Inhibition of mussel suspension feeding by surfactants of three classes
S. A. Ostroumov1,* & J. Widdows2
**
1 Department of Hydrobiology, Faculty of Biology, Moscow State University, 119992, Moscow, Russia;
2 Plymouth Marine Laboratory, Prospect Place, West Hoe, PL1 3DH, Plymouth, England;
(*Author for correspondence: E-mail: ar55@yandex.ru)
**
Key words: surfactants, filter-feeders, clearance rates, marine mussels, toxicity
**
A short summary:
The first paper that reports experiments that showed that all three main kinds of synthetic surfactants (detergent chemicals) slow down the filtration of water by marine organisms, filter-feeders (bivalve mussels of Atlantic Ocean, Latin name Mytilus edulis). The 3 main types of surfactants that were studied were representatives of the 3 classes: anionic, cationic, and non-ionic surfactants.
Ostroumov S.A., Widdows J. Inhibition of mussel suspension feeding by surfactants of three classes. - Hydrobiologia. 2006. Vol. 556, No.1. P. 381 – 386.
http://www.scribd.com/doc/45958156/; scribd.com/doc/59544597/;
DOI: 10.1007/s10750-005-1200-7
Indexed in Web of science.
**
Abstract:
Effects of three surfactants on the filtration rates by marine mussels were studied. The xenobiotics tested represented anionic, cationic and non-ionic surfactants (tetradecyltrimethylammonium bromide, a representative of a class of cationic surfactants; sodium dodecyl sulphate, a representative of anionic alkyl sulfates; and Triton X-100, a representative of non-ionic hydroxyethylated alkyl phenols). All three surfactants inhibited the clearance rates. The significance of the results for the ecology of marine ecosystems is discussed.
Abbreviations: CR – clearance rate; EMIS – the electromagnetic induction system; SDS – sodium dodecyl
sulphate; TDTMA – tetradecyltrimethylammonium bromide; TX100 – Triton X-100
Text of the paper:
Introduction
Suspension feeders (filter-feeders) play a significant
functional role in aquatic ecosystems. The important
role of filter-feeders (particularly molluscs) is
due to their high rates and volumes of water filtration
(Walz, 1978; Alimov, 1981; Jørgensen
et al., 1986; Kryger & Riisga˚ rd, 1988; Shulman &
Finenko, 1990; Zaika et al., 1990; Dame, 1996). As
a result of biological filtration, suspended particles
and cells of phytoplankton and microbial plankton
are removed from the water. This process also
accelerates mineralization of organic substances in
the filtered matter. Therefore, biological filtration
contributes significantly to water purification in
aquatic ecosystems.
Filter-feeders can accelerate carbon fluxes in
ecosystems, because the production of biodeposits
(faecal and pseudofaecal pellets) leads to enhanced
rates of sedimentation. As a result, bivalves were
shown to influence material flux at the sediment–
water interface (Smaal et al., 1986; Kautsky &
Evans, 1987; Jaramillo et al., 1992; Dame, 1996;
Widdows et al., 1998).
Biodeposition rates were estimated as high as
60 gm)2 h)1 at a density of 1400 mussels m)2 (i.e.,
50% surface cover) in a mussel (Mytilus edulis)
bed at Cleethorpes (Humber estuary, England)
(Widdows et al., 1998), which is higher than
maximum recorded biodeposition rates of
25 gm)2 h)1 for M. edulis in the Oosterschelde in
the Netherlands (Smaal et al., 1986) and
18 gm)2 h)1 for M. chilensis in an estuary in Chile
(Jaramillo et al., 1992). Biodeposition rates in
some ecosystems were up to 40 times the natural
sedimentation rates. Kautsky & Evans (1987)
estimated annual biodeposition per g mussel (M.
