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BORDEAUX AQUACULTURE 2001
Contaminants in marine foodwebs
A. ABARNOU, V. LOIZEAU, A.-M. LE GUELLEC and A. JAOUEN-MADOULET
IFREMER, Centre de Brest, B.P. 70, F-29280 Plouzané, Direction de l’Environnement et de l’Aménagement du Littoral, Département d’Écologie Côtière
e-mail : [email protected]
SUMMARY
RÉSUMÉ
The occurrence of organic contaminants in the environment raises important questions on their fate in trophic chains and thus on the exposition of
end consumers to such potentially harmful substances. This brief presentation of our studies begins with results obtained within the french marine
monitoring programme whose main objectives are the evaluation of status
and trends of contaminants. Examples are given for PCBs for which higher
contamination level are measured close to estuaries in relation with large
inputs from their whole catchment area. During last decade, decreasing
trends of the contamination are observed in most situations, similar improvements have been also observed in other developed countries, at least for
organic contaminants which are commonly monitored. The bioaccumulation model is presented; it has been validated for PCBs in the seabass foodweb in the Seine estuary and relies upon detailed biological functions of the
various species and the appropriate parameterisation of these functions. The
model demonstrates the importance of food as a major source of contamination for higher consumers. The improvement of the model and its use in
the case of less persistent compounds requires further studies in order to
take into account biotransformation. At last, recent results are given concerning the contamination dioxins (PCCDs/Fs) and «dioxin-like» PCBs ; it
appears that this group of «dioxin-like» contribute the most to the dioxin
toxicity.
Les contaminants dans les chaînes alimentaires marines. Par A.
ABARNOU, V. LOIZEAU, A.-M. LE GUELLEC et A. JAOUENMADOULET
KEY-WORDS : PCBs - PAHs - dioxins - foodweb - monitoring - bioaccumulation model - Seine.
MOTS-CLÉS : PCB - HAP - dioxines - réseaux trophiques
- monitoring - modèle de bioaccumulation - Seine.
The public awareness of the degradation of the environment, the fear of being exposed to potentially hazardous substances as well as the availability of more and more sensitive
and specific analytical techniques have prompted huge
amount of studies on the distribution and the fate of organic
chemical substances in the environment. Our group is greatly
involved in such studies in the coastal marine environment.
Firstly, our interest in organic contaminants in marine organisms is related to our participation in pollution monitoring
programmes whose main objectives are the assessment of
space-time variations of chemicals in coastal environment.
Secondly, we are currently studying organic contaminants in
marine organisms in our approach to the modelling of bioaccumulation of those substances in marine foodwebs. In this
Revue Méd. Vét., 2002, 153, 6, 425-432
La présence de contaminants organiques dans l’environnement pose la
question importante de leur devenir dans les réseaux trophiques et, finalement, celle de l’exposition des consommateurs finaux à de telles substances
potentiellement toxiques. Ce bref exposé de nos travaux démarre par une
présentation des résultats obtenus dans le cadre de programmes de surveillance du milieu marin littoral ayant pour objectifs l’évaluation des
niveaux et des tendances de la contamination. L’exemple des PCB montre
que des niveaux élevés sont mesurés à proximité des estuaires en lien avec
d’importants apports en provenance de l’ensemble du bassin versant. Cette
dernière décennie, des tendances à la baisse de cette contamination sont
observées fréquemment, de telles améliorations ont été observées en
d’autres pays développés, tout au moins pour les contaminants organiques
qui sont suivis dans le cadre de la surveillance continue. Le modèle de bioaccumulation est ensuite présenté, il a été validé dans le cas des PCB dans
le réseau trophique du bar en baie de Seine et il repose sur la connaissance
précise des fonctions biologiques des différentes espèces et de leur correcte
paramètrisation. Ce modèle démontre l’importance de la nourriture en tant
que source majoritaire de la contamination des consommateurs supérieurs.
L’amélioration du modèle et son utilisation plus générale à des substances
moins persistantes requiert de nouvelles investigations pour mieux prendre
en compte la biotransformation des substances. Finalement, les récents
résultats sont donnés sur la contamination par les dioxines (PCDD et PCDF)
et les PCB apparentés aux dioxines, il apparaît ainsi que ce sont les PCB qui
contribuent le plus à l’équivalent toxicité dioxine.
