BORDEAUX AQUACULTURE 2001
Biomarkers : useful tools for the monitoring
of aquatic environments
L. LAGADIC
UMR 985 INRA-ENSAR Écobiologie et Qualité des Hydrosystèmes Continentaux, 65 rue de Saint-Brieuc,F-35042 Rennes Cedex
Tél: (33) 02.23.48.52.37, Fax: (33) 02.23.48.50.20, E-mail : [email protected]
SUMMARY
RÉSUMÉ
The approaches for monitoring environment quality can be classified in
two different categories : (1) the detection and/or quantification of stressors
in both physical and biological compartments of the ecosystems (physicochemical approach), and (2) the evaluation of exposure of living organisms
and subsequent effects at the individual, population and/or community
levels (biological approach). Indices have been defined for both approaches.
Threshold levels for pH, temperature, conductivity, oxidizable matter
content, oxygen saturation, nitrogen, phosphorus and ion concentrations,
organic contaminant and metal levels are used as physico-chemical indices
to assess the quality of aquatic environments and water resources. Similarly,
biological indicators have been developed to evaluate the impact of environmental stress on aquatic organisms at various levels of biological organisation. Among these biological indicators, biomarkers are used as tools to
assess molecular, biochemical, cellular, physiological or behavioural
changes that may reveal exposure of organisms to environmental chemicals.
In some cases, biomarkers are able to indicate that chemicals specifically
affect metabolic pathways or physiological functions in exposed individuals. Therefore, biomarkers can be used as both diagnostic and predictive
tools. A number of case-studies demonstrated that biomarkers are useful
tools to detect the presence of xenobiotics in living organisms and to diagnose individual health. However, interference with natural environmental
factors or endogenous parameters may complicate the interpretation of biomarker responses, and sampling and measurement procedures must be properly designed and accurately followed. A more recent and fairly promising
way to use biomarkers is based on mechanistic links that can be established
between effects revealed in individuals and subsequent changes in populations and communities. Though rarely applied to natural ecosystems, the
use of such an approach should be able to predict the effects of stress on
populations and/or communities from measurements of biomarkers in individuals of selected species sampled in the field.
Les biomarqueurs, des outils pour le suivi de la qualité des milieux
aquatiques. Par L. LAGADIC.
KEY-WORDS : biomarker - environmental quality assessment - diagnostic - pollutants - endocrine disruptor physiological energetics - aquatic organisms.
MOTS-CLÉS : biomarqueur - qualité de l’environnement
- diagnostic - polluants - perturbateur endocrinien métabolisme énergétique - organismes aquatiques.
Revue Méd. Vét., 2002, 153, 8-9, 581-588
Le suivi de la qualité de l’environnement fait appel à deux types de
méthodes (1) la détection et/ou la quantification des facteurs de stress dans
les compartiments physiques et biologiques des écosystèmes (approche
physico-chimique) et (2) l’évaluation de l’exposition des organismes et de
ses répercussions au niveau de l’individu, de la population et de la communauté (approche biologique). Des indices ont été définis pour chacune de
ces deux approches. Des valeurs-seuils de pH, température, conductivité,
taux de matière organique, taux de saturation en oxygène dissous, concentrations en azote, en phosphore ou en ions, concentrations en polluants
organiques ou en métaux sont autant d’indices physico-chimiques utilisables pour évaluer la qualité des milieux aquatiques et des ressources en
eau. De façon comparable, des indicateurs biologiques ont été développés
afin d’évaluer l’impact de stress environnementaux sur les organismes
aquatiques, et ce à différents niveaux d’organisation biologique. Parmi ces
indicateurs biologiques, les biomarqueurs sont utilisés en tant qu’outils pour
déceler les changements moléculaires, biochimiques, cellulaires, physiologiques ou comportementaux susceptibles de révéler l’exposition d’un organisme à des polluants chimiques présents dans l’environnement. Dans certains cas, les biomarqueurs peuvent même renseigner sur les atteintes spécifiques d’une voie métabolique ou d’un processus physiologique. De nombreuses études de cas montrent que les biomarqueurs sont des outils performants pour détecter la présence de xénobiotiques dans les organismes et
pour effectuer un diagnostic de l’état de santé des individus exposés.
