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Article

Distribution of Nereilinum murmanicum (Annelida, Siboglinidae) in the Barents Sea in the Context of Its Oil and Gas Potential

by
Nadezda Karaseva
1,
Madina Kanafina
1,
Mikhail Gantsevich
1,*,
Nadezhda Rimskaya-Korsakova
1,
Denis Zakharov
2,3,
Alexey Golikov
4,
Roman Smirnov
3 and
Vladimir Malakhov
1
1
Department of Invertebrate Zoology, Faculty of Biology, M. V. Lomonosov Moscow State University, 119991 Moscow, Russia
2
Polar Branch of the All-Russian Scientific Research Institute of Fisheries and Oceanography, 183038 Murmansk, Russia
3
Zoological Institute, Russian Academy of Sciences, 199034 St. Petersburg, Russia
4
Department of Zoology, Kazan (Volga Region) Federal University, 420008 Kazan, Russia
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2021, 9(12), 1339; https://doi.org/10.3390/jmse9121339
Submission received: 15 October 2021 / Revised: 16 November 2021 / Accepted: 26 November 2021 / Published: 29 November 2021
(This article belongs to the Special Issue Benthic Species and Habitats)

Abstract

:
Frenulate siboglinids are a characteristic component of communities living in various reducing environments, including sites with hydrocarbon seeps. High concentrations of hydrocarbons in the sediments of the Arctic basin seas, including the Barents Sea, suggest the presence of a rich siboglinid fauna there. This reflects the fact that microbiological oxidation of methane occurs under reducing conditions, generating high concentrations of hydrogen sulfide in the sediment. This hydrogen sulfide acts as an energy source for the sulfide-oxidizing symbionts of siboglinids. Here we report on the findings of the frenulate siboglinid species Nereilinum murmanicum made between 1993 and 2020 in the Barents Sea. These data significantly expand the range of this species and yield new information on its habitat distribution. The depth range of N. murmanicum was 75–375 m. The species was most abundant from 200 to 350 m and was associated with temperatures below 3 °C and salinities from 34.42 to 35.07. Most of the findings (43 locations or 74%) fall on areas highly promising for oil and gas production. Twenty-eight locations (48%) are associated with areas of known oil deposits, 22 locations (37%) with explored areas of gas hydrate deposits. N. murmanicum was also found near the largest gas fields in the Barents Sea, namely Shtokman, Ludlovskoye and Ledovoye.

