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The role of microalgae of the genus prorocentrum in the Diet of mussels mytilus galloprovincialis (Lamarck, 1819) (Black Sea) in suspended culture

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The aim of this work was to study the role of microalgae of the genus Prorocentrum in the diet of the Black Sea mussel Mytilus galloprovincialis . The work analyzed the qualitative and quantitative composition of dinophytes of the genus Prorocentrum: P. compressum, P. cordatum, P. micans, P. scutellum, P. pusillum, P. balticum, P. maximum, P. lima in three types of samples (phytoplankton, mussel stomachs and their bio-sediments). Differences in the species composition of microalgae are described for three types of samples. It was noted that P. cordatum and P. micans predominate in plankton in winter, P. balticum and P. cordatum - in spring, P. cordatum, P. micans, P. balticum and P. pussilum - in summer, and P. micans - in autumn. At the same time, P. compressum and P. micans dominate in stomachs throughout the year. P. compressum was found in bio-sediments throughout the year, reaching almost 100% of the total number of dinophytes of the genus Prorocentrum in April; P. micans prevailed in winter, summer and autumn; P. cordatum was dominant in February, March and May. Different types of microalgae of the genus Prorocentrum are expected to have different degrees of digestion.
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The role of microalgae of the genus prorocentrum in the Diet of mussels
mytilus galloprovincialis (Lamarck, 1819) (Black Sea) in suspended
culture
To cite this article: N Pospelova and A Priimak 2021 IOP Conf. Ser.: Earth Environ. Sci. 937 022072
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IOP Conf. Series: Earth and Environmental Science 937 (2021) 022072
IOP Publishing
doi:10.1088/1755-1315/937/2/022072
1
The role of microalgae of the genus prorocentrum in the Diet
of mussels mytilus galloprovincialis (Lamarck, 1819) (Black
Sea) in suspended culture
N Pospelova1,* and A Priimak1
1A.O. Kovalevsky Institute of Biology of the Southern Seas of RAS (IBSS),
Nakhimov avenue, 2, 99011, Sevastopol, Russia
E-mail: nvpospelova@mail.ru
Abstract. The aim of this work was to study the role of microalgae of the genus Prorocentrum
in the diet of the Black Sea mussel Mytilus galloprovincialis. The work analyzed the qualitative
and quantitative composition of dinophytes of the genus Prorocentrum: P. compressum, P.
cordatum, P. micans, P. scutellum, P. pusillum, P. balticum, P. maximum, P. lima in three types
of samples (phytoplankton, mussel stomachs and their bio-sediments). Differences in the species
composition of microalgae are described for three types of samples. It was noted that P. cordatum
and P. micans predominate in plankton in winter, P. balticum and P. cordatum - in spring, P.
cordatum, P. micans, P. balticum and P. pussilum - in summer, and P. micans - in autumn. At
the same time, P. compressum and P. micans dominate in stomachs throughout the year. P.
compressum was found in bio-sediments throughout the year, reaching almost 100% of the total
number of dinophytes of the genus Prorocentrum in April; P. micans prevailed in winter, summer
and autumn; P. cordatum was dominant in February, March and May. Different types of
microalgae of the genus Prorocentrum are expected to have different degrees of digestion.
1. Introduction
Phytoplankton forms the basis of the diet of bivalve mollusks at all stages of their development. The
qualitative composition of food resources determines the indicators of survival, mortality and growth
rates of mollusks [1-4].
In the Black Sea, the nutritive base of bivalve mollusks is formed by diatoms, coccolithophores and
dinoflagellates [5-7], and the latter are the least studied in terms of nutritional value. The works devoted
to the nutrition of bivalve mollusks with dinophytes (dinoflagellates) are mainly reduced to a
quantitative comparison of their content in stomachs and water samples [1, 8, 9] or the effect of toxic
species on the vital activity of mollusks [10-14].
Due to the fact that dinoflagellates are one of the dominant classes of microalgae in the Black Sea,
and their role in the diet of the Black Sea mussels is almost not studied, this work is relevant for
replenishing information on the role of dinophytes of the genus Prorocentrum in the diet of Mytilus
galloprovincialis.
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2. Methods
2.1. Sampling site characteristics
Sampling was carried out at the mussel and oyster farm located on the outer harbor of the Sevastopol
Bay, 700 m from the coast at a depth of 5-10 m between the Karantinnaya and Sevastopolskaya bays.