426
communication we intend to present a few examples of our
results. Starting with the status of the PCB (polychlorinated
biphenyls) contamination of the French coastal area, we will
then follow these compounds in the foodwebs and will end
by presenting very recent results on dioxins and dioxin-like
PCBs in mussels.
1. The monitoring programme :
the present status of the PCB
contamination
The French pollution monitoring programme RNO
(Réseau National d’Observation de la qualité du milieu
marin) was implemented in 1975. First hydrological surveys,
mainly on nutrients and environmental characteristics, were
initiated at that time whereas studies on contaminants in biota
began in 1979. Those investigations rely upon the capacity of
filtering bivalves like oysters or mussels to accumulate
contaminants from the water column and thus to integrate
over time the variability of the abiotic medium. The main
characteristics of this mussel watch programme has been
given yet [10]. Very briefly, depending on the species availability, mussels or oysters are sampled each quarter in
approximately 80 stations along the French coasts and analyzed for trace metals and organic contaminants among which
α and γ hexa-chloro-cyclohexanes (HCHs), PCBs, DDT and
its metabolites. PCBs are currently followed since the beginning of the RNO.
Amongst PCBs, the congeners CB153 and CB138 [6] eare
always the major contaminants in all biotic samples.
Moreover, it appears that the PCB composition in bivalves in
all the studied samples remains similar whatever the species,
(oysters or mussels), the date and period of sampling (year,
season), the origin of the samples (contamination level, geo-
ABARNOU (A.) AND COLLABORATORS
graphic origin). It follows that any congeners or any combination of congeners (sum of PCB congeners) might be used
to describe the PCB contamination along the coast.
The figure 1 and table I shows that CB153 concentrations
along French coasts vary within two orders of magnitude.
The main results on this contamination are :
- the median concentration in bivalves is approximately
40 ng.g-1 dry weight,
- low concentrations, around 5-10 ng.g-1 d. w., are measured in areas, like Northern Brittany, which are not influenced
by large riverine inputs,
- high concentrations, about 100 ng.g-1 d. w., are measured
in bivalves from areas close to estuaries or industrial and
urban areas,
- very high PCB concentrations, in the range are 300-500
ng.g-1 d.w., are found in mussels from the Seine estuary and
its adjacent area.
The Seine estuary and the Baie de Seine are heavily exposed to man made chemicals from terrestrial origin; the Seine
catchment area (about 79000 km2) is very urbanized (16 millions inhabitants) and industrialized (40 % of the French economic activity). The influence of the river Seine is observed
all along the shoreline of the whole bay. A contaminant
concentration gradient is found decreasing from the estuary
toward the open sea in relation with the residual circulation
of water masses within the bay. Moreover, concentrations are
higher in samples collected in winter than in those taken in
summer. On one hand, higher precipitation in the whole
catchment area might trigger higher inputs of contaminants
to the marine environment due to surface water streaming,
higher freshwater discharges within the estuary, and higher
tidal currents. These processes result in a greater availability
of contaminated sediments to filtering organisms due to
resuspension of surperficial sediment and larger inputs of
FIG. 1. — PCB contamination along the French coast. Concentrations in mussels or oysters used as «sentinelle species». CB153 in ng.g-1 dry weight. Data RNO,
1994 4th quarter.
FIG. 1. — Contamination en PCB des côtes françaises. Concentrations dans des «espèces sentinelles» : les moules ou les huîtres. CB153 exprimé en ng.g-1 de
poids sec.
Revue Méd. Vét., 2002, 153, 6, 425-432
CONTAMINANTS IN MARINE FOODWEBS
particles from the river to the coastal waters. On the other
hand, in spring and summer conditions, higher feeding rate,
acts as dilution factors which potentially decrease contamination levels in bivalves which live in cleaner conditions.
