Doklady Biological Sciences, Vol. 390, 2003, pp. 252–255. Translated from Doklady Akademii Nauk, Vol. 390, No.

3, 2003, pp. 423–426. Original Russian Text Copyright © 2003 by Ostroumov, Walz, Rusche.

GENERAL BIOLOGY

Effect of a Cationic Amphiphilic Compound on Rotifers
S. A. Ostroumov*, N. Walz**, and R. Rusche**
Presented by Academician V.L. Kas’yanov September 25, 2002 Received September 30, 2002

Hydrobiont filter-feeders are an element of the socalled “biosphere apparatus” [1] (according to V.I. Vernadsky, the biosphere apparatus consists of functioning organisms, which transform the environment into the biosphere) and a component of aquatic ecosystems [2–5]. Rotifers are filter-feeders whose filtration activity often reaches 0.04–0.3 ml per animal specimen per day [4]. Filter-feeders participate in the processes leading to self-purification of aquatic ecosystems [5, 6]. It was also found that cationic surfactants reduced the filtration activity of rotifer [7] and other hydrobionts [5, 8]. A special device (turbidostat) was developed to study the trophic (filtration) activity of rotifers. In this device, rotifers are cultivated together with algae, the population of the algae being maintained at a steady-state level based on a dynamic equilibrium between the rate of uptake of algae by rotifers and the rate of supply of a fresh suspension of algae to the turbidostat tank [9]. The rate of supply of the algal suspension is automatically changed by a computer to compensate for the trophic (filtration) activity of rotifers observed in experiments. The higher the filtration activity of rotifers, the shorter the time interval required to take up the algae and the higher the rate of supply of the suspension of algae to the tank where rotifers are cultivated together with algae should be. The rate of supply of the suspension of algae to the tank is continuously monitored, and this value provides information about the filtration activity of the rotifer population. The goal of this work was to study the effect of a cationic surfactant on the trophic (filtration) activity of an experimental rotifer population in a turbidostat. The experimental results obtained in this work are consistent with the working hypothesis that cationic surfactant may inhibit the filtration activity of the rotifer population. Experiments were performed in a two-stage turbidostat [9] at 20°C as described in [10]. A combined culture of the rotifer Brachiopus calcifiorus and the alga

*Moscow State University, Vorob’evy gory, Moscow, 119992 Russia **Institute of Freshwater Ecology and Fishery, Berlin, Germany

Nannochloropsis limnetica (Eustigmatophyceae; cell size, from 1.5 to 6 µm) was cultivated in the turbidostat. The medium volume in the turbidostat tank was 135 ml. The Bourelly mineral medium was pumped to the tanks using a peristaltic pump. Before pumping to tanks, the medium was aerated. The medium was sterilized by filtering through a Schliecher and Schuell cellulose-PTFE filter with 0.2-µm pores (Germany). Air was sterilized by filtering through a Sartorius Midisart 2000 PTFE-Filter filter with 0.2-µm pores. The concentration of the cationic surfactant tetradecylcetyltrimethylammonium bromide (TDTMA, 0.5 mg/l) was chosen on the basis of the results of preceding experiments [5, 8]. The effect of TDTMA on the rotifer population size was studied in control experiments. Each tank contained 100 ml of rotifer culture (96 specimens per ml) and alga, N. limnetica (21 × 106 cells per ml; cell count of alga was determined using a Coulter counter).Tanks were incubated in the dark at 20°C in the room, where the turbidostat was installed. Rotifers were counted with the use of a Nicon SMZ-U stereoscope and a Sedgewick Rafter Cell 850 counter camera (United Kingdom). The so-called dilution rate was measured in the experiments. This parameter represents the rate of supply of a fresh suspension of algae to the experimental tank (the higher the filtration activity of rotifers, the higher the dilution rate). The rate of dilution was set by a computer on the basis of the results of continuous monitoring of the momentary values of the rate of uptake of the algae. The dilution rate in the turbidostat tank containing TDTMA was lower than in the control turbidostat (without TDTMA). The decrease in the dilution rate implied that the rate of filtration (therefore, the rate of ingestion of algae by rotifers) was decreased. The TDTMA-induced decrease in the feeding (filtration) activity of the rotifer population in the turbidostat experimental tank persisted for more than 12 h. The dilution rate in the experimental tank containing TDTMA within the first 6 h after the addition of the xenobiotic was 68–77% of the control level, which indicated the corresponding decrease in the filtration activity. After that, the filtration activity value gradually returned to the control level.