To the north of the Sevastopol Bay, the Belbek River flows into the sea, and the Chernaya River flows
directly into the bay. The velocities of the currents on the farm are 5-20 cm/s, which ensures a stable
water exchange. This area is characterized by latent, non-surface squeezing processes (upwellings),
which are observed with steady winds of the eastern and northeastern components. The waters in the
area of the farm are classified as mesotrophic. From February to August 2020, the water temperature
varied from 9.2 to 25.6°C.
2.2. Research material
The material for the study was phytoplankton samples collected from the water surface. Samples were
taken with a bathometer into plastic containers with a volume of 1 - 1.5 liters and thickened by the
method of reverse filtration through nuclear membranes (manufactured in Dubna) with a pore diameter
of 1 μm to a volume of 20-40 ml. The samples were processed by the method of direct counting in a live
and concentrated drop (V=0.01 ml) and in a chamber (V=0.8 ml). Concentrated samples were fixed with
Lugol' solution (2 ml per 100 ml of sample). The samples were processed under a JENAVAL light
microscope. Calculations of the density and biomass of phytoplankton were carried out using a computer
program developed at the Institute of Biology of the Southern Seas of RAS.
To determine the taxonomic composition and number of microalgae in the food lump of the mussel,
5 specimens of commercial size mollusks (shell length more than 50 mm) were taken from the collectors
of the farm, and the contents of their stomachs were removed.
To collect bio-sediments, mussels were cleaned immediately after catching and placed individually
in filtered seawater (after filtration through nuclear filters with a pore diameter of 0.5 μm) with a constant
air supply by a compressor for 4 hours in order to empty their stomachs. The excrement was collected
with a pipette. The number of microalgae in stomachs and bio-sediments was determined by counting
cells under a microscope in triplicate.
3. Results
Our observations showed that in 2020, in plankton, mussel stomachs and bio-sediments, there were 8
dinophytes of the genus Prorocentrum: P. compressum, P. cordatum, P. micans, P. scutellum, P.
pusillum, P. balticum, P. maximum, P. lima. Of these, P. maximum is noted only in plankton, P. lima
(toxic species) - only in stomachs in August and October. There are 5 species recorded in bio-sediments.
In January and July, only one species, P. micans, was common in all three samples (plankton, stomachs,
and bio-sediments), and in February - P. cordatum. The maximum number of common species (4) in
three types of samples was recorded in October; these are P. compressum, P. cordatum, P. micans, P.
pusillum.
It should be noted that, in most cases, the species composition of dinophytes of the genus
Prorocentrum in plankton is similar to that in the stomachs and bio-sediments of mussels. In some
periods, the species diversity in plankton was higher than in stomachs and bio-sediments. This may be
due either to the selectivity of the diet of mollusks (they prefer some species more), or to a different rate
of digestion of cells of certain species.
In winter and summer, differences in the species composition of algae were noted for three types of
samples. So, in February - P. pusillum, June - P. balticum, in July and August - P. pusillum and P.
cordatum were not found in stomachs, but were recorded in plankton and bio-sediments. In February,
June, and July, P. compressum was recorded in stomachs and bio-sediments, which were absent in
phytoplankton. In March, a similar situation was noted for P. cordatum, in August - for P. balticum. This
can be explained by the different speed of passage of different types of cells through the gastrointestinal
tract, as well as the ability of microalgae to survive the adverse conditions of the acidic environment of
the stomach in the form of a cyst.
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It was shown that the proportion of dinophytes of the genus Prorocentrum in the composition of
seawater plankton is minimal and varies from 0.02% to 2% of the total phytoplankton density (Figure
1). In the stomachs of mussels, the proportion of dinophytes of the genus Prorocentrum, in the total
number of microalgae, ranged from 2 to 66% (Figure 2). It is noteworthy that both the maximum
(November) and increased (January, June, August, October) relative values of the density of dinophytes
of the genus under study in the plankton and stomachs of mussels coincide by month.
Figure 1. Proportion (%) of cells of dinophytes of the genus Prorocentrum
in relation to the total number of cells of microalgae in plankton.
Figure 2. Proportion (%) of cells of dinophytes of the genus Prorocentrum in
relation to the total number of cells of microalgae in the stomachs of mussels.
