Chemosphere, Vo!.10, No. 6, DP 575 - 603, 1981 Printed in Great Britain
0045-6555/81/060575-29~02.00/0 ©]981 Pergamon Press Ltd.
POSSIBILITIES FOR MARINE POLLUTION RESEARCH AT THE ECOSYSTEM LEVEL W.Chr. de Kock and J. Kuiper Division of Technology for Society TNO Delft, The Netherlands
i. Introduction Biological
systems show a tendency to resist change and to remain in a state of equilibrium.
This homeostasis is thought to operate at different levels of biological orgaDization organisms,
populations etc.), including the ecosystem level.
It is important however to realize
that good homeostatic control comes only after a period of evolutionary adjustment This implies that the self-maintenance
(cells,
(Odum,
and self-regulation capabilities of ecosystems and their
component populations and organisms have come into operation over a long period of time turies).
In contrast,
1971).
~cen-
the increasing stress on natural environments by chemical waste from in-
dustrialized human societies has become significant over a much shorter period
(decades).
The number of well-estabished causal relationships between the presence of toxic substances in the sea and toxic effects in natural systems is still low; examples do however exist and, as a result,
in the last decade much research has been initiated in both the laboratory and the
field. In The Netherlands at least two clear cases have been described in which the effects on components of the marine ecosystem could be related to a certain cause. The first case
(Roskam,
1965,
1966) concerned the illegal dumping of copper sulphate
(CuSO 4)
on a stretch of beach and its subsequent distribution along the Dutch shoreline which resulted in mass mortality of fish. The second case involved the demonstration of a relation between acute and sublethal effects of a number of chlorinated hydrocarbons the sandwich tern ( S t e ~
(particularly the insecticide telodrin)
on populations of
8~dVid~ns~8) and of the eider (Somater~a moZZis8~) in the Dutch
Wadden Sea and an industrial point source ca. 90 miles away
(Koeman and Van Genderen,
1972);
this distance is equivalent to a transportation time of about 40 days under the prevailing hydrographical conditions
(Van Bennekom et al.,
1974).
The receiving estuarine system may have worked as a trap in which concentrations of the pollutants built up with time and reached the birds through food chains. A comparable incident has been reported from California,
USA
(Risebrough et al.,
egg-shell thinning and a consequent population decline of brown pelicans
1970) where
(PeZeeanu8 oee~dental{8)
was related to industrial discharge of DDT into the sea and accumulation in marine organisms serving as the pelican's food source.
575
576
Other examples that have been described include the well-known industrial mercury pollution of Minamata Bay, Japan
(Study Group on Minemata Disease,
1968), the effects of 'oil pollution
catastrophes involving supertankers in the English Channel area Amoco Cadiz: Hess,
(Torrey Canyon: Smith,
1978) and perhaps also, as recently suggested by Reynders
the reproductive failure of harbour seals ( P ~ o ~
V~nG)
(1980a,
1968;
1980b),
from the Dutch Wadden Sea in rela-
tion to PCB pollution in the area. Notwithstanding the scarcity of data on specific toxicological cause-effect relationships in natural systems, -
some important conclusions can be drawn from the relevant cases:
Sometimes the ecosystem shows a lack of homeostatic control over the invasion of new c h e m i c a l s Sensitive components have been shown to exist at, at least, endotherm and higher trophic levels.
It is however possible that micro-organisms and lower trophic levels
zooplankton) -
can show genetic adaption to chronic chemical stress
(Fisher,
As has been shown in the case of industrial leaks, long periods of time between the initial entry of a pollutant, (Goldberg,
(phytoplankton, 1977).
(years)
usually pass
the awareness of a problem and the solution to it
1976).
- Marine ecosystems with a relatively autochtonous character and undisturbed species diversity on different trophic levels have a signal function related to public health and hitherto unsuspected pollution sources. This is one of the reasons why preservation of such natural areas within national coastal management schemes is desirable. The concept of marine parks coral reefs, rocky shores, tidal flat areas and salt marshes)) that of their terrestrial equivalents;
(e.g.
is relatively new compared to
it is however gaining interest
(Bj6rklund,
1974).
- Future pollution research should produce results with a predictive character and which can be applied to the protection of human health as well as the conservation of marine ecosystems, including fishery resources. The ultimate aim of pollution research must be the analysis of situation.
(possible)
effects in the field
The need to test chemicals on possible environmental harm is related to this factual
situation and coastal water management authorities have to rely on relevant ecotoxicological research data when formulating national dumping policies. The extent to which the results of laboratory experiments
(toxicity, bioaccumulation,
biodegradation)
can be extrapolated to the com-
plex natural conditions of the sea is, however, unclear; ecological observations are thus necessary in order to validate laboratory test schemes. In the next two sections in ecotoxicological
(2 and 3) an outline will be given of the rdle that fieldwork can play
research.
We shall dis~inquish between field studies with a retrospective character which deal with existing pollution situations and in which the dose is not known and
(semi-)
field experiments of a
prospective kind with a defined dose, designed to increase understanding of the fate and effects of pollutants in the marine ecosystem or for toxicity testing in natural multispecies environments. Figure i illustrates how field observations fit into a simple scheme leading from recognition of a pollution problem to correction measures.
577
FIELD STDDIES~ R e t r o s p e c t i v e (dose not known) m
Environmental a n a l y s i s :
Dumping chemical waste
license a
p
biological
: - species composition change - p h y s i o l o g i c a l s i g n a l s (end-predators)
chemical
: - survey p o l l u t a n t l e v e l s i n b i o t i c and a b i o t i c f r a c t i o n s
~
PROBLEM IDENTIFICATION I d e n t i f y : - chemicals ( e . g . mixtures) - marine a r e a c h a r a c t e r i s t i c s (hydrography, r e p r e s e n t a t i v e species) - literature
data
EXPERIMENTAL RESEARCH
Sequential test schemes
- toxicity - bio-accmmalation
validation ~
- biodegradation
- c o n t r o l l e d ecosystem e x p e r i ments (enclosures) analysis disasters
Non-toxicological I
[criteria - set standard - enforce regulations
F-IEL._..DD CO._._~O..~_L chemical monitoring monitoring I- (active) biological
Fig. I The rBle of field studies in the environmental management of pollution problems. 2. Retrospective
field studies
2.1. General remarks Structurally,
the living part of ecosystems tends to evolve towards maximum species diversity
and complete niche exploitation under the prevailing abiotic conditions. maturation process is accompanied by increasing efficiency in the cycling position)
Functionally,
this
(synthesis and decom-
of matter. There is a high degree of species diversity in marine areas where stable
environmental conditions have been acting for long periods of time and faunal assemblages of the large ocean basins,
(Sanders,
1969). The floral
including coastal zones within direct reach
578
of their currents
(e.g. oceanic islands) must be considered in this light. Population dyna-
mics in such situations are primarily controlled by biotic interrelationships and the resistance to anthropogenic stress is considered to be low (Kinne, 1977). In contrast,
some areas,
such as estuaries,
dex and naturally unstable populations environmental
factors
contain ecosystems with a low species diversity in-
(Wolff, 1973). This is due to the large variability of
(light, temperature,
salinity etc.) in combination with an often short
history on the evolutionary time scale. Stress resistance is considered to be relatively high as far as natural chemical and physical factors are concerned,
it is however as yet impossible
to say if this is also true for xenobiotic chemicals introduced by man. Fisher on the basis of experimental evidence,
(1977) postulates,
that phytoplankton and other organisms which have evolved
in and adapted to physically variable environments are better able to tolerate any toxic compound than are morphologically
similar organisms adapted to stable environments.
