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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.


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 so- Nannochloropsis limnetica (Eustigmatophyceae; cell
called “biosphere apparatus” [1] (according to V.I. Ver- size, from 1.5 to 6 µm) was cultivated in the turbidostat.
nadsky, the biosphere apparatus consists of functioning The medium volume in the turbidostat tank was 135 ml.
organisms, which transform the environment into the The Bourelly mineral medium was pumped to the tanks
biosphere) and a component of aquatic ecosystems [2–5]. using a peristaltic pump. Before pumping to tanks, the
Rotifers are filter-feeders whose filtration activity often medium was aerated. The medium was sterilized by fil-
reaches 0.04–0.3 ml per animal specimen per day [4]. tering through a Schliecher and Schuell cellulose-PTFE
Filter-feeders participate in the processes leading to filter with 0.2-µm pores (Germany). Air was sterilized
self-purification of aquatic ecosystems [5, 6]. It was by filtering through a Sartorius Midisart 2000
also found that cationic surfactants reduced the filtra- PTFE-Filter filter with 0.2-µm pores.
tion activity of rotifer [7] and other hydrobionts [5, 8]. The concentration of the cationic surfactant tetrade-
A special device (turbidostat) was developed to study cylcetyltrimethylammonium bromide (TDTMA,
the trophic (filtration) activity of rotifers. In this device, 0.5 mg/l) was chosen on the basis of the results of pre-
rotifers are cultivated together with algae, the popula- ceding experiments [5, 8].
tion of the algae being maintained at a steady-state level The effect of TDTMA on the rotifer population size
based on a dynamic equilibrium between the rate of was studied in control experiments. Each tank con-
uptake of algae by rotifers and the rate of supply of a tained 100 ml of rotifer culture (96 specimens per ml)
fresh suspension of algae to the turbidostat tank [9]. and alga, N. limnetica (21 × 106 cells per ml; cell count
The rate of supply of the algal suspension is automati- of alga was determined using a Coulter counter).Tanks
cally changed by a computer to compensate for the were incubated in the dark at 20°C in the room, where
trophic (filtration) activity of rotifers observed in exper- the turbidostat was installed. Rotifers were counted
iments. The higher the filtration activity of rotifers, the with the use of a Nicon SMZ-U stereoscope and a
shorter the time interval required to take up the algae Sedgewick Rafter Cell 850 counter camera (United
and the higher the rate of supply of the suspension of Kingdom).
algae to the tank where rotifers are cultivated together
with algae should be. The rate of supply of the suspen- The so-called dilution rate was measured in the
sion of algae to the tank is continuously monitored, and experiments. This parameter represents the rate of sup-
this value provides information about the filtration ply of a fresh suspension of algae to the experimental
activity of the rotifer population. tank (the higher the filtration activity of rotifers, the
higher the dilution rate). The rate of dilution was set by
The goal of this work was to study the effect of a cat- a computer on the basis of the results of continuous
ionic surfactant on the trophic (filtration) activity of an monitoring of the momentary values of the rate of
experimental rotifer population in a turbidostat. uptake of the algae.
The experimental results obtained in this work are The dilution rate in the turbidostat tank containing
consistent with the working hypothesis that cationic TDTMA was lower than in the control turbidostat
surfactant may inhibit the filtration activity of the roti- (without TDTMA). The decrease in the dilution rate
fer population. implied that the rate of filtration (therefore, the rate of
Experiments were performed in a two-stage turbi- ingestion of algae by rotifers) was decreased. The
dostat [9] at 20°C as described in [10]. A combined cul- TDTMA-induced decrease in the feeding (filtration)
ture of the rotifer Brachiopus calcifiorus and the alga 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
*Moscow State University, Vorob’evy gory, Moscow, xenobiotic was 68–77% of the control level, which
119992 Russia indicated the corresponding decrease in the filtration
**Institute of Freshwater Ecology and Fishery, Berlin, activity. After that, the filtration activity value gradually
Germany returned to the control level.

