3
S15	40.43972	27.99798	9	1	1.5	0.2	low	10.0
S16	40.45417	28.02427	2	1	0.3	0.2	low	33.3
S17	40.45926	28.02315	0	0	–	–	n/a	–
S18	40.46991	28.02912	15	4	2.5	0.7	low	21.1
S19	40.47558	28.03070	0	0	–	–	n/a	–
S20	40.47920	28.02766	0	0	–	–	n/a	–
S21	40.48652	28.01089	0	0	–	–	n/a	–
S22	40.48691	27.99423	0	0	–	–	n/a	–
S23	40.48864	27.99000	0	0	–	–	n/a	–
S24	40.49167	27.97581	0	0	–	–	n/a	–
S25	40.49251	27.96547	0	0	–	–	n/a	–
S26	40.49494	27.96095	0	0	–	–	n/a	–
S27	40.49693	27.95068	0	0	–	–	n/a	–
S28	40.50659	27.90369	0	0	–	–	n/a	–
S29	40.50707	27.90100	0	0	–	–	n/a	–
S30	40.51256	27.87456	0	0	–	–	n/a	–
S31	40.51352	27.85627	0	0	–	–	n/a	–
S32	40.51023	27.83493	0	0	–	–	n/a	–
S33	40.51337	27.80522	0	0	–	–	n/a	–
S34	40.51822	27.80386	0	0	–	–	n/a	–
S35	40.52132	27.80237	0	0	–	–	n/a	–
S36	40.51508	27.79872	0	0	–	–	n/a	–
S37	40.50661	27.78614	91	7	15.2	1.2	very high	7.1
S38	40.51731	27.74518	12	5	2.0	0.8	low	29.4
S39	40.52064	27.73406	32	19	5.3	3.2	average	37.3
S40	40.51941	27.72579	22	14	3.7	2.3	low	38.9
S41	40.51739	27.71219	20	13	3.3	2.2	low	39.4
S42	40.51704	27.70776	13	9	2.2	1.5	low	40.9
S43	40.50965	27.69865	15	7	2.5	1.2	low	31.8
S44	40.50093	27.68458	56	50	9.3	8.3	average	47.2
S45	40.49071	27.68719	113	92	18.8	15.3	very high	44.9
S46	40.45622	28.07348	52	8	8.7	1.3	average	13.3
S47	40.45225	28.08595	87	12	14.5	2.0	high	12.1

^* n/a: none, low: <5 ind·100 m^-2, average: 5-10 ind·100 m^-2, high: 10-15 ind·100 m^-2, very high: ≥15 ind·100 m^-2. Note: A total area of 600 m² was scanned at each station

This study revealed distinct patterns of spatial distribution and habitat preferences for P. nobilis. Distribution patterns indicate that the fan mussel can be found in various habitats along the scanned area, encompassing both shallow and deeper waters (up to 30.1 meters). Hot spot areas were observed at high densities with 6.1 and 8.3 ind·100 m^-2 in the 0-5 m and 5-10 m depth range. Dense clustering was recorded in alive populations reaching 9.9 ind·100 m^-2 at a distance range of 50-100 m from the shore. The highest density of individuals, reaching up to 13.6 ind·100 m^-2, was observed in sandy habitats. Seagrass meadows were found to be the second most preferred habitat for P. nobilis, with an average density of 7.3 ind·100 m^-2. The density of fan mussel was generally low in rocky, gravelly and shellfish habitats in this study. In contrast, P. nobilis was completely absent in muddy areas.

