2001.Effect.of.Amphiphilic.Chemicals.on.Filter-Feeding.Marine.Organisms.–Doklady.Biol.Sci.v.378p248–250
Ostroumov S. A. Effect of Amphiphilic Chemicals on Filter-Feeding Marine Organisms. - Doklady Biological Sciences, 2001, Vol. 378, p. 248–250
Published: Ostroumov S. A. Effect of Amphiphilic Chemicals on Filter-Feeding Marine Organisms. - Doklady Biological Sciences, 2001, Vol. 378, p. 248–250. Translated from Doklady Akademii Nauk, Vol. 378, No. 2, 2001, pp. 283–285. Original Russian Text Copyright © 2001 by Ostroumov.ISSN 0012-4966 (Print) 1608-3105 (Online); DOI 10.1023/A:1019270825775
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Microsummary: For the first time, oysters were used as the test-organisms in bioassay of synthetic surfactants and detergents. The new data revealed a novel type of hazard to mariculture. New negative effects of surfactants and chemical mixtures on water filtering activity of Crassostrea gigas were discovered.
The abstract, key words, full text and Addendum (with references of recent relevant publications) are below.
ABSTRACT: Effects of amphiphilic chemicals on filter-feeding marine organisms. S.A.Ostroumov
For the first time, oysters were used as the test-organisms in bioassay of synthetic surfactants. As surfactants are one of key components of water pollution from municipal waste waters, from ports and ships, the new data revealed a novel type of hazard to mariculture of oysters. New negative effects of several amphiphilic chemicals (surfactants) and chemical mixtures on oysters and other marine bivalves were discovered. An anionic surfactant, sodium dodecylsulphate (SDS), and a cationic surfactant, tetradecyltrimethylammonium bromide (TDTMA) inhibited water filtering activity of oysters (Crassostrea gigas). Similar effects were exhibited by some chemical mixture products (detergents) that included surfactants as components of the mixtures. Those mixture products inhibited filtering activity by Crassostrea gigas and Mytilusgalloprovincialis. The mixture products tested were: the SD1(L), Lanza-automat (Benckiser); SD2(I), IXI Bio-Plus (Cussons); LD1 (E), dish washing liquid E (Cussons International, Ltd.); and LD2 (F), dish washing liquid Fairy (Procter & Gamble, Ltd.). The new results are in agreement with the author’s previous experiments, where a number of xenobiotics and/or pollutants inhibited the filtering activity of several species of marine and freshwater bivalves. The filtering activity contributes to improving water quality. This experimental approach is helpful in assessment of environmental hazard from man-made chemicals that contaminate marine ecosystems.
KEY WORDS: mariculture of oystersCrassostrea gigas, surfactants, detergents, filtering activity, Mytilusgalloprovincialis, xenobiotics, pollutants, bivalves, assessment of environmental hazards, marine ecosystems
Effect of Amphiphilic Chemicals on Filter-Feeding Marine Organisms
S. A. Ostroumov
Presented by Academician M.E. Vinogradov October 9, 2000;
Received October 17, 2000;
Moscow State University, Vorob’evy gory, Moscow, 119991 Russia;
It has been previously shown that some amphiphilic chemicals (surfactants) and surfactant-containing chemical mixtures affect filtering activity of mussels [1, 2]. Taking into account the ecological importance of this effect [3–6], it was of interest to broaden the view of this problem and to determine whether organisms important for aquiculture may be affected by these compounds. Bivalves are the most important cultured marine species. It was shown that the average annual production of marine bivalves grown in aquaculture significantly exceed that of marine fish (9.7-fold) and Crustaceans (4-fold) grown in mariculture [7]. Owing to the importance of mariculture, it is necessary to determine the factors that may disturb physiological activity of objects grown in mariculture (including bivalves) and deteriorate their living and culturing conditions.
The goal of this study was to determine whether surfactants and surfactant-containing chemical mixtures inhibit the filtering activity of bivalves grown in mariculture, particularly oysters Crassostrea gigas Thunberg (= Ostrea laperousi auct.).
The experiments were performed according to the previously described procedure [2] with some modifi- cations. The filtration rate was determined by the decrease in optical density of the incubation medium at 550 nm as a result of removal (due to filtration) 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/l (dry weight). The temperature is indicated in the tables. The optical density was measured using a 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 (National Academy of Sciences of Ukraine) and the State Oceanarium of Ukraine.
We analyzed the effects of sodium dodecyl sulfate (SDS), tetradecyltrimethylammonium bromide (TDTMA), several synthetic detergents (SDs), and liquid detergents (LDs). In this paper, the following denotations are used: SD1(L), Lanza-automat (Benckiser); SD2(I), IXI Bio-Plus (Cussons); 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 filtering activity of C. gigas (Table 1). The yeast suspension concentration differed from the control more than twofold and more than sevenfold 5 and 20 min after the addition of TDTMA, respectively.
