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Biology Bulletin, Vol. 28, No. 1, 2001, pp. 95–102. Translated from Izvestiya Akademii Nauk, Seriya Biologicheskaya, No. 1, 2001, pp. 108–116.

Original Russian Text Copyright © 2001 by Ostroumov.

HYDROBIOLOGY

An Amphiphilic Substance Inhibits the Mollusk Capacity to Filter out Phytoplankton Cells from Water
S. A. Ostroumov
Moscow State University, Vorob’evy gory, Moscow, 119899 Russia
Received March 30, 1997

Abstract—The effect of synthetic anionic surface active substance (SAS) sodium dodecylsulfate (SDS, 4 mg/l) on the kinetics of water filtration by mussel Mytilus edulis was studied. A suspension of algae Isochrysis galbana was added to the vessel with the mussels, and their filtration activity was measured by counting the concentration of the algae cells in the experimental vessels. Algae concentration was measured every 30 min for an hour and a half. The inhibiting effect on the mollusk filtration rate (FR) was qualitatively described. After the first 30 min filtration at 4 mg/l initial SDS concentration, the cell density was 322% of the control. The inhibiting effect was observed later as well. Due to FR inhibition in the vessels with the above specified initial SDS concentration, the algae cell density was 6.4 and 14.7 times that of the control after 1 and 1.5 h, respectively. Thus, SAS SDS can decrease the natural capacity of aquatic ecosystems for self-purification and disturb other aspects of ecosystem functioning through inhibiting the filtration activity of mussels. The obtained data are discussed in the context of environment and hydrosphere protection from pollution.

Bivalves were repeatedly used in the studies of hydrosphere pollution. Among other aspects, the accumulation of pollutants, effects of metals, oil carbohydrates, pesticides and other xenobiotics on the filtration rate have been studied in mussels (e.g., Donkin et al., 1991, Donkin, 1994; Stephanson et al., 1995; Sericano et al., 1995). Organic toxicants affected the stability of lysosomal membrane in individual cells in addition to the effect on filtration rate (Wraige et al., 1994). Amphiphilic compounds—synthetic surface-active substances (SSAS)— pollute the environment and, particularly, aquatic and marine ecosystems (Lewis, 1991; Yablokov and Ostroumov, 1991; Singer et al., 1995). At the same time, SSAS are sometimes not included in top-priority pollutants (e.g., Scientific Committee on Toxicity and Ecotoxicity of Chemicals of European Economical Council; Bro-Rasmussen et al., 1994) or their pollution hazard is considered unclear. Bailey (1996) proposed that many SSAS are virtually nontoxic for aquatic organisms according to the tests developed by US Environment Protection Agency. Anionic and other SAS have negative or stimulating effects on some biological systems (e.g., Goryunova and Ostroumov, 1986; Nagel’ et al., 1987), including the effects of linear alkylbenzene sulfonate on mussels Mytilus galloprovincialis Lmk (Bressan et al., 1989) and M. edulis L. (Granmo, 1972). However, the effect of alkylsulfates on the capacity of mussel M. edulis to filter sea water remained unclear. In this work we studied kinetics of water biofiltration removing suspended particles by mussel M. edulis in the presence of anionic alkylsulfate SSAS—sodium dodecylsulfate (SDS). Here we demonstrate that alkylsulfate SSAS SDS at the above specified concentration

significantly affects the kinetics of phytoplankton removal from the aquatic environment by mussel M. edulis and state a list of environmental disturbances inducible by decelerated water biofiltration. MATERIALS AND METHODS Mussels were collected from coarse-sand bottom of Exmouth estuary at the south of England and kept in tanks with automatic flux and reflux imitation. The mollusks were manually cleared of attached barnacles. The animals were incubated in 2 l vessels with magnet stirrers. The vessels were kept in a temperature-controlled room at 16°C. Sea water was collected 15 km off the Plymouth coastline and filtered through 0.45 μm nitrocellulose WCN filters (Whatman, England). Sixteen animals were used in each experiment; eight were subjected to xenobiotic action and the other eight served as the control. SAS was added to the experimental vessels 1.5 h prior to the start of the experiment. SAS concentration specified in the tables and mentioned in the discussion is always the initial concentration at the moment of a given xenobiotic addition to the vessel. In addition to the eight vessels where 16 animals were kept in pairs (total wet weight of two mollusks was 16–20 g), the ninth vessel of the same volume (2 l) was used. The ninth vessel served as the control for algae suspension density in the absence of water biofiltration; equal volume of algae suspension was simultaneously added to all nine vessels. Biofiltration was measured by the decreased concentration of algae Isochrysis galbana Parke cells (strain CCAP 927/1). The strain was obtained from NERC Culture Collection of Algae and Protozoa (Dun-