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It was interesting to study if TDTMA exerted an effect on the rotifer population size. The results of the experiment with incubation of rotifers in the presence of TDTMA are given in Table 1. Although the mean count of rotifers in tanks containing TDTMA was slightly lower than in the control, it is presently difficult to interpret these data unambiguously.The insignificant deviation from the control (towards a decreased population size) was due to either an experimental error or an actual decrease in the rotifer count per unit volume of the medium. Daily monitoring of rotifer count demonstrated that, within several hours of observation, the rotifer count in the control went slightly above the initial number of animals in the initial culture. The increase was insignificant and it could be conceivably explained by a practically natural reproduction of animals in the presence of food in the culture medium. The decrease in the dilution rate observed in our experiments in tanks containing TDTMA represented a corresponding decrease in the rate of elimination of algae from the culture medium by rotifers, and it was consistent with the working hypothesis that the addition of a cationic surfactant toa rotifer habitation area may cause a decrease in the total filtration activity of the rotifer population (i.e., a decrease in the volume of aqueous medium filtered by the rotifer population per unit time). These results are in agreement with our previous findings that TDTMA can inhibit the filtration activity of another rotifer species, B. angularis Gosse [7]. Many researchers (e.g., [4, 11, 12]; Table 2) studied the filtration activity of hydrobionts. It was shown [11] that the dependence of the filtration activity of the rotifer B. angularis on animal body weight was described by the following equation: F = 31.288 W 0.417, where F is the filtration rate, µl per animal per hour; W is the dry body weight, µg. Many researchers demonstrated that the filtration activity of rotifers depended on the following factors (cited from [4]). (1) Temperature. The filtration rate increased from 1 to 8 µl per specimen per hour upon increasing the temperature from 5 to 20–25°C. (2) The biomass of algae in the incubation medium. The rate of filtration decreased as the biomass of algae exceeded 60 mg/l. (3) The species of the alga. The maximum rate of filtration in experiments with B. calyciflorus was observed in the case of feeding on various strains of Scenedesmus, Lagerheimia, Cyclotella, and Niazschia (31–63 ml per mg per day), whereas the minimum rate of filtration was observed in the case of feeding on the green alga Chlorella (5–6 ml per mg per day). Note that the range of variation of the filtration (from 5 to 63 ml per mg per day) was significantly
DOKLADY BIOLOGICAL SCIENCES Vol. 390 2003

Table 1. Rotifer count (specimens per ml of medium) under the conditions of treatment with tetradecylcetyltrimethylammonium bromide (TDTMA) (0.5 mg/l) Tank 1 Incubation with duration, h TDTMA 0 (tarting point of treatment) 3 6 23 96 arithmetic Tank 2 mean with (in tanks 1 TDTMA and 2 with TDTMA) 96 96 Control tank without TDTMA 96

88 72 79

108 78 90

98 75 84.5

120 112 123

broader than the range of variation of the daily food allowance (from 41 to 190% of the wet weight of rotifers, i.e., an average of 115%). The daily amount of food eaten by rotifers changed as the biomass of algae in the incubation medium increased. For example, a more than tenfold increase in the biomass of the alga Ch. vulgaris (from 38 to 450 mg/l) was accompanied by a more than twofold increase in the daily amount of food eaten by the rotifer B. calyciflorus (from 31 to 64%) (Ovchinnikova and Glazacheva, 1972; cited from [4]). When the rotifer B. calyciflorus was fed on the alga Scenedesmus obliquus (the concentration of the alga changed from 5 to 20 mg/ml), the assimilability of food ranged from 48 to 80% [4]. The filtration activity of the rotifer B. calyciflorus fed on the infusoria Coleps sp. was 6–30 µl per animal per hour [12]. The maximum rate of filtration was detected at an infusoria density of 50 specimens per ml. The rate of filtration of the rotifer B. calyciflorus fed on the infusoria Tetrachymena pyriformis ranged from 3 to 13.6 µl per animal per hour. The rate of filtration of the rotifer B. rubens fed on the infusoria Coleps sp. was 4–9.3 µl per animal per hour, the maximum number of the infusoria Coleps sp. cells ingested by the rotifer B. calyciflorus ranging from 0 to 7 per animal per hour. The number of the infusoria T. pyriformis ingested by the rotifer ranged from 0 to 5 per animal per hour [12]. It follows from these and some other data available from the literature that the filtration activity of rotifers (and other filter-feeders) is a very variable characteristic of the physiological activity of animals. This parameter varies over a broad range, being dependent on many environmental factors (temperature, food concentration, species composition of food, etc.). The results of our experiments show that the concentration of the pollutant (cationic surfactant) also belongs to the environmental factors affecting the filtration activity. Our experiments demonstrated that this conclusion was valid at least for one xenobiotic (TDTMA). We expect