1. Introduction

The Siboglinidae are a family of sedentary marine annelids whose representatives all lack a digestive tract. Symbiotic bacteria inhabiting a special parenchymal organ—the trophosome—assume the digestive functions [1,2,3]. Modern taxonomy distinguishes four siboglinid groups: Vestimentifera, Monilifera (genus Sclerolinum Southward, 1961), Frenulata, and Osedacinae (genus Osedax Rouse, Goffredi & Vrijenhoek, 2004) [4,5,6,7,8]. Representatives of the Osedacinae live on the sunken skeletons of whales and other large vertebrates and have heterotrophic symbionts [9,10,11]. The trophosome in representatives of Vestimentifera, Monilifera and Frenulata is populated by chemoautotrophic bacteria. The possible presence of both sulfide and methane-oxidizing bacteria has currently been shown for representatives of the latter two groups [12,13,14,15,16].
Representatives of Vestimentifera inhabit hydrothermal oases and cold hydrocarbon seeps. The presence of sulfide-oxidizing symbionts was initially shown for vestimentiferans [17,18]. More recent data indicate that the endosymbionts of at least some vestimentiferans are capable of switching between autotrophic and heterotrophic metabolism, or might be mixotrophic [19,20].
Representatives of Monilifera live on sunken wood, ropes, etc., although some species live on muddy substrates [21,22,23,24,25]. Moniliferans, according to some reports, have methane-oxidizing symbionts [13], but other studies confirm the presence of sulfide-oxidizing bacteria [16].
Species of the Frenulata group (Pogonophora sensu stricto) contain symbionts of various types. Thus, Siboglinum fiordicum Webb, 1963 and one undescribed species of frenulate from the Japanese trough have sulfide-oxidizing symbionts [26,27]. The presence of methane-oxidizing symbionts has been confirmed for one species of frenulate pogonophore (Siboglinum poseidoni Flügel & Langhof, 1983) [28], but a number of publications also indicate the possible presence of methane-oxidizing symbionts in several other species (O. haakonmosbiensis, Siboglinum atlanticum Southward & Southward, 1958, Siboglinum ekmani Jägersten, 1956) (see [1,15]). Contradictory data on the presence of methane- or sulfide-oxidizing symbionts were provided by studies on two species of the genus Oligobrachia (Oligobrachia haakonmosbiensis Smirnov, 2000 and Oligobrachia mashikoi Imajima, 1973) [14,15,16,29,30,31].
Importantly, regardless of the type of symbionts contained, siboglinids are a characteristic component of communities living at hydrocarbon seep sites. This is because, under reducing conditions, microbiological oxidation of methane occurs with the participation of sulfates. This yields high concentrations of hydrogen sulfide in the sediment. The generated hydrogen sulfide acts as an energy source for sulfide-oxidizing symbionts of siboglinids [32,33,34,35,36]. This explains why siboglinids bearing sulfide-oxidizing symbionts are confined to such hydrocarbon seep sites.
The Arctic seas are characterized by major deposits of oil, gas and gas hydrates [37,38,39,40,41] This leads to the assumption that the diversity of siboglinids is very high in the Arctic. Nonetheless, data on findings of siboglinids in the Arctic Ocean are still scarce. Only three species of siboglinids are known in the Barents Sea. Two species of frenulates (N. murmanicum and O. haakonmosbiensis) and one species of moniliferan (S. contortum) are known from the Barents Sea [24,42]. While N. murmanicum is widely distributed there, the two other species of siboglinids in the Barents Sea are known only from the Haakon Mosby Mud Volcano at the border between the Barents and Norwegian Seas [24,43]. N. murmanicum was first discovered by L.I. Moskalev in the Barents Sea in the collections of 1958 and 1959; it was the first known frenulate pogonophore for this basin and was initially identified as a representative of the genus Diplobrachia [44]. Specimens were found at several stations in the southern part of the Barents Sea near 70° N 40° E (see [44], Figure 1). The first finds stem from muddy soils at a depth of 170–300 m and a water temperature from −1.22 °C to 4.08 °C. Later, A.V. Ivanov recognized those worms as belonging to a new species and genus of frenulates and provided a full zoological description without, however, discussing its distribution [42]. Ivanov later published more specific data on the geographic and bathymetric distribution in a monograph [45]. Accordingly, the species resulted to inhabit the Barents Sea at various latitudes (69°–75° NN; 35°–40° EE) and depths (170–325 m), but the coordinates of specific stations were not detailed [45]. Subsequently, N. murmanicum was found several more times in the Barents Sea, but all the sites fell within the abovementioned area [46]. The literature also points to findings of N. murmanicum in the Norwegian Sea [47,48].

2. Materials and Methods

In this paper, we report previously unpublished data on the distribution of N. murmanicum in the Barents Sea based on new findings made during the period from 1993 to 2019. Frenulates were collected during cruises of the research vessels “Dalnie Zelentcy” in 1993, “Romuald Muklevich” in 2003, “Fridtjof Nansen” in 2005, 2006, “Smolensk” in 2006, “Vilnius” in 2007, 2018, 2019, “Professor Boyko” in 2008 and 2011, R/V “Academik Treshnikov” in 2019 and R/V “Professor Levanidov” in 2020. In all cruises, the material was collected using a 0.1 m2 Van Veen grab. The bottom grab samples were washed in a gas conical washing sieve with a mesh size of 0.75 mm.
The samples yielded adult and juvenile individuals, empty tubes, and tubes in which embryos and larvae were found in addition to adults. All samples werefixed in 4% formalin on the filtered seawater. N. murmanicum adult individuals in tubes, larvae and embryos were collected at 53 locations (in cases when several stations were located very close to each other, they were combined and counted as one location) at depths of 75.2–375 m (Table 1).
Observations of specimens for species identification were made using a stereomicroscope Olympus SZX-ZB7 (Olympus Corp., Tokyo, Japan).
Data on temperature and salinity of the water bottom layer were received by CTD-probe Mark 3B (Falmouth Scientific, Inc., Pocasset, MA, USA) at 30 of the stations (Table 1). The granulometric sediment composition was determined at 44 stations, whereby this work considers only the dominant granulometric fraction. The method used for grain size determination is wet sieving (method ISO 11277:2009, applied to fractions above 63 μm).
The maps were constructed using Surfer v 22 (Golden Software, Golden, CO, USA) for the Barents Sea region bounded in the west and east by longitudes of 10° E and 60° E, in the south and north—at latitudes 67° N and 80° N. Maps using for final illustration were additionally edited in Adobe Photoshop and Adobe Illustrator (Adobe Inc., San Jose, CA, USA).
Diagrams of distribution of stations in relation to abiotic environmental factors were built using standard tools of Microsoft Excel 365 (Microsoft Corp., Redmond, WA, USA).