Table 2. Pinna nobilis densities (ind·100 m^-2) in different depth, distance from shore and habitats

Variables		Count (n)		Density (ind·100 m^-2)
Variables		Alive	Dead	Alive	Dead
Depth range (m)	0-5	246	98	6.1	2.4
	5-10	212	96	8.3	3.8
	10-15	64	26	3.3	1.3
	15-20	12	20	1.2	1.9
	20-25	8	2	2.5	0.6
	25-30	1	1	0.7	0.7
	30-35	1	2	1.0	2.0
	35-40	0	0	0	0
Distance from shore (m)	0-25	25	43	1.8	3.2
	25-50	105	46	6.2	2.7
	50-75	169	67	9.9	3.9
	75-100	128	34	7.5	2.0
	100-125	89	27	5.2	1.6
	125-150	26	26	1.5	1.5
	150-175	2	2	0.6	0.6
Habitat type	Sandy	144	120	13.6	11.3
	Seagrass	364	92	7.3	1.8
	Gravelly	15	12	1.5	1.2
	Rocky	13	16	1.6	2.0
	Shellfish	8	5	0.4	0.3
	Muddy	0	0	0	0
Total		544	245	5.3	2.4

The mean H_t was estimated as 20.1 ± 0.35 cm (11.8-31.4 cm) in alive and 23.2 ± 0.42 cm (11.8-32.5 cm) in dead individuals (Fig. 2). The ratio of juveniles to adults in the alive population was found to be evenly distributed (Fig. 3), with both comprising 50% of the population. A statistically significant difference in mean H_t was observed between alive and dead individuals (t₍₃₅₇₎ = -5.737, p < 0.05). Mortality rates were recorded as 25.9% and 50.9% in juvenile and adult individuals, respectively.

Despite the widespread mortality events in the Mediterranean Sea, the Sea of Marmara continues to host alive populations. Studies encompassing diverse regions, with a particular emphasis on the southern area of the Sea of Marmara, revealed notable population densities: 27.0 ind·100 m^− 2 in Acarlı et al. (2022), 71.2 ind·100 m^− 2 in Karadurmuş and Sarı (2022a), 112 ind·100 m^− 2 in Acarlı et al. (2021a), ind·100 m^− 2 in Çınar et al. (2021a), and 240 ind·100 m^− 2 in Çınar et al. (2021b), 25.2 and ind·100 m^− 2 in Öndeş et al. (2020b). The patchy distribution pattern of the fan mussel in the study area implies localized concentrations rather than a homogenous distribution across the study area. The salinity difference between the Mediterranean Sea and the Black Sea causes water column stratification in the Dardanelles and Istanbul straits and the Sea of Marmara. This stratification shapes the current system, with fresh Black Sea waters flowing on the surface towards the Sea of Marmara and the Aegean Sea, while more saline Mediterranean waters current towards the Black Sea at the bottom. Additionally, meteorological factors like rainfall, wind speed, and direction can influence the currents, potentially causing local deviations in the main current systems in the Sea of Marmara (Beşiktepe et al. 1994; Meriç et al. 2018). The water current characteristic of the northern shores of the peninsula (from S18 to S36) and the eastern side of the bay (from S1 to S3) are clearly different from the other stations in the study area. This area is greatly affected by bottom currents from the Mediterranean and surface currents from the Black Sea (Fig. 1). So, the deprivation of populations at these stations can be associated with strong water currents. Because high currents in certain areas may create turbulent conditions and strong water flows that make it challenging for the mussels to maintain their attachment to the substrate. Hydrodynamic processes, including coastal currents, upwelling, and eddies, play a crucial role in the long-distance dispersal and connectivity between different populations of fan mussels (Kersting and García-March 2017). These currents may also facilitate or prevent the dispersal and settlement of larvae, thereby affecting the distribution of the species. Various researchers (Hendriks et al. 2011; Prado et al. 2021) have reported that fan mussel populations are vulnerable to severe weather events. As a defense mechanism, the mussels tend to avoid such areas and seek refuge in more sheltered habitats (Hendriks et al. 2011). The absence of individuals in areas with high currents is likely a result of the combined factors mentioned above.