Nearshore and estua-
rine areas are nevertheless especially threatened by toxic stressors because of their geographical position,
frequently in the vicinity of industrialized areas with associated polluted river
wa~er run-off,
the trapping of contaminated particles in estuarine sediments and the resulting
general higher ambient concentrations of toxic chemicals. Retrospective
field investigations are oriented towards the description of existing pollution
situations in an attempt to correlate observable biological effects with the degree of pollution. A differentiation can be m a d e ~ e t w e e n
research at the level of communities and research d i r e c t e d
towards the use of individual species
(bio-indicators)°
2.2. The community approach The living part of the ecosystem can be regarded as an integrating information-yielding unit (Kaesler et al,
1974)
showing a causal relationship between the stressing dose and the effect,
manifest in the composition of the living community. in decreased resilience and diversity,
Stress on the ecosystem generally results
expressed by a tendency towards the removal of larger
organisms with longer life spans and the appearance of opportunistic spans,
~]e numbers of which strongly fluctuate in space and time
species with shorter life
(FAO, 1972). Concerning the
large pelagic oceanic systems an interesting hypothesis which merits further investigation, offered by Greve and Parsons
(1977). These authors observe that under polluted conditions there
is a tendency towards predomination of nanophytoplankton in microphytoplankton
is
(e.g. small flagellates)
and a decrease
(e.g. large diatoms).
This could indirectly result in a decrease in energy transfer up the food web of the sea as far as fish stocks lead to an advantage for planktonpredating ctenophore or medusae populations. Eppley and Weiler
(1979) however doubt if there is sufficient evidence that stress by pollutants
causes a shift to ~-fl~gellates. It is clear that qualitative and quantitative inventarisations of the component species populations in ecosystems
(if necessary restricted to certain categories,
e.g. macro-zoobenthos)
can
in principle provide much information on the degree of disturbance within the ecosystem. The detection of significant changes in species composition and abundance as a result of pollution are, however, often hampered by a low signal-to-noise ratio.
In estuarine areas it is es-
pecially difficult to measure in this way the influence of pollution on species populations;
579
this influence being superposed on a high natural spatial and temporal variability. Impoverishment of marine areas has been ascribed to pollution on several occasions. et al.
Bellamy
(1972) have conducted an ecological monitoring study of the sublittoral kelp forest
community
(Lamina~a hyperborea)
down to a depth of 12 m along pollution gradients on the
east coast of Britain. The gross reaction of this system seems to be clear - suspended material
(table 1):
from pollutant sources reduces light penetration and therefore gives
rise to attenuation of primary production over the lower depth range; -
faunal species diversity expressed as a diversity index is consistently lower at ~ e
Table I
(Margalef,
polluted sites;
Selected data from Bellamy et al. (1972) concerning a study of pollution induced effects on the kelp forest ecosystem (L~ncmia hy~erborea) of rocky substrates along the east coast of Britain. A non-polluted site is compared with a heavy polluted one.
Name site
St.Abbs,Petticoewick
Position
55°55'N,02°09'W
Type of pollution
Faecal bacteria -i PO 4 Ug.l NO 3 NH 4
1968)
none
100 ml -I
17 0.4
~g.l -I -i ug.l
Suspended solids mg.l
-i
Av. faunal diversity index Depth range kelp'forest,
(Margalef 1968)
m below MLW
Av. net annual production of Laminaria individuals,
Souter 54°48'N,01°21'W Heavy (industrial, colliery, domestic) 2000 3
2
19
2
14
12
200
3.9
2.2
2 - 12
2 - 4
610
416
g.m -2
Number of individuals in trophic groups, % of total number of individuals, mean 1967-1970: Omnivores Carnivores Herbivores Deposit feeders Suspension feeders
40 15 4 0.5 40
6 7 1 0.7 85
Heavy metal levels in animal tissue, ~g.g-I dry weight
Mytilus edulis Asterias rubens Nucella lapillus
CU 8, Pb 125 Cu 10, Pb 170 Cu 10, Pb 146
Cu 13, Pb 343 Cu 21, Pb 305 CU 20, Pb 313
580
- suspension feeders
(M~tilu8 eduli8, Sabellaria 8pinulosa)
tend to dominate the polluted system,
opportunistically using energy-rich sewage as a food source; their population numbers showing considerable fluctations with time; -
compared to unpolluted sites, copper and lead levels are higher in tissues of some faunal ponents
(AsteriG8 ruJ2ens, Nude~a Zapillus, M~tilu8 BduZ~8)
com-
on the polluted sites. Biomagni-
fication of these metals in the food chain has not been observed. Another example from the same geographical area has been described by Edwards
(1972) who showed
that the benthic marine algal vegetation of the Tees estuary has deteriorated since 1930's, when an inventarisation was carried out estuaries:
those of the Wear
(temporal change). Edwards also showed that three neighbouring
(relatively unpolluted),
the Tyne
(receiving untreated sewage from
106 persons, pollution largely of the nutrient type) and the Tees
(pollution largely of the toxic
chemical type, including acid waste, metals, cyanide and phenol) differ in the composition of their euryhaline marine benthic algal flora; these results indicate the probable detrimental effect of toxic chemical pollution especially in the Tees area Gray
(1976)
(spatial change).
showed that there had been a dramatic reduction in the number of species of bivalves
and polychaetes in the same estuary since 1935, although absence of some of those species cannot be related exclusively to industrial discharges More recently Gray
(Gray,
1979).
(1979) criticized the use of diversity indices
(such as the Shannon-Wiener
index) derived from informaiion theory, as a measure of the effect of pollution on community structures. Both this diversity index and the rarefaction method of Sanders
(1968) are considered
by him to be of insufficient sensivity to trace early effects of pollution on benthic faunal assemblages.
A sensitive alternative seems to be offered by the empirical fact that the distri-
bution of individuals over species in large samples from a cormnunity is nearly always log-normal (May 1975). Plots on probability paper of the cumulative percentage species against the number of individuals per species grouped in geomtric classes are linear. This relationship is sensitive of disturbance by pollution.
Under slight polluted conditions a break occurs in the line; the
log-normal distribution is again restored under heavy polluted conditions,
however the line then
extends over more geometric classes than in the unpolluted case. This has been demonstrated with the extensive data of Pearson
(1975) who studied the effects of organic pulp mill pollution on
the benthic fauna of Loch Ell
(Scotland). The method has also been applied more recently to the
pollution situation in Oslo Fjord cies is responsible
(Gray,
1980). Normally, only a relatively low number of spe-
for the deviation of the log-normal distribution under slight pollution.
Presumably the application of adaptive strategies in the life histories of these few species (e.g. the capacity to produce planktonic as well as benthic larvae in
Polydora ciliata),
Capitella aapitata
and
rather than a relative lack of sensitivity for toxic stress, is primarily
responsible for the effects observed. A common disadvantage of the above-mentioned descriptive methods at the couununity level is their non-specificity with regard to chemical stressors operating in nature.
2.3. Indicator species Another retrospective approach to the pollution problem is the use of certain indicator species
5el
under marine field conditions. The term "indicator species" is often used rather loosely, but Hueck and Hueck-Van der Plas (1976) have pointed out that a general classification into three types of bio-indicators pollution is possible:
i) target organisms with a negative reaction,
for
2) tolerators with a
neutral reaction and 3) exploiters with a positive reaction to pollution. The existence of these different types might be revealed by field surveys of species composition and abundance in ecosystems
(2.2). Tolerators may be useful for determination of speci-
fic chemical stress in the natural situation because of their bioaccumulating characteristics; those species do not possess sufficient regulating capacity to prevent polluting substances entering their internal environment. by Phillips
The extensive literature on this subject has been reviewed
(1977, 1978).
The general advantages of the analysis of pollutants in tissues of organisms can be summarized as follows: -
Bioavailability is measured at the actual site of pollution. Chemicals entering the environment may undergo changes, which are not easily simulated in a laboratory experiment and this may affect their rates of absorption onto cell membranes,
rates of diffusive or active transport
into the cell and final concentrations reached within the organism.
For example, metal spe-
ciation in aquatic systems effects both the bioacct~nulation potential and the toxicity and Fowler,
(Engel
1979); organic chemicals may become degraded with as yet unknown rate constants
or undergo other reactions with the receiving system. In addition the presence of a number of~ different chemical stressors in the environment can give rise to antagonistic or synergistic effects on accumulation and toxicity when they reach the organism simultaneously. -
The accumulating organism is to a certain extent capable of time-integrating ambient concentrations of pollutants in water.
It may therefore represent a moving time-average value for
bioavailable chemical waste. This is advantageous for monitoring purposes and cost-saving in comparison with measurements of waste substances in water samples where larger short term variations necessitate a more frequent sampling scheme to allow a reliable estimation of average pollutant concentrations. - Pre-concentration of the pollutant within the organism, often by large concentration factors, increase accessibility
for chemical analysis.