Table 1. Inhibition of the C. gigas filtering activity and uptake of unicellular organisms from water by TDTMA (0.5 mg/l)
Measurement / Incubation
time, min / Optical density at 550 nm / B/A, %
variant A (without TDTMA) / variant B (with
TDTMA) / variant C (S. cerevisiae alone, without bivalves and TDTMA)
1
2
3 / 5
11
20 / 0.080
0.043
0.018 / 0.194
0.148
0.137 / 0.307
0.305
0.303 / 242.5
344.2
761.1
Note: Each experimental vessel contained 10 one-year-old bivalves. Total wet weight of the bivalves with shells was 47.3 g and 55.2 g in vessels A and B, respectively. Incubation temperature was 27C. The volume of the incubation medium was 500 ml.
Table 2. Inhibition of the C. gigas filtering activity and uptake of unicellular organisms from water by SDS (0.5 mg/l)
Measurement / Incubation
time, min / Optical density at 550 nm / B/A, %
variant A
(without SDS) / variant B (with
SDS) / variant C (S. cerevisiae alone, without bivalves and TDTMA)
1
2
3
4 / 4
12
20
29 / 0.117
0.074
0.048
0.035 / 0.181
0.156
0.111
0.074 / 0.176
0.179
0.174
0.164 / 154.70
210.81
231.25
211.43
Note: Each experimental vessel contained 16 one-year-old bivalves. Total wet weight of the bivalves with shells was 23.5 g and 23.6 g in vessels 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 filtering activity of the bivalves
Measurement / Chemical (described in the text) / Organism / Note
1 / SDS / C. gigas / New data
2 / TDTMA / C. gigas / New data
3 / SD1 (L) / M. galloprovincialis, C. gigas / New data
4 / LD1 (E) / M. galloprovincialis, C. gigas / New data
5 / LD2 (F) / M. galloprovincialis, C. gigas / New data
6 / SD2 (I) / M. galloprovincialis / New data
7 / SDS / M. edulis / [1]
8 / SDS / M. galloprovincialis / [6]
10 / Triton X-100 / M. edulis / [2]
Table 4. Filtration of water by mollusks (examples)
Organism and
measurement unit / Values / Notes, references
Mytilus galloprovincialis, % of suspension
removal from a 3-m benthic water layer for 6 h / 20 / The measurement and estimates refer to the shelf ecosystem of the northern Black Sea with regard for the real size structure of mussel population [10]
Unioniidae, Volume filtered, m3 m–2 day –1 / 0.14 / The Hudson River estuary [11]
Dreisseniidae, m3 m–2 day–1 / 0.1–5 / Rivers and lakes of North America [12], the main range of data
Dreisseniidae, % of the filtered volume of water column per day / 70–125 / Rivers and lakes of North America [12], during the summer vegetation period
SDS is an important anionic surfactant contained in numerous industrial mixtures that contaminate water bodies. We discovered that SDS also inhibits the filtering activity of C. gigas : after 12–29 min of incubation with SDS, the concentration of the yeast suspension differed from the control more than twofold (Table 2).
Similar results were obtained for surfactant-containing mixtures (Table 3). To enable the comparison and to provide a comprehensive idea of the problem, Table 3 summarizes the data obtained not only on oysters, but also on other bivalves important for mariculture, namely, mussels Mytilus edulis and Mytilus galloprovincialis .
All experiments showed that the decrease in water turbidity due to filtration by the bivalves is associated with the formation of pseudofecal pellets, which precipitate onto the bottom. When filtration rate reduced as a result of the effect of a surfactant or surfactant-containing mixture, the pellet amount decreased.
Two points concerning the results of this study should be noted. First, the inhibitory effects demonstrated in this study were observed at surfactant concentrations of 0.5 mg/l or higher, which are actually detected in aquatic ecosystems [8].
Second, the rate of water filtration by invertebrates is relatively high ([9–12] and Table 4), which has a constant conditioning effect on aqueous environment. The decrease in this effect and filtering activity has a significant impact on the state of ecosystems. The biomass of mussels in natural marine habitats can exceed 1 kg/m 2[10]. The biomass of unionid bivalves inhabiting the Hudson River estuary is 5–100 g/m 2(dry weight without shells) [11]. In mariculture, the biomass of bivalves per unit area may be higher, and the effect of filtering activity and its alteration on the ecosystem can be even more pronounced. Parameters, characteristics, and components of aquatic ecosystems that may be significantly influenced by the filtering activity of the bivalves include microzooplankton (the number and composition), macrozooplankton, phytoplankton, bacterioplankton, suspended solids, dissolved inorganic nitrogen (DIN), transparency (Secchi discs), and soluble reactive phosphorus (SRP) [1, 6, 12].