The interior of Bandırma Bay is subjected to significant coastal uses and multiple industrial activities. The Bay is home to two heavy industry facilities, an international multi-purpose port with large berths, and a fishing port. The bay is also exposed to domestic pollution of the highly populated district through the deep discharge system (Özen et al. 2023). Heavy industry activities can introduce pollutants such as chemicals, heavy metals, and toxins into the water, which can have detrimental effects on the fan mussels' health and survival. Additionally, domestic pollution can lead to eutrophication, oxygen depletion, and the accumulation of pollutants in the water, making it unsuitable for the fan mussels (Basso et al. 2015). In addition, secondary bottom current and local surface current, which have a cyclical effect in the inner parts of the bay, prevent the pollution from leaving the bay and contribute to the continuity of the pollution pressure (Fig. 1). The bay also hosts the high-speed ferry route and busy anchorage area. Marine operations often involve negative impacts, which generate significant disturbances in the water and along the seabed (Öndeş et al. 2020a). The absence of fan mussels at stations in this region (from S4 to S8) is thought to be a result of the above-mentioned multi-faceted intense activities. The absence or limited number of fan mussels at stations in the bay is thought to be a result of the multi-faceted intense activities mentioned above.

The western portion of the study area, spanning from S37 to S45, along with Fener Island (S46) and Hali Ada (S47) on the eastern side, both of which are isolated from the peninsula, exhibited fan mussel populations characterized by exceptionally high densities. Contrary to Acarlı et al. (2022) new discoveries of one or two individuals were obtained at the stations scanned in the area between S9 and S18 in Bandırma Bay. Previous research (Acarlı et al. 2022; Karadurmuş and Sarı 2022a) has also documented the presence of thriving populations in Erdek Bay, situated to the west of the peninsula, which further corroborates the region's ability to support survival and settlement populations of live fan mussels. These areas boast more stable environmental conditions and exhibit lower water velocities, factors that are conducive to the successful survival and settlement of fan mussels. Notably, these regions remain entirely free from anthropogenic influences, preserving a sheltered and protected environment that further supports the proliferation of fan mussels. Understanding the complex relationships between environmental features and the distribution of fan mussels is crucial for effective conservation and management strategies. Further research in the study area should focus on understanding the multiple factors (environmental, physical, chemical, hydrodynamic, anthropogenic) that drive distribution patterns and explore additional potential areas that may contribute to the conservation of this species.

The distribution pattern of populations in the study area was mainly connected to depth and habitat type. Individuals were dense, mainly with the shallow zone between the shoreline and 10 m, and their density gradually decreased with depth. Similarly, areas of sandy bottom and seagrass meadow were also represented by a significant density of alive mussels. Normally, seagrass areas are the primary habitat for fan mussel (Vázquez-Luis et al. 2014; Karadurmuş and Sarı 2022a). However, light transmittance decreases due to the high suspended solid load in the Sea of Marmara, and therefore, seagrass meadows can spread up to a maximum depth of 6–7 m (Cirik et al. 2006). Therefore, sandy habitats are the primary habitat for P. nobilis in the study area. Such depth (Šiletić and Peharda 2003; Garcia-March et al. 2007a; Karadurmuş and Sarı 2022a) and habitat (Katsanevakis and Thessalou-Legaki 2009; Hendriks et al. 2011; Deudero et al. 2015; Acarlı et al. 2022; Karadurmuş and Sarı 2022a) related diversities have an important impact on fan mussels’ survival and recruitment. Key environmental factors such as hydrodynamics, light intensity, temperature, and productivity in shallow waters strongly support the existence of the species (Prado et al. 2014; Russo 2017; Tsatiris et al. 2018). Results indicating that sandy grounds and seagrass beds are the primary habitats where the species thrives. Sandy bottoms provide the most convenient environment for the implantation of byssus filaments (García-March et al., 2007b), while seagrass meadows ensure shelter against hydrodynamic factors (García-March and Kersting, 2006; Hendriks et al., 2011). These habitats offer protection, food resources, and suitable substrate for attachment, making them important habitats for the species (Vázquez-Luis et al., 2014). Muddy substrates seem to be unsuitable for attachment and may not provide the necessary conditions for the survival and growth of the species (Katsanevakis, 2006; Tsatiris et al., 2018).