This is especially important for the detection
of xenobiotic organic compounds which may escape attention in water analyses because of their low ambient concentrations. Two examples demonstrate the type of data that can result from field surveys of pollutant levels in marine organisms living in waste gradients caused by land-based sources. Example
I. Figure 2 shows a hitherto unpublished case of severe copper pollution along the east
coast of Ireland. Copper mining was accompanied by the dumping of Cu-rich mine sludge and drainage water into the Avoca River, entering the Irish Sea near Arklow. Cu-analyses in sea water along a coastal stretc~ from 20 km north to 80 km south of Arklow did not show a gradient. The Cu-concentrations
in total homogenized soft tissues of
Fueus species, Mytilu8 edu~i8 and
Patella ~Tzlgata from the intertidal zone did however show a clear gradient both northwards and
582
tO km
W,cklow
copper mining Mizet~
9 23
Patella L. vul@ata, L. 20 32
52
69
54
1217
74 44 21 33
1621 I05 20 39
5
6
Fucu8 spec
Woldrum)
-~'~_~ Ark/owl
Cud,schorge 9 kg. hr'1
Keystone quorries ) "
~
86
~ - /
39
d
Fig. 2 Ireland, East Coast, intertidal zone, survey 13-15 October 1973. Copper levels in tissue homogenate8 of Fucu8 species, ~tilu8 edulis and Patella vul~ata. Cu-concentration8 in pg.g-1 dry we~----~ght. southwards from Arklow. These concentrations are given in figure 2 on a dry weight base. in M~tilu8 edul~s was 74 ~g.g -1 at the local distribution limit some
The highest Cu-level found
small distance from the river discharge point. It is interesting to compare this to the data in table 2 showing experimental evidence from both a toxicological
laboratory study
(Adema,
1972) and a field accumulation experiment
(De Wolf et
1972) that lethal Cu-levels in Mytilus eduli8 tissue are to be found between 50 and 100 ~g.g -I (ash-free dry weight). Scott and Major (1972) reported a comparable level in ~jtilus
al.,
eduli8
from cape Rosier, Maine, USA, where active copper mining restarted in 1968. In contrast,
583
Table 2
Toxicity and accumulation data for Cu applied as CuCl 2 to Mytilus edulis, L. (length class 3-3.5 cm~ LC 50 values are given for different exposure times in laboratory experiments (Adema et al., 1972) together with the accumulated levels in total soft tissues of mussels still surviving. The field experiment data mentioned (intertidal musselbed; De Wolf et al., 1972) are given for comparative purposes. Here, in the natural population, LC 50 values were not determined exactly. However, high or low mortalities are indicated by + or - respectively.
Mytil~s edulis, L.
(experiments TNO, Cu-LC 50 value
Cu levels in tissues
dosed concentrations
mg.kg -I dry weight
Exposure time
in wg.l -I
days
4
280
4
+
(223) field exp.
100
140
-
8
80
-
10
45
50
11
-
19
(42) field exp.
80
25
27
-
48
bivalves e.g.
-
6
much higher levels
1972)
60
(21) field exp.
50
17
,
80
(up to an order of magnitude higher) can be found in tissues of other marine
Crassostrea giga8
(Boyden and P~meril, 1974). This demonstrates that an integra-
tion of field survey data and dose-controlled experiments is necessary to estimate environmental harm of a pollutant. Example 2. During 1971-1975 an extensive survey was carried out to investigate the distribution of mercury in Dutch coastal waters, making use this metal
o f ~ t i l u 6 edulis
as a known bioaccumulator of
(Koeman and Van Genderen, 1972). Intertidal samples were mainly used
(length class
3.0-3.5 cm), although some samples from North Sea buoys were included. Except for these buoys, which were visited irregularly in the period of 1973-1975, all sites were visited bimonthly from March 1971 to March 1973. The temporal variation in Hg-content on those sites, expressed as the 100 s variation coefficient v = ~ (in which s = standard deviation and ~ = average) ranged from 27% to 68% at different locations over the two-year period. In figure 3 the results are given for the Dutch Wadden Sea area and the adjacent North Sea
(ca. 40 NM offshore). The upper part
of the Hg-level gradient could be related to industrial pollution sources in the Eems-Dollard estuary. Significant differences between the mercury load in
(albeit at a somewhat lower level of pollution) were also found
Mytilus
edulis from the central and western section of the Dutch
Wadden Sea. This can be related to the influence of polluted coastal water from southern origin entering the area from the south-west. The results from the open North Sea and from samples
584
/
//
NOrthSea
Total Ng t.lg g-'
/
ti: i
I
J',',si
I
7 ~(t6/
/
area
el2)
I
base/,be At/ coast North Sea Buoys
I
I
Dutch Wodden Sea West
Dutch Wadden Sea East
I
Eems Do//ard Estuary
Fig. 3 Mercury levels in soft tissues of ~tilus eduiis, L. expressed on an ashL+~ee dry weight basis. Survey Outch Wadden Sea 1971-1973 (intertidal) and a~4acent North Sea 1973-1975 (buoys). Between Brackets: number of samples per site; each sample consisted of 60-100 individuals of 3-3.5 cm length. c o l l e c t e d o n the south c o a s t of Ireland s h o w still lower values i n d i c a t i n g base line levels in m o r e r e m o t e A t l a n t i c waters. The t e m p o r a l v a r i a b i l i t y e n c o u n t e r e d a t each sample site w a s a s s u m e d to arise, a t l e a s t partially, from d i f f e r e n c e s in the v e r t i c a l p o s i t i o n in the i n t e r t i d a l zone o n d i f f e r e n t s a m p l i n g dates; an a t t e m p t w a s t h e r e f o r e m a d e in the p e r i o d
1974-1975 to e l i m i n a t e this source o f v a r i a t i o n b y con-
t i n u o u s e x p o s u r e o f m u s s e l s in c a g e s a t t a c h e d to b u o y s at a number o f sites in the area. To this
585
~ t i l u s edulis were composed from a relatively unpolluted population in
end uniform samples of
the open North Sea by a random selection procedure, each sample consisting of 80 individuals of 4-5 cm lenght. Total mercury levels were measured in a time series over about 250 days after transfer of the test animals to the industrial !~lluted Eems-Dollard estuary. Figure 4 shows a rapid rise to different plateau values within a month on three experimental sites followed by a certain amount of variation in time.
,
Total Hg ,n tissue /ug. g -t (ash-free dry)
~
TT
4
~.,~.
,to7
~
lOkm
EMS -
DOLLARD
i
H
site
0.5
[ ~"open North Sea level i
I
I
100
200
300
~-~days
Fig. 4
Active bio-monitoring with Mytilus edulis, L. (May 19?4-February 1975, length class 4-5 cm). Random samples of test animals were transferred from the open North Sea to sites hr. I, 2 and 3 in the Ha-polluted Eems-Dollard estuary. C indicates an experimental reference level (Mytilu~ edulis, 3-3.5 em) from a field study in which a continuous average dose of 0.4 Vg H~a++.l-I was applied during a period of about 100 days to the sea water overflowing an intertidal musselbed (ref. figure 7).
These variations showed a synchronous course at different distances from the pollution source, indicating that the variation is caused by a factor in the environment operating simultaneously at the three locations. The temporal variability could indeed be expressed as a lower variation coefficient as compared with the earlier results from the intertidal zone
(fiqure 5). Thus, as already mentioned by
586
Mon,torlnc],_Mytdus eduhs
achve experiments Cor~t/nuous expos 1974 -'75 analytical varlo tl On total Hg "~I mean concentration in tissue (pprn, a s h - free d r / weight)
passwe samphng
total Hg mean cone tn water ,ng/l
,i
;
® ~00 n
300
Hg-po/luted estuary ( Eems -Do/lord]
,-," :K ,',( -,,..
o
t #t, rt 0
tO
l
,~
~00
)K
coastal waters (Dutch Woddensea)
>', .<
o
20
30
I
I
I
~0
50
50
Petten 'Z n~ean v(~iu~" 50 .- 30 world oceans
open sea (Nort~j ~"S e a )
I
80
90
70 coeff,clent
F~g. 5
200
I
tOO % ,
tO0 s ,
of vanahon i v=---~--- j
Temporal variation, expressed as Pearson's coefficient of variation (v), resulting from different monitoring schemes o ~ a mercury gradient (Eems-Dollard) to open sea. I00 8 v , in which s is the standard deviation and ~ is the mean Ha-concentration f r o m a time series o f m e a s u r e m e n t s at a c e r t a i n location. "4 o * *
Hueck
-= -=
intertidal mussels subtidal mussels d i s s o l v e d m e r c u r y in w a t e r total m e r c u r y in w a t e r
(1976),
"active biD-monitoring"
seems to provide a reliable estimation of bioavailable
mercury levels along a pollution gradient. Pirie
(1978)
This view is supported by the work of Davies and
in the Firth of Forth, Scotland.