Cependant, les interférences avec des facteurs environnementaux naturels
ou avec des régulations physiologiques endogènes peuvent parfois compliquer l’interprétation des réponses des biomarqueurs. Les conditions
d’échantillonnage et de mesure sont donc déterminantes pour garantir la fiabilité des informations apportées par les biomarqueurs. Actuellement, l’utilisation des biomarqueurs s’oriente de plus en plus vers une approche basée
sur les relations mécanistes pouvant être établies entre les effets observés au
niveau des individus et les changements au niveau des populations et des
communautés. Bien qu’encore rarement appliquée dans les écosystèmes
naturels, cette approche pourrait permettre de prédire l’évolution des populations et/ou des communautés à partir de mesures de biomarqueurs réalisées chez des individus directement prélevés dans des milieux soumis à des
pollutions chroniques.
582
LAGADIC (L.)
Introduction
The general framework of the monitoring of ecosystem
quality can be defined on the basis of the following four
questions [1] :
How bad is the situation ?
Is it getting better or worse ?
Why do we have these problems ?
What can we do to improve the situation ?
The first question refers to the assessment of ecosystem
quality, whereas the second implies a dynamic approach
which tries to establish how the ecosystem quality is changing. The third question refers to the origin of environmental
changes, and may result in a more fundamental approach
based on experimental works. The last question has at least
two major components: a scientific component which may
result in proposals for remediation, and a socio-economic
component which involves efforts from public authorities
and industries. This last question will not be further developed in the present paper. Instead, emphasis will be placed on
how invertebrates can help to answering the first three questions.
Monitoring the quality of the
environment : the Biomarker
Approach
A) SIMPLIFIED PRESENTATION
Broadly speaking, biomarkers are biochemical or physiological parameters that can be measured in individuals to
indicate exposure to environmental chemicals and, for some
of them, to detect toxic effects [2-6]. As such, biomarkers
describe individual health, and therefore can be considered as
diagnostic tools. When individual changes revealed by bio-
markers can be connected to actual or potential changes at the
population level, those biomarkers can be considered as predictive tools [7, 8]. Both approaches are important components of the assessment of the extent of ecological damage,
and of the evolution of ecosystem quality, especially when
remediation has been undertaken (Fig. 1).
B) DIAGNOSTIC APPROACH : BIOMARKERS AND
ENVIRONMENTAL IMPACT OF POLLUTANTS
A number of biomarkers have been identified [3, 7], and
some of them, such as cytochrome P450, acetylcholinesterase, metallothioneins, and DNA damage, which have the
advantages of specificity, sensitivity and applicability are at
an advanced stage of usage or development as diagnostic
tools [9] (Fig. 2).
When higher than natural variability, the response of a biomarker indicates that environmental changes may have affected the individuals in which the biomarker has been measured. Then, the origin of the disturbance must be determined.
Various approaches may be used to detect the presence of
pollutants and, in the best cases, to identify them or on the
contrary, to show that pollutants may not be responsible for
biomarker response. This situation describes the most common case, because every biomarker presently used is not specific for one unique type of pollutant.
However, some biomarkers respond to a relatively restricted range of pollutants. Thus, cytochrome P4501A (or related
isoforms) is classicaly recognized as specific for the presence
of polycyclic aromatic hydrocarbons, though other compounds such as pesticides are known to cause its induction
[10-13]. Similarly, acetylcholinesterase reacts quite specifically to organophosphorous compounds and carbamates,
though it also responds to metals [14,15]. Even if they do not
unequivocally indicate the nature of the contaminants, such
biomarkers allow to limit the analytical screening to a few
chemical families, thus significantly reducing the cost of analyses.
FIGURE 1.— Biomarkers as diagnostic and predictive tools for environmental quality assessment.
Les biomarqueurs : des outils de diagnostic et de prévision pour l’évaluation de la qualité environnementale.
Revue Méd. Vét., 2002, 153, 8-9, 581-588
BIOMARKERS : USEFUL TOOLS FOR THE MONITORING OF AQUATIC ENVIRONMENTS
583
FIGURE 2.— Batteries of biomarkers available for the diagnostic of environment quality.
Batteries de biomarqueurs disponible pour l’évaluation de la qualité de l’environnement.