Most of the current P. nobilis population was characterized by a predominance of juveniles across all areas studied. This situation often suggests a stable population, as it implies successful recruitment and reproduction. On the other hand, the recorded mortalities are alarming, and as stated in previous studies (Öndeş et al., 2020b; Çınar et al., 2021a, Acarlı et al., 2021a, Çınar et al., 2021b, Acarlı et al., 2022, Karadurmuş and Sarı, 2022a), mortalities in P. nobilis have been recorded in the Sea of Marmara due to multiple factors such as fisheries, anchoring, tourism and diving activities. Although it is well known that environmental factors and human effects cause mortalities, pathogens, parasites, or other disease-causing agents may also have affected the fan mussel populations in the study area (Vázquez-Luis et al., 2017; Katsanevakis et al., 2019; Grau et al., 2022). Individuals in the large size group were more affected by deaths (Fig. 3). Given their superior response to pathogens (Šarić et al., 2020), juveniles exhibit a notably high survival rate in an area (Acarlı et al., 2011). However, the presence of pathogens that cause mass deaths in the Mediterranean is not yet known in the study area. As far as we know best, the last spread of the disease is limited to the Dardanelles Strait (Künili et al., 2021). In the most recent occurrence, a significant marine mucilage outbreak took place in the Sea of Marmara, spanning from November 2020 to August 2021. Consequently, numerous benthic species within marine communities experienced extensive mass extinctions (Karadurmuş and Sarı, 2022b; Karakulak et al., 2023). This phenomenon proved fatal to pelagic fish and crustaceans, with individuals being severely affected by suffocation due to the presence of mucilage or anoxia (Karadurmuş and Sarı, 2022b). This devastating event may cover the benthic habitats where bivalves like P. nobilis reside, potentially smothering them and reducing their access to food and oxygen. The phenomena can alter the availability and distribution of planktonic food sources for bivalves, which might affect their feeding and distribution patterns. Acarlı et al. (2021b) claimed that the mucilage event in the Sea of Marmara may have a negative impact on fan mussel populations either directly or through habitat loss (especially seagrass meadows). There is no conclusive evidence that mucilage is responsible for fan mussel deaths, although various potential effects have been predicted.

This study demonstrates the discovery of new P. nobilis populations in addition to previous studies in the south of the Sea of Marmara. Findings present a unique opportunity to investigate the factors contributing to the resilience and survival of P. nobilis in the face of widespread extinction events. Despite the concerning situation observed in many areas, the Sea of Marmara continues to serve as a vital refuge for fan mussel populations, with certain regions supporting thriving and high-density communities. The presence of juveniles indicates successful recruitment and settlement, but the higher mortality rates among adults raise significant concerns. The lessons learned from the survival of these populations could provide valuable insights to guide conservation strategies aimed at rejuvenating the species in its former Mediterranean Sea habitats. To ensure the conservation and survival of P. nobilis, continued monitoring and in-depth studies on the species are imperative, including investigations into potential threats from pathogens and anthropogenic activities. While this study sheds light on the southern part of the Sea of Marmara, it is crucial to conduct additional research covering the entire of the Sea of Marmara to gain a comprehensive understanding of fan mussel populations in the region. Furthermore, immediate investigation into the presence of infections causing deaths is strongly recommended to address potential threats to the species' survival. By undertaking such efforts, we can enhance our ability to safeguard this ecologically significant species and contribute to the preservation of biodiversity in the Mediterranean Sea.

Funding

This work was supported by Sustainable Benefit Program funded by Borusan Holding and Impact Hub Istanbul.

Competing Interests

The authors have no relevant financial or non-financial interests to disclose.

Author Contributions

U.K.: Conceptualization, Methodology, Formal analysis, Investigation, Writing - Original Draft, Visualization, Project administration. M.S.: Conceptualization, Methodology, Investigation, Writing - Review & Editing, Project administration, Funding acquisition. All authors read and approved the final manuscript.

Acknowledgement

The authors would like to thank first-class divers Tacan Benli, Rafet Bıçaklı, Gökhan Erdoğan and Samet Avcı who voluntarily accompanied the dives throughout the fieldwork.