1062-3590/01/2801-0095$25.00 © 2001 MAIK “Nauka /Interperiodica”

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Table 1. Time pattern of 0.5 mg/l sodium dodecylsulfate (SDS) effect on filtration of algae Isochrysis galbana cells by mussel Mytilus edulis Experimental vessels Time after the algae addition, min 5 number of cells in individual vessels with SDS per 0.5 ml 16544.3 14344.7 14905.7 17806.3 5234.0 3853.0 3856.0 8221.7 2146.0 2219.7 962.7 2414.3 661.7 714.0 370.0 1001.7 (A) mean number of cells (standard error) 15900.3 (788.3) Control vessels number of cells in individual vessels without SDS per 0.5 ml 16133.0 15117.7 16296.3 17563.7 4669.0 4078.7 5546.0 5379.0 2219.7 1276.7 2066.3 1749.7 903.0 514.3 804.0 673.0 (B) mean number of cells (standard error) 16277.7 (501.7)

35

5291.2 (1029.5)

4918 (338)

65

1935.7 (329.2)

1828 (208)

95

686.8 (129.4)

724 (84)

Note: The number of cells at the experiment start was 19533 per 0.5 ml. Numbers of cells per 0.5 ml were averaged for three measurements at Coulter counter. The mean indication of Coulter counter were below 200 for filtered sea water (prior to the algae addition). Dr. P. Donkin participated in this work.

staffnage Marine Laboratory, P.O. Box 3, Oban, Argyll, PA34 4AD, Scotland, UK). The algae were cultivated at constant aeration by air flow in 20 l spherical glass vessels at constant illumination. The medium for algae growth contained 1 ml nitrate-phosphate medium (solution 1) and 0.1 ml vitamins solution (solution 2) per 1 l filtered sea water. Nitrate-phosphate medium (solution 1) contained 4.5 g/l Na2EDTA; 100 g/l NaNO3; 33.6 g/l H3BO3; 20 g/l NaH2PO4 × 12 H2O; 0.36 g/l MnCl2 × 4 H2O; and 1.3 g/l FeCl3. It also included 1 ml microelements solution (solution 3) per 1 l. Microelements solution was added to the nitrate-phosphate medium after its sterilization and cooling. Microelements solution (solution 3) contained 2.1 g ZnCl2, 2 g CoCl2 × 6 H2O, 0.9 g (NH4)6Mo7O24 × 4 H2O, and 2 g CuSO4 × 5 H2O per 100 ml distilled water. If necessary, 2–3 drops of concentrated HCl were added for better dissolution. The vitamins solution (solution 2) contained 0.2 g Aneurin-HCl (vitamin B1, thiamin) and 0.1 g cyanocobalamin (vitamin B12) per 200 ml distilled water. The vitamin solution was kept in the dark in refrigerator. Active illumination was avoided during use.

