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Introduction
Since the Black Sea is a semi-enclosed sea, it is more sensitive than open seas and therefore more easily negatively influenced (Bat et al. 2018). Bat et al. (2011) characterized the Black Sea as a highly productive ecosystem at all trophic levels. The Black Sea food chain became dominated by jellyfish in the 1990s and the biodiversity of its ecosystem degraded as a consequence (Shiganova 1998). Disruption of the ecological balance in the Black Sea led to dominant macro-zooplankton species. Due to changing dietary network relationships, a large part of the secondary production (zooplankton biomass) began to be consumed by jellyfish species. After entering the Black Sea ecosystem in the early 1980s, Ctenophore Mnemiopsis leidyi Agassiz, 1865 – that is transported with ballast waters – has resulted in radical changes. M. leidyi that occupy the same trophic level as fish has seen a decline in fish stocks and ichthyoplankton in the Black Sea. In the same way, after entering the Black Sea ecosystem in 1997, Ctenophore Beroe ovata Bruguière, 1789, feeding on M. leidyi, has led to improvements in the fish stocks of the Black Sea (Finenko et al. 2003; Svetlichny et al. 2004; Anninsky et al. 2005; Finenko et al. 2006; Oguz et al. 2008; Mutlu 2009).
Despite being largely underappreciated up until now, jellyfish play a significant role in controlling global marine plankton ecosystems, including biomass, spatiotemporal dynamics, and the community structure of the plankton. The jellyfish (more specifically medusae of the Phylum Cnidaria: Orders Rhizostomeae and Semaeostomeae) within coastal marine systems have received much attention recently. There are seven gelatinous macrozooplankton in the Black Sea ecosystem. These species are: Cnidaria Rhizostoma pulmo (Özer & Çelikkale 1998), Aurelia aurita (Demir 1954), Chrysaora hysoscella (Öztürk & Topaloğlu 2009), Ctenophora Pleurobrachia pileus, Beroe ovata, Mnemiopsis leidyi (Mutlu et al. 1994), Bolinopsis vitrea (Öztürk et al. 2011).
R. pulmo which is the most conspicuous and largest macro gelatinous species in the Black Sea has been observed in large numbers in the north-west part of the sea in the late 1960s and early 1990s. Afterwards, populations of R. pulmo have decreased between the years 1973 and 1974 in the north-west (Zaitsev & Mamaev 1997).
Although common gelatinous zooplankton species work well in the Black Sea, studies of the barrel jellyfish are limited (İşinibilir et al. 2017). R. pulmo is an important species in the Black Sea ecosystem and is a significant food source for many marine organisms, including fish, birds, and marine mammals. Its abundance and biomass can impact the dynamics of the food web and energy transfer within the ecosystem. R. pulmo is primarily a carnivore (Dönmez & Bat, 2019). The presence or absence of R. pulmo in the Black Sea can serve as an indicator of the state of the ecosystem’s health (Oguz et al. 2001). Changes in R. pulmo’s population size or distribution can reflect shifts in environmental conditions, such as changes in the water temperature, nutrient availability, or pollution levels (Purcell et al. 1999). However, it is important to note that large blooms of R. pulmo can have negative impacts on the ecosystem, such as reducing the availability of oxygen and potentially causing harm to other marine organisms. Thus, monitoring and understanding the population’s dynamics and the ecology of R. pulmo is crucial for the sustainable management of the Black Sea’s ecosystem. The scarcity of studies on the distribution of R. pulmo in the Black Sea makes it even more important to conduct further research on this species. Therefore, in this study, the distribution of R. pulmo in the region between Kızılırmak and Yeşilırmak, two of the most important and largest rivers flowing into the Black Sea, was studied.
Materials and methods
Measurement of physical parameters
The transparency of the water was measured at six stations details below with a 20 cm diameter Secchi disc. A Sınar brand mercury thermometer was used for temperature measurement, while pH values were determined with a KL-012 professional type pH meter.
Sampling period and area
The study was carried out between the Kızılırmak and Yeşilırmak rivers of the southern Black Sea. Six stations were chosen in different areas along the coast of Samsun; station 2 and 3 were in Atakum city, stations 1 and 4 in Ilkadım city; Station 5 was in Bafra city located 400 m from the stream mouth of the Kızılırmak river; Station 6 was located 800 m northeast of the stream mouth of the Yeşilırmak river (Figure 1). Monthly samples of the barrel jellyfish were obtained from April 2008 to March 2010, over a period of 23 months. In addition to horizontal and vertical samplings, the line transect method was carried out for the estimate of the medusa’s abundance.