If we consider the total number of cells of microalgae of this genus in water, then the minimum values
were typical for February (100 cells/L), and the maximum - for June (more than 3000 cells/L) (Figure
3). There is a coincidence of maximum/increased values (June, August, November) and minimum
(February, April) of the total number with the proportion of cells of the genus Prorocentrum in relation
to the total number of cells of microalgae in plankton (Figure 1, 3), which indicates the dominance
dinophytes during these months. The discrepancy in these indicators in the remaining months indicates
the dominance of other groups of microalgae in plankton. Analysis of the number of cells of individual
species of microalgae of the genus Prorocentrum in plankton shows that the most common species
during the year were P. micans, P. compressum, and P. cordatum (Figure 3).
The stomach fullness of mussels with dinophytes of the genus Prorocentrum varied from 67 to 50,000
cells/mussel (Figure 4). In December, the fullness reached maximum values of 50,000 cells/mussel,
more than 50% of which was P. micans, about 30% - P. compressum, while P. micans dominated in
plankton. In January, the proportion of P. micans in stomachs was similar, but with a smaller number of
cells, and the proportion of P. compressum increased to 37%, while P. micans remained dominant in
plankton. In February, when the total number of microalgae cells in the stomachs of mussels decreased
to 4000 cells/mussel, the number of P. compressum cells reached the highest value of 90% (Figure 4,
5), while being absent in the phytoplankton composition, where 80% cells accounted for P. cordatum
(Figure 6).
0
0.5
1
1.5
2
%
1 2 3 4 5 6 7 8 10 11 12
month
1 2 3 4 5 6 7 8 10 11 12
month
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Figure 3. The number of cells of dinophytes of the genus Prorocentrum in
plankton.
In the spring, the number of cells of microalgae in the stomachs ranged from 400 to 1500 cells/mussel.
In March, the number of P. compressum cells was 825 (about 90%), while P. balticum dominated in
plankton (50%), and the number of P. compressum cells was less than 10%. In April, P. compressum
prevailed in stomachs, reaching almost 100% of the total number of cells of the genus Prorocentrum,
while P. balticum cells predominated in plankton (40%). In May, the maximum diversity of species of
the genus under study was observed in stomachs in the spring: 1000 cells/mussel of P. compressum, 350
cells/mussel of P. compressum, 350 cells/mussel - P. micans, 150 cells/mussel - P. balticum, and 67
cells/mussel - P. cordatum (Figure 4, 5). At the same time, P. balticum cells continued to dominate in
plankton (more than 40%) (Figure 6).
In summer, the range of fluctuations in numbers was wider than in spring - 67 - 2720 cells. During
the entire period, P. micans was the dominant species (50-75%). At the same time, P. cordatum and P.
balticum prevailed in plankton in June - 40% and 30%, respectively. In July, their number decreased
with an increase in the proportion of P. pussilum and P. micans (more than 30%). In August, the plankton
was again dominated by P. micans (more than 70%). Prorocentrum lima, a producer of domoic acid and
ciguatoxin, which cause diarrheal shellfish and ciguatera fish poisoning in humans, was found in the
stomachs of mussels only in August, its number in the stomachs of mussels averaged 40 cells/mussel
(1-2%). This species was not recorded in plankton (Figure 4-6).
In October and November, the indices of the number of cells in the stomachs were quite high: 3,600
cells/mussel and 10,100 cells/mussel, respectively. The dominant species were P. compressum (40-50%)
and P. micans (37-47%). In November, P. cordatum also made a significant contribution (10%) (Figure
4, 5). In October and November, plankton was dominated by P. micans - 40 and 80% of cells,
respectively (Figure 6).
Thus, P. compressum dominated in stomachs from February to May and in October, while its presence
in plankton was insignificant. In spring, the species P. balticum dominated in plankton. In summer, in
November and December, P. micans dominated in stomachs, while in water its density reached its
maximum values from August to December. In February and June, P. cordatum predominated in
plankton. The difference in the species composition and quantitative parameters of microalgae of the
genus Prorocentrum in samples of water and stomachs of mussels may indicate a different degree of
digestibility of the species of the studied genus of microalgae by bivalve mollusks.
0
1000
2000
3000
4000
cells/L
Prorocentrum
maximum
Prorocentrum
pusillum
Prorocentrum
balticum
Prorocentrum
scutellum
Prorocentrum
micans
Prorocentrum
cordatum
1 2 3 4 5 6 7 8 10 11 12
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Figure 4. The number of cells of dinophytes of the genus Prorocentrum in the
stomachs of mussels, cells/mussel.