edulis, dry weight including shells) as high as
1.76 g dry weight, 0.33 g ash-free dry weight,
0.13 g carbon, 1.7 10)3 g nitrogen and
2.6 10)4 g phosphorus. The annual biodeposition
is 11.7 g dry weight per g mussel shell-free dry
weight. When average mussel biomass was
620 gm)2 (dry weight including shells) or 91 gm)2
(dry flesh weight), the annual biodeposition per m2
was 1092 g (dry weight), including 80.7 g C, 10.4 g
N, 1.6 g P (Kautsky & Evans, 1987). The average
composition during the year, expressed as percent
Hydrobiologia (2006) 556:381–386 Springer 2006
S. Ostroumov (ed.), Water Quality: From Assessment and Ecotoxicology to Remediation
DOI 10.1007/s10750-005-1200-7
of dry weight of biodeposition, was 12.88% C,
1.54% N, and 0.19% P. With a total mussel biomass
of about 10,000 tons in the total 160 km2
research area (the northern Baltic proper), the
annual contribution from mussels biodeposition
would be 1300 tons of carbon, 170 tons of nitrogen,
and 26 tons of phosphorus, which means that
the total annual deposition (sedimentation) of C,
N, and P is increased by about 10% by mussels as
a result of their filtering activity (Kautsky &
Evans, 1987).
Therefore the measurement of filtration rates is
of ecological importance.
The marine mussels (Mytilus edulis, M. galloprovincialis
and their hybrids) are important filterfeeders
and dominant members of many benthic
communities and marine ecosystems. Mussels
(M. edulis) have been the focus of many studies
concerning accumulation of pollutants and their
biological effects (Donkin et al., 1989, 1991, 1997).
However, few studies have investigated the toxic
effects of synthetic surfactants.
Generally, surfactants (with very few exceptions)
are not included in the list of priority
pollutants (e.g., Scientific Committee for Toxicity
and Ecotoxicity of Chemical Substances, European
Commissions – see Bro-Rassmunsen et al.,
1994) or are considered of uncertain hazard to the
environment. According to Bailey (1996), many
surfactants are considered virtually non-toxic for
aquatic organisms, provided that the criteria of the
Environmental Protection Agency (USA) are
valid.
Alkyl sulphates, hydroxyethylated alkyl
phenols, and quaternary ammonium compounds
are important classes of surfactants. Previous research
has reported inconsistent effects of surfactants
on certain organisms (Ostroumov, 2000a,
2001a) (i.e. both negative and stimulating effects
have been recorded). However, at present there is
little information on how these surfactants may
affect the feeding rate of bivalve molluscs, such as
marine mussels.
The primary aim of this work was to quantify
the effect of surfactants of three classes on the
feeding rate of mussels on the algal cell (Isochrysis
galbana). The surfactants studied were sodium
dodecyl sulphate (SDS), a representative of alkyl
sulfates; Triton X-100 (TX100), a representative
of hydroxyethylated alkyl phenols; and tetradecyltrimethylammonium
bromide (TDTMA), a
representative of quaternary ammonium compounds.
Materials and methods
The methods used were similar to those described
by Ostroumov (2002a, 2003b). Mussels (M. edulis)
were collected from a coarse-sand substrate at
Exmouth (Devon, England) and used in experiments
with SDS and TX100. Mussels (natural
hybrids M. edulis/M. galloprovincialis) were
collected from the intertidal rocks at Whitsand
Bay (Cornwall, England) for use with TDTMA.
Mussels were placed in 2-l beakers equipped with
magnetic stirrers and kept at 16 C in a thermostatically
controlled room. Seawater was collected
from the Eddystone ( 15 km offshore from
Plymouth) and filtered through WCN nitrocellulose
filters with a pore diameter of 0.45 lm
(Whatman, Great Britain). A total of 16 animals
were studied in each experiment. Eight of them
were treated with the xenobiotic, the other eight
were controls (no toxicant). The surfactants were
added to the experimental beakers 1.5 h before the
experiment. The surfactant concentrations shown
in the tables and the text are the initial concentrations
of the xenobiotics added to the beakers.
In the experiments with SDS and TX100, eight
beakers contained eight pairs of mussels with a
raw weight of 16–20 g per beaker. An additional
beaker containing the 2 l of seawater was used as a
reference to confirm that there was no significant
change in algal cell concentration in the absence of
a mussel and biological filtration of the water.
Equal volumes of algal suspension were added
simultaneously to the nine beakers.