Figure 1
Sampling stations: (Station I: N 41°18’47.4’’ – E0 36°21’18.5’’, Station II: N 41°20’5.4’’ – E0 36°17’32.3’’, Station III: N 41°21’12. 6’’ – E0 36°15’34.4’’, Station IV: N 41°16’01.8’’ – E0 36°23’11.2’’, Station V N 41°44’18.1” – E0 35°57’35.3’’, Station VI N 41°23’01.2”– E0 36°40’23.2’’)
The estimation of the abundance and biomass of Rhizostoma pulmo
Both horizontal and vertical tows were used, implementing the same type of plankton net (mesh size, 1 mm; diameter, 80 cm; length, 3 m). In the vertical sampling, the barrel jellyfish were collected by vertical tows of a plankton net from depths of 25-30 cm to the sea surface for stations 1, 4 and 6. Horizontal sampling was towed by boat at speeds of 2 miles h-1 (15-20 min) for all stations. All the collected samples were measured with a digital hand scale. With regard to the Line Transect, to estimate the abundance of the barrel jellyfish per square metre the length and width of each transect was established at 40 m to 5 m in all sampling stations. Furthermore, the number of (individuals of) medusae per square metre was counted with visual observations on a gangboard (150 m far from the coast).
Statistical analysis
Statistical comparisons were computed using the Minitab 16 package. Biological, physical and chemical data were obtained via the Spearman rank correlation coefficient and one-way analyses of variance (ANOVA) and analyses of covariance (ANCOVA). Spearman correlation tests were used to determine the comparison of the relationships between the abundance of the biomass of R. pulmo and the temperature (Zar 1996).
Results
Barrel jellyfish were observed along the whole coast of Samsun. The barrel jellyfish reached values of maximum abundance and biomass in summer and autumn. In the sampling areas between the Kızılırmak and Yeşilırmak rivers, R. pulmo was seen only for a period of 5 months in 2008, but this extended to 7 months during 2009.
Environmental parameters
A 24-month sampling was carried out at stations I, II, III and IV between April 2008 and March 2010, and a 15-month sampling was carried out at stations V and VI between January 2009 and March 2010. Sampling could not be made at stations II and III in June 2008 and at stations V and VI in February 2009 due to weather conditions. The sea water temperatures and pH values of the stations studied are given in Figure 2.
Figure 2
The sea water temperatures and pH values of the stations between the Kızılırmak and Yeşilırmak rivers of the southern Black Sea
The highest surface water temperature detected at station I was 26.5°C in August 2009, and the lowest surface water temperature value was 7.9°C in January 2009. The highest and lowest temperature values observed at station II were measured as 26.8°C in August 2009 and 7.2°C in January 2009, respectively. The highest surface water temperature measured at station III was observed in August 2009 as 27°C. The lowest temperature value was measured as 8.2°C in January 2009. In August 2008, when the surface water temperature was the highest at station IV, the water temperature was 27.1°C, the highest value measured at all the sampling stations (as mentioned by Dönmez & Bat, 2019). The lowest value of the surface water temperature was measured in January 2009 with 8.1°C. The highest temperature value measured at station V was measured as 26.3°C in August 2009. The lowest temperature value was measured as 7.2 in January 2009, and this value was the lowest temperature value among all the stations where temperature measurements were made (as mentioned by Dönmez & Bat, 2019). In the 14-month temperature measurements made at station VI located in the area where Yeşilırmak empties into the sea, the highest temperature value was determined as 26°C in August 2009 and the lowest temperature value as 7.3°C in January 2009.
It has been determined that seasonal pH values generally increase in spring and summer and decrease in autumn and winter. During the study period, the pH values measured in the surface waters of the stations varied between 7.8-8.9. The light transmittance values measured along the water column varied greatly depending on the wind conditions, precipitation, wave heights, cloudiness and the presence of overgrowth species, and these values varied between 1.1-10.8 m (Figure 3).
Figure 3
The Secchi disc depths
Abundance and Biomass
Vertical distribution
The barrel jellyfish were observed in July, August, September, October, and December during all study periods for the vertical tows. The peak biomass value became 11.792 g m-2 in October 2009 at station IV. The barrel jellyfish abundance reached the highest values (10 n/m2) in November 2008 at station IV and September 2009 at station VI (Figure 4). It was determined that the highest abundance value of R. pulmo at station I for 2008 and 2009 was in August with 8 n/m2. The highest biomass value of R. pulmo individuals collected in vertical samples at station I was observed in October 2009 with 9.581 g/m2.