Mytilu8 e~lis,
In contrast to the results obtained with
the analysis of water samples over the period of investigation in the Wadden
Sea area showed a relative high variability both for dissolved mercury alone and for dissolved and suspended mercury together
(fiqure 5).
Sewage and Wastewater Treatment,
(Data from the Netherlands Government Institute for
see also Essink,
1980).
5s7
Figure 5 also shows that the analysis method used
(neutron activation analysis)
is responsible
for a contribution of about 15% to the variation coefficient. The filterfeeding genus Goldberg et al., abundance,
Mytilus eduli8 has been applied in extensive monitoring schemes (e.g.
1978). This has become feasible for practical reasons
size, ease of collecting,
long life span, euryhalinity,
(e.g. distribution,
general stress tolerance,
accumulation ability and high concentration factors of several chemicals). However,
the suitability of a number of other bivalves as bio-indicators for pollution has also
been investigated. Some depositfeeding species e.g. the genera
Scrobidularia (Bryan and Hummerstone, 1978) and
Maeoma (Luoma and Jenne, 1977) have been studied because of their association with polluted sediments. Biomonitoring is also possible on a lower trophic level; an elegant example being given by Eide and Jensen
(1979), who studied the growth and development of three diatom species enclosed,
in situ, in dialysis bags under different heavy metal pollution stress. The diatoms were solely exposed to dissolved metal species and not limited by depletion of nutrients as normally occurs with batch cultures.
The three species showed marked differences
in their sensitivity to heavy
metal concentrations in two Norwegian fjords, when measured either by mortality of the most sensitive phytoplankton species used most tolerant species
(Thalassio~ira pseudonana) or by reduced growth rate of the
(Phaeodadtylum tricornutz~m). The test algae accumulated heavy metals even
from low ambient concentrations,
indicating the degree of pollution in cases where no reduced
growth rate was observed. Tolerant indicator species possessing good accumulation characteristics need not to be insensitive to pollution.
This has been discussed in a recent controversy between Gray
(1980) and Bayne
~tilu8 eduli8 as a pollution monitor species. Bayne
et al.
(1980) concerning the choice of
et al.
(1979) make clear that, although research with other species could also be rewarding,
biological response is relevant enough in their studies with mussels.
Physiological
the
indices
(scope for growth and 0:N ratio) and some adaptive cytochemical and specific biochemical
respon-
ses to pollution have been demonstrated as feasible indicators of sublethal effects resulting from environmental
insult. Of these factors,
the "scope for growth", which is defined as the
difference between the assimilated ratio of food consumed and the respiratory heat loss, measures the potential
for both the somatic growth and the production of gametes; it cannot easily
be related to a specific type of pollutant. The same non-specificity applies to the cytochemical measurement of the induction of free hydrolase activity in cytoplasm, which occurs when the scope for growth is negative and the animal utilizes stored energy for metabolic maintenance. Biochemical
studies carried out with petroleum hydrocarbons,
activity of some enzymes of the mixed function oxygenase This is an important development;
however,
suggest that increased
system might be more stressor-specific.
sensitive and rapid techniques might thus become available
which relate sublethal physiological
effects directly to accumulated levels of specific pollu-
tants in suitable indicator organisms.
58S
3. Prospectiv e field studies 3.1. General remarks Modern industrial societies produce substantial quantities of chemical waste, much of which is disposed of in the sea. Whilst this may be economically the most favourable solution to the disposal problems,
the ecological consequences are not always apparent. An important aspect of eco-
toxicology is the development of test procedures yielding results which can be applied in decision making on dumping of chemical waste in natural waters. Ecotoxicology is however still in its infancy
(Hueck- van der Plas and Hueck,
1979) and the test-
procedures that are under consideration for national or international use must be submitted to continuous review. It is not realistic to expect conclusive proof that, in the long term, a pollutant is biologically harmless, but the tests devised should provide the information needed to judge environmental hazards. The marine system as such is not accessible for experimental manipulation, with tankers might be considered as unintentional application of oil and dispersants (e.g. Levell,
although catastrophes
largescale experiments and the intentional
to estuarine benthic biota has been reported in the literature
1976). A research methodology,
permitting extrapolation of the results of labora-
tory test schemes to natural waters is still needed to optimalize the formulation of dumping criteria. The deficiencies of small scale laboratory experiments have already been noted by several authors faced with the scope of the problem Perkins,
(e.g. Koeman,
1976; Menzel and Case,
1977; Zeitschel,
1978;
1979) and can be summarized as follows.
- There is a dissimilarity between the dose applied in standard laboratory routines and that reaching biota under actual field conditions.
This difference arises from
(i) a lack of know-
ledge regarding the chemical form of pollutants in the direct natural surroundings of organisms, where modification of model substances may well take place; duration of many laboratory routine tests
(2) the difference between the
(often acute shortterm tests of 48 or 96 hours dura-
tion) and the much longer time scale for the action of persistent pollutants in nature. This difference is especially important when organisms with long generation periods are concerned as, from an ecological viewpoint, potential of populations;
toxicity should preferably be related to the reproduction
(3) the unrealistically high concentrations of pollutants often
applied to establish easy measurable effects
(e.g. LC 50 values), whereas in nature less easi-
ly detectable sublethal effects may have significant consequences at much lower ambient pollutant concentrations. - The non-representativeness
of biota used in routine laboratory test schemes makes the observa-
tion of ecological effects i~0ossible.
(I) This applies to a range of experimental procedures,
from the choice of an appropriate inoculum in biodegradation studies to the choice of test organisms in toxicity- and bioaccumulation studies,
for which normally only a restricted num-
ber of hardy marine species is available. When estuarine areas are the target of pollution research it will be appropriate to use estuarine species of relative natural tolerance that are also capable of withstanding laboratory treatment.
It should however be noted that as
589
yet the majority of open ocean species cannot be maintained or cultured in the laboratory (although Perkins under laboratory
(1979)
cals in open sea. of many laboratory
levels
laboratory involved
tests,
Appropriate
are, however,
interaction
food webs
in normal
needed and the costs
1978).
aquatic ecosystem experiments literature of the last decade indicates un upsurge in activities
testing of polluting chemicals to place relevant,
has not always been the principal motive.
recognizable
properties
of the natural
whilst at the same time realizing that natural ecosystems
directed at the
control,
although the
These activities
system in an experimental
attempt
situation,
cannot be copied. This relevance
is
in one of two approaches:
(i) The functional
long-term approach,
in which the maintenance
is attempted by the regulation of processes, nutrients
tial dimensions
cycling of nutrients,
which ran for many
This is attained by spatial separation of autotrophic, dimensions
her-
for these subsys-
Their system thus ensured high mineralization
whereas the regulation of prey-predator
activity and re-
accessibility
(monocellular
DGphnia magna) improved population stability, although the main-
algae serving as food for
tenance of the steady-state herbivore
that overall spa-
A promising example is that of
subsystems and by choosing appropriate
tems relative to each other.
steady-state
and decomposing biota.
(1978), who set up fresh water micro-ecosystems
years without nutrient addition. bivoric and decomposing
heterotrophic
similarity with nature, but have the advantage
need not limit their use in laboratories.
Ringelberg and Kersting
of an ecological
e.g. primary production and the recycling of
and organic matter in a system of autotrophic,
Such systems lack structural
was better at the level of the primary producers
than at the
level.