Another main objective of pollution monitoring programs
is the assessment of contamination temporal trends, particularly in relation with the observation of effects of regulatory
decisions like restrictions on the use of specific chemicals. In
the case of PCBs this cannot be done straightforwardly
because of the change of the analytical protocol in 1992. For
that purpose, banked mussel samples were re-analysed using
the new analytical methodology (analysis of individual
congeners using capillary column GC instead of quantification based on technical mixture equivalent obtained by packed column GC). Results for samples collected at the Cap de
La Hève, very close to the Seine estuary (fig. 2), show that in
summer contamination levels remain almost stable whereas
in winter the concentrations are much more variable and
decrease with an approximate mean rate of 4 % per year.
427
Similar observations have been reported in other European
countries [7] as results of limitations on the use of these substances (restricted use to closed systems in the 70s, reduction
and end of their production in most of the developed countries by the end of 80’s) Despite this improvement of the
water quality, PCB contamination remains at very high levels
in the Seine estuary which ranks it as one of the most contaminated coastal area in Europe.
2. PCBs and PAHs in foodwebs
The fate of organic contaminants in biota were investigated
in the bay and in the Seine estuary. In that respect, PCBs are
particularly interesting compounds : these man made chemicals are very hydrophobic and persistent and thus bio-accumulate and bio-magnify through foodwebs. Their well
known physico-chemical properties depend on the number
and position of chlorine atoms on the molecule. PAHs (poly
aromatic hydrocarbons) represent an other major group of
TABLE I. — Concentrations of PCBs (CB153) and PAHs in biota expressed in ng.g-1 dry weight. The compounds
are CB153, phenanthrene (Phen), pyrene (Pyr), benzo-a-pyrene (B-a-P), dibenzo-ah- anthracene (D-ah-A); the
species are: benthic species : Abra alba ; shrimp : Crangon crangon; goby : Pomatoschistus microps ; seabass :
Dicentrarchus labrax ; flounder : Platichtys flesus.
TABLEAU I. — Concentrations en PCB (CB153) et HAP dans le biote, exprimées en ng.g-1 de poids sec.
FIG. 2. — PCB contamination trends near the Seine estuary (Cap de La Hève).
FIG. 2. — Evolution de la contamination en PCB près de l’estuaire de la Seine (Cap de La Hève).
Revue Méd. Vét., 2002, 153, 6, 425-432
428
ABARNOU (A.) AND COLLABORATORS
organic contaminants of terrestrial origin. Their major
sources in the coastal marine environment are either from
petroleum origin (petrogenic hydrocarbons) as leakages
occur during the transport and the use of oil or from combustion processes (pyrogenic hydrocarbons) associated with the
production energy production (thermic power plants, combustion engines,...) and the incineration of solid wastes.
1) PCBS AND PAHS IN PLANKTON
PCBs and PAHs were measured in plankton within the
frame of the PNEC research project (Programme National
d’Environnement Côtier, Chantier Baie de Seine). These
compounds have similar hydrophobicity (Kow 103 to 107)
and are assumed to enter the food chain, in a similar way, by
passive exchanges of contaminants from the water column
onto the surface of phytoplanktonic cells. This step corresponds to bioconcentration and has been described by various
empirical relationships [12, 11, 2].
In the present study, carried out in May 1998 in the eastern
part of the Baie de Seine, plankton was collected by filtering
surface water using successive plankton nets with decreasing
mesh size (from 500 to 20 µm) enabling to separate zooplankton (> 200 µm) from phytoplankton and detritic material. Preliminary results (fig. 3) shows the presence of both
PCBs and PAHs in the lower part of the food chain: the two
classes of compounds are bioconcentrated by phytoplankton.
In higher trophic levels, PCBs are concentrated from phytoplankton to zooplanktonic species whereas PAHs behave differently depending on their chemical structure. Apart from
the bioaccumulation processes which differ between PCBs
and PAHs, these contaminants appear also to behave differently, depending on environmental conditions, whether sampling was carried out during or after the phytoplanktonic
bloom.