3. Results

We analyzed collections of frenulates from 53 stations sampled in the Barents Sea (Table 1). In total, 310 juveniles and adult individuals, 128 embryos, and 177 larvae of a frenulate Nereilinum murmanicum were discovered at 46 stations in different parts of the Barents Sea. Empty tubes that are identical to those of N. murmanicum were recorded at 35 stations. At seven stations only empty tubes were sampled (Table 1). The embryos were found in nine tubes of N. murmanicum sampled between June and September. Tubeworm females that were brooding embryos were present at nine different stations (Table 1). Larval stages were found in tubes of 22 adults of N. murmanicum sampled from June to November. In total, individuals with larval stages in tubes were found at 12 stations (Table 1).

3.1. Geographical and Bathymetric Distribution

The findings of the adults and empty tubes of N. murmanicum were distributed over a large area of the Barents Sea basin. Adult and juvenile N. murmanicum were collected at the depth range from 75.2 to 375.3 m. We present here the map with the updated species distribution in the Barents Sea from the northernmost to the southernmost latitudes as well as from the easternmost to the westernmost longitudes (Figure 1). This area bounded by 69.05–79.63 NN, and 16.25–51.01 EE.
Most of the findings were detected in the central part of the Barents Sea basin and along the coast of the Kola Peninsula. With respect to the central part of the basin, most findings were from the Central shifting and along its periphery, especially in the area east of the Central shifting. In this area, N. murmanicum individuals were discovered at 13 stations. A total of 82 adults and juveniles of N. murmanicum were found at these stations. Importantly, two stations within this area yielded the highest numbers of individuals per grab: 34 specimens (R/V Vilnius, station #18, 74.83 NN, 46.66 EE) and 25 individuals (R/V Vilnius, station #22, 74.97 NN, 45.26 EE). In the Kola Peninsula area, a large part of the findings were concentrated to the east of the Rybachy Peninsula in the Motovsky Bay. There, we recorded N. murmanicum at eight stations.
The northernmost finding of N. murmanicum available to us stems from the southwest of the Franz Josef Land archipelago. Two adult N. murmanicum were found at this station at a depth of 126 m. The southernmost finding was off the coast of the Kola Peninsula. Only one specimen of N. murmanicum was recorded there.
Juveniles were recorded at two stations: to the west of the Central shifting at a depth of 257.6 m and in the area of the Rybachy Peninsula off the coast of the Kola Peninsula at a depth of 204 m.
Embryos were found in the adult tubes from two stations: in the region of the Rybachy Peninsula in Motovsky Bay, and at seven stations located to the south, southeast, and west of the Central Barents Sea. Those embryos stem from depth ranges of 204–341 m.
Larval stages were found in the adult tubes at three stations in the Motovsky Bay: one station off the coast of the Kola Peninsula, specifically east of the Motovsky Bay, seven stations to the south and east of the Central shifting, and a station east of the Persey shifting. Larval stages were found at depths of 190–287 m.
Empty tubes were recovered at more than the half of all stations (35), including seven stations at which only empty tubes were collected and no other material related to N. murmanicum was found. Stations with only empty tubes were encountered south of Spitsbergen (single station), all around the Central shifting and off the coast of the Kola Peninsula at depths of 175–367 m.