Algae concentration was measured by a Coulter counter (Coulter Electronics, Industrial D model). The rate of filtration (FR, l/h) was calculated from formula: FR = V ( ln C 1 – ln C 2 )/ ( t 2 – t 1 ), where V is the water volume in the vessel (2 l), C1 is the cell concentration at the beginning of time interval, C2 is the cell concentration at the end of time interval, and (t2 – t1) is the duration of time interval, h. RESULTS AND DISCUSSION The rate of sea water filtration by mussels did not significantly change at the 0.5 mg/l initial SDS concentration (Table 1). For instance, after 1 h filtration the concentration of algae cells decreased approximately tenfold in both the control and experiment with 0.5 mg/l initial SDS concentration. The data presented in Table 1 also suggest that the method used to measure the biofiltration rate is relatively stable. However, in the case of 0.5 mg/l initial SDS concentration, variability of the data between measurements in individual vessels where the mussels were kept during the experiment increased according to the increase in the standard error (Table 1).
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Table 2. Time pattern of 4 mg/l sodium dodecylsulfate (SDS) effect on filtration of algae Isochrysis galbana cells by mussel Mytilus edulis Experimental vessels Control vessels Time after (A) mean number number of cells (B) mean number the algae addition, number of cells in individual vessels of cells in individual vessels of cells min with SDS per 0.5 ml (standard error) without SDS per 0.5 ml (standard error) 5 1644.7 16552 18179 17914.3 13370.7 9411.8 16116.2 12901 14114 7221 14889 9517.7 13162 4415.3 10960 5817 17272.5 (450.75) 14647.7 14670.3 15141.7 15050 4814.2 3967.2 3286.2 4038 2374.7 1603.3 1447 1698 772 563.3 508 515.7 14877.4 (127.57)

A/B × 100%

116.1

35

12949.9 (1376.1)

4026.5 (312.5)

321.6

65

11435.4 (1838.1)

1780.8 (204.6)

642.2

95

8588.6 (2074.4)

583 (63.3)

1473.2

Note: The number of cells at the experiment start was 17983.3 per 0.5 ml. Numbers of cells per 0.5 ml were averaged for three measurements at Coulter counter. The mean indication of Coulter counter were 301 for filtered sea water (prior to the algae addition). Dr. P. Donkin participated in this work.

A significant difference (over thrice) between the experiment and control was observed after the first 30 min incubation when the initial SDS concentration was increased to 4 mg/l. Table 2 demonstrates that experimental concentration of the cells after 1 h was over six times that of the control, which indicates a significant SAS-induced disturbance of normal mode of sea water biofiltration. Continuation of the experiment demonstrated an even more pronounced difference in the algae cell concentration between the control and experiment: it was over 14 times after 90 min filtration (Table 2). This agrees with the data on the effect of anionic SAS—linear alkylbenzene sulfonate (LAS)—on mussel growth (Bressan et al., 1989). Concentrations as low as 0.025 and 0.5 mg/l decreased the growth increment along the main axis of the shell; however, a significant period was required to reveal the effect—up to 70 days. No significant effect was observed within 30 experimental days. When the experiment continued for over 160 days, the increment decreased twice at 0.25 mg/l SAS. Decreased water filtration by the mollusks was observed under the influence of 1 mg/l LAS; however, 7 days of observation (rather than 1.5 h used in this work) were required to reveal the effect (Bressan et al., 1989). The use of different anionic SAS is another sigBIOLOGY BULLETIN Vol. 28 No. 1 2001

nificant distinction between our experiments and those of Bressan et al. (1989). The role of filter feeders in aquatic ecosystems has been repeatedly noticed (e.g., Zaika et al., 1990). Additional indication of it was obtained by studying the freshwater bivalve Hyridella menziesi in New Zealand. The mollusk population in Tuakitoto Lake filters the water volume of the whole lake each 32 h (Ogilvie and Mitchell, 1995). Ogilvie and Mitchell believe that mollusks are responsible for the low content of chlorophyll a (reflecting concentration of phytoplankton cells) in the lake water—only 10% of the value expected in this ecosystem from the established relationship are split between phosphorus and chlorophyll concentration. Biofiltering mussels exert a conditioning and controlling influence on the aquatic ecosystem. This influence can include several effects: (1) removal of algae and microbial cells from aquatic environment; (2) removal of organic particles subjected to biooxidation and increased biochemical oxygen consumption, an important index of water quality; (3) prevention of the decreased rate of water filtration by other filter feeders, which may be induced by the high content of nutrition particles in the water; (4) increased water transmittance and improved conditions for photosynthetic activity of