0012-4966/03/0506-0252$25.00 © 2003 MAIK “Nauka /Interperiodica”


It was interesting to study if TDTMA exerted an Table 1. Rotifer count (specimens per ml of medium) under
effect on the rotifer population size. The results of the the conditions of treatment with tetradecylcetyltrimethylam-
experiment with incubation of rotifers in the presence monium bromide (TDTMA) (0.5 mg/l)
of TDTMA are given in Table 1. Although the mean arithmetic
count of rotifers in tanks containing TDTMA was Control
Tank 1 Tank 2 mean
slightly lower than in the control, it is presently difficult Incubation tank
with with (in tanks 1
to interpret these data unambiguously.The insignificant duration, h without
TDTMA TDTMA and 2 with
deviation from the control (towards a decreased popu- TDTMA
lation size) was due to either an experimental error or
an actual decrease in the rotifer count per unit volume 0 (tarting 96 96 96 96
of the medium. point of
Daily monitoring of rotifer count demonstrated that,
within several hours of observation, the rotifer count in 3 88 108 98 120
the control went slightly above the initial number of 6 72 78 75 112
animals in the initial culture. The increase was insignif- 23 79 90 84.5 123
icant and it could be conceivably explained by a practi-
cally natural reproduction of animals in the presence of
food in the culture medium. broader than the range of variation of the daily food
The decrease in the dilution rate observed in our allowance (from 41 to 190% of the wet weight of roti-
experiments in tanks containing TDTMA represented a fers, i.e., an average of 115%).
corresponding decrease in the rate of elimination of The daily amount of food eaten by rotifers changed
algae from the culture medium by rotifers, and it was as the biomass of algae in the incubation medium
consistent with the working hypothesis that the addition increased. For example, a more than tenfold increase in
of a cationic surfactant toa rotifer habitation area may the biomass of the alga Ch. vulgaris (from 38 to
cause a decrease in the total filtration activity of the 450 mg/l) was accompanied by a more than twofold
rotifer population (i.e., a decrease in the volume of increase in the daily amount of food eaten by the rotifer
aqueous medium filtered by the rotifer population per B. calyciflorus (from 31 to 64%) (Ovchinnikova and
unit time). Glazacheva, 1972; cited from [4]). When the rotifer
These results are in agreement with our previous B. calyciflorus was fed on the alga Scenedesmus obliq-
findings that TDTMA can inhibit the filtration activity uus (the concentration of the alga changed from 5 to
of another rotifer species, B. angularis Gosse [7]. 20 mg/ml), the assimilability of food ranged from 48 to
Many researchers (e.g., [4, 11, 12]; Table 2) studied 80% [4].
the filtration activity of hydrobionts. It was shown [11] The filtration activity of the rotifer B. calyciflorus
that the dependence of the filtration activity of the roti- fed on the infusoria Coleps sp. was 6–30 µl per animal
fer B. angularis on animal body weight was described per hour [12].
by the following equation: The maximum rate of filtration was detected at an
F = 31.288 W 0.417, infusoria density of 50 specimens per ml. The rate of
where F is the filtration rate, µl per animal per hour; W filtration of the rotifer B. calyciflorus fed on the infuso-
is the dry body weight, µg. ria Tetrachymena pyriformis ranged from 3 to 13.6 µl
per animal per hour. The rate of filtration of the rotifer
Many researchers demonstrated that the filtration B. rubens fed on the infusoria Coleps sp. was 4–9.3 µl
activity of rotifers depended on the following factors per animal per hour, the maximum number of the infu-
(cited from [4]). soria Coleps sp. cells ingested by the rotifer B. calyci-
(1) Temperature. The filtration rate increased from 1 florus ranging from 0 to 7 per animal per hour. The
to 8 µl per specimen per hour upon increasing the tem- number of the infusoria T. pyriformis ingested by the
perature from 5 to 20–25°C. rotifer ranged from 0 to 5 per animal per hour [12].
(2) The biomass of algae in the incubation medium. It follows from these and some other data available
The rate of filtration decreased as the biomass of algae from the literature that the filtration activity of rotifers
exceeded 60 mg/l. (and other filter-feeders) is a very variable characteris-
(3) The species of the alga. The maximum rate of fil- tic of the physiological activity of animals. This param-
tration in experiments with B. calyciflorus was eter varies over a broad range, being dependent on
observed in the case of feeding on various strains of many environmental factors (temperature, food con-
Scenedesmus, Lagerheimia, Cyclotella, and Niazschia centration, species composition of food, etc.). The
(31–63 ml per mg per day), whereas the minimum rate results of our experiments show that the concentration
of filtration was observed in the case of feeding on the of the pollutant (cationic surfactant) also belongs to the
green alga Chlorella (5–6 ml per mg per day). environmental factors affecting the filtration activity.