The threat of disturbance of the filtering activity as a result of chemical pollution of water should be taken into consideration to ensure effective sustainable use of aquatic bioresources and evaluation of the ecological hazard of aquatic-system pollution [13–15].
ACKNOWLEDGMENTS
We are grateful to G.E. Shul’man, 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 State Oceanarium NANU). We thank 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 conference on Aquatic Ecosystems and Organisms (Moscow, June 23–24, 2000), 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).
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ADDENDUM
(added after publishing this paper, when it was put at the website)
Additional relevant bibliography is given below.
After publishing this paper the author did several new research projects that confirmed the main conclusions.
It was discovered that the inhibition of water filtration by surfactants was a typical response of not only oysters but a broad spectrum of filter –feeders including also freshwater bivalves [ 1 ], rotifers [24 ] and crustaceans [ 34 ]. Filtration activity of invertebrates is a component of the contribution of aquatic biota to water self-purification. It is a part of ecosystem services towards maintaining and improving water quality.
The results of the detailed studies that used a variety of filter-feeders (suspension feeders) were summarized in the monographs [1, 36-38]. Those publications got positive evaluations in the reviews [39-43], and won several awards and diplomas (the list of them see below, after the list of the publications).
1.Ostroumov S. A. Biological Effects of Surfactants. CRC Press. Taylor & Francis. Boca Raton, London, New York. 2006. 279 p. ISBN 0-8493-2526-9 [new facts and concepts on assessment of hazards from chemicals, new look on the factors important to water quality, to sustainability; new priorities in environmental safety]
2.Ostroumov S. A. Biological filtering and ecological machinery for self-purification and bioremediation in aquatic ecosystems: towards a holistic view // Rivista di Biologia / Biology Forum. 1998. V. 91(2). P.221-232.
3.Ostroumov S. A., Donkin P., Staff F. Filtration inhibition induced by two classes of synthetic surfactants in the bivalve mollusk Mytilus edulis // Doklady Biological Sciences, 1998. Vol. 362, P. 454-456.
4.Ostroumov S. A. The concept of aquatic biota as a labile and vulnerable component of the water self-purification system - Doklady Biological Sciences, Vol. 372, 2000, pp. 286–289.
5.Ostroumov S. A., Kolesnikov M. P. Biocatalysis of Matter Transfer in a Microcosm Is Inhibited by a Contaminant: Effects of a Surfactant on Limnea stagnalis. - Doklady Biological Sciences, 2000, 373: 397–399. Translated from Doklady Akademii Nauk, 2000, Vol. 373, No. 2, pp. 278–280.
6.Ostroumov S. A. An aquatic ecosystem: a large-scale diversified bioreactor with a water self-purification function.- Doklady Biological Sciences, 2000. Vol. 374, P. 514-516.
7.Ostroumov SA. Criteria of ecological hazards due to anthropogenic effects on the biota: searching for a system. - Dokl Biol Sci (Doklady Biological Sciences). 2000; 371:204-206.
8.Ostroumov S. A. An amphiphilic substance inhibits the mollusk capacity to filter out phytoplankton cells from water. - Biology Bulletin, 2001, Volume 28, Number 1, p. 95-102.
9.Ostroumov S. A. Inhibitory Analysis of Regulatory Interactions in Trophic Webs. -Doklady Biological Sciences, 2001, Vol. 377, pp. 139–141. Translated from Doklady Akademii Nauk, 2000, Vol. 375, No. 6, pp. 847–849. [In the paper, the author developed a new approach to analyze the fundamental ecological issue, the interactions between organisms in ecosystems. He suggested to use the methodology of inhibitory analysis to study interactions in trophic chains. Important situation is the top–down control of plankton by benthic filter-feeders. This control, as author’s experiments have shown, might be removed by chemical inhibitors (the latter may enter the ecosystem as pollutants)]. ;
10.Ostroumov SA. The synecological approach to the problem of eutrophication. - Dokl Biol Sci. (Doklady Biological Sciences). 2001; 381:559-562.
11.Ostroumov SA. The hazard of a two-level synergism of synecological summation of anthropogenic effects. - Dokl Biol Sci. (Doklady Biological Sciences). 2001; 380:499-501.
12.Ostroumov SA. Responses of Unio tumidus to mixed chemical preparations and the hazard of synecological summation of anthropogenic effects. - Dokl Biol Sci (Doklady Biological Sciences). 2001; 380: 492-495.