Data Availability

Data will be made available on request.

Acarlı S, Lök A, Yiğitkurt S, Palaz M (2011) Culture of fan mussel (Pinna nobilis, Linnaeus 1758) in relation to size on suspended culture system in Izmir Bay, Aegean Sea, Turkey. Journal of the Faculty of Veterinary Medicine, Kafkas University 17:995-1002.
Acarlı S, Acarlı D, Kale S (2021a) Current status of critically endangered fan mussel Pinna nobilis (Linnaeus 1758) population in Çanakkale Strait, Turkey. Mar Sci Tech Bull 10:62-70. https://doi.org/110.33714/masteb.793885
Acarlı S, Acarlı D, Kale S (2021b) The effects of mucilage event on the population of critically endangered Pinna nobilis (Linnaeus 1758) in Ocaklar Bay (Marmara Sea, Turkey). Acta Nat Sci 2:148-158. https://doi.org/10.29329/actanatsci.2021.350.09
Acarlı D, Acarlı S, Kale S (2022) The struggle for life: Pinna nobilis in the Marmara Sea (Turkey). Thalassas 38:1199-1212. https://doi.org/10.1007/s41208-022-00470-0
Alomar C, Vázquez-Luis M, Magraner K, Lozano L, Deudero S (2015) Evaluating stable isotopic signals at bivalve Pinna nobilis under different human pressures. J Exp Mar Biol Ecol 467:77-86. https://doi.org/10.1016/j.jembe.2015.03.006
Basso L, Vázquez-Luis M, García-March JR, Deudero S, Alvarez E et al (2015) The pen shell, Pinna nobilis: A review of population status and recommended research priorities in the Mediterranean Sea. Adv Mar Biol 71:109-160. https://doi.org/10.1016/bs.amb.2015.06.002
Beşiktepe ŞT, Sur HI, Özsoy E, Latif MA, Oğuz T et al (1994) The circulation and hydrography of the Marmara Sea. Prog Oceanogr 34:285-334. https://doi.org/10.1016/0079-6611(94)90018-3
Butler A, Vicente N, Gaulejac B (1993) Ecology of the pterioid bivalves Pinna bicolor Gmelin and Pinna nobilis L. Mar Life 3:37-45.
Cabanellas-Reboredo M, Vázquez-Luis M, Mourre B, Álvarez E, Deudero S et al (2019) Tracking the mass mortality outbreak of pen shell Pinna nobilis populations: a collaborative effort of scientists and citizens. Sci Rep 9:13355. https://doi.org/10.1038/s41598-019-49808-4
Caldwell ZR, Zgliczynski BJ, Williams GJ, Sandin SA (2016) Reef fish survey techniques: assessing the potential for standardizing methodologies. PLoS ONE 11:e0153066. https://doi.org/10.1371/journal.pone.0153066
Catanese G, Grau A, Valencia JM, García-March JR, Vázquez-Luis M et al (2018) Haplosporidium pinnae sp. nov., a haplosporidian parasite associated with mass mortalities of the fan mussel, Pinna nobilis in the Western Mediterranean Sea. J Invertebr Pathol 157:9-24. https://doi.org/10.1016/j.jip.2018.07.006
Cirik Ş, Akçalı B, Özalp HB (2006) Determination of Posidonia oceanica borders at Dardanelle Strait and Marmara Sea by using marking method. EU J Fish Aquat Sci 23:45-48.
Colvocoresses J, Acosta A (2007) A large-scale field comparison of strip transect and stationary point count methods for conducting length-based underwater visual surveys of reef fish populations. Fish Res 85:130-141. https://doi.org/10.1016/j.fishres.2007.01.012
Çınar M, Bilecenoğlu M, Yokeş M, Güçlüsoy H (2021a) Pinna nobilis in the south Marmara Islands (Sea of Marmara); it still remains uninfected by the epidemic and acts as egg laying substratum for an alien invader. Medit Mar Sci 22:161-168. https://doi.org/10.12681/mms.25289