3.2. Relation of Distribution to Abiotic Factors

For the listed collections, we compared the data on the abiotic factors of the habitats of N. murmanicum, including temperature, salinity, and the granulometric composition of the sediment.
Temperature of the bottom water in the areas of the tubeworm habitats was obtained at 30 out of 53 stations. N. murmanicum temperature ranges were from −0.31 to 4.76 °C. The distribution of stations by temperature values was as follows: two stations featured values < 0 °C; six stations were in the range from 0 to 1 °C, eleven stations in the range from 1 to 2 °C, six stations in the range from 2 to 3 °C, (Figure 2). Two stations with the coldest bottom water temperatures (<0 °C) were located to the south and southeast of the Central shifting and were measured in September 2006. The warmest water stations were located in different regions: one was to the south of Spitsbergen in the area of the Medvezhinsko-Nadezhdinskaya uplift (4.43 °C in August 2006), another was in the Motovsky Bay (4.76 °C in August 2003). Individuals with larvae in tubes were found in a wide temperature range, from 0.05 to 3.49 °C. Embryos were present at those stations with a sediment temperature from −0.31 to 2.9 °C.
All the records of frenulates in the Barents Sea were associated with salinities in a very narrow range, from 34.42 to 35.07. The station with the highest salinity overlapped with one of the stations with the highest temperatures, which were located south of Spitsbergen in the area of the Medvezhinsko-Nadezhdinskaya uplift. Only empty tubes of N. murmanicum were found at this station. The lowest salinity was recorded at one of the stations in the Motovsky Bay. Individuals with larvae and embryos in tubes were detected at the stations with salinity ranges from 34.45 to 35.03.
According to the granulometric composition, we subdivided all stations into four categories according to the main granulometric component of sediments: silt (23 stations), sand (11 stations), clay (11 stations), and “stones” (rocky ground, one station) (Figure 2). In the category “silt” we included silt, clayey silt, sandy and fine sandy silt. The category “sand” included sand, silty sand with stones and gravel, silty sand with clay and gravel. Clay and silty clay as well as clay with coarse sand were assigned to the category “clay”.
At the large majority of stations (45), the number of adult specimens per station was less than 10. At 39 of these stations, no more than three specimens were collected per station. Two of the stations from the east side of the Central shifting yielded the highest numbers of individuals per grab: 34 (R/V Vilnius, station #18, 74.83 NN, 46.66 EE) and 25 (R/V Vilnius, station #22, 74.97 NN, 45.26 EE). At these stations the following abiotic factors were recorded in October 2018. At station #18, the specimens were sampled at a depth of 221 m, in the silty sediment, a bottom water temperature of 1.45 °C and a salinity of 34.88. At station #22, the tubeworms were collected from 269 m (silty sediment, bottom water temperature 1.45 °C, salinity 34.90). In addition to adults, larvae and empty tubes were also found at these stations.
The maximum number of specimens per station is 36 adults. Two stations yielded this number of specimens from the studied collections in the Barents Sea. The first station was located to the west of the Central shifting (R/V Fridtjof Nansen, station #12, 74.5 NN, 33.48 EE). The tubeworms were collected from silty sediment at a depth of 257.6 m in September 2006. The bottom water temperature was 0.08 °C, salinity 35.03. The 36 individuals reflect the sediment content of four grabs. In addition to adults, juveniles and empty tubes were collected at the station. The second station was located in the Motovsky Bay (R/V Romuald Muklevich, station #22, 69.55 NN, 32.87 EE). At this station, the material was collected from silty sediment at 224.8 m; at the season of collection, August 2003, the bottom water temperature was 2.9 °C, salinity 34.45. The 36 individuals reflect the examination of sediment from five grabs. In addition to adults, empty tubes were present at this station.

4. Discussion

4.1. Geographical and Bathymetric Distribution

The new findings considerably expand the known range of N. murmanicum. In the Barents Sea, this species was found within the area bounded by 69.05–79.63 NN, and 16.25–51.01 EE (Figure 1). The northern boundary of the N. murmanicum habitat is the south-eastern part of the Persey shifting. From the west, the area is limited by the Medvezhinsko-Nadezhdinskaya uplift on the border of the Barents and Norwegian Seas. The southernmost findings approach the coast of the Kola Peninsula. In the east, the range is limited by the Central Depression and the south-eastern coast of Juzhnyi Island in the Novaya Zemlya archipelago. The depth range at which N. murmanicum was found is 75.2–375.3 m. Most of the findings (81%) were made at depths between 200 and 350 m (Figure 2A). Other findings surround the Central shifting at depths <200 m and are located to the east and west of the Spitzbergen’s shifting at depths <100 m. The findings in the southern part of the Barents Sea are confined to the trough between the coast and the Murmansk uplift. Note that the findings of N. murmanicum in the Norwegian Sea were made at significantly greater depths, i.e., 1300 m [47,48].