On a larger scale De Wilde and Kuipers mud-flat ecosystem,
(diatoms)
(1977)
constructed
a large indoor multi-species
with a closed water circuit and artificially
ture- and tidal circulation gae
in marine
not easily sustainable
development of complex aquatic systems that can be kept under experimental
expressed
character
marine food webs of more than two
because of the spatial and temporal dimensions
(Menzel and Steele,
The scientific
importance.
not included)
for the dumping of chemi-
is also apparent in the mono-species
such tests neglect the multi-species
ecological
(decomposers
facilities,
3.2. Controlled
an increasing ability to breed and rear marine animals
in large tanks); this is of importance
(2) Non-representativeness
which is of fundamental trophic
observes
conditions
characteristics.
eolo~, both polychaetes)
light-,
tempera-
The sediment system was seeded with benthic al-
and subsequently with macrofaunal
elements
and tended to reach steady-state
with a sufficient mineralization
controlled
tidal
(Arenicola marina, Nerei8 diversicharacteristics
after two years,
of organic matter in the sediment and recycling of nutrients,
enhanced by a high rate of bioturbation. (2) The short-term
"enclosure"
tural ecosystems
approach,
within artificial
ability to bring natural mention that experimental
in which the isolation of representative
enclosures
species assemblages
is attempted.
portions of na-
This approach depends on the
under experimental
control.
It is imperative
control here implies the ability to arrange duplicates
to
containing
59o
similar populations in the experimental design. Recent studies with such enclosures have resulted in a growing literature pertaining to coastal land-based flow-through facilities such as in Loch Ewe, Scotland 1975) and Narrangansett Bay, Rhode Island, USA based constructions anchored to the sea floor et al.,
1977; Menzel and Case,
(Oviatt et al., (Reeve et al.,
(Saward et al.,
1980), as well as to sea-
1976; Kuiper,
1977a; Gamble
1977).
The pelagic {n 8~tu bag, which is suspended from floats at the sea surface, is probably the most frequently used enclosure type
(Zeitzschel,
sions range from about I m 3 (France, Lacaze,
1978; Davies and Gamble,
1979) The dimen-
1971, 0.3 m3; The Netherlands,
1.5 m 3) to more than 1000 m 3 (CEPEX, B.C. Canada, Parsons,
Kuiper,
1977a,
1978, 1300 m3). A common feature
of those systems is that they have no proven steady-state characteristics and have only been used in pollution studies for periods up to several months. The primary intention of this experimental
set-up is however the observation of possible effects of sublethal doses of pol-
lutants on structural and functional aspects of pelagic marine communities,
including i~di-
rect effects occurring through interactions of different trophic levels. Considering the length of the reproductive cycles of most planktonic organisms,
this can be done on such a
time scale. Structural shifts in the system are no less important than functional changes and should ideally be studied together because changes in functional dynamics of the system are probably expressed in the composition of the living c o , u n i t y .
Some examples from our
own experience are given below to illustrate the usefulness of enclosures in field pollution studies. Example i. "Land"-based facility. A basin experiment on an intertidal mussel bed; best described as an accumulation experiment under field conditions.
The enclosures used were timber
constructfons driven into the sediment underlying a large intertidal musselbed
(~tilu8
edulis) in the Dutch Wadden Sea (figure 6). These basins had a square surface area of 50 m 2 and were connected with the outside estuarine waters by an opening at ground level, through which the tide could enter and withdraw. The mean HW level on the bed over the experimental period of 100 days
(May-September
1972) was 76 cm, the average immersion was
64% of the time and - considering the shape of the tidal" curve in the area - the average water volume in the basins amounted to 25 m 3 during periods of immersion. the diurnal tide mercury
(II) chloride
three of the basins to yield calculated average concentrations of 4.0, respectively,
Every cycle of
(HgCl 2) was dosed into the incoming water entering 1.3 and 0,4 ~g Hg.l -I
although only about 40% of these concentrations could be detected as dissolved
Hg by atomic absorption spectrometry.
A fourth basin served as a control.
The musselbed,
both in the basins and on an outside plot, was sampled every 10 days, during periods of low tide, using a random sampling procedure. The continuous mercury additions were stopped after i00 days and the basins removed;
the sampling of mussels continued for some time thereafter.
Figure 7 shows respectively the accumulation and elimination of total mercury neutron activation analysis)
and methyl mercury
(measured by
(CH3Hg, measured by emission spectrometry).
The results show that metl,ylation of inorganic mercury occurs in this estuarine mud-flat environment which is rich in micro-organisms.
A lag-phase of several weeks elapsed however
before the accumulation of CH3Hg became discernible in the basins with the two highest mer-
591
Fig. 6
Aerial photograph of experimental basins (? x 7 m) on a intertidal musselbed during low tide (copyri.ckt KL~ Aerocarto). The basins fill with coastal water through an opening at ,around level with the rising tide. Catwalks connect the units to a small laboratory cabin built on poles. Design and construction by TNO, Den Helder. BaZ.azand, Dutch Wadden Sea, summer 1972.
592
35 Total Hg concentration ~n
tissue H g . g
{ash- free dry/
-7
30 I I I I 1
25
I I i i i
20
l !
o -~---
/,
15
/
"'6
~',1 /~.
, / I'
70
b '
,J
--I
// ~
x .o,, o ,,,
"
X Ii \ i>
/,,l
"""o ,,,,,,oter . :
"i \
i if-
.7
=
/ 0 / . ~ ...o_....e....~.~ ~ ~°~'-tp--e.--~ ---e . . . .
I ~ ' ' ~ 0./. ug./"t e-~..P'-R~.~.-o,.--e. . . . I control basin
musselbed 0 • -- - - ~--',. ........... ,e-...4-..-:e.--..e--4---..e-..---~.~---'.~-...e-.e ............ .--e outside contro~plot
?, I / ",dl, p
10 CH3 Hg concentrohon in tissue ,ug,g-1 (ash-free dry)
,
',
/
~o '\
#
~
I
2.5
2,0 z ~ g . i -~ #3 jug. {"~ ~5
/
1,0
I®\.
.~
e...
""
"
~_1
"°'f~"~"
i
,~,
.,Q1o~...
/"..--o 7-" \, \
0.5
~'~ e....e
...... '-,
e--e----e
o4"
",l.....e.....e,...,l" . . . . . .
-e.. •
t" i
~e control basin outside mussetbed control plot
..... i
" ".........
I
0 i
june
'
july
'
aug.
I
!..
~ept.
I
oct.
I
7972
I
I start HgCIz dose
Fig. ?
stop d o s i n g
In situ accumulation and subsequent elimination of total mercury (figure 7a) and methyl mercury (CH3Hg , figure 7b) in soft tissue of a selected length class (3.03.5 cm) of M~tilus eduli8 from an intertidal musselbed in the Dutch Wadden Sea. Number of mussels per sample: I00. Dose: HgCZ 2. Dosing period about 100 days. Diurnal tide. A, B, C, O and E indicate calculated levels in tissues for Hg++-doee concentrations of 4.0, 1.3, 0.4, 0 (control basin) and 0 (outside control plot) ~g. 1-1 (respectively), to co~encate for biomass loss {in the basins) or gain (outside control plot) at the end of the dosing period.
593
cury concentrations. The mercury concentrations in the mussel tissue should be corrected for a substantial ash free dry weight loss of the animals during the experiment. for the time when Hg addition stopped.
The loss of biomass
basin, but not outside) was a serious disadvantage,
This is shown in figure 7
(also occurring in the control
and indicated either food shortage due
to the restricted water volume relative to the number of mussels in the basins or a negative influence of smothering due to increased sedimentation on top of the bed. When compared to a flow-through laboratory accumulation experiment with ~ t i Z u 8 a comparable HgCl 2 dose, large differences are noted
eduli8 and
(figure 8).
mercury in mu.~seLs •
20
I "
fS
sI ts S 0
n
%%
%
0 sSfJ • pJ O S
70
~,~
~
~
&% %%
.~._~._o__~--o50
%0
%
Oj
o--~ ....... 100
t,me [doysJ
150
Fig. 8 Accumulation and elimination of mercury and methyl mercu~d in mussels (Mytilus edulis). Comparison of laborato~j and fielddata. . 2+ ~-1 Laborato~# experiment: flow-through dose 0.4 ua ~g .~ • Field experiment: f~ow-through dose 1.3 Vg Hg'Z~.l-I --I~ --o~ ---m----o---
mercury in laboratory experiment methyl mercury in laboratory experiment mercury in field experiment methyl mercury in field experiment
The arrow ~ indicates the discontinuation of the mercury supply.