Figure 5. Proportion of dinophytes of the genus Prorocentrum in the stomachs
of mussels.
Figure 6. Proportion of cells of microalgae of the genus Prorocentrum in
plankton.
Comparative analysis of the contribution of algae of the studied genus to the total number of
microalgae in the stomachs and bio-sediments of mussels showed a significant predominance of the
proportion of algae in feces compared to stomachs in January, March and April, July and August,
November and December (Figure 7). During periods of mass development of microalgae (April), this
may be caused by the dominance of the small-celled and well-digested coccolithophorids Emiliania
0
10000
20000
30000
40000
50000
cells/mussel
Prorocentrum lima
Prorocentrum
balticum
Prorocentrum
compressum
Prorocentrum
pusillum
Prorocentrum
micans
1 2 3 4 5 6 7 8 10 11 12
0%
20%
40%
60%
80%
100%
Prorocentrum lima Prorocentrum balticum
Prorocentrum compressum Prorocentrum pusillum
Prorocentrum micans Prorocentrum cordatum
1 2 3 4 5 6 7 8 10 11 12
month
0%
20%
40%
60%
80%
100% Prorocentrum
maximum
Prorocentrum
pusillum
Prorocentrum
balticum
Prorocentrum
scutellum
Prorocentrum micans
Prorocentrum
cordatum
Prorocentrum
compressum
1 2 3 4 5 6 7 8 10 11 12
month
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huxleyi. Thus, the plankton contained enough easily digestible food, while the Prorocentrum, which had
rather strong valves, were absorbed worse and were mostly excreted undigested. In June, against the
background of a high density of Prorocentrum in plankton, their density both in stomachs and in bio-
sediments was also high, as was the share in the total density of microalgae (over 50%), i.e. the mollusks
did not have time to digest a large number of cells, and many of them were excreted in the feces. In July,
the share of microalgae of the genus Prorocentrum in stomachs did not exceed 10%, while in feces it
was more than 40%. Perhaps, against the background of the high temperature of sea water (+ 24°C),
mollusks reduced the filtration rate, the rate of passage of food through the digestive tract slowed down,
and digestibility decreased. As a result, the Prorocentrum with their strong valves lingered longer in the
stomachs. At the same time, more easily digestible food was digested, and the Prorocentrum were mostly
excreted undigested. In August, despite the high number of Prorocentrum cells in the stomachs, their
proportion in feces was just over 5%. In August, plankton was dominated by large-celled diatoms, which
were inaccessible for nutrition of mussels, and due to the lack of food, the digestibility of Prorocentrum
was high.
Figure 7. Proportion (%) of algae of the genus Prorocentrum in relation to the
total number of microalgae cells in the stomachs of mussels and bio-sediments.
If we analyze the species composition of Prorocentrum in water, stomachs, and bio-sediments in
relative units (%), then we can assume the selectivity of mussels in feeding and digesting certain species.
It was noted that P. cordatum and P. micans predominate in plankton in winter, P. balticum and P.
cordatum in spring, P. cordatum, P. micans, P. balticum and P. pussilum in summer, and P. micans in
autumn (Figure 6). At the same time, P. compressum and P. micans dominate in stomachs throughout
the year (Figure 5). P. compressum was found in bio-sediments throughout the year, reaching almost
100% in April. In winter (except February), in summer and autumn, P. micans prevailed. In February,
March, and May, P. cordatum predominated (Figure 8).
Figure 8. Relative number (%) of cells of dinophytes of the genus
Prorocentrum in bio-sediments of mussels.
4. Discussion
There are two known hypotheses regarding the mechanisms underlying the increase in the proportion of
dinophytes in the stomachs of mussels:
1. mussels prefer this group of microalgae to diatoms;
0
50
100
%
1 2 3 4 5 6 7 8 10 11 12
month
feces
stomachs
0%
50%
100% Prorocentrum
balticum
Prorocentrum
pusillum
Prorocentrum
cordatum
Prorocentrum
micans
1 2 3 4 5 6 7 8 10 11 12
month
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2. dinophytes are much more resistant to extracellular digestion than diatoms and stay longer in
the intestine [15].