4.2. Environment

All the finds where the sediment composition was recorded except one are confined to soft sediments (silt, silted sand, clay), and 72% of those finds are confined to sandy and silty sediments (Figure 2C). Frenulate tubes are positioned vertically or almost vertically in the substrate [26,49,50]. As the frenulates grow, they sink into the sediment, burying themselves with the help of an opisthosome, which protrudes through the lower open end of the tube [22,51]. Accordingly, stony substrates are unsuitable for frenulate settlement: only one finding of N. murmanicum was on a stony substrate. Dense clays can hinder the diffusion of fluids containing dissolved gases. Such gases, however, are necessary for the vital activity of symbionts. In our material, 11 finds (25%) are confined to clay-containing sediments (Figure 2C).
The Barents Sea is characterized by low bottom water temperatures, and most of the findings (83%) are associated with temperatures below 3 °C (Figure 2B). Siboglinids are not found in desalinated areas of the world oceans. At first glance, this pattern appears to be violated by the presence of Crispabrachia yenisei and Galathealinum karaense in the Yenisey Bay in the estuary area of the great Siberian Yenisey River [52,53]. However, this area is characterized by strongly stratified waters: at a depth of 28 m, where frenulates were collected, the salinity approaches that of oceanic values [54]. All the records of frenulates in the Barents Sea are associated with salinities in a narrow range from 34.42 to 35.07.
The new findings significantly expand the range of N. murmanicum in the Barents Sea. Together with previously known locations, records are now available from 58 locations. Interestingly, most of the findings (43 locations or 74%) fall in areas known as highly promising for oil and gas production (Figure 1C). Twenty-eight locations (48%) are associated with areas of known oil deposits, and 22 locations (37%) are associated with areas explored for gas hydrate deposits (Figure 1B,D). N. murmanicum was also found near the largest gas fields in the Barents Sea, namely Shtokman, Ludlovskoye and Ledovoye (Figure 1B).