Çınar M, Bilecenoğlu M, Yokeş M, Güçlüsoy H (2021b) The last fortress fell: mass mortality of Pinna nobilis in the Sea of Marmara. Medit Mar Sci 22:669-676. https://doi.org/10.12681/mms.27137
Davenport J, Ezgeta-Balic D, Peharda M, Skejic S, Nincevic-Gladan Z et al (2011) Size-differential feeding in Pinna nobilis L. (Mollusca: Bivalvia): exploitation of detritus, phytoplankton and zooplankton. Estuar Coast Shelf Sci 92:246-254. https://doi.org/10.1016/j.ecss.2010.12.033
Deudero S, Vázquez-Luis M, Álvarez E (2015) Human stressors are driving coastal benthic long-lived sessile fan mussel Pinna nobilis population structure more than environmental stressors. PLoS ONE 10:e0134530. https://doi.org/10.1371/journal.pone.0134530
García-March JR, García-Carrascosa AM, Luís Peña Á (2002) In situ measurement of Pinna nobilis shells for age and growth studies: a new device. Mar Ecol 23:207-217. https://doi.org/10.1046/j.1439-0485.2002.02781.x
García-March JR, Kersting DK (2006) Preliminary data on the distribution and density of Pinna nobilis and Pinna rudis in the Columbretes Islands Marine Reserve (Western Mediterranean, Spain). Org Divers Evol 6:6-16.
García-March JR, García-Carrascosa AM, Peña Cantero AL, Wang YG (2007a) Population structure, mortality and growth of Pinna nobilis Linnaeus, 1758 (Mollusca, Bivalvia) at different depths in Moraira bay (Alicante, Western Mediterranean). Mar Biol 150:861-871. https://doi.org/10.1007/s00227-006-0386-1
García-March JR, Pérez-Rojas L, García-Carrascosa AM (2007b) Influence of hydrodynamic forces on population structure of Pinna nobilis L., 1758 (Mollusca: Bivalvia): the critical combination of drag force, water depth, shell size and orientation. J Exp Mar Biol Ecol 342:202-212. https://doi.org/10.1016/j.jembe.2006.09.007
Grau A, Villalba A, Navas JI, Hansjosten Z, Valencia JM et al (2022) Wide-geographic and long-term analysis of the role of pathogens in the decline of Pinna nobilis to critically endangered species. Front Mar Sci 9:666640. https://doi.org/10.3389/fmars.2022.666640
Hendriks IE, Cabanellas-Reboredo M, Bouma TJ, Deudero S, Duarte CM (2011) Seagrass meadows modify drag forces on the shell of the fan mussel Pinna nobilis. Estuaries Coasts 34:60-67. https://doi.org/10.1007/s12237-010-9309-y
IUCN (2023) International Union for Conservation of Nature: Habitats Classification Scheme (Version 3.1). https://www.iucnredlist.org/resources/habitat-classification-scheme (Accessed 20 August 2023).
Karadurmuş U, Sarı M (2022a) The last hope: the struggle for survival of fan mussels in the Gulf of Erdek, Sea of Marmara, Turkey. Medit Mar Sci 23:473-483. https://doi.org/10.12681/mms.28474
Karadurmuş U, Sarı M (2022b) Marine mucilage in the Sea of Marmara and its effects on the marine ecosystem: mass deaths. Turk J Zool 46:93-102. https://doi.org/10.3906/zoo-2108-14
Karakulak FS, Kahraman AE, Uzer U, Gül B, Doğu S (2023) Effects of mucilage on the fisheries in the Sea of Marmara. p. 193-215. In: Mucilage Problem in the Sea of Marmara. Albay, M. (Ed.). Istanbul University Press, Istanbul.
Katsanevakis S (2006) Population ecology of the endangered fan mussel Pinna nobilis in a marine lake. Endanger Species Res 1:1-9. http://dx.doi.org/10.3354/esr001051