In the experiments with TDTMA, there were 16
beakers that each contained one mussel (average
wet weight with shell 4.5–5 g). The clearance rate
by mussels was determined from the exponential
decline in algal cell concentration (I. galbana
Parke, strain CCAP 927/1). The algal strain was
obtained from the NERC Culture Collection
of Algae and Protozoa, Dunstaffnage Marine
Laboratory, PO Box 3, Oban, Argyll, PA34 4AD,
Scotland, UK). Algal cell concentrations were
counted with a Coulter Electronics counter
(Industrial D model).
382
Results
The clearance rate, or the volume of water cleared
of algal cells per hour, was calculated for each
experimental surfactant concentration and control
condition. The clearance rate at each toxicant
concentration was expressed as a percentage of the
control value (the clearance rate in control mussels
was 100%). The effects of the anionic surfactant
SDS on clearance rate are presented in Table 1.
There was increasing inhibition of clearance rate
with increasing toxicant concentration. The
inhibitory effects of SDS on clearance rate appeared
to decline with exposure time during the
course of the 90-min experiment from the moment
labeled as T0 (the beginning of the experiment) to
the moment labeled as T3 (the end of the third
30-min period). These findings are consistent with
the results obtained in another bivalve species
(Bressan et al., 1989).
Triton X-I00, a non-ionogenic detergent of the
group of hydroxyethylated alkyl phenols, also
inhibited the clearance rate by mussels (Table 2).
TDTMA also inhibited the clearance rates of
mussels in the experiments with M. edulis/M.
galloprovincialis (Table 3). Clearance rate ceased
at 1 mg l)1 and was substantially inhibited at
0.3 mg l)1. The concentrations in the range 0.05–
0.3 mg l)1 are similar to those found in the most
polluted ecosystems (Review on the Ecological
State of Seas, 1992).
Discussion
The levels of surfactants in marine ecosystems often
go above maximum permissible concentrations
(MAC) reaching levels of >10 MAC and more
(Review on the Ecological State of Seas, 1992). In
addition, samples of seawater for testing pollutants
are usually collected at a distance of >300–
500 m from the source of pollution. Therefore, the
concentration of pollutants within the area of
several hundred meters between the site of
sampling and the source of pollution is even
higher. This area may include very important
coastal ecosystems. Therefore, the results obtained
in this study suggest significant deleterious effects
caused by environmental levels of surfactants.
Previous studies have shown that the suspension
feeding activity of M. edulis is also inhibited
by other pollutants, including some pesticides
(Donkin et al., 1997). Low concentrations of
organic pollutants were found to cause a decrease
in the feeding rate by M. galloprovincialis (Bressan
et al., 1989). Furthermore, some commercial
detergents (mixtures of several chemicals including
surfactants) inhibited water filtering by
M. galloprovincialis (Ostroumov, 2001a, c).
Similar effects of inhibiting the filtration rate
were found when studying effects of TDTMA
(0.5 mg l)1) and SDS (0.5 mg l)1) on Crassostrea
gigas (Ostroumov, 2003b).
Using the electromagnetic induction system
(EMIS), it has been shown that several pollutants
(copper, cadmium, zinc, lead, tributyltinoxide,
chlorine, dispersed crude oil) induced the valve
closure response of M. edulis (Kramer et al., 1989).
Table 1. Inhibition by the anionic surfactant SDS of the mean
clearance rates (CR) of mussels (Mytilus edulis)
SDS
(mg l)1)
Time
period
(30 min each)
CR
(% of control)
0.5 T0–T1 95.4
T1–T2 No inhibition
measured
T2–T3 No inhibition
measured
1 T0–T1 77.2
T1–T2 80.8
T2–T3 88.2
2 T0–T1 55.3
T1–T2 72.3
T2–T3 No inhibition
measured
4 T0–T1 23.2
T1–T2 17.9
T2–T3 30.5
5 T0–T1 4.3
T1–T2 11.9
T2–T3 10.3
CR is expressed relative to the control (suspended matter: algae
Isochrysis galbana) (calculated on the basis of the data of
Ostroumov et al., 1997, 1998; Ostroumov, 2001a).
Note. At each of the concentration there were 8 molluscs tested,
with 4 experimental and 4 control beakers. There were two
molluscs in each of the experimental and control beakers.
383
The same toxicants (except crude oil) were detected
by the valve closure response of Dreissena
polymorpha measured by the EMIS (Kramer et al.,
1989).
Therefore, the effects observed in this study
are consistent with the results of other authors.