Figure 4
Vertical biomass and abundance variation of R. pulmo measured at stations I, IV and VI during the sampling period
Horizontal distribution
When the horizontal distribution of R. pulmo according to the stations is evaluated seasonally, it has been determined that this species is not seen at all in spring; it reaches high abundance and biomass values in summer and autumn, it is represented in small numbers in the first half of winter and is not seen at all in February (Figure 5). When the abundance and biomass ratios of R. pulmo were compared according to the months, it was observed that the abundance and biomass values were generally high in August and October and were represented with a low rate in December and January. The highest abundance and biomass values determined as results of horizontal sampling were 7.6 n/100 m3 and 12.587.5 g/100 m3, respectively. The abundance and biomass values observed in November and December of 2009 were lower than November and December of the previous period.
Figure 5
Horizontal biomass and abundance variation of R. pulmo measured at all stations during the sampling period
The abundance values of R. pulmo obtained from the surface observations.
The abundance values of R. pulmo individuals counted by surface observations were calculated for all stations and the results were compared with the monthly temperature values (Figure 6).
Figure 6
The abundance values of R. pulmo individuals with monthly temperature
The highest and lowest values of the number of individuals were 0.31 n/m2 and 0.007 n/m2. It was determined that the number of individuals of R. pulmo increased towards the end of the summer months and was observed in high numbers in the autumn months. Parallel to the increase in temperature, R. pulmo individuals, which started to be seen towards the end of July, generally reached the highest abundance values in August and October. They disappeared in November, December, and January. The total number of individuals counted at station III was 563, with the highest abundance among the stations.
Length distribution of R. pulmo by months
The height of 696 R. pulmo individuals captured during the sampling period varied between 15.6-49 cm (Figures 7A and 7B.). The highest average length was 31 cm in September and October 2009. The average length of R. pulmo during the study period was 27 cm. In general, the length of R. pulmo individuals started to increase in August, and it was determined that the average heights reached the highest level in September and October for the study period.
Figure 7
A. Length-frequency relationship of R. pulmo individuals (August 2008-July 2009); B. Length-frequency relationship of R. pulmo individuals (August 2009-January 2010)
Discussion
There are very few studies on the distribution of R. pulmo in the southern part of the Black Sea. Özer & Çelikkale (1998), studied the distribution of R. pulmo on the Trabzon coast between 1990-1992. They determined that individuals were seen between August and January, and that they reached the highest umbrella diameter (39.5 cm) and biomass values in November and December. In our study, the highest umbrella diameter and wet weight were 42.5 cm and 4730 g, respectively. These values have been the highest values recorded for the southern Black Sea so far. The months with the highest abundance and biomass values of R. pulmo for the coasts of the southern Black Sea between Kızılırmak and Yeşilırmak were August and October. The emergence and disappearance periods of the barrel jellyfish during the year are similar to the data obtained for the Trabzon coast (Özer & Çelikkale 1998). Mutlu (2009) emphasized that although R. pulmo is the most common species, especially along the southern coasts of the Black Sea, this species was not observed in his research conducted between 2006-2007. However, in our study carried out between 2008 and 2010, R. pulmo was found intensively.
Environmental factors can directly affect the population size of jelly-like organisms (Purcell et al. 2007). Among these environmental factors, abiotic factors such as temperature, salinity, solar radiation and currents, and biotic factors such as nutrient availability, affect the presence of medusa (Wiebring et al. 2010). Considering the increased abundance of Rhizostoma species distributed in European waters at high temperatures, it has been suggested that warmer summer months lead to Rhizostoma spp. growth (Lilley et al. 2009). Boero et al. (2016) pointed out that the two main global drivers of jellyfish blooms are global warming and overfishing. In this sense, they concluded that this gelatinous zooplankton appears to be expanding their distribution, as seen in the Mediterranean, probably due to both temperature increases and the gradual expansion of the Suez Canal.
In this study, it was determined that the monthly temperature values measured during the study period did not make a significant difference between the stations (p > 0.05). Lilley et al. (2009), based on the temperature values, when the distribution of R. pulmo individuals along the Samsun coast was examined, for the first half of the study period (2008), the maximum abundance of the distribution of R. pulmo individuals at the station IV was reached in August, when the temperature was 26°C. R. pulmo individuals, individuals which were seen for a total of 7 months in the second half of the study period, were observed in July 2009, unlike the previous study period, and reached the highest abundance in August and October (2009).