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Table 2. Filtration and trophic activities of filter-feeders (rotifers and other aquatic invertebrates) Measured parameter Dilution rate in turbidostat Filtration rate Food for filter-feeders used in this study Results of experiments and measurements References and comments

Rotifers B. calyciflorus Alga Nannochloropsis limnetica Decrease (68–77% of control level) after addition of 0.5 mg/l TDTMA Chlorella, Oocystis, Coelastrum, 5–26 ml per mg per day Kirchneriella, and Ankistrodesmus Scenedesmus acuminatus, 44–62.9 ml per mg per day Lagerheimia ciliata, and Cyclotella meneghiniana Clorella 0.072 ml per specimen per day S. acuminatus S. obliquus Infusoria Coleps sp. Infusoria Tetrahymena pyriformis 0.320 ml per specimen per day 0.048 ml per specimen per day 6–30 µl per specimen per h 3–13.6 µl per specimen per h B. rubens 4–9.3 µl per specimen per h B. calyciflorus up to 18.5 ng per specimen per h B. rubens up to 13.3 ng per specimen per h Daphnia 1106 ml per mg dry weight per h

Results of this work

L.A. Erman, 1962, 1963 (cited from [4]) L.A. Erman, 1962, 1963 (cited from [4]) U. Halbach, G. Halbach-Keup, 1974 (cited from [4]) L.A. Erman, 1962 (cited from [4]) G.A. Galkovskaya, 1963 (cited from [4]) [12] [12] [12] K.O. Rothhaupt, 1990 (cited from [12]) K.O. Rothhaupt, 1990 (cited from [12]) D. magna (size, 2.37 mm; dry weight of one specimen, 0.104 mg) [3] Daphnia sp.

Filtration rate Carbon assimilation

Coleps sp. Green alga Monoraphidium minutum M. minutum

Filtration rate

About 22 ml per specimen per day (at 23–24°C) About 12 ml per specimen per day (at N.M. Kryuchkova, 1989 temperature about 20°C or 26°C) (cited from [4]) Calanoida (Eudiaptomus gracilis, E. graciloides, Diaptomus oregonensis, and D. siciloides) Various algae and natural usually 1.4–2.1, rarely 0.2–2.6 ml Data of many authors phytoplankton, 15–20°C per specimen per day (cited from [4]) Bryozoa Plumatella fungosa Reaches 2.2 ml per mg dry weight [4] of colony per h Mussel Mytilus edulis Alga Phaeodactylum aricurnutum 6.17 l per g (dry weight of soft Mussel specimens were from the untissue) per h contaminated area Gluss Voe [13] Alga Ph. aricornutum 3.09 l per g (dry weight of soft Mussel specimens were from the tissue) per h contaminated area Swale [13] M. edulis × M. galloprovincialis (natural hybrids) Alga Isochrysis galbana 1.1–1.9 l per animal specimen per h New data (Ostroumov, Widdows) (fresh weight with shell, 3.7–5.9 g) Alga I. galbana 0.24–0.9 l per animal specimen per h In the presence of 0.3 mg/l (fresh weight with shell, 3.7–5.9 g) TDTMA (new data of Ostroumov, Widdows)
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that some other compounds with similar activities will be found. The results of our experiments provide additional evidence for the validity of the concept of aquatic biota as a vulnerable component of the mechanisms of selfpurification of stagnant water and water courses [14]. Our results also confirm that it would be reasonable to introduce a new class of ecological hazard of chemical substances (the hazard of the inhibition of ecological remediation and maintenance of water quality) [15]. On the one hand, filter-feeders regulate the phytoplankton population. On the other hand, filter-feeders themselves are an object of regulation in ecosystems. Filter-feeders provide an at least triple control of the phytoplankton population. Planktonic crustaceans, rotifers, and benthic filter-feeders control the phytoplankton population. In turn, the populations of crustaceans and rotifers are under a double combined control provided by organisms of the next upper trophic layer, including fish, bivalve mollusks (Bivalvia); phyllopods (Phylliopoda); Cladocera; water-fleas (Copepoda); mysids (Mysidacea; for example, the plankton– benthic mysid Mysis relicta actively eats not only phytoplankton but also daphnias, Bosmina, and rotifers); spiders (Araneina; the food of the water spider Agryroneta aquatica includes daphnias; the biomass of daphnias eaten per day in some cases reached 150% of the spider body weight); Hydracarina (the food of some Eylaidae, Hydrobaidae, and other families of this order was found to contain Cladocera and Ostracoda); freshwater shrimp (Amphipoda; Daphnia magna accounts for as much as 29% of the daily food of the amphipod Gammarus lacustris); decapods (Decapoda; Cladocera and Ostracoda account for 20% of the daily food of the shrimps Palaemon modestus and Palaemoneaes sinensis); dragonfly larvae (Odonata; the daily food of the dragonfly Sympycna fusca larvae fed on the daphnia D. magna was 167.5%; dragon-fly larvae often kill more daphnias than they are able to eat); bugs (Hemiptera; particularly, representatives of the families Nepidae, Cerridae, and Corixidae); caddis-flies (Trichoptera; daphnias were found in the food of representatives of the families Phrygameidae, Molannidae, Leptoceridae, and Limnophilidae); midges (Chironomidae; Cladocera, Copepoda, and Ostracoda were found in the food of the midge Ablabesmia monilis); mosquitoes Culicidae (rotifers were found in the food of Anopheles; many species of Chaoborus feed on Cladocera, Copepoda, and Rotatoria) (works of many authors cited in [4]). In spite of the double control provided by the upper trophic layers, there are large oscillations of the populations of planktonic organisms in aquatic ecosystems, which are indications of the imbalance of regulatory factors. This indicates the potential hazard of the development of phytoplankton population regulation disor-

