Hydrobiologia 500: 341344, 2003. K. Martens (ed.), Aquatic Biodiversity. 2003 Kluwer Academic Publishers. Printed in the Netherlands.

341

Studying effects of some surfactants and detergents on lter-feeding bivalves

S. A. Ostroumov
Moscow State University, Vorobevy gory, Moscow, 119899 Russia
Received 29 April 2003; in revised form 30 April 2003; accepted 30 April 2003

Abstract Effects of several surfactants and chemical mixtures on marine bivalves were studied. An anionic surfactant, sodium dodecylsulphate (SDS), and a cationic surfactant, tetradecyltrimethylammonium bromide (TDTMA), inhibited the ltering activity of oysters (Crassostrea gigas). Similar effects were exhibited by some chemical mixtures that included surfactants. Those mixtures inhibited the ltering activity of Crassostrea gigas and Mytilus galloprovincialis. The new results are in agreement with the authors previous experiments, where a number of xenobiotics and/or pollutants inhibited the ltering activity of several species of marine and freshwater bivalves, e.g., it had been shown that SDS inhibited ltering activity of Mytilus edulis (e.g., Ostroumov, 2000c, 2001a). This experimental approach is helpful in assessment of environmental hazards from man-made chemicals that can contaminate marine systems. Abbreviations: LD liquid detergent; SDS of sodium dodecyl sulfate; TDTMA tetradecyltrimethylammonium bromide; SD synthetic detergent Introduction It has previously been shown that some amphiphilic chemicals (surfactants) and surfactant-containing chemical mixtures affect ltering activity of mussels (e.g., Ostroumov et al., 1997, 1998). Taking into account the ecological importance of this effect (e.g., Ostroumov, 1998, 2000a,b,c), it was of interest to broaden the study of this issue and to determine whether some other organisms important for aquaculture may be affected by those compounds. It should be underlined that bivalves are among the most important cultured marine species. The average annual production of marine bivalves grown in aquaculture signicantly exceed that of marine sh (9.7-fold) and crustaceans (4-fold) grown in mariculture (World Resources. . . , 1994). Owing to the importance of mariculture, it is necessary to determine the factors that may disturb some physiological activities of objects grown in mariculture (including bivalves) and deteriorate their living and culturing conditions. The aim of this study was to determine whether some surfactants and surfactant-containing chemical mixtures inhibit the ltering activity of the important bivalve species grown in mariculture, namely the oyster Crassostrea gigas Thunberg. The experiments were performed according to the previously described procedure (Ostroumov et al.,1998; Ostroumov, 2001a, b) with some slight modications. The ltration rate was determined by the decrease in the optical density of the incubation medium at 550 nm as a result of the removal (due to ltration) of Saccharomyces cerevisiae cells that were preliminarily added to the marine water. The concentration of S. cerevisiae cells (SAF-Moment, S.I. Lesaffre, 59703 Marcq-France) was 100 mg l1 (dry weight). The temperature is indicated in the tables. The optical density was measured using the SF-26 LOMO spectrophotometer, the optical way length was 10 mm. The average weight of the oysters and the volume of the incubation medium are indicated in the notes to the tables. The oysters were grown at the mariculture farm of the Institute of South Sea Biology

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Table 1. Inhibition of the C. gigas ltering activity and uptake of unicellular organisms from water by TDTMA (0.5 mg l1 ) Measurement, No. Incubation time, min Optical density at 550 nm Variant A Variant B Variant C (control, S. (control, without (with cerevisiae alone, TDTMA) TDTMA) without bivalves and TDTMA) 0.080 0.043 0.018 0.194 0.148 0.137 0.307 0.305 0.303 B/A, %

1 2 3

5 11 20

242.5 344.2 761.1

Note: Each experimental beaker contained 10 one-year-old bivalves. Total wet weight of the bivalves with shells was 47.3 g and 55.2 g in beakers A and B, respectively. Incubation temperature was 27 C. The volume of the incubation medium was 500 ml. Table 2. Inhibition of the Crassostrea gigas ltering activity and uptake of unicellular organisms from water by SDS (0.5 mg l1 ) Measurement, No. Incubation time, min Optical density at 550 nm Variant A Variant B Variant C (control, S. (control, without (with cerevisiae alone, SDS) SDS) without bivalves without SDS) 0.117 0.074 0.048 0.035 0.181 0.156 0.111 0.074 0.176 0.179 0.174 0.164 B/A, %

1 2 3 4

4 12 20 29

154.70 210.81 231.25 211.43

Note: Each experimental beaker contained 16 one-year-old bivalves. The total wet weight of the bivalves with shells was 23.5 g and 23.6 g in beakers A and B, respectively. Incubation temperature was 23 C. The volume of the incubation medium was 250 ml. Table 3. Some chemicals that have an adverse effect on the ltering activity of the bivalves Measurement Chemical (described in the text) SDS TDTMA SD1 (L) LD1 (E) LD2 (F) SD2 (I) SDS SDS Triton X-100 Triton X-100 TDTMA Organism Reference