In the laboratory mussels were not fed, artificial sea water was used, suspended matter was lacking and the experiment lasted only 60 days
(an accumulation period of 30 days followed
by a 30-day period in Hg-free water). The laboratory experiment uave rise to a more rapid
59~
increase of total Hg in the test animals, whereas contrary to the field observations,
Hg-
elimination did not take place after discontinuation of the mercury supply. Furthermore, accumulation of methyl mercury was not observed.
Reasons for these differences are probably
related to the changed bioavailability of the added mercury due to adsorption and speciation, to microbial methylation and to different feeding behaviour of the mussels in the basins. The results clearly demonstrate the difficulty of extrapolating results from a laboratory experiment to actual field conditions. Example 2. In 8it-~ bag experiments with plankton communities. i) For several years ecotoxicological
investigations have been carried out with North Sea
plankton communities in Den Helder, the Netherlands
(Kuiper, 1977a,
1977b,
1981)
to
trace the fate and effects of model compounds on natural coastal marine plankton communities enclosed in floating plastic bags with a volume of 1.5 m 3 (figure 9).
Fig. 9
Enclosures for pollution studies with marine plankton come,unities. TNO, Den Helder, The Netherlands.
In the simple experimental
set-up several bags
(usually 6-8) are filled simultaneously by
careful pumping through a branch pipe device that ensures random distribution of plankton organisms over the different bags. Large components pollutants are added as single doses,
(> 2 mm) are filtered out. The model
since single additions are a close approximation of
the "normal" situation in marine waters if the source of a pollutant is an outfall, a river- or a dumping event
(Menzel and Case,
weeks, the development of decomposers,
1977). During the experiment, which lasts 4-6
phytoplankton and zooplankton is monitored,
as various abiotic parameters influencing the various trophic assemblages. tal results have been reviewed by Kuiper Figure
as well
The experimen-
(1981b).
i0 illustrates the development of phytoplankton in an experiment in which mercury
595
~00 200
chlorophylt (rag rn-3 )
/~"..~
~
z~/,/"~,, "
P.
100 50 20 7.0 05 02 07 005
\ \
002
I V I
o + os, 9.gt-' o 50
I
I
I
70
I
I
20
I
I
30
I
40 t,me [doys)
Fig. 10
The influence of a single mercury addition (as HaCZ^, indicated on time axis) on the development of chlorophyll concentrations " ~"~n ~a coastal plankton community enclosed by a plastic bag.
was added in different initial concentrations to different bags
(Kuiper,
1981a).Dissolved
mercury concentrations rapidly decreased due to adsorption to settling particles and volatilization into the atmosphere. Methylation was observed in the settled sediment. rophyll concentrations
The chlo-
in replicate bags indicate firstly a similar development op phyto-
plankton assemblages under idential conditions and secondly that major differences between the course of chlorophyll concentrations dition of the pollutant.
in the various bags can be attributed to the ad-
In this experiment the single addition of mercury inhibited phy-
toplankton growth as long as concentrations of mercury in the water were higher than about -1 1.5 Hg Hg.l . A further important effect was the shift in species dominance, expressed as the selection of larger cells at higher mercury doses. Species composition also changed in periphyton assemblages grown on glass slides susper~ed in the bags
(Groll~ and Kuiper,
were also found
(Kuiper,
1980). Significant effects on zooplankton and decomposers
1981a).
These results demonstrate the feasibility of conducting experiments with a complex system containing several interacting trophic levels and many competing species. The underlying
596
operating mechanisms,
however, are hardly understood.
sentive for natural conditions, pollution stress.
If the enclosed community is repre-
similar phenomena might be expected i n the open sea under
Structural changes on the autotrophic level might subsequently influence
the development of higher trophic levels in the food web. Observations of this kind might be an important supplement to toxicity data derived from routine laboratory experiments. 2)
In situ validation of biodegradation tests may be also important. In a series of experiments organic compounds were added as model pollutants to
bags to study their biodegradation under semi-natural conditions.
in situ
Figure 11 sun~arizes
results on the biodegradation of phenol in two different baq experiments and in laboratory tests. The phenol was deqraded rapidly by micro-organisms procedure
(cf. De Kreuk and Hanstveit,
in the standard laboratory
this volume).
x
% degrodahon ~00
/ o
/,
/
/
/
50
/ /
o
o
o
•
bog,
Aug
"77
o b a g , Sept
"78
x l a b . Sept
" 78
P
hme. days
I 5
10
Fig. 11 Degradation of phenol in two bag experiments (August 1977, initial dose 9 mg.Z-1; September 1978, 3.8 mg.1-1) and a laboratory experiment with the same water as used in the bag experiment (initial dose laboratory 3 mg.l-1). A high degradation rate was also observed in one bag experiment; however,
the other bag experiment,
showed biodegradation of phenol occurring at a much slower rate. Contrary to the
usual exponential decrease, bag experiment,
concentrations decreased linearly with time in this second
indicating that a factor other than the phenol substrate was limiting bac-
terial growth rates. Throughout this experiment ambient dissolved nitrate and phosphate concentrations were very low and the phenol-degrading bacteria had to compete for available
597
nutrients with other micro-organisms present.
Similar results were obtained with
4-chlorophenol. Extensive world ocean areas are oligotrophic probable that current laboratory
for large parts of the year. It seems therefore
biodegradation tests tend to overestimate the degradation
rate of organic compounds in nature; one factor in such tests being the exclusion of competition for nutrients between the compound-degrading bacteria and phytoplankton or other microorganisms.
4. Concludin~ remarks I) Literature data suggest that those chemicals that show biomagnification leading to physiological harmful concentrations in end predators,
in the food web,
are the most suspect.
Such pollutants are often persistent and lipophilic° 2) Retrospective
field studies can provide early warning signals of environmental damage caused
by pollution. Appropriate new techniques for the analysis of natural benthic co~Hnunities may provide a means of ecological m~hitoring
(e.g. the deviation of log-normal distributions ex-
hibited by the relative abundance of component species in large samples). At the individual species level, however, physiological or cytological techniques are becoming available that may be as sensitive and perhaps quicker.
Both approaches as yet lack sufficient chemical
specificity.
The bioavailability of specifi~ chemicals can be best detected or monitored by
experimental
exposure of suitable bioaccumulators.
Research into specific biochemical
indi-
ces should be pursued. 3) The development of prospective controlled ecosystem testing devices as validators for laboratory tests and as a final test in step sequence testing schemes should be supported. ~ile
changes in structural and chemical stress can be studied in the comparative short-
term by enclosing parts of ecosystems that serve as testing units, the building of indoor ecosystems with steady-state characteristics that can be studied under long-term low-level chemical stress, must be considered as important. 4) Standard routine toxicity studies in the laboratory are useful as a screening procedure to determine relative toxicities of single chemicals or mixtures.
Present-day scientific know-
ledge does not permit ready extrapolation to natural conditions. 5) Bioaccumulation
studies in the laboratory are useful in providing reference levels of pollu-
tant loads in tissues,
related either to sublethal,physiological,
cytological or biochemical
effects or to the interpretation of accumulated pollutant levels in biomonitoring studies with indicator organisms in the field. 6) Controlled ecosystems can be of important supplementary use in biodegradation studies or organic pollutants.
Persistency of such polluting chemicals in nature may be dependant on
competition for nutrients at lower trophic levels in the ecosystem. 7) Ecological factors concerning dose-effect relationships consultation procedures for international
in nature must be considered in
conventions to prevent aquatic pollution.
598
5. References • Adema, D.M.M., S.I. de Swaaf-Mooy and P. Bais:Laboratory investigations concerning the influence of copper on mussels
(MytiZu8 edulis).
TNO-Nieuws 27, 482-486
(in Dutch)
(1972).
• Bayne, B.L., M.N• Moore, J. Widdows, D.R. Livingstone and P. Salkeld: Measurement of the responses of individuals to environmental stress and pollution: Studies with bivalve mollusc~ Phil. Trans. R. Soc. Lond. B 286, 563-581
(1979).