ders in the case of the appearance of an even larger imbalance in regulation factors under the conditions of exposure to anthropogenic inhibitors of the trophic (filtration) activity of hydrobionts [8] (e.g., the rotifers studied in this work). ACKNOWLEDGMENTS We are grateful to Christian Steinberg, V.D Fedorov, V.V. Malakhov, N.V. Kartasheva, and other researchers of Moscow State University and Institute of Freshwater Ecology and Fishery (Berlin) for stimulating discussion, assistance, and valuable criticism. This study was supported by the Open Society Foundation. REFERENCES
1. Vernadskii, V.I., Biosfera (The Biosphere), Moscow: Noosfera, 2001. 2. Alimov, A.F., Elementy teorii funktsionirovaniya vodnykh ekosistem (Elements of the Theory of Water Ecosystem Functioning), St. Petersburg: Nauka, 2000. 3. Sushchenya, L.M., Kolichestvennye zakonomernosti pitaniya rakoobraznykh (Quantitative Relationships in Crustacean Feeding), Minsk: Nauka i Tekhnika, 1975. 4. Monakov, A.V., Pitanie presnovodnykh bespozvonochnykh (Feeding of Freshwater Invertebrates), Moscow: IPEE, 1998. 5. Ostroumov, S.A., Biologicheskie effekty poverkhnostnoaktivnykh veshchestv v svyazi s antropogennymi vozdeistviyami na biosferu (Biological Effects of Surfactants as Related to Anthropogenic Impact on the Biosphere), Moscow: MAKS, 2000. 6. Ostroumov, S.A., Hydrobiologia, 2002, vol. 469, pp. 117–129. 7. Kartasheva, N.V. and Ostroumov, S.A., Toksikol. Vestn., 1998, no. 5, pp. 30–32. 8. Ostroumov, S.A., Biologicheskie effekty pri vozdeistvii poverkhnostno-aktivnykh veshchestv na organizmy (Biological Effects of Surfactants on Living Organisms), Moscow: MAKS, 2001. 9. Walz, N., Hintze, T., and Rusche, R., Hydrobiologia, 1997, vol. 358, pp. 127–132. 10. Walz, N., Rusche, R., and Ostroumov, S.A., Ecol. Stud. Hazard. Solut., 2001, vol. 5, p. 39. 11. Walz, N., Plankton Regulation Dynamics, Berlin: Springer, 1993, pp. 106–122. 12. Mohr, S. and Adrian, R., Limnol. Oceanogr., 2000, vol. 45, no. 5, pp. 1175–1180. 13. Widdows, J., Donkin, P., Brinsley, M.D., et al., Mar. Ecol. Prog. Ser., 1995, vol. 127, pp. 131–148. 14. Ostroumov, S.A., Dokl. Akad. Nauk, 2000, vol. 372, no. 2, pp. 279–282. 15. Ostroumov, S.A., Dokl. Akad. Nauk, 2002, vol. 385, no. 4, pp. 571–573.

DOKLADY BIOLOGICAL SCIENCES

Vol. 390

2003

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