13.Ostroumov SA, Kolesnikov MP. Pellets of some mollusks in the biogeochemical flows of C, N, P, Si, and Al. - Dokl Biol Sci (Doklady Biological Sciences). 2001; 379:378-381.
14.Ostroumov SA. Imbalance of factors providing control of unicellular plankton populations exposed to anthropogenic impact. - Dokl Biol Sci (Doklady Biological Sciences). 2001; 379:341-343.
15.Ostroumov SA. Effect of amphiphilic chemicals on filter-feeding marine organisms.- Dokl Biol Sci (Doklady Biological Sciences). 2001; 378:248-250.
16.Ostroumov S. A. Inhibitory analysis of top-down control: new keys to studying eutrophication, algal blooms, and water self-purification // Hydrobiologia. 2002. vol. 469. P.117-129.
17.Ostroumov S. A. Polyfunctional role of biodiversity in processes leading to water purification: current conceptualizations and concluding remarks // Hydrobiologia. 2002. v. 469 (1-3): P.203-204.
18.Ostroumov SA. Identification of a new type of ecological hazard of chemicals: inhibition of processes of ecological remediation. - Dokl Biol Sci (Doklady Biological Sciences). 2002; 385:377-379.
19.Ostroumov SA. System of principles for conservation of the biogeocenotic function and the biodiversity of filter-feeders. - Dokl Biol Sci (Doklady Biological Sciences). 2002; 383:147-150.
20.Ostroumov SA. A new type of effect of potentially hazardous substances: uncouplers of pelagial-benthal coupling. - Dokl Biol Sci (Doklady Biological Sciences). 2002; 383:127-130.
21.Ostroumov SA. Biodiversity protection and quality of water: the role of feedbacks in ecosystems. - Dokl Biol Sci (Doklady Biological Sciences). 2002; 382:18-21.
22.Ostroumov S. A. Studying effects of some surfactants and detergents on filter-feeding bivalves // Hydrobiologia. 2003. Vol. 500. P. 341-344.
23.Ostroumov S.A. Anthropogenic effects on the biota: towards a new system of principles and criteria for analysis of ecological hazards. - Rivista di Biologia/Biology Forum. 2003. 96: 159-170. Review. PMID: 12852181 [PubMed - indexed for MEDLINE]
24.Ostroumov SA, Walz N, Rusche R. Effect of a cationic amphiphilic compound on rotifers. - Dokl Biol Sci. (Doklady Biological Sciences) 2003; 390: 252-255.
25.Ostroumov S. A. On the biotic self-purification of aquatic ecosystems: elements of the theory. - Doklady Biological Sciences, 2004, Vol. 396, Numbers 1-6, p. 206-211.
26.Ostroumov S. A. Suspension-feeders as factors influencing water quality in aquatic ecosystems. - In: The Comparative Roles of Suspension-Feeders in Ecosystems, R.F. Dame, S. Olenin (Eds), Springer, Dordrecht, 2004. p. 147-164.
27.Ostroumov S. A. Some aspects of water filtering activity of filter-feeders // Hydrobiologia, 2005. Vol. 542, No. 1. P. 275 – 286 .
28.Ostroumov S. A. On some issues of maintaining water quality and self-purification. - Water Resources. 2005,Volume 32, Number 3, p. 305-313.
29.Ostroumov S. A. On the multifunctional role of the biota in the self-purification of aquatic ecosystems // Russian Journal of Ecology, Vol. 36, No. 6, 2005, p. 414–420.
30.Ostroumov S. A. Biomachinery for maintaining water quality and natural water self-purification in marine and estuarine systems: elements of a qualitative theory // International Journal of Oceans and Oceanography. 2006. Volume 1, No.1. p.111-118. [ISSN 0973-2667]. Publisher: Research India Publications, Dehli]. Basic elements are formulated for a qualitative theory of the polyfunctional role of the biota in maintaining self-purification and water quality in aquatic ecosystems. The elements of the theory covers the following: (1) sources of energy for the mechanisms of selfpurification; (2) the main functional blocks of the system of self-purification; (3) the list of the main processes that are involved; (4) analysis of the degree of participation of the main large taxons; (5) degree of reliability and the main mechanisms providing the reliability; (6) regulation of the processes; (7) the response of the system towards the external influences (man-made impacts); (8) the analogy between ecosystems and a bioreactor; and (9) conclusions relevant to the practice of biodiversity conservation. In support of the theory, results are given of the author's experiments which demonstrated the ability of some pollutants (surfactants, detergents, and some others) to inhibit the water filtration activity of marine filter-feeders (namely, the bivalve mollusks Mytilus galloprovincialis, Mytilus edulis, and Crassostrea gigas).