2) PCBS AND PAHS IN ESTUARINE FOODWEBS
These two groups of compounds were analyzed in the
flounder (Platichtys flesus) and seabass (Dicentrarchus
labrax) foodwebs in the estuary within the research project
Seine Aval [13, 3]. The partial results, limited to a few compounds, show that PCBs are bio-accumulated from phyto-
CB153 ng g-1 d.w.
plankton to higher trophic levels (fish) whereas on the opposite PAHs enter the food chain and are rapidly bio-transformed depending on their structure and on the capacity of the
various organisms to metabolize these compounds.
3) THE SEABASS BIOACCUMULATION MODEL
During the research project Seine Aval, PCBs were systematically measured in the seabass and organisms that compose its foodweb in order to built and validate a bioaccumulation model (Fig. 4). This work has been successfully performed thanks to an efficient cooperation between biologists,
ecotoxicologists, modellers and chemists. The simplified
seabass foodweb includes phytoplankton, detritus, zooplankton (represented by the copepod Eurytemora sp.), supra benthic species including shrimps (Palaemon longirostris,
Crangon crangon) and gobies (Pomatoschistus microps) and
the sea bas as the top predator.
At the lower part of this food chain, concentrations in phytoplankton and detritus are forced variables calculated from
measurements in water (truly dissolved concentrations) [18]
using empirical relationships found elsewhere [8]. The model
is a bio-energetic model relying upon biological functions
which act on the uptake and clearance of contaminants [19,
17, 4, 15, 16]. For each species, the basic equation of bioaccumulation describes a mass balance budget between inputs
and outputs of the chemical substances:
dCi/dt =
Ri . aiw .Cw + ∑ij Fi. Pij. aij. Cj - (Ei + Gi + Repi + Mi). Ci
where CW, Ci and Cj are respectively the concentrations of
contaminant in water, in the organism and in its preys ; Ri, Fi,
Ei, Gi, Repi and Mi are respectively the respiration, feeding,
elimination, growth, reproduction (loss of contaminants
during spawning) and metabolization rates of the ith organism; Pij represents the contribution of the various preys j to
the diet of i whereas aiw and aij are the assimilation efficiency
coefficients of the contaminant by the ith organism when it is
absorbed from the water or from the jth prey. The physiological functions, obtained from literature survey, are functions
of the size of the organisms (size or weight - age relationships) and depend on environmental conditions like dissolved oxygen and temperature.
Chrysene ng g-1 d.w.
40
300
20
150
5 may
17 may
0
0
20
43
80
200
500
size (µm)
20
43
80
200
500
size (µm)
FIG. 3. — PCBs (CB153) and PAHs (chrysene) in plankton.
FIG. 3. — Teneur en PCB (CB153) et HAP (chrysene) dans le plancton.
Revue Méd. Vét., 2002, 153, 6, 425-432
CONTAMINANTS IN MARINE FOODWEBS
429
FIG. 4. — Validation of the bioaccumulation model : PCBs in seabass, comparison of calculated concentrations with measurements.
FIG. 4. — Validation du modèle de bioaccumulation : teneurs en PCB des bars, comparaison entre valeurs calculées et valeurs mesurées.
The model has been validated in steady state conditions in
the case of male seabass in its 3rd year and in may. Within
these conditions there are no effects of the reproduction and
of metabolization. PCBs are assumed not to be biodegraded
in this food chain an assumption supported by their highly
persistent character. Calculated concentrations are in very
good agreement with actual measurements. The steady state
version of the model may be used to calculate the relative
contribution of water and food to the PCB contamination ; it
appears that, in the case of these highly hydrophobic compounds feeding is by far the largest source of contamination
for seabass, accounting for more than 90 % of the total load.
The contribution of water, due to respiration, would increase
either in the case of slightly more soluble substances or for
species from lower trophic levels.
The agreement between modelled PCB concentrations and
field data would suggest that biological processes have been
correctly described by the model and that, in principle, this
model could be used to simulate the fate of any compounds in
the seabass foodweb. This will be true when metabolization
is precisely described and simulated by the model : the comparison of PAHs and PCBs [13, 4] clearly indicates the
importance of this process.