4.3. General Connection of Siboglinids Findings to Hydrocarbons

Siboglinids are quite often confined to areas of hydrocarbon seeps. Thus, cold seep vestimentiferans—representatives of the genera Lamellibrachia, Seepiophila and Escarpia—reach high numbers around hydrocarbon seeps in the Gulf of Mexico and on the slope off Louisiana [55,56,57,58,59,60,61,62,63]. This pattern is also valid for siboglinids of the subfamilies Frenulata and Monilifera [16,31,48,64,65,66,67,68,69,70,71,72,73,74,75,76,77].
The Arctic has enormous oil and gas reserves [78]. According to the United States Geological Survey, at least 13% of the world’s undiscovered oil reserves and at least 30% of the world’s undiscovered gas reserves are located above the Arctic circle, most offshore at depths <500 m [37,38,39]. Among the Russian Arctic seas, the Barents Sea and the Kara Sea are the most promising regions in terms of oil and especially gas production. Two-thirds of the undiscovered gas reserves in the Arctic are presumably located in four regions: South Kara Sea, South Barents Basin, North Barents Basin, and the Alaska Platform [37,38]. The geological structure of the Barents Sea shows great promise for large hydrocarbon reserves [79,80,81,82,83,84,85,86,87,88,89,90,91]. Several of the richest deposits have been discovered in the Russian part of the Barents Sea, including the Shtokmanovskoe (Shtokman), Ledovoe, Ludlovskoe, Murmanskoe, and Severo-Kildinskoye fields, with total gas reserves of at least 4.4 trillion m3. A major part of the reserves falls on the Shtokmanovskoe field, containing, according to Gazprom Corporation, at least 3.9 trillion m3 of gas and 39 million tons of gas condensate [92].
High concentrations of hydrocarbons in the sediments of the Arctic basin seas suggest the presence of a rich siboglinid fauna. In recent years, significant progress has been made in the study of Arctic Sea siboglinids. Eleven species of frenulate pogonophorans belonging to 7 genera are known in the basin of the Arctic Ocean along with its border seas (Crispabrachia yenisey Karaseva, Rimskaya-Korsakova, Ekimova, 2021, Galathealinum arcticum Southward, 1962, Galathealinum karaense Smirnov, Zaitseva & Vedenin, 2020, Siboglinum ekmani, Siboglinum hyperboreum Ivanov, 1960, Siboglinum norvegicum Ivanov, 1960, Nerelinum murmanicum Ivanov, 1961, Nereilinum squamosum Smirnov, 1999, Oligobrachia haakonmosbiensis, Polybrachia gorbunovi (Ivanov, 1949), Polarsternium rugellosum Smirnov, 1999 [24,42,45,46,52,53,93,94,95,96]. Moreover, the moniliferan Sclerolinum contortum Smirnov, 2000, known for its bipolar distribution, is found in this region [43]. The most diverse fauna of frenulate pogonoforans in the Arctic region is described from the Laptev Sea (N. squamosum, O. cf. haakonmosbiensis, Pol. gorbunovi, P. rugellosum, S. hyperboreum) and the Central basin (S. ekmani, S. hyperboreum, S. norvegicum, N. squamosum, O. haakonmosbiensis) [24,45,46,93,94,95,96]. Very recently, two new species were described close to each other in the Kara Sea in the area of Yenisey River estuary (C. yenisey, G. karaensis) [52,53]. One species has been described (in the sense found) in the East Siberian (O. cf. haakonmosbiensis) [97] and Greenland (S. hyperboreum) [46] seas and another one in the Beaufort Sea (G. arcticum) [94]. Representatives of the genus Oligobrachia have also been reported in the Beaufort Sea, exhibiting a high similarity in 18S-RNA c to O. haakonmosbiensis; they also have symbionts closely related to O. haakonmosbiensis symbionts from the Barents Sea and the Laptev Sea [98]. Thus, among Arctic marginal seas, the Chukchi Sea is the only one lacking any frenulate (or siboglinid) species.
Many of the siboglinid findings in the seas of the Arctic basin were associated with high concentrations of hydrocarbons [52,53,74,76,97,99]. Recent studies have shown that Oligobrachia is a reliable indicator of methane seeps in the Laptev Sea [31,76,77,100]. Currently, only very few findings of frenulate siboglinid worms are available from the Kara Sea [52,53]. They are confined to the estuarine areas of the Yenisei River, where increased methane concentrations are probably associated with the result of the degradation of permafrost strata under the influence of river runoff [101,102]. Given the high hydrocarbon potential of the Kara Sea (see [37,38,82]), we expect a much wider distribution of siboglinids in this sea. Frenulate Oligobrachia and moniliferan Sclerolinum form high-density populations at the underwater mud volcano Haakon Mosby in the Norwegian Sea [67,68]. Frenulate siboglinids in several areas of the North Atlantic also prefer sediments with a higher methane concentration [48]. The frenulate worm S. poseidoni, for which the presence of methane-oxidizing symbionts has been reliably established, was detected at high methane concentrations in the sediment: 3.4 × 106 nmol/L in the Skagerrak Strait [103] and 5.5 × 106 nmol/L around the underwater mud volcano Captain Arutyunov (Gulf of Cadiz) [70]. Six species of frenulate worms are reported in the Sea of Okhotsk [45,93,104,105,106], confined mostly to areas where the sediment methane concentration varies between 0.22 and 4.46 × 109 nmol/kg, whereas areas with normal background concentrations were comparatively rarely inhabited [107,108]. Moniliferan Sclerolinum was found in Antarctica near Hook Ridge along the Antarctic Peninsula at methane concentrations of 26 × 103 nmol/L [66,72].

5. Conclusions

The first representative of Siboglinidae was found in seas close to the Sunda Archipelago in 1914 [109]. Over the next several decades, siboglinids were found in all oceans [23,24,45,93,94,95,104,105,110,111,112,113,114,115,116,117,118,119]. While the feeding mechanism of the frenulate pogonophorans was not discovered until 1980 [120,121,122], the authors describing new species of frenulates from different regions of the World Ocean had no idea about the association of pogonophorans with hydrocarbon seeps and never linked their findings with areas of high concentrations of hydrocarbons. Later, it became clear that some frenulates inhabit locations within areas of underwater deposits of oil and gas, for example the Gulf of Mexico, the Norwegian Sea, and the Barents Sea [23,24,42,112]. The example of the Sea of Okhotsk is very indicative. In the 1950s–1960s, the Soviet expeditions, yielded numerous findings of frenulates in the Sea of Okhotsk [105,123,124,125,126]. At that time, however, there was no evidence of symbiotrophic feeding of frenulates. Later, it was revealed that frenulate finds in the Sea of Okhotsk overlap with areas of high hydrocarbon concentrations in the sediment and bottom water [107,108].
There is still no information about the presence of hydrocarbon seeps in numerous areas of frenulate habitats in the World Ocean. The fact that the nutrition of frenulates relies on methane- or sulfide-oxidizing bacterial symbionts suggests that the locations inhabited by frenulates should coincide with hydrocarbon-rich regions. This makes frenulates indicator organisms: wherever frenulates are found, one should seek high methane concentrations (of any origin) there.