1 2 3 4 5 6 7 8 10 11 12

C. gigas C. gigas M. galloprovincialis, C. gigas M. galloprovincialis, C. gigas M. galloprovincialis, C. gigas M. galloprovincialis M. edulis M. galloprovincialis M. edulis Unio tumidus U. pictorum

New data New data New data New data New data New data Ostroumov et al. (1997) Ostroumov (2000c) Ostroumov et al. (1998) Ostroumov (2001a) Ostroumov (2001a)

(National Academy of Sciences of Ukraine) and the State Oceanarium of Ukraine. We analysed some effects of sodium dodecyl sulfate (SDS), tetradecyltrimethylammonium bromide

(TDTMA), several synthetic detergents (SDs), and liquid detergents (LDs) on bivalves. In this paper, the following denotations are used: SD1(L), Lanzaautomat (Benckiser); SD2(I), IXI Bio-Plus (Cussons);

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Table 4. Filtration of water by bivalves (some examples) Organism and measurement unit Mytilus galloprovincialis, % of suspension removal from the 3-m near-bottom water layer during 6 h Values measured Comments, references

20%

The measurement and estimates refer to the shelf ecosystem of the northern Black Sea, taking into attention the real size structure of mussel populations (Zaika, 1992) The Hudson River estuary (Strayer et al., 1999) Rivers and lakes of North America (Strayer et al., 1999), a range of various data (Strayer et al., 1999), during the summer vegetation period

Unioniidae, the volume ltered by the bivalves of 1 m2 of the bottom, per day Dreisseniidae, the volume ltered by the bivalves of 1 m2 of the bottom, per day Dreisseniidae,% of the ltered volume of water column per day

0.14 m3 m2 day1

0.15 m3 m2 day1

70125%

LD1 (E), dish washing liquid E (Cussons International, Ltd.); and LD2 (F), dish washing liquid Fairy (Procter & Gamble, Ltd.). We discovered that a typical cationic surfactant containing a tertiary ammonium group, TDTMA, inhibited the ltering activity of C. gigas (Table 1). The optical density of the cell suspension differed from the control more than twofold 5 min after the addition of TDTMA. The optical density differed from the control more than sevenfold (by the factor 7.6) 20 min after the addition of the cationic surfactant. SDS is an important anionic surfactant contained in numerous industrial mixtures that contaminate water bodies. We discovered that SDS also inhibits the ltering activity of C. gigas: after 1229 min of incubation with SDS, the concentration of the cell suspension differed from the control more than twofold (Table 2). Similar results were obtained when some surfactantcontaining mixtures were tested (Table 3). To enable the comparison and to provide a more comprehensive vision of the problem, Table 3 includes the data obtained not only with the oysters, but also when studying some other bivalves important for mariculture, namely, the mussels Mytilus edulis and Mytilus galloprovincialis. All experiments showed that the decrease in water turbidity due to the ltration by the bivalves was associated with the formation of pseudofecal pellets,

which precipitate onto the bottom. When the ltration rate reduced as a result of the effect of the surfactant or surfactant-containing mixture, the amount of pellets decreased. We would like to emphasise two points concerning the results of this study. First, the inhibitory effects demonstrated in this study were observed at the surfactant concentration of 0.5 mg l1 or higher, which was actually detected in some polluted aquatic ecosystems (Review on. . . 1976). Second, the rate of water ltration by invertebrates is relatively high (Alimov, 1981; Zaika, 1992; Dame, 1996; Strayer et al., 1999; and Table 4). The ltration of water has some conditioning effect on aquatic ecosystems (Alimov, 1981; Ostroumov, 2001a, 2002). The decrease in this effect and ltering activity has a signicant impact on the state of ecosystems. The biomass of mussels in natural marine habitats in the Black Sea exceeds 1 kg m2 (Zaika, 1992). The biomass of bivalves in some marine habitats was found to be up to over 10 kg m2 (with shells) (Ostroumov, 2001a, 2002). In mariculture, the biomass of bivalves per unit area may be higher, and the effect of ltering activity and its alteration on the ecosystem can be even more pronounced. Parameters, characteristics, and components of aquatic ecosystems that may be signicantly inuenced by the ltering activity of the bivalves include microzooplankton (the number and composition), macrozooplankton, phytoplankton,