These findings place a particular emphasis on the
disturbances to suspension feeders and biofiltration
in aquatic systems, a new aspect of the
ecological hazard resulting from chemical contamination
of the environment with surfactants.
Water pollution with sublethal concentrations of
synthetic surfactants of various classes can inhibit
biofiltration in ecosystems, thereby giving rise to
additional aspects of ecological hazards (Ostroumov,
2002a, b, 2004). The ecological consequences
of biofiltration inhibition may include impairment
of water clearance (Ostroumov, 1998), disturbance
of biogeochemical fluxes of carbon, increased
turbidity and reduced light penetration in the
Table 2. Effect of the non-ionic surfactant Triton X-100 (TX100) on the mean clearance rates (CR) of mussels (Mytilus edulis)
expressed relative to the control (suspended matter: algae Isochrysis galbana)
TX100
(mg l)1)
Time period
(30 min each)
CR
(+TX100) l h)1
CR in control
()TX100) l h)1
CR
(% of control)
Coefficient
of inhibition (%)
1 T0–T1 4.04 5.23 77.25 22.75
T1–T2 4.95 6.13 80.75 19.25
T2–T3 3.74 4.24 88.21 11.79
2 T0–T1 1.765 4.48 39.42 60.58
T1–T2 2.77 4.65 59.62 40.38
T2–T3 2.86 4.72 60.85 39.15
4 T2–T3 0.43 3.02 14.24 85.76
T3–T4 0.59 1.84 32.06 67.94
Note. At each of the concentration there were 8 molluscs tested, with 4 experimental and 4 control beakers. There were two molluscs in
each of the experimental and control beakers.
Table 3. Effect of the cationic surfactant TDTMA on the mean clearance rates (CR) of mussels (Mytilus edulis/M. galloprovincialis)
expressed relative to the control (Suspended matter: algae Isochrysis galbana)
TDTMA
(mg l)1)
Time period
(50 min each)
CR
(+TDTMA) l h)1
CR in control
()TDTMA) l h)1
CR
(% of control)
0.05 T0–T1 1.005 1.559 64.47
T1–T2 1.096 1.290 84.98
T2–T3 0.936 1.013 92.47
0.1 T0–T1 0.708 1.479 47.84
T1–T2 0.668 1.383 48.28
T2–T3 0.455 1.099 41.41
0.3 T0–T1 0.645 1.620 39.82
T1–T2 0.819 1.640 49.92
T2–T3 0.350 1.053 33.25
1 T0–T1 0.114 1.168 9.74
T1–T2 0.100 1.218 8.21
T2–T3 0.048 0.971 4.89
5 T0–T1 0.051 1.334 3.84
T1–T2 0.028 1.248 2.20
T2–T3 0.028 0.871 3.16
Note. At each of the concentration there were 8 molluscs tested, with 8 experimental and 8 control beakers. There was one mollusc in
each of the experimental and control beakers.
384
water column (Ostroumov et al., 1997, 1998) with
adverse effects on phytoplankton and phytobenthos,
as well as other important ecological processes
in aquatic ecosystems (Ostroumov, 2000b,
2001b, d, e), which provides further evidence in
support of the new approach to prioritization of
anthropogenic effects on biota (Ostroumov et al.,
2000, 2003a).
The ecological significance of the data on
pollutant-induced inhibition of the filtration rate
was discussed in depth in (Ostroumov, 2002c, d).
Our studies of organisms that are part of
benthic communities (‘societies’) make us think of
a new interpretation of the poetic words:
There is society, where none intrudes,
By the deep sea, and music in its roar:
I love not man less, but nature more.
Lord Byron 1788–1824:
Childe Harold’s Pilgrimage (1812–1818).
Acknowledgements
We are grateful to Professors V.V. Malakhov,
E.A. Kriksunov, A.G. Dmitrieva, and researchers
from the Departments of Hydrobiology and
Department of Ichthyology, Moscow State
University, and Plymouth Marine Laboratory
(PML) for stimulating discussion, to Mr. F. Staff
(PML) for help with some experiments, and to Ms.
K. Schneider for help in collecting mussels. This
study was in part supported by the European
Environmental Research Organization and by
Open Society Foundation (RSS).
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