Author Contributions

Conceptualization—N.K. and V.M.; methodology—V.M.; software—N.K. and M.G.; validation—N.K. and M.G.; formal analysis—N.K.; investigation—N.K. and M.K.; resources—N.K., M.K., D.Z., A.G. and R.S.; data curation—N.K.; writing—N.K. and V.M.; N.R.-K. writing—review and editing—N.K., V.M., M.G. and N.R.-K.; visualization—N.K.; supervision—V.M.; project administration—M.G.; funding acquisition—V.M., N.K. and M.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Russian Science Foundation, grant number 18-14-00141-P.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We thank the captains and crews of the research vessels Dalnie Zelentcy (1993), Boyko (1993, 2008, 2011), Romuald Muklevich (2003), Fridtjof Nansen (2005, 2006), Smolensk (2006), Vilnius (2007, 2018, 2019), Academik Treshnikov (2019), Levanidov (2020) for their excellent collaboration during the field work.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

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Figure 1. Distribution of Nereilinum murmanicum in the Barents Sea. (A)—physical map of the Barents Sea, (B)—gas hydrate deposits and most significant gas deposits, (C)—estimated significance of the area for hydrocarbon production (according to Stupakova, 2011), (D)—area of known oil deposits (according to Stupakova, 2011).
Figure 1. Distribution of Nereilinum murmanicum in the Barents Sea. (A)—physical map of the Barents Sea, (B)—gas hydrate deposits and most significant gas deposits, (C)—estimated significance of the area for hydrocarbon production (according to Stupakova, 2011), (D)—area of known oil deposits (according to Stupakova, 2011).
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Figure 2. Distribution of stations with new finds of Nereilinum murmanicum in relation to abiotic environmental factors. (A)—distribution of stations by depth, (B)—distribution of stations by bottom water temperature, (C)—distribution of stations by sediment type.
Figure 2. Distribution of stations with new finds of Nereilinum murmanicum in relation to abiotic environmental factors. (A)—distribution of stations by depth, (B)—distribution of stations by bottom water temperature, (C)—distribution of stations by sediment type.
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Table 1. Data on newly collected material of Nereilinum murmanicum in the Barents Sea from 1993–2020. (A—adults, E—embryos, J—juveniles, L—larvae, T—empty tubes).
Table 1. Data on newly collected material of Nereilinum murmanicum in the Barents Sea from 1993–2020. (A—adults, E—embryos, J—juveniles, L—larvae, T—empty tubes).
R/VStationsNNEEDateDepth, mTemp., °CSalinitySedimentMaterial
R/V Vilnius3769.0539.718 August 2007226.7 SiltA, T
R/V Dalnie Zelentcy3669.2135.9626 June 1993195 SandA
R/V Dalnie Zelentcy3469.4337.2124 June 1993185 A
R/V Professor Boyko2011-569.4835.218 July 2011175.5 SandT
R/V Professor Boyko3869.5136.0027 June 1993200 A
R/V Romuald Muklevich23-269.5332.8812 August 20032543.0834.489SiltA
R/V Professor BoykoC-169.5532.595 July 2011204 SandA, J, L
R/V Romuald Muklevich22-169.5532.8711 August 2003224.82.934.451SiltA, E, L, T
R/V Romuald Muklevich19-169.5532.5911 August20032044.76 A, T
R/V Romuald Muklevich20-469.5632.6511 August 2003241.82.7634.418SiltA, L, T
R/V Romuald Muklevich27-269.5833.1013 August 2003225.63.1234.501SiltA
R/V Romuald Muklevich28-169.5933.1513 August 2003232.62.9434.451SiltA
R/V Professor Boyko15-169.5936.3423 November 2008190.33.4934.599SiltA, L
R/V Dalnie Zelentcy3269.6740.0024 June 1993170 SandA