Note that the range of variation of the filtration Our experiments demonstrated that this conclusion was
(from 5 to 63 ml per mg per day) was significantly valid at least for one xenobiotic (TDTMA). We expect


254 OSTROUMOV et al.

Table 2. Filtration and trophic activities of filter-feeders (rotifers and other aquatic invertebrates)
Measured Food for filter-feeders used Results of experiments and
References and comments
parameter in this study measurements
Rotifers B. calyciflorus
Dilution rate Alga Nannochloropsis limnetica Decrease (68–77% of control Results of this work
in turbidostat level) after addition of 0.5 mg/l
Filtration rate Chlorella, Oocystis, Coelastrum, 5–26 ml per mg per day L.A. Erman, 1962, 1963
Kirchneriella, and Ankistrodesmus (cited from [4])
Scenedesmus acuminatus, 44–62.9 ml per mg per day L.A. Erman, 1962, 1963
Lagerheimia ciliata, and (cited from [4])
Cyclotella meneghiniana
Clorella 0.072 ml per specimen per day U. Halbach, G. Halbach-Keup,
1974 (cited from [4])
S. acuminatus 0.320 ml per specimen per day L.A. Erman, 1962 (cited from [4])
S. obliquus 0.048 ml per specimen per day G.A. Galkovskaya, 1963
(cited from [4])
Infusoria Coleps sp. 6–30 µl per specimen per h [12]
Infusoria Tetrahymena pyriformis 3–13.6 µl per specimen per h [12]
B. rubens
Filtration rate Coleps sp. 4–9.3 µl per specimen per h [12]
B. calyciflorus
Carbon Green alga Monoraphidium up to 18.5 ng per specimen per h K.O. Rothhaupt, 1990
assimilation minutum (cited from [12])
B. rubens
M. minutum up to 13.3 ng per specimen per h K.O. Rothhaupt, 1990
(cited from [12])
Filtration rate – 1106 ml per mg dry weight per h D. magna (size, 2.37 mm; dry weight
of one specimen, 0.104 mg) [3]
About 22 ml per specimen per Daphnia sp.
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 un-
tissue) 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,



that some other compounds with similar activities will ders in the case of the appearance of an even larger
be found. imbalance in regulation factors under the conditions of
The results of our experiments provide additional exposure to anthropogenic inhibitors of the trophic (fil-
evidence for the validity of the concept of aquatic biota tration) activity of hydrobionts [8] (e.g., the rotifers
as a vulnerable component of the mechanisms of self- studied in this work).
purification of stagnant water and water courses [14].
Our results also confirm that it would be reasonable to ACKNOWLEDGMENTS
introduce a new class of ecological hazard of chemical
substances (the hazard of the inhibition of ecological We are grateful to Christian Steinberg, V.D Fedorov,
remediation and maintenance of water quality) [15]. V.V. Malakhov, N.V. Kartasheva, and other researchers
On the one hand, filter-feeders regulate the phy- of Moscow State University and Institute of Freshwater
toplankton population. On the other hand, filter-feeders Ecology and Fishery (Berlin) for stimulating discus-
themselves are an object of regulation in ecosystems. sion, assistance, and valuable criticism.