Since biomarkers may only reveals a (more or less recent)
past exposure to toxicants [16] and considering the specificity of response of some of them, the relevance of chemical
analysis is questionable. Basically, two distinct cases may be
considered. In the first case, the exact nature of the pollutants
is known and the sources of discharges are identified and
even controlled. The use of biomarkers allows to ensure that
the conditions of discharge (defined using physico-chemical
criteria and more rarely toxicological criteria) are respected.
In particular it gives the opportunity to ensure that discharge
levels do not exceed the capacities of the receiving medium
or of organisms which live therein. In the second case, biomarkers give the opportunity to detect accidental, illicit,
and/or diffuse discharges. According to the intensity and
extent of biomarker response, alert procedures may therefore
(or not) be activated to identify the source of pollution
without any information on the nature of contaminants.
C) PREDICTIVE APPROACH : BIOMARKERS AND
ENVIRONMENTAL RISK ASSESSMENT
Since biomarkers can be used to detect the presence of
environmental contaminants and may provide informations
on the effects of pollutants on organisms, they may be used
for the assessment of environmental quality. Is it possible to
predict the effects of pollutants on populations, communities
and ecosystems from measurements performed at the individual level ? The assessment of ecological risk associated with
the release of chemicals in the environment is a key problem
in the context of sustainable development and long-term
conservation of environmental quality. The relevance of biomarkers for environmental risk assessment has recently been
under discussion and some interesting perspectives have
been drawn [17-20]. All the arguments that have been presented in this debate are not reviewed here in detail but, it
seems interesting to recall the definition and rationale of ecological risk assessement in order to investigate the possible
role of biomarkers in such an approach.
Revue Méd. Vét., 2002, 153, 8-9, 581-588
Environmental risk assessment corresponds to an estimate
of the probability that an adverse effect will occur in response
to the presence of one or several factors of disturbance [18,
21]. Risk assessment for chemicals is based on four successive steps [22] :
- Hazard identification is performed using toxicity test data
obtained for both target and non-target organisms.
- Establishment of dose-response relations is used to experimentally determine the toxic activity of compounds.
- Exposure assessment is based on evaluation of the nature
and size of populations or ecosystems at risk, as well as the
frequency, duration, and intensity of contact with the chemical.
- Risk characterization is performed using data from the
three preceding steps. It provides a quantitative and qualitative prediction of the probability that a harmful effect will
occur.
Most biomarkers fulfil the two first steps but the extrapolation of individual responses to changes in populations or
communities is still difficult [23]. No in situ study has yet
demonstrated that the effect of a chemical on a critical target
in an individual was responsible for changes in the population to which it pertains. A posteriori studies on the effects of
organochlorine pesticides (DDT, DDE) on certain bird populations (peregrine falcon in Great Britain, fish-eating birds in
the North American Great Lakes) have shown that population changes were linked with effects of toxicants on individuals [5]. Although interesting from a scientific point of
view, this approach is at the opposite of the ecological risk
assessment approach since there is no prediction of the
effects at the population level but only a reconstruction of
passed phenomena.
So far, the use of biomarkers in environmental risk assessment for chemicals still depends on the identification of causal relationships or mechanistic links between the reaction of
individuals to exposure and changes in populations and com-
584
LAGADIC (L.)
munities. Some studies have already initiated this research
for aquatic animals [24], but extrapolation of effects of pollutants across different levels of biological organization still
largely depends on theoretical or conceptual links. Although
this approach can be justified in the context of research and
development of biomarkers, it rarely meets the needs of
managers of environmental quality who are generally looking for a diagnostic of the state of the environment. Since
one of the future prospects of biomarkers is their use in environmental risk assessment, suitable validation procedures
should be rapidly implemented [18, 25, 26].
Extrapolation from the individual to the population and community
A) GENERAL OVERVIEW
The action of environmental pollutants on the individual
may result in various internal changes (Fig. 3). Once a chemical penetrates the organism, it binds to various molecules
within different tissues. Those molecular interactions result
in metabolic changes which may affect different functions at
the cellular and tissue levels with consequences at the individual level (e.g. disease development, reduced growth, altered
behaviour, impaired reproduction). In this respect, impact on
the nervous system usually results in serious disorders in
individuals and also in changes in inter-individual relationships.