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Table 3. Certain causalities in the structure and function of aquatic ecosystems modifiable or disturbable by chemical pollution of the environment by SSAS and other pollutants Physicochemical or biotic factor (phenomenon) affecting another one specified in the next column Decreased consumption of phytoplankton biomass due to inhibited biofiltration by mollusks Stability of water column (depends on water mixing through activity of filter feeders) Penetration of UV radiation in the thickness of water (depends on water turbidity) Physicochemical or biotic factor (phenomenon, process) References or comments affecting another one specified in the previous column Disbalanse between formation and consumption of phytoplankton biomass can lead to accumulation of excessive biomass in Spring and oxygen deficit in spring–summer The level of water (un)stability affects species composition of phyto- and bacterioplankton; e.g., unstable water column favored certain cyanobacterium species Inhibition of primary and bacterial production; inhibition of bacterial destruction of organic matter Malone et al., 1996 Zhang, Prepas, 1996

Israel’ et al., 1995; Nielsen and Ekelund, 1995; Lindell and Edling, 1996 Penetration of UV radiation Natural UV irradiation favors photolysis of humic sub- Wetzel et al., 1995; stances of soluble organic matter and release of organic Bushaw et al., 1996 acids maintaining and stimulating bacterial growth Content of nutrition particles per Increased content of nutrition decreases the rate of water Roper and Hichey, 1995; volume unit (increases with inhibition biofiltration by other plankton and benthic filter feeders Chan, 1994 of biofiltration) (apart from mussels) Content of suspended particles in water Excessive content of algae cells and other particles Zaika et al., 1990 (depends on the activity of filter feeders) increases sedimentation of blues detritus; soil silting induces degradation of mussel populations and, possibly, other benthic filter feeders Content of suspended particles (depends Suspended particles in the water can inhibit activity of Gorbunova, 1988; Yamaon activity of filter feeders) plankton filtrators and corals su and Mizofuchi, 1989 Water transmittance (depends on Favors growth of bottom algae density and photosynthesis Steinman, McIntire, filtration activity of bivalves) 1987; Lowe, Pilesbury, 1995 Filtration activity of bivalves Control of population and species diversity of Lavrentyev et al., 1995 protozoans and other plankton species Active mixing of bottom layer of Active mixing of water can improve was her flow around The presence of actively water resulting from filtration other benthic animals and, thus, improve their oxygen filtered water zone is inactivity of bivalves supply conditions dicated by the presence of increased transmittance zone e.g., Zaika et al., 1990; Concentration of microalgae cells Microalgae control the content of hydrogen peroxide Batovskaya et al., 1988 in natural water Release of dissolved organic matter by Dissolved organic substances released by mussels can Reviewed in Zaika mussels (can decrease with decreased affect species composition and population of plankton et al., 1990 rate of filtration and nutrition) Decreased density of mussel population Decreased density of zoobenthos leads to decreased Koyama, 1993 resulting from decreased rate of nutrition formation of gas in detritus (including N2 and CH4) and growth Formation of pseudofaeces by bivalves Pseudofaeces accumulate and remove organic and Palaski, Booth, 1995 mineral toxicants from water layer Formation of pseudofaeces Activity of microbial eggs enzymes is increased in Sala, Gude, 1993 and accumulation of detritus the areas of detritus accumulation Formation of pseudofaeces Segmentation of pseudofaeces increases arrival Agrees with numerous and accumulation of organic matter in detritus publications on the role and consumption of pollutants by the sediments of organic matter content in bottom sediments for consuming pollutants from water SSAS-induced deceleration Decreased conduct between mussels and water and subse- Inevitable consequence of water filtration quent decreased accumulation of other pollutants is apparent decrease in bioaccumulation of various pollutants
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AN AMPHIPHILIC SUBSTANCE INHIBITS THE MOLLUSK CAPACITY Table 4. Certain data on water biofiltration by hydrobionts and its disturbance Organisms Mussel Mytilus edulis Aquatic systems Data on biofiltration 1.5–2.3 l/h per mussel References Original data