Alparslan (2001) stated that R. pulmo was not found in abundance in Çanakkale Harbour in any season, and that it is rarely found in summer and autumn. Alparslan (2001) did not observe the barrel jellyfish in the months of June and November and did so only at a low rate in June and November. Alparslan (2001) pointed out that the productivity of R. pulmo is mainly affected by temperature, salinity, and zooplankton biomass. In a study conducted in the Gulf of Izmit between July 2001 and November 2002, Isinibilir (2004) determined that the R. pulmo species was found at the end of summer and in the autumn months and stated that the occurrence of R. pulmo in this period was due to the water temperature. Similarly, Lilley et al. (2009) argue that the high abundance of Rhizostoma spp. distributed in European waters may be related to temperature. Fuentes et al. (2011) determined that the barrel jellyfish was extensively distributed on the Catalan coasts of the Mediterranean and reached its highest numbers in July and August during the study period. In this study conducted between 2008 and 2010, the number of R. pulmo individuals identified was 242 for 2008 and 454 for 2009. Reyes Suárez et al. (2022) pointed out that blooms of R. pulmo in the North Adriatic Sea have been reported since the late 1800s and observed that the observed jellyfish density in 2021 reached more than 10 specimens per square metre.
Kogovšek et al. (2010) and Brotz & Pauly (2012) stated that the recurrence of R. pulmo blooms has increased in the last few decades. Similarly, between 2009 and 2015, the total number of sightings and number of bloom sightings of the most important common jellyfish taxa, including R. Pulmo, were observed along the Italian coastline. R. pulmo has been identified in increasing numbers over the years (Boero et al. 2016).
The results of this study show parallelism with the seasonal distribution studies of R. pulmo conducted outside of Turkish waters. Lakkis (1991) observed that the barrel jellyfish formed a heap in June-July 1986, depending on environmental conditions. Lakkis (1991) determined that in late May and early June 1986, when the surface water temperature suddenly rose from 23°C to 27.5°C, clusters of R. pulmo appeared along the Lebanese coast and continued until mid-August. It can be said that this effect created by the sudden increase in water temperature along the Lebanese coast in 1986 is also valid for the month of July in our study, when medusa were first seen in 2009. While no barrel jellyfish were encountered in July of the previous study period (2008), R. pulmo was found in all observation stations in July 2009. The temperature value of 16.2°C for June 2009 was determined as 25°C in July 2009. It was concluded that the temperature increases of about 9°C may have triggered the emergence of the barrel jellyfish seen in July 2009.
The fact that the average umbrella diameter sizes of the barrel jellyfish, which started to appear towards the end of the summer during the sampling period, vary according to the months, suggests that there may be more than one breeding period. There is evidence that water temperature changes trigger strobilation in many Rhizostoma spp. (Arai 1997; Holst et al. 2007). In addition to the fact that the release of ephyra has occurred due to the increase in temperature, the triggering of the release of ephyra with the decrease in temperature often occurs. It has been suggested that Rhizostoma octopus can reproduce twice a year in the German Gulf, in the spring and autumn seasons (Holst et al. 2007). This data, which was determined from the German Gulf, showed a parallelism in this study period, indicating that two growth periods were observed in the autumn season after the decrease in temperature and in the spring season due to the increase in temperature. On the other hand, Leoni et al. (2021) reported that blooming events of R. pulmo were observed in warm temperatures and benefited from warm temperatures.
The increasing populations of jellyfish may reflect the asexual reproductive success of benthic polyps (Scyphistomae) that produce young jellies (ephyra). Environmental factors such as nutrients, temperature, salinity, and the photoperiod are important for reproductive success and the seasonal timing of reproduction in marine invertebrates (Liu et al. 2008). Podocytes do not open below 10°C and the opening rate of podocytes increases at temperatures between 15 and 30°C. Increasing temperature from 2-10°C to 22°C triggers strobilation within 2 weeks. Although the temperature required for ephyra varies between 16-28°C, the optimum temperature is 24°C (Dong et al. 2009). This finding may explain why R. pulmo began to disappear from midwinter during the sampling period.
There are studies showing that the low flow of the river during the summer season leads to an increase in the number of gelatinous areas near the coast (Kingsford et al. 2000; Nicholls & Klein 2005). There is a positive relationship between the inflow of fresh water from rivers and the abundance of barrel jellyfish (Kingsford et al. 2000). High productivity is expected in areas where rivers flow into the sea due to nutrient input. When the R. pulmo was compared with the other 4 stations in terms of abundance and biomass values at stations V and VI, no significant difference was observed. It has been observed that R. pulmo individuals are more concentrated in the Adriatic Sea along the west coast, where the freshwater effect is more pronounced, than in the other areas where it is distributed (Kogovšek et al. 2010). Considering these findings, the fact that the R. pulmo, which is expected to be more dense than other jelly species and stations, is lower than predicted in terms of abundance and biomass values at stations V and VI can be attributed to its competition with other gelatinous species and its different ecological needs.