In our opinion, hypothesis 1 is unlikely. Although we cannot completely exclude it, since
dinoflagellates are round in shape, which makes them easier to consume. Hypothesis 2, in turn, is
confirmed by the results of this work.
P. balticum cells are small and, most likely, are well digested by mussels. Therefore, they are rarely
found in stomachs and feces, when from March to July they are found in plankton in the range of 100-
350 cells/l. The toxic species P. lima was recorded in stomachs in minimal amounts only in August. It
was not found in water and bio-sediments. P. compressum was found in stomachs in large quantities
from January to May. It was recorded in bio-sediments and pseudofeces, while its values in water were
minimal. In February, P. compressum was absent in water, and its content in stomachs was about 90%,
while P. cordatum dominated in water and bio-sediments. In April, the share of P. compressum in mussel
stomachs and bio-sediments was almost 100%, when the values in water reached only 20 cells/l. In
addition to the aforementioned species, P. cordatum, P. balticum, and P. maximum were recorded in the
water plankton in April. It is possible that P. compressum was poorly digested by mussels and was
slowly excreted from their stomachs in feces (Figure 5, 6, 8).
P. cordatum cells were found in almost all water and bio-sediment samples, and in stomachs they
were found in minimal amounts. In February, this species made up about 80% of all microalgae of this
genus per 1 liter of water, in bio-sediments - 70%, while in the stomachs, its number was only 47 cells
(when P. compressum was more than 3000 cells). It is possible that this type of dinophytes is poorly
absorbed by mussels and, at the same time, is well excreted from the stomachs as part of feces (Figure
5, 6, 8).
P. micans cells are found in large numbers in water, stomachs and bio-sediments in January and July
to December. In June, the number of cells of microalgae of this species in water is minimal, and in
stomachs and bio-sediments - about 70%, which indicates the worst digestibility in comparison with P.
balticum, the proportion of which was high in water and was almost absent in stomachs and bio-
sediments.
Thus, the emergence of selectivity in the phytoplankton diet of mussels is confirmed. Different
degrees of digestibility of different species of microalgae of the genus Prorocentrum are assumed, but
this issue requires further research.
5. Conclusion
1. In 2020, 8 following species of dinophytes of the genus Prorocentrum were recorded in
seawater, mussel stomachs and their bio-sediments: P. compressum, P. cordatum, P. micans, P.
scutellum, P. pusillum, P. balticum, P. maximum, P. lima. In three samples, from 1 to 3 types
were common. The highest occurrence (90-100%) was noted for three species - P. micans, P.
cordatum, and P. compressum.
2. Throughout 2020, two species of Prorocentrum, P. micans and P. compressum, dominated in
water plankton, stomachs, and bio-sediments. It can be assumed that these species are the
main food source of the genus Prorocentrum for bivalve mollusks. However, there are many
of these cells in feces. Perhaps, due to the dense valves, they are not well enough digested.
3. The digestibility of dinophytes of the genus Prorocentrum varies depending on the
presence/absence of easily digestible microalgae of other species in the seawater plankton.
4. P. balticum is best absorbed by mussels, as its cells are the smallest (9-17 µm in width and 7-
10 µm in length) and have a rounded shape. P. cordatum and P. compressum are assimilated
worse, but at the same time they are removed from the stomachs of mussels in different ways:
P. cordatum is faster than P. compressum. This may be caused by the difference in cell size: P.
compressum cells are much larger.
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Acknowledgements
The reported study was funded by the Russian Foundation for Basic Research and the Government of
Sevastopol (project number 20-44-925001), and also by the Ministry of Science and Higher Education
of the Russian Federation (grant no. 121030300149-0).
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Edulis L. from two populations: comparison with its food supply Journal of Shellfish Research
24(1) pp 5-14 https://doi.org/10.2983/0730-8000(2005)24[5:PCOTSC]2.0.CO;2
... From these, Cowan & Huisman (2015) chose P. bidens as an accepted name for D. compressa sensu Stein (1883), advocated by Josef Schiller himself, who later considered P. bidens to be a synonym of P. compressum (Schiller, 1933). It is worth noting that the scientific community did not follow this conclusion (or is not even aware of the problem) as since 2015, published reports of the species use without exception P. compressum but not P. bidens (Baytut et al., 2016;Caroppo et al., 2017;Mao et al., 2021;MucinoMárquez et al., 2018;Pospelova & Priimak, 2021). ...
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