344 bacterioplankton, suspended solids, dissolved inorganic nitrogen (DIN), transparency (Secchi discs), and soluble reactive phosphorus (SRP) (Dame, 1996; Ostroumov et al., 1997; Strayer et al., 1999; Ostroumov, 2000c). The threat of a disturbance of the ltering activity should be taken into consideration when the evaluation is made of the ecological hazard of the chemical pollution of aquatic ecosystems (Yablokov, Ostroumov, 1985, 1991; Ostroumov, 1986, 2001).
ekologhicheskoj opastnosti antropoghennykh vozdejstvij na biotu: poiski sistemy). Doklady Biological Sciences 371: 204206 (the Russian edition: Dokl. Akad. Nauk 371: 844846). Ostroumov, S. A., 2000b. The concept of aquatic biota as a labile and vulnerable component of the water self-purication system (Kontzeptzija vodnoi bioty kak labilnogo i ujazvimogo zvena sistemy samoochishchenija vody). Doklady Biological Sciences 372: 286289 (the Russian edition: Dokl. Akad. Nauk). Ostroumov, S. A., 2000c. Biologicheskie effekty poverkhnostnoaktivnykh veshchestv v svyazi s antropogennymi vozdeistviyami na biosferu (Biological Effects of Surfactants as Related to Anthropogenic Impact on the Biosphere), Moscow: MAX-Press. 116 pp. Ostroumov, S. A., 2001a. Biological Effects of Surfactants on Organisms. MAX Press, Moscow. 334 p. Ostroumov, S. A., 2001b. Effects of amphiphilic chemicals on marine organisms lter-feeders (Vozdeistvie amlnykh veshchestv na morskikh gidrobiontov-ltratorov). Doklady Biological Sciences (Doklady Akademii Nauk). 378: 283285. Ostroumov, S. A., 2002. Inhibitory analysis of top-down control: new keys to studying eutrophication, algal blooms, and water self-purication. Hydrobiologia. 469: 117129. Ostroumov, S., P. Donkin & F. Staff, 1997. Inhibition by the anionic surfactant, sodium dodecyl sulphate, of the ability of mussels Mytilus edulis to lter and purify the sea water (Anionnoje poverkhnostno-aktivnoje veshchestvo inghibirujet sposobnost midij ltrovat i ochishchat morskuju vodu). Vestnik Moskovskogo Universiteta. Ser. 16. Biologija. (Bulletin of Moscow University. Ser. 16. Biology) 3: 3036. Ostroumov, S. A., P. Donkin & F. Staff, 1998. Filtration inhibition induced by two classes of synthetic surfactants in the bivalve mollusc (Narushenije ltracii dvustvorchatymi molluskami pod vozdejstvijem poverkhnostno-aktivnykh veshchestv dvukh klassov). Doklady Biological Sciences (Dokl. Akad. Nauk) 362: 574576. Review on the Pollution Status of the Black Sea and the Sea of Azov, 1976. (Obzor sostoyaniya zagryazneniya Chernogo i Azovskogo morei), Sevastopol. 180 pp. Strayer, D., N. Caraco, J. Cole, S. Findlay & M. Pace, 1999. Transformation of freshwater ecosystems by bivalves. Bioscience 49: 1927. World Resources 19941995, 1994. New York: Oxford Univ. Press. 404 pp. Yablokov, A. V. & S. A. Ostroumov, 1985. Levels of Living Nature Conservation (Urovni Ohrany Zhivoi Prirody). Nauka Press, Moscow. 176 pp. Yablokov, A. V. & S. A. Ostroumov, 1991. Conservation of Living Nature and Resources: Problems, Trends, Prospect. Springer Verlag, Berlin, Heidelberg, New York. 271 pp. Zaika, V. E., 1992. Long-term Changes in Zoobenthos of the Black Sea (Mnogoletnie Izmeneniya Zoobentosa Chernogo Morya). Naukova Dumka, Kiev. 247 pp.

Acknowledgements We are grateful to G.E. Shulman, G.A. Finenko, Z.A. Romanova, A.A. Soldatov, and other researchers at INBYuM NANU for their help. The bivalves were grown by V.I. Kholodov, A.V. Pirkova, and A.Ya. Stolbov (INBYuM and the State Oceanarium NANU). We thank V.D. Fedorov, M.E. Vinogradov, A.F. Alimov, V.V. Malakhov, E.A. Kriksunov, A.S. Konstantinov, A.O. Kasumyan, A.P. Kuznetsov, researchers at the Moscow State University and Russian Academy of Sciences, participants of the series of conferences on Aquatic Ecosystems and Organisms (Moscow, 1999 2002), members of ALSO and Consortium for Aquatic Sciences, and other colleagues for the discussion. This study was partly supported by RSS, Open Society Foundation (project no. 1306/1999).

References
Alimov, A. F., 1981. Functional Ecology of Freshwater Bivalves (Funktzionalnaja Ekologija Presnovodnykh Dvustvorchatykh Molluskov). Nauka press, Leningrad. 248 pp. Dame, R. F., 1996. Ecology of Marine Bivalves. An Ecosystem Spproach. CRC Press, Boca Raton. 277 pp. Ostroumov, S. A., 1986. Introduction to Bio-Chemical Ecology. (Vvedenie v Biohimicheskuju Ekologiju). Moscow University Press, Moscow. 176 pp. Ostroumov, S. A., 1998. Biological ltering and ecological machinery for self-purication and bioremediation in aquatic ecosystems: towards a holistic view. Rivista di Biologia/ Biology Forum. 91: 247258. Ostroumov, S. A., 2000a. Criteria of ecological hazards due to anthropogenic effects on the biota: searching for a system (Kriterii