Filter-feeders provide an at least triple control of the This study was supported by the Open Society
phytoplankton population. Planktonic crustaceans, Foundation.
rotifers, and benthic filter-feeders control the phy-
toplankton population. In turn, the populations of crus-
taceans and rotifers are under a double combined con- REFERENCES
trol provided by organisms of the next upper trophic 1. Vernadskii, V.I., Biosfera (The Biosphere), Moscow:
layer, including fish, bivalve mollusks (Bivalvia); phyl- Noosfera, 2001.
lopods (Phylliopoda); Cladocera; water-fleas (Copep- 2. Alimov, A.F., Elementy teorii funktsionirovaniya vod-
oda); mysids (Mysidacea; for example, the plankton– nykh ekosistem (Elements of the Theory of Water Eco-
benthic mysid Mysis relicta actively eats not only phy- system Functioning), St. Petersburg: Nauka, 2000.
toplankton but also daphnias, Bosmina, and rotifers); 3. Sushchenya, L.M., Kolichestvennye zakonomernosti
spiders (Araneina; the food of the water spider Agry- pitaniya rakoobraznykh (Quantitative Relationships in
roneta aquatica includes daphnias; the biomass of Crustacean Feeding), Minsk: Nauka i Tekhnika, 1975.
daphnias eaten per day in some cases reached 150% of 4. Monakov, A.V., Pitanie presnovodnykh bespozvonoch-
the spider body weight); Hydracarina (the food of some nykh (Feeding of Freshwater Invertebrates), Moscow:
Eylaidae, Hydrobaidae, and other families of this order IPEE, 1998.
was found to contain Cladocera and Ostracoda); fresh- 5. Ostroumov, S.A., Biologicheskie effekty poverkhnostno-
water shrimp (Amphipoda; Daphnia magna accounts aktivnykh veshchestv v svyazi s antropogennymi vozde-
for as much as 29% of the daily food of the amphipod istviyami na biosferu (Biological Effects of Surfactants
Gammarus lacustris); decapods (Decapoda; Cladocera as Related to Anthropogenic Impact on the Biosphere),
and Ostracoda account for 20% of the daily food of the Moscow: MAKS, 2000.
shrimps Palaemon modestus and Palaemoneaes sinen- 6. Ostroumov, S.A., Hydrobiologia, 2002, vol. 469,
sis); dragonfly larvae (Odonata; the daily food of the pp. 117–129.
dragonfly Sympycna fusca larvae fed on the daphnia 7. Kartasheva, N.V. and Ostroumov, S.A., Toksikol. Vestn.,
D. magna was 167.5%; dragon-fly larvae often kill 1998, no. 5, pp. 30–32.
more daphnias than they are able to eat); bugs (Hemi- 8. Ostroumov, S.A., Biologicheskie effekty pri vozdeistvii
ptera; particularly, representatives of the families Nepi- poverkhnostno-aktivnykh veshchestv na organizmy (Bio-
dae, Cerridae, and Corixidae); caddis-flies (Tri- logical Effects of Surfactants on Living Organisms),
choptera; daphnias were found in the food of represen- Moscow: MAKS, 2001.
tatives of the families Phrygameidae, Molannidae, 9. Walz, N., Hintze, T., and Rusche, R., Hydrobiologia,
Leptoceridae, and Limnophilidae); midges (Chirono- 1997, vol. 358, pp. 127–132.
midae; Cladocera, Copepoda, and Ostracoda were 10. Walz, N., Rusche, R., and Ostroumov, S.A., Ecol. Stud.
found in the food of the midge Ablabesmia monilis); Hazard. Solut., 2001, vol. 5, p. 39.
mosquitoes Culicidae (rotifers were found in the food 11. Walz, N., Plankton Regulation Dynamics, Berlin:
of Anopheles; many species of Chaoborus feed on Cla- Springer, 1993, pp. 106–122.
docera, Copepoda, and Rotatoria) (works of many 12. Mohr, S. and Adrian, R., Limnol. Oceanogr., 2000,
authors cited in [4]). vol. 45, no. 5, pp. 1175–1180.
In spite of the double control provided by the upper 13. Widdows, J., Donkin, P., Brinsley, M.D., et al., Mar.
trophic layers, there are large oscillations of the popu- Ecol. Prog. Ser., 1995, vol. 127, pp. 131–148.
lations of planktonic organisms in aquatic ecosystems, 14. Ostroumov, S.A., Dokl. Akad. Nauk, 2000, vol. 372,
which are indications of the imbalance of regulatory no. 2, pp. 279–282.
factors. This indicates the potential hazard of the devel- 15. Ostroumov, S.A., Dokl. Akad. Nauk, 2002, vol. 385,
opment of phytoplankton population regulation disor- no. 4, pp. 571–573.