Katsanevakis S, Thessalou-Legaki M (2009) Spatial distribution, abundance and habitat use of the protected fan mussel Pinna nobilis in Souda Bay, Crete. Aquat Biol 8:45-54. https://doi.org/10.3354/ab00204
Katsanevakis S, Tsirintanis K, Tsaparis D, Doukas D, Sini M et al (2019) The cryptogenic parasite Haplosporidium pinnae invades the Aegean Sea and causes the collapse of Pinna nobilis populations. Aquat Invasions 14:150-164. https://doi.org/10.3391/ai.2019.14.2.01
Katsanevakis S, Carella F, Çinar ME, Čižmek H, Jimenez C et al (2021) The fan mussel Pinna nobilis on the brink of extinction in the Mediterranean. Imperiled: The Encyclopedia of Conservation (pp. 700-709). https://doi.org/10.1016/B978-0-12-821139-7.00070-2
Kersting DK, García-March JR (2017) Long-term assessment of recruitment, early stages and population dynamics of the endangered Mediterranean fan mussel Pinna nobilis in the Columbretes Islands (NW Mediterranean). Mar Environ Res 130:282-292. https://doi.org/10.1016/j.marenvres.2017.08.007
Kersting D, Benabdi M, Čižmek H, Grau A, Jimenez C et al (2019) Pinna nobilis. The IUCN Red List of Threatened Species 2019:e.T160075998A160081499. https://dx.doi.org/10.2305/IUCN.UK.2019-3.RLTS.T160075998A160081499.en. (Accessed 5 October 2021).
Künili İE, Gürkan SE, Aksu A, Turgay E, Çakır F et al (2021) Mass mortality in endangered fan mussels Pinna nobilis (Linnaeus 1758) caused by co-infection of Haplosporidium pinnae and multiple Vibrio infection in Çanakkale Strait, Turkey. Biomark 26:450-461. https://doi.org/10.1080/1354750x.2021.1910344
Levene H (1960) Contributions to Probability and Statistics: Essays in Honor of Harold Hotelling. Stanford University Press, USA.
Meriç E, Yokeş MB, Yümün ZÜ, Eryılmaz M, Yücesoy-Eryılmaz F (2018) Alien benthic foraminifers from Turkish Strait System. International Journal of Environment and Geoinformatics 5:68-75. https://doi.org/10.30897/ijegeo
Öndeş F, Kaiser MJ, Güçlüsoy H (2020a) Human impacts on the endangered fan mussel, Pinna nobilis. Aquat Conserv: Mar Freshw 30:31- 41. https://doi.org/10.1002/aqc.3237
Öndeş F, Alan V, Akçalı B, Güçlüsoy H (2020b) Mass mortality of the fan mussel, Pinna nobilis in Turkey (eastern Mediterranean). Mar Ecol 41:e12607. https://doi.org/10.1111/maec.12607
Özalp HB, Kersting DK (2020) A pan-Mediterranean extinction? Pinna nobilis mass mortality has reached the Turkish straits system. Mar Biodivers 50:81. https://doi.org/10.1007/s12526-020-01110-7
Özen Ç, Sarı E, Arslan Kaya TN, Gül M, Kurt MA et al (2023) Paleo environmental pollution assessment of Erdek and Bandırma Bays in the Sea of Marmara, Türkiye. Soil Sediment Contam. https://doi.org/10.1080/15320383.2023.2200863
Prado P, Caiola N, Ibáñez C (2014) Habitat use by a large population of Pinna nobilis in shallow waters. Sci Mar 78:555-565. https://doi.org/10.3989/scimar.04087.03A
Prado P, Grau A, Catanese G, Cabanes P et al (2021) Pinna nobilis in suboptimal environments are more tolerant to disease but more vulnerable to severe weather phenomena. Mar Environ Res 163:105220. https://doi.org/10.1016/j.marenvres.2020.105220
Rabaoui L, Tlig-Zouari S, Hassine OKB (2008) Distribution and habitat of the fan mussel Pinna nobilis Linnaeus, 1758 (Mollusca: Bivalvia) along the northern and eastern Tunisian coasts. Cah Biol Mar 49:67-78.