To summarize, our main results on these two classes of
compounds show that PCBs are bioaccumulated or biomagnified through food-webs with conservation of the PCB
patterns in the various organisms. On the contrary, PAHs are
not at all bioaccumulated but are bio-transformed. This biotransformation of PAHs is related both to the chemical structure of the compounds and to the metabolizing capacity of the
species which leads to different PAH fingerprints in the
various organisms that make up the foodwebs.
Revue Méd. Vét., 2002, 153, 6, 425-432
A next step in our attempt in modelling the fate of xenobiotic compounds in biota should include the processes
acting on bio-transformation. This is particularly needed in
the case of compounds which can temporarily enter food
chains and due to their toxic properties might cause deleterious effects to sensitive organism and modify the functioning of the foodwebs.
3. Dioxins and «dioxin-like»
compounds
As far as the toxicological aspects of organic contamination are concerned, we might think of dioxins which are
structurally related to the aforesaid compounds and which are
considered as the most toxic pollutants ever produced.
The generic name of dioxins includes PCDDs (poly chloro
dibenzo para dioxins) and PCDF (poly chloro dibenzo
furans). This large group of distinct compounds,- 75 and
135 congeners for PCDDs and PCDFs respectively- has
never been intentionally produced. They are unwanted byproducts of chemical processes like the production of chlorophenols and chloro phenoxy-acetic acids (used during the
Vietnam war as defoliant agent), the «old» chloro-bleaching
processes used in pulp and paper production, and they are
also formed during combustion, notably the incineration of
solid urban wastes which is now the major source of emission
of dioxins in the environment [1]. It has been claimed that
dioxins have been present in the environment since the event
of fire [9] but their presence in the environment increased
significantly with the development of industry in the 19th and
20th centuries and peaked around 1970-80 [14].
430
ABARNOU (A.) AND COLLABORATORS
Within PCDDs and PCDFs, the 2,3,7,8-tetrachloro
dibenzo-p-dioxin or Seveso dioxin, is very toxic and has been
thoroughly studied. Other structurally related compounds
with the same 2,3,7,8- substitution scheme possess similar
activity based on the same mechanism as that of 2,3,7,8TCDD. On behalf of various international agencies, experts
in toxicology agreed on the potential toxicity of this group of
2,3,7,8- substituted PCDDs and PCDFs. These dioxins were
given toxic equivalent factors (TEF) related to the 2,3,7,8TCDD. The TEF concept (table II) is very useful to express
measurements in term of the TEQ (Toxic Equivalent
Quantity) by simply adding «TEF weighted» concentrations
of dioxins in the samples (TEQ = ∑ici x TEFi) which is much
simpler than considering concentrations of 17 different compounds and informs on the potential toxicity of complex mixtures.
More recently, TEF were also established for «dioxin-like»
PCBs (table II) ; these molecules with no or only one chlorine
in ortho position may possess a stereo-chemistry very close
to that of the 2378 TCDD molecule (coplanarity and similar
dimensions). This approach to the PCB toxicity which is
mainly based on quantitative structure-activity relationship
(QSAR) developments might appear too simplistic and is still
under debate among toxicologists. The questions are related
to the over simplification of the biological effects of PCBs
which act on very different receptors unlike dioxins and have
many very different types of effects. For these reasons, the
generalised use of TEF might be done with caution and only
give indications of a potential toxicity related to specific
modes of action.
Dioxins and «dioxin-like» PCBs in bivalves have been studied very recently within the research project «LiteauDioxines». The main objective was to get information on the
presence of these controversial pollutants along the French
coastline. For that purpose, these compounds were analysed
in a limited set of mussels and oysters samples collected in
pre selected stations currently monitored within the RNO.
The 18 sampling stations were chosen in order to describe the
whole situation of the French coasts.
It is well beyond the scope of this presentation to point out
the precise distribution of dioxins along our coast ; this will
be done in a further report by considering both the concentrations and the relative distribution of dioxins in samples as a
potential information on their origin. These preliminary
results are given (table III) in TEQ which is currently done
for dioxins and might be questionable for dioxin-like PCBs.
Higher dioxins concentrations are measured in estuarine
waters, which obviously is also true for «dioxin-like» PCBs
which follow the same trend as the aforesaid indicator PCBs
currently monitored.