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Estuary at the south of England (Devon) Bivalves Dnepr–Bug liman, northern coast of Black Sea To bivalves Hyridella menziesi Tuakitoto Lake, New Zealand Black Sea mussels with community density about 100 sp/m2 Filtering plankton crustaceans To plankton crustaceans To plankton crustaceans All plankton filter feeders Mussels Mytilus edulis Cladocerans Ceriodaphnia dubia, rotifers Brachionus and plicatilis, and ciliates Paramecium aurelia Bottom layer of water (Black Sea) 3 m thick Oligotrophic reservoir Mesotrophic reservoir Eutrophic reservoir Upper part (0–500 m) of the ocean Experimental systems Experimental systems

16.5 volumes of the liman are filtered Alekseenko and during the vegetation period Alexandrova, 1995 100% lake volume is filtered each 32 h Ogilvie, Mitchell, 1995 According to the estimates, about Zaika et al., 1990 20% suspension is removed from this layer within 6 h 5–60% water volume per day Gutel’makher, 1986 (at biomass 0.2–1.0 mg/l) 15–50% water volume per day Gutel’makher, 1986 (at biomass 1–2 mg/m) 5–90% water volume per day Gutel’makher, 1986 (at biomass 2–6 mg/l) It is filtered for about 20 days Bogorov, 1969 SSAS inhibited biofiltration Chlorpyriphos (Dursban), mercury, and cadmium decreased the rate of food consumption Original data Juchelka, Snell, 1995

aquatic organisms; (5) prevention of excessive sedimentation of loose detritus and, thus, the prevention of bottom silting (inducing degradation of mussel colonies); (6) removal of turbid particles of the bottom sediments with possible toxicity; (7) acceleration of detritus formation and accumulation of organic matter in the bottom sediments; and (8) enhanced carbon transfer from atmosphere to detritus. All these factors may affect other important indices of aquatic ecosystems, for instance, the transmittance and turbidity of water affect the penetration of biologically active UV radiation, which has various effects, including the inhibition of primary production and the bacterial destruction of organic matter (e.g., Izrael’ et al., 1995). On the other hand, UV radiation can favor the photolysis of dissolved organic matter including humic and fulvic acids (Wetzel et al., 1995). UV radiation can release organic acids (Wetzel et al., 1995) and biologically available nitrogen compounds (Bushaw et al., 1996) from dissolved organic matter, which may be utilized by bacteria and stimulate their growth. Hence, the changes in UV light penetration in water column can affect the balance in the algae–bacteria community structure. A complex network of interactions and mutual influences of various physicochemical and biotic indices which can be affected by SSAS- or other induced pollutants decrease the rate of water biofiltration by mollusks (Table 3).
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The possible initiation of catastrophic consequences for the ecosystems by disturbed natural water biofiltration makes the new data on water pollution influence on efficient water biofiltration by mollusks more interesting. According to our experiments, two mussels with a total weight of about 17 g (wet weight with the shell) filtered 2 l water for 1 h. The density of the mussel community can reach 1–2 kg/m2 on silt or even more on the rocks: 8 and over 45 kg/m2 in surfy and low-surfy habitats, respectively (Zaika et al., 1990). It follows that the total capacity of the community for water filtration can reach 100 l and much more over m2/h. Certain data describing the rate of water biofiltration by various benthic and plankton organisms are presented in Table 4. Disturbance of this active process can significantly decrease the quality of water, disturb various structural and functional aspects of aquatic ecosystems (some of them are mentioned in Table 3), and, hence, degrade the habitat for many species of aquatic ecosystems. Note another dangerous aspect of disturbed water biofiltration by benthic organisms: their activity favoring the formation of sedimenting pellets (faeces and pseudofaeces) contributes to the geochemically significant flow of carbon from the atmosphere to detritus. The total volume of this flow is quite significant. For instance, Jonsson and Carman (1994) estimated that, due to organic matter sedimentation, its content in the Baltic Sea soil increased 1.7 times from 1920 to 1980,