R/V Fridtjof Nansen43-272.3040.0028 September 20063410.1534.99SiltA, E, T
R/V Smolensk23-572.3051.0111 September200675.20.1134.73StonesA
R/V Smolensk19-372.3048.607 September2006175.22.9834.49SiltA, T
R/V Fridtjof Nansen44-272.9938.0128 June 20062370.6335.03SandA, E, L, T
R/V Smolensk21-173.0047.0210 September2006312.6−0.1234.96ClayA, T
R/V Smolensk22-373.0049.0210 September2006243.71.9334.99ClayA, T
R/V Smolensk3373.3035.5925 Septembe 2006261 SiltT
R/V Smolensk25-373.3045.1012 September2006321.5−0.3134.96ClayA, E, T
R/V Smolensk34-273.3038.0325 September 2006263.5 ClayA, T
R/V Professor LevanidovD273.5841.337 August 2020275 ClayA, T
R/V Vilnius5173.9741.5424 October20182740.1534.964SiltA
R/V Smolensk32-374.0035.6024 September2006228.9 SiltA, T
R/V VilniusLud1574.3645.9910 July 2019287 A, L, T
R/V Professor LevanidovLud1574.2243.3830 July 2020289 ClayA, T
R/V Vilnius674.3646.0117 October 20182861.6234.964SiltA, L, T
R/V Professor LevanidovLud674.4445.591 August 2020292 ClayA, E, T
R/V VilniusLud1074.4845.649 July 2019306 A
R/V Professor LevanidovLud774.4946.382 August 2020221 ClayA, E, L, T
R/V Fridtjof Nansen12-174.5033.482 September 2006257.60.0835.03SiltA, J, T
R/V Professor LevanidovLud274.5245.352 August 2020291 ClayA
R/V Professor LevanidovLud374.5846.162 August 2020270 ClayA, E, T
R/V VilniusLud674.7245.959 July 2019297 A, T
R/V Vilnius1774.7345.9818 October 20182961.5534.956SiltA, T
R/V VilniusLud774.8246.658 July 2019222 T
R/V Vilnius1874.8346.6618 October 20182211.4534.883SiltA, L, T
R/V Fridtjof Nansen6-474.8317.4429 August 2006296.44.4335.065SiltT
R/V Vilnius2274.9745.2618 October 20182691.4534.908SiltA, L, T
R/V Vilnius374.9746.258 July 2019279 A, L, T
R/V Fridtjof Nansen16-575.0029.904 September 2006375.31.3535.06SandA
R/V Fridtjof Nansen60-575.0127.485 October 2005311.41.5835.05SiltT
R/V Fridtjof Nansen15-275.5030.484 September 2006367.11.2735.06SiltT
R/V Fridtjof Nansen14-175.5033.493 September2006223.11.3035.07SandA, E
R/V Smolensk2775.6038.0123 September2006248.1 ClayT
R/V Fridtjof Nansen18-475.8629.936 September2006303.21.8835.07SandA, T
R/V Fridtjof Nansen5-176.0616.2528 August 2006364.62.6135.01SiltA
R/V Fridtjof Nansen21-276.6130.008 September 2006282.62.0535.07SandA, T
R/V Fridtjof Nansen24-477.5133.548 September2006150.91.8134.94SandA
R/V Fridtjof Nansen35-378.0343.0015 September2006267.60.0534.99SandA, L, T
R/V Academik Treshnikov39B79.6344.726 May 2019126 A
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Karaseva, N.; Kanafina, M.; Gantsevich, M.; Rimskaya-Korsakova, N.; Zakharov, D.; Golikov, A.; Smirnov, R.; Malakhov, V. Distribution of Nereilinum murmanicum (Annelida, Siboglinidae) in the Barents Sea in the Context of Its Oil and Gas Potential. J. Mar. Sci. Eng. 2021, 9, 1339. https://doi.org/10.3390/jmse9121339

AMA Style

Karaseva N, Kanafina M, Gantsevich M, Rimskaya-Korsakova N, Zakharov D, Golikov A, Smirnov R, Malakhov V. Distribution of Nereilinum murmanicum (Annelida, Siboglinidae) in the Barents Sea in the Context of Its Oil and Gas Potential. Journal of Marine Science and Engineering. 2021; 9(12):1339. https://doi.org/10.3390/jmse9121339

Chicago/Turabian Style

Karaseva, Nadezda, Madina Kanafina, Mikhail Gantsevich, Nadezhda Rimskaya-Korsakova, Denis Zakharov, Alexey Golikov, Roman Smirnov, and Vladimir Malakhov. 2021. "Distribution of Nereilinum murmanicum (Annelida, Siboglinidae) in the Barents Sea in the Context of Its Oil and Gas Potential" Journal of Marine Science and Engineering 9, no. 12: 1339. https://doi.org/10.3390/jmse9121339

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