On a fat basis, the mean concentration of dioxins, 54 pg.g-1
extractable material, is very similar to results given for crustaceans and shellfish in a previous French survey on the
dioxins in food where it was found TEQ equal to 50 pg.g-1
[5]. The normalisation of the compounds concentration to
lipid content can lead to misinterpretation of the results : this
mode of calculation (ratios of concentrations) penalises products with low fat content which in many case are considered
as safer in view of the overfeeding problems of people from
rich countries. Moreover, the fat content is in most case an
operationally defined parameter (the weight of an extract in
defined conditions according to a specified procedure)which
does not qualify properly a component or a group of components and whose composition can vary. In the case of fish and
sea products, this fat content and its composition depend on
many various biological factors (species, age, sex, physiologic status,...) as well as on environmental parameters (temperature, starvation,...).
There are no environmental guidelines to ascertain the
importance of these results on dioxins. An attempt was done
using the more recent WHO recommendation which established the TDI (Tolerable Daily Intake) range between 1 and 4
pg TEQ /kg body weight for dioxins and dioxin-like PCBs
TABLE II. — TEF (toxicity equivalent factors ) for dioxins (PCDDs and PCDFs ) and dioxin-like compounds.[20].
TABLEAU II. — Facteur d’équivalence toxique pour les dioxines et les furanes et les PCB.
Revue Méd. Vét., 2002, 153, 6, 425-432
CONTAMINANTS IN MARINE FOODWEBS
[21]. It means that based on the mean dioxins concentrations
we found in mussels (2.5 pg.g-1 dry weight or 0.5 pg.g-1 wet
weight) the TDI will be reached by a man with a 60 kg body
weight, who consumes 120 g mussels. Much lower amount
would be sufficient to reach the TDI by eating mussels from
contaminated areas and taking into account PCBs concentrations which, despite their potential lower effects and lower
TEF, are present at concentration several orders of magnitude
higher than dioxins. These troublesome observations must be
also relativised by other observations on contamination
trends which indicate a general improving situation, at least
for measured and monitored substances.
Conclusions
The examples given above were obtained within environmental studies whose objectives are related to the status of
the contamination along the French coast and the processes
acting on the distribution of contaminants in coastal marine
organisms. Did they answer to underlying question of this
symposium concerned with the scientific bases for the evaluation of chemicals risk associated with sea farm and sea
food products ?
Limited examples have been given on PCBs and dioxins in
monitoring surveys that show that residues of these hazardous substances are present everywhere, sometimes in high
concentrations. Such work on the baseline level of contaminants should be maintained and encouraged, with if necessary a more adapted sampling strategy or methodology in
view to answer the different objectives, environmental
impact and food safety. There is a need to enlarge a similar
approach to other compounds that can reach marine ecosystems and affect marine organisms.
Further examples were provided with our approach to
modelling the fate of persistent compounds in biota. Our
PCB bioaccumulation model, as well as other similar models,
have demonstrated the importance of food as a major source
of contamination by hydrophobic and persistent compounds.
Such models may be very useful tools for risk assessment as
they differentiate the exposure routes. However, the use of
our PCB model would overestimate predicted concentrations
of less persistent compounds, which in term of prediction is
safer because predicted concentrations represent a worst
case. There is a need to account for bio-transformation in
future models which will improve the accuracy of prediction
particularly in relation with the assessment of the exposure of
aquatic species to hazardous substances.
431
Acknowledgements
Most of the examples presented come from work carried
out recently within different projects. We thank our colleagues from Ifremer responsible for those projects, D.
CLAISSE (DEL-PC, Nantes) for the Réseau National
d’Observation du milieu marin, A. MÉNESGUEN (DEL-EC
Brest) for the Programme National d’Environnement Côtier Chantier Baie de Seine, A. ROMAÑA (DEL-PC Toulon) for
the Programme Scientifique Seine-Aval. We are also indebted to the Ministère de l’Aménagement du Territoire et de
l’Environnement for funding the project Liteau-Dioxines and
permitting us to present preliminary results. Many thanks
also to our colleague A.-C. LE GALL (Ifremer DEL-EC
Brest) for improving our text.
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