Rhizostoma individuals appear in large numbers on the water surface in still weather, but they go deeper into the water in rainy and windy weather. They show positive geotaxis in sunlight. On the other hand, it is also stated that they are found in heaps on the water surface when the sky is covered with clouds. Among the factors affecting the distribution of R. pulmo species, the effect of flow velocity plays a more dominant role than light intensity (Figure 8A, B). It can be said that the prevailing winds blowing from the sea to the land in autumn and the currents and waves formed by these winds carry the R. pulmo towards the shores. As a matter of fact, it was observed that the medusa drifted towards the shores with the waves formed by the autumn winds blowing from the north (north-west wind, north, north-east wind) during the study period formed heaps on the beach, especially in October and November. Considering the seasonal distribution, it is observed intensely in late summer and the autumn months. The medusa are thrown ashore by storms in autumn and winter (Figure 8C, D). The mass transfer of R. pulmo to the coastline with the autumn winds blowing towards the shores of the Black Sea stands as an important result. Unusual mass deaths of R. pulmo have been observed near the Dutch Wadden Sea (Lilley et al. 2009), the Sea of Marmara (Öztürk & Sümen 2020), and in the Gulf of Trieste (Reyes Suárez et al. 2022). The barrel jellyfish, which is thrown out of the sea by the waves with the autumn winds, may play an indirect role in reducing the effects of eutrophication. For this reason, the study areas consisting of the coastal strip and sandy areas should be monitored throughout the process.
Figure 8
A.Rhizostoma pulmo in the dark, Atakum, B.R. pulmo clusters observed at Samsun Port station. R. pulmo individuals washed ashore by waves after the storm C. Atakum, D. Bafra (Original)
It is interesting that R. pulmo individuals were rarely detected in the night observations carried out in August (2009) when the abundance of R. pulmo was high. Diurnal vertical migration is a common phenomenon seen in zooplankton species (Dupont et al. 2009). The daily migration of pelagic barrel jellyfish occurs, at least in part, as an active response to light levels. Mayer (1910) stated that Rhizostoma spp. show positive geotaxis to sun rays and cluster on the surface, and, on the contrary, they can show positive geotaxis in cloudy weather. Similar findings to those of Mayer (1910) were obtained in our current study area. The statistical correlation between light transmittance and distribution of R. pulmo was r = 0.40 and p < 0.05 (Spearman’s rank correlation). Lakkis (1991) determined the statistical relationship between the distribution and light transmittance of R. pulmo as r = 0.90. A low positive correlation was observed with the effect of sun exposure, which is one of the climatic features, on the distribution of R. pulmo during the study period.
The highest known umbrella diameter of 70 cm for R. pulmo was obtained in the Aegean Sea and Burgaz Bay (Özer & Çelikkale 1998). The umbrella diameter of 42.5 cm, determined from the shores of the southern Black Sea between Kızılırmak and Yeşilırmak, collected from the shores of Lebanon (40 cm) in 1986 (Lakkis, 1991) and Trabzon (39.5 cm) in 1992 (Özer & Çelikkale 1998), was larger than the umbrella diameter of the R. pulmo samples. Commercial classification of edible medusa is generally made by measuring the umbrella diameter (Kingsford et al. 2000; Duyar & Sönmez 2006). If the umbrella diameter of the medusa exported to China is around 33 cm, it is considered as Class A, if it is between 25-33 cm, as Class B, if the diameter range is 17-25 cm, as Class C, and if the diameter group is less than 17 cm, it is considered as class D (Duyar & Sönmez 2006). The mean umbrella diameter of R. pulmo individuals obtained as a result of the study was 24.3 cm. In this study, R. pulmo is in the C class group according to the umbrella diameter averages.
Pérez-Ruzafa et al. (2002) stated that the overgrowth of R. pulmo and Cotylorhiza tuberculata, which are widely distributed along the shores of the Mar Menor, with increasing nutrient input will contribute positively to the regulation of nutrient balances and the elimination of eutrophication effects (Kingsford et al. 2000; Perez-Ruzafa et al. 2002). The Black Sea is one of the semi-enclosed polluted seas of a eutrophic character (Gucu, 2002; Oguz and Velikova 2010). The Samsun coasts, especially Kızılırmak, are under the influence of low flow untreated domestic, industrial, and agricultural wastes (Bakan & Böke Özkoç 2007; Bat et al. 2018). Pérez-Ruzafa et al. (2002) stated in their study, that R. pulmo and other gelatinous species distributed in the Black Sea may contribute to the elimination of high levels of productivity caused by excessive nutrient input and the improvement of the Black Sea’s ecosystem.