Rabaoui L, Tlig-Zouari S, Cosentino A, Ben Hassine OK (2009) Associated fauna of the fan shell Pinna nobilis (Mollusca: Bivalvia) in the northern and eastern Tunisian coasts. Sci Mar 73:129-141. https://doi.org/10.3989/scimar.2009.73n1129
Rouanet E, Trigos S, Vicente N (2015) From youth to death of old age: the 50-year story of a Pinna nobilis fan mussel population at Port-Cros Island (Port-Cros National Park, Provence, Mediterranean Sea). Scientific Reports of the Port-Cros National Park 29:209-222.
Russo P (2017) Lagoon malacofauna: results of malacological research in the Venice Lagoon. Boll Malacol 53:49-62.
Šarić T, Župan I, Aceto S, Villari G, Palić D et al (2020) Epidemiology of noble pen shell (Pinna nobilis L. 1758) mass mortality events in Adriatic Sea is characterised with rapid spreading and acute disease progression. Pathogens 9:776. https://doi.org/10.3390/pathogens9100776
Scarpa F, Sanna D, Azzena I, Cossu P, Casu M (2021) From dark to light and back again: is Pinna nobilis, the largest Mediterranean shellfish, on the brink of extinction?. Vet 70:1-14. https://doi.org/10.51607/22331360.2021.70.1.1
Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591-611. https://doi.org/10.2307/2333709
Šiletić T, Peharda M (2003) Population study of the fan shell Pinna nobilis L. in Malo and Veliko Jezero of the Mljet National Park (Adriatic Sea). Sci Mar 67:91-98. https://doi.org/10.3989/scimar.2003.67n191
Sokal RR, Rohlf FJ (1969) Introduction to Biostatistics. W.H. Freeman and Company, New York.
Tsatiris A, Papadopoulos V, Makri D, Topouzelis K, Manoutsoglou E et al (2018) Spatial distribution, abundance and habitat use of the endemic Mediterranean fan mussel Pinna nobilis in Gera Gulf, Lesvos (Greece): comparison of design-based and model-based approaches. Medit Mar Sci 19:642-655. https://doi.org/10.12681/mms.14156
Vafidis D, Antoniadou C, Voultsiadou E, Chintiroglou C (2014) Population structure of the protected fan mussel Pinna nobilis in the south Aegean Sea (eastern Mediterranean). J Mar Biol Assoc 94:787-796. https://doi.org/10.1017/S0025315413001902
Vázquez-Luis M, Álvarez E, Barrajón A, García-March JR, Grau A et al (2017) S.O.S. Pinna nobilis: A mass mortality event in western Mediterranean Sea. Front Mar Sci 4:220. https://doi.org/10.3389/fmars.2017.00220
Vicente N (1990) Estudio ecológico y protección del molusco lamelibranquio Pinna nobilis L., 1758 en la costa mediterránea. Iberus 9:269-279.
Zavodnik D, Hrs-Brenko M, Legac M (1991) Synopsis on the fan shell Pinna nobilis L. in the eastern Adriatic Sea. p. 169-178. In: Les Espèces Marines à Protèger en Mèditerranèe. Boudouresque, C.F., Avon, M., Gravez, V. (Eds). GIS Posidonie publications, Marseille.

Download PDF

Journal Publication

published 08 Mar, 2024

Read the published version in Marine Biology →

Reviewers agreed at journal
11 Sep, 2023
Reviewers invited by journal
08 Sep, 2023
Editor assigned by journal
07 Sep, 2023
First submitted to journal
05 Sep, 2023

You are reading this latest preprint version

Combating mass extinctions: Discovering new Pinna nobilis populations in the Sea of Marmara

Status:

Journal Publication

Version 1

Abstract

Figures

Introduction

Materials and Methods

Results

Discussion

Conclusion

Declarations

Funding

Author Contributions

Acknowledgement

Data Availability

References

Status:

Journal Publication

Version 1