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while, starting from late 1980s, it increased by 9 g C/m2 a year. The process of carbon burial in the sea bottom is one of the main processes opposing an anthropogenic increase in the atmospheric content of carbon dioxide (consumption of fossil fuel). Hence, filter feeders contribute to counteracting possible global warming due to the accumulation of carbon dioxide. It follows that the inhibition of filter feeder activity due to anthropogenic stress by pollutants is also dangerous in relation to global warming. Our data on the decreased physiological activity of mussels induced by sublethal SAS concentrations agrees with the data on effect of other pollutants—heavy metals. Sublethal concentrations of copper (0.1 mg/liter) and zinc (1 mg/liter and more) proved to decrease the heart activity of bivalve Scrobicularia plana (Akberali and Trueman, 1985). Possible SSAS action on the larval stage of bivalve development should not be missed. Our previous experiments on mollusk Mercenaria mercenaria larvae demonstrated that sublethal SSAS concentrations induced a behavioral response in the larvae—they stopped soaring in the water and segmented to the bottom of the tank. The dangerous effect of pollutants on the early stages of hydrobiont ontogenesis outlined by Yablokov and Ostroumov (1985) has been confirmed by studies of the embryos and larvae of bivalves (Malakhov and Medvedeva, 1991). For instance, embryos of various bivalves outperformed adult specimens by 2–3 orders of magnitude by sensitivity to the toxic effect of heavy metals (Malakhov and Medvedeva, 1991). Disturbing the normal chain of events from the onset of gametogenesis to larvae attachment and subsequently decreasing the rate of nutrition and growth of the attached specimen inevitably contributes to population reproduction and a decrease in their important ecosystem function—water biofiltration. Due to the important role of Mytidae in the maintenance of marine ecosystems, one cannot avoid concluding that there is a sharp decrease in their abundance in polluted ecosystems (Zaika et al., 1990). Biomass of M. adriaticus in the bottom ecosystems of Novorossisk Bay decreased over 30 times from 1960 to 1979. The top annual population of Mytidae larvae observed at the exit of Sevastopol Bay decreased approximately tenfold in just four years (1981–1985) (Zaika et al., 1990). Another ecological process—mineralization of xenobiotics by microorganisms—is quite significant in aquatic ecosystems. This aspect of ecosystem self-purification can also be disturbed by SSAS. The experiments on microcosms demonstrated that seven various SSAS inhibited the mineralization of phenanthren by microorganisms that destroy polyaromatic carbohydrates (Tsomides et al., 1995). Hence, summation of the SSAS biological effects of various types can significantly disturb the natural capacity of marine ecosystem for self-purification.

Here we used SDS as an SSAS affecting the mussels. We propose that other SSASs can have similar effect on mussels and inhibit water filtration. Thus, the obtained and published data (Ostroumov and Tret’yakova, 1990; Uoterberi and Ostroumov, 1994; Fisher et al., 1996; Khristoforova et al., 1996) corroborate the conclusion (Ostroumov, 1986, 1990, 1991; Yablokov and Ostroumov, 1983, 1985, 1991) show that SSAS are more dangerous pollutants than previously considered. This should be taken into account when fulfilling requirements of Ecological Law of Russian Federation, including the Federal Law on Ecological Examination. Note that information on the influence of various anthropogenic substances on mollusk capacity for water filtration and purification has another applied aspect, since mollusks can function as a component of artificial ecosystems—a unit of lifesupport systems for long-term space investigations. The obtained data demonstrate that the presence of SSAS in the aquatic medium of life-support system can significantly decelerate its filtration and purification by bivalves. ACKNOWLEDGMENTS We thank Dr. P. Donkin and F. Staff (Plymouth Marine Laboratory) for participation in the work, Prof. J. Widdows, Prof. V.V. Malakhov, O.F. Filenko, A.G. Dmitrieva, G.D. Lebedeva and others at Moscow State University and Maryland University for discussion. This work was supported by EERO, IBG, and Open Society Support Scheme (RSS grant no. 1306/1999). Early experiments on the bivalves were carried out in the State University of New York and supported by International Programs of this University. REFERENCES
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2001