• Bayne, B.L., D.R. Livingstone, M.N. Moore, A.R.D. Stebbing and J. Widdows: Ecological Monitoring (letter). Mar. Poll. Bull. ii, 8 p. 238
(1980).
• Bellamy, D.J., D•M. John, D.J. Jones, A. Starkie and A. Whittick: The place of ecological monitoring in the study of pollution of the marine environment• In: Marine Pollution and Sea Life, FAO (1972), pp 421-425
(Ed. Mario Ruivo) Publ. Fishing News
(Books)
Ltd.,
England (1972). • Bennekom, A.J. van, E. Krijgsman-Van Hartingsveld, G.C.M. van der Veer and H.F.J. van V o o r s t e The seasonal cycles of reactive silicate and suspended diatoms in the D u t c h W a d d e n Sea. J. Sea Res. 8
(2-3), 174-207
(1974).
• Bj6rklund, M.I.: Achievements in Marine Conservation• I. Marine Parks Environmental Conservation ~, 205-223
(1974).
• Boyden, C.R. and M.G. Romeril: A trace metal problem in pond oyster culture. Mar. Poll. Bull. 5 (7), 74-78
(1974).
• Bryan, G.W. and L.G. Hummerstone: Heavy metals in the burrowing bivalve
S$robicularia plana
from contaminated and uncontaminated estuaries• J. Mar. Biol. Ass. U.K. 58, 401-419 (1978). • Davies, J.M. and J.M. Pirie: The mussel
t.~tiZu8 eduZis
in sea water• Mar. Poll. Bull. ~, 5, 128-132
as a bio-assay organism for mercury
(1978).
• Davies, J.M. and J.C. Gamble: Experiments with large enclosed ecosystems• Phil. Trans. R. Soc. Lond. B 286, 523-544
(1979).
• Edwards, P.: Benthic algae in polluted estuaries• Mar. Poll. Bull. ~, 55-60 • Eide, I. and A. Jensen: Application of
in 8itu
(1972).
cage cultures of phytoplankton for monitoring
heavy metal pollution in two Norwegian fjords• J. Exp. Mar. Biol. Ecol. 37, 271-286 (1979). • Engel, D.W. and B.A. Fowler: Factors influencing cadmium accumulation and its toxicity to marine organisms• Environmental Health Perspectives 28, 81-88
(1979).
• Eppley, R.W. and C.S. Weiler: The dominance of nanaplankton as an indication of marine pollution: a critique. Oceanologica Acta ~, 241-245
(1979).
• Essink, K.: Mercury pollution in the Ems estuary. Helgol~nder wiss. Meeresunters. 33, 111-121
(1980).
• FAO: Summary of discussion, section 4, Ecosystem modifications and effects on marine communities. In: Marine Pollution and Sea Life, pp 348-349 (Ed. Mario Ruivo). Publ. Fishing News
(Books) Ltd., England
(1972).
• Fisher, N.S.: On the differential sensitivity of estuarine and open-ocean diatoms to exotic chemical stress. The American Naturalist 111, 981, 871-895
(1977).
599
Gamble, J.C., J.M. Davies and J.H. Steele: Loch Ewe Bag Experiment, Bull. Mar. Sci. 27,
I, 146-175
Goldberg, i.D.: The health of the oceans. The Unesco Press, Paris Goldberg,
1974.
(!977).
E.D., V.T. Bowen, J.W. Farrington,
(1976).
G. Harvey, J.H. Martin, P.L. Parker,
R.W. Risebrough, W. Robertson,
E. Schneider and E. Gamble: The mussel watch. Environmen-
tal Conservation ~, 2, 101-125
(1978).
Gray, J.S.: The fauna of the polluted river Tees estuary. Estuar. Coast. Mar. Sci. 4, 653-676
(1976).
Gray, J.S.: Pollution-induced changes in populations. 545-561
Phil. Trans. R. Soc. Lond. B 286,
(1979).
Gray, J.S.: Why do Ecological Monitoring?
(Viewpoint). Mar. Poll. Bull. Ii, 3, 62-65
Greve, W. and T.R. Parsons: Photosynthesis and fish production: climatic change and pollution.
(1980).
Hypothetical effects of
Helgol~nder wiss. Meeresunters. 30, 666-672
(1977).
Groll~, T. and J. Kuiper: Deyelopment of marine periphyton under mercury stress in a controlled ecosystem experiment. Hess, W.D.
Bull. Environm.
Contam. Toxicol. 24, 858-865
(1980).
(ed.): The Amoco Cadiz oil spill, a premliminary scientific report. US Dept.
of Commerce & US Environm. Agency,
281 pp, 66 plates
(1978).
Hueck, H.J.: Active surveillance and use of bioindicators. determining ecological criteria on hydrobiocenoses
In: Principles and Methods for
( C o m ~ s s i o n of the European Communi-
ties). Pergamon Press, Oxford, New York, pp 275-286
(1976).
Hueck, H.J. and E.H. Hueck-Van der Plas: A system of tests for the assessment of potential effects of chemicals and quality data in the aquatic environment. Methods for determining ecological criteria on hydrobiocenoses. European Scientific Colloquium Luxembourg, pp. 467-528
November
1975
In: Principles and
Proceedings of the
(Ed. R. Amavis and J. Smeets)
(1976).
Hueck-Van der Plas, E.H. and H.J. Hueck: The prospective assessment of environmental effects of chemicals. Kaesler,
Drug Design ~, 311-354
(1979).
R.L., J. Cairns Jr. and J.S. Crossmann:
Water Res. 8, 637-642
Redundancy in data from stream surveys.
(1974).
Kinne, O.: International Helgoland Symposium "Ecosystem Research": and closing".
Helgol~nder wiss. Meeresunters. 30, 709-729
Summary, conclusions
(1977).
Koeman, J.H.: Toxicologische aspecten van de oppervlaktewater kwaliteit. Proceedings of the Nationaal Symposium Milieuhygi~ne Landbouwhogeschool 89-92. Publ. PuDOC, Wageningen
Wageningen,
24-26 May 1976, pp
(1976).
Koeman, J.H. and H. van Genderen: Tissue levels in animals and effects caused by chlorinated hydrocarbon insecticides,
chlorinated biphenyls and mercury in the marine environment
along the Netherlands coast.
In: Marine Pollution and Sea Life, FAO
(Ed. Mario Ruivo). Publ. Fishing News
(Books) Ltd., Engeland
(1972), pp 428-435
(1972).
Kuiper, J.: Development of North Sea coastal plankton communities in separate plastic bags under identical conditions.
Mar. Biol. 44, 97-107
(1977a).
Kuiper, J.: An experimental approach in studying the influences of mercury on a North Sea coastal plankton community.
Helgol~nder wiss. Meeresunters. 30, 652-665
(1977b).
6OO
. Kuiper, J.: Fate and effects of mercury in marine plankton c o ~ u n i t % e s sures. Ecotoxicology and Environmental Safety• • Kuiper, J.: Ecotoxicological
In Press•
(1981a).
experiments with marine plankton communities in plastic bags.
Proceedings symposium on enclosed marine experimental ecosystems, Aug.
1980. Springer,
in experimental enclo-
New York. In Press•
Sidney, B.C. Canada,
(1981b)
• Ldcaze, J.C.: Utilisation d'un dispositif experimental
simple pour l'~tude de la pollution
des eaux in situ. Effets compar4s de trois agents ~mulsionnants antip4troles. 705-716
Tethys 3,
(1971).
• Levell, D.: The effect of Kuwait Crude Oil and the dispersant BP 1100 X on the lugworm
A~n~coZa mGl~na L. In: Marine ecology and oil pollution (Ed. J.M. Baker) pp 131-185. Applied Science Publishers Ltd., England
(1976).
• Luoma, S.N. and E.A. Jenne: The availability of sediment-bound cobalt,
silver and zinc to
a deposit-feeding clam. In: Biological implications of metals in the environment (Ed.: H. Drucker and R.E. Wildung), pp 213-231, • Margalef,
US NTIS, Conf. 750929
(1977).
R.: Perspectives in ecological theory. Chicago University Press,
iii pp, Chicago
(1968). • May, R.M.: Patterns of species abundance and diversity• munities
In: Ecology and evolution of com-
(Ed. M.L. Cody & J.M. Diamond), pp 81-120, Cambridge Mass.: Bellknap Press
(1975)• • Menzel,
D.W. and J. Case: Concept and design: controlled ecosystem pollution experiment.
Bulletin of Marine Science 27, • Menzel,
I, I-7 (1977)•
D.W. and J.H. Steele: The application of plastic enclosures to the study of pelagic
marine biota. Rapp. P.-v. Reun. Cons. int. Explor. Mer.,
173, 7-12
• Odum, E.P.: Fundamentals of Ecology, W.B. Saunder Cy., Philadelphia
(1978).
(1971).
• Oviatt, C.A., H• Walker and M.E.Q. Pilson: An exploratory analysis of microcosm and ecosystem behaviour using multivariate techniques. Marine Ecology - Progress Series 2, 179- 191 (1980).
• Parsons, T.R.: Controlled aquatic ecosystem experiments in ocean ecology research Mar. Poll• Bull. ~, 8, 203-205
(viewpoint).
(1978).
• Pearson, T.H.: The benthic ecology of Loch Linnhe and Loch Eil, a sealoch system on the westcoast of Scotland.
IV. Changes in the benthic fauna attributable to organic enrichment.
J. Exp. Mar. Biol. Ecol. 20,
1-41
(1975).
• Perkins, E.J.: The need for sublethal studies• Phil. Trans. R. Soc. Lond. B 286, 425-442 (1979). • Phillips,
D.H.J.: The use of biological indicator organisms to monitor trace metal pollution
in marine and estuarine environments - a review• Environ• •
Phillips,
Pollut.
13 (4), 281-317
(1977).
D.H.J.: Use of biological indicator organisms to quantitate organochlorine pollu-
tants in aquatic environments
- a review• Environ•
• Reeve, M.R., G.D. Grice, V.R. Gibson, M.A. Walter, ronmental pollution experiment zooplankton under toxic stress. Lockwood). Univ. Press
Pollut. 16,
167-229
(1978).
K. Darcy and T. Ikeda: A controlled envi-
(CEPEX) and its usefulness in the study of larger marine In: Effects of Pollutants on Aquatic Organisms
(Ed. A.P.M.
Society for Experimental Biology Seminar Series, vol. 2, 145-162, Cambridge (1976).
601
Reijnders,
P.J.B. Organochlorine and heavy metal residues in harbour seals from the Wadden
Sea and their possible effects on reproduction. Reijnders,
Neth. J. Sea Res.
P.J.H. Managements and conservation in the harbour seal
lation in the international Wadden Sea area. Biol. Conserv. Ringelberg,
J. and K. Kersting:
duction to the prototypes.
14 (1)
(Phoca vituZina) popu-
18 (4)
(1980b).
Properties of an aquatic micro-ecosystem: Arch. Hydrobiol. 83,
i, 47-68
(1980a).
I.General intro-
(1978).
Roskam, R.Th.: A case of copper pollution along the Dutch shore. In: C.M. Council Meeting, ICES, Near Northern Seas Comm., Paper no. 40 Roskam, R.Th.: Kopervergiftiging in zee. Water, Risebrough,
R.W., J. Davis and D.W. Anderson:
(1965). Bodem, Lucht 56,
H.L.: Marine benthic diversity:
I, 40-53
(1970).
a comparative study. Am. N~t.
Sanders, H.L.: Benthic diversity and the stability-time hypothesis. 22, 71-81
(1968).
Brookhaven Symp. Biol.
Experimental studies on the effects of copper on
a marine food chain. Marine Biology 29, 351-361 Scott, D.M. and C.W. Major: The effect of copper rate in the common blue mussel
196 pp
102, 243-282
(1969).
Saward, D., E.A. Stirling and G. Topping:
Smith, J.E.
(1966).
Effects of various chlorinated hydrocarbons.
Oregon State Univ. Env. Health Sci. Series, no. Sanders,
19-23
(1975).
(II) on survival, respiration and heart
MytiZu8 Bdulis. Biol. Bull. 143, 679-688 (1972).
(Ed.): Torrey Canyon Pollution and Marine Life. Cambridge University Press, (1968).
Study Group on Minemata D~sease
(Ed.): Minamata Disease. Kumamot9 University, Japan, 499 pp
(1968). Wilde, P.A.W.J. de and B.R. Kuipers: A large indoor tidal mud-flat ecosystem. Helgol~nder wiss. Meeresu/Iters. 30, 334-342
(1977).
Wolf, P. de, W.C. de Kock and A. Stam: Field experiments on the influence of copper and mercury in a natural musselbed. TNO-Nieuws 27, 497-504 Wolff, W.J.: The estuary as a habitat. Zeitzschel,
(in Dutch)
(1972).
Diss. Leiden. E.J. Brill, pp 1-242
(1973).
B,: Controlled environment experiments in pollution studies. Oceanology
International 78, 21-32
(1978).
Go2
Discussion after ~aper by W.Chr. de Kock and J. Kuiper I.Q.
J. Blok You showed data on the mercury contents of mussels in the Eems-Doliard estuary for 1974. Since then the discharge has been reduced drastically;
do you know what the
mercury contents was in 19797 A.
W.Chr. de Kock Information for later years is indeed available. The mercury contents is mussels has dropped since 1975/1976 and is now low. The same gradient that we showed for mussels was also observed for Macoma balthica, which has a depositfeeding behaviour for part of the time. The contents in this organism may still be higher than in filterfeeding mussels because of elevated mercury levels in the sediment. This particular problem should be further investigated.
2. Q.
Mommaerts Have the plastic bag experiments also provided data on physiological responses apart from the variations of chlorophyll contents or other stock variations? I refer here particularly to the ratio of primary production over biomass that has the same dimensions as a growth rate. Was it affected by the addition of mercury? How?
A.
J. Kui~er In the experiments in which mercury has been added to the enclosed plankton community primary productivity has been measured with the C-14 method. Results indicated that the primary productivity per unit chlorophyll was inhibited directly after the addition of mercury. However, indications were obtained that the division rate was inhibited over a longer period than the relative primary productivity. We have also found effects of addition of mercury and other model compounds on the enclosed com~/nity resulting from the changed interactions between primary producers and herbivores.
In the experiment ~n which mercury was added, the development of the
copepod populations was inhibited. of larger phytoplankton
Lower numbers of copepods resulted in the dominance
species, probably because of selective feeding of larger par-
ticles by the zooplankton.
3. Q.
A. Verloop The differences between the results of studies on the fate of pollutants in marine ecosystems on the one hand and in laboratory systems on the other, could be used to improve the laboratory testing systems. For example the differences observed in the case of mercury, as discussed by the authors, led to the suggestions that the laboratory test system Mytilus-water should be replaced by a system Mytilus-water-suspended
solids, so as to include also the physical and macro-
605
biological influences of the sediment,
in this case the methylation of the mercury.
Similar changes have been made or suggested for the laboratory testing systems used in the registration of pesticides, water-suspended
solids/hydrosoils
e.g. a fish-water system to be replaced by a fishfor the US EPA and the possible replacement of the
ditchwater system by a ditchwater-hydrosoil
system for the Dutch registration proce-
dure for pesticides. A.
W.Chr. de Kock We tried to point out that existing laboratory test routines as yet do not allow a feasible extrapolation to the field situation.
Incorporation of suspended matter in
the laboratory routine could therefore be a realistic improvement,
provided that the
ecological role of sediment is taken into account. This means that sediment variability itself is considered
(e.g. organic contents,
including living micro-organisms),
that there is enough insight into pollutant partitioning processes between water and sediment under different natural environmental conditions processes
(e.g. methylation of mercury in sediment)
(pH, 0 2) and that slow-rate
are included in the design. This
will be no easy task.
4.
Q,
A. Jensen You mentioned a concentration of I ppb mercury;
it was not clear to me if it was in
the water or in the bag after addition of mercury. A.
J. Kuiper Mercury was added to the bags in single doses at the start of the experiment to obtain initial concentrations of 0.5, 5 or 50 wg Hg.l -I in the water. The background concentrations in coastal waters near Den Helder are much lower.