Most metabolic processes and individual functions are
mediated by hormones and require energy. Hormonal control
and energetic balance are therefore of primary importance as
they both determine eventually the reproductive capacity of
the individual, and reproduction is the key-process that links
the individual to the population. Successful reproduction is
essential for the continuation of the species. The reproductive
success of individuals determines population characteristics
in terms of structure/composition, density/size, and stability/evolution.
Community level effects depend on both population functions and interactions between populations. Population functions result from both the previous demoecological parameters (structure/composition, density/size, stability/evolution)
FIGURE 3.— Extrapolation of effects from the individual to the population and community : General overview.
Extrapolation des effets de l’individus aux populations et aux communautés : vue d’ensemble du problème.
Revue Méd. Vét., 2002, 153, 8-9, 581-588
BIOMARKERS : USEFUL TOOLS FOR THE MONITORING OF AQUATIC ENVIRONMENTS
and individual health, and may induce changes in physicochemical conditions. Interactions between populations are
considered as an essential component of community stability
and ecosystem function. If the external perception of environmental factors in individuals is affected by neurotoxic
pollutants, changes in interspecific relationships may occur,
with potential consequences on communities.
Animal reproduction, as expressed through fecundity and
fertility, can be impaired as a result of both direct impact of
toxicants on the endocrine system, and indirect effect on
energy allocation. Besides alterations in courtship and
mating behaviour, changes in reproduction can be caused by
changes in maturation of gametes, fertilization process and
age of sexual maturity, or by morphological abnormalities in
adults. Reduction of fertility result from the effects of contaminants on egg viability, larval development, or hatching of
youngs. Hormonal and energetic biomarkers can be used to
detect changes in fecundity and fertility, and can also be related to individual growth [7, 23, 27, 28]. Such biomarkers are
therefore considered as potential predictive indicators of
changes in populations, with possible consequences on communities. However, only a few studies have so far demonstrated causal links between hormonal or energetic alterations
in individuals and changes in populations and communities.
This requires a good knowledge of the succession of pollutant effects across levels of biological organisation, as illustrated by the following examples.
B) EFFECTS OF ENDOCRINE DISRUPTORS IN INVERTEBRATES : CASE-STUDY OF TRIBUTYLTIN (TBT) IN
COASTAL ECOSYSTEMS
The effect of pollutants on the endocrine system have
received considerable attention over the past five years [29].
Endocrine-disrupting effects of environmental chemicals
have long been demonstrated in invertebrates. A number of
plant allelochemicals are known to affect growth and reproduction of insects by acting as hormone mimics [30].
Synthetic hormone mimics have also been developed as
insecticides against insect pests (e.g. diflubenzuron, teflubenzuron, tebufenozide) [31-33]. More recently, endocrine-disrupting effects of environmental chemicals have been identified in freshwater crustaceans [34-37] and marine molluscs
[38, 39]. In these latter, tributyltin (TBT) was identified as
the compound acting on the reproductive system of individuals, and from a twenty year long field survey, the progression of effects from the molecular level to communities has
been established, as summarized below.
TBT is an organotin compound used in antifouling paints
applied onto boats. Long-term studies on marine gastropod
populations have demonstrated that TBT induces a phenomenon named ‘imposex’ which results in the development of
male characteristics in females. This change was first identified in Nucella lapillus [40] and Nassarius obsoletus
(= Ilyanassa obsoleta) [41] and has been reported in more
than 40 species of marine mollusc exposed to TBT [42]. The
dogwhelk Nucella lapillus and the oyster drill Ocinebrina
aciculata are highly susceptible to TBT and are being largely
used for investigating its effects at sub-cellular, individual
Revue Méd. Vét., 2002, 153, 8-9, 581-588
585
and population levels [reviews in 38, 39, 43]. In females,
TBT may inhibit cytochrome P450-dependent aromatase
which converts testosterone to 17β-oestradiol. Inhibition of
sulphur conjugation and excretion of testosterone and its
metabolites is another putative pathway of TBT mode of
action. In any of those situations, the level of male steroids
increases, leading to anatomical changes in the reproductive
system. Following the development of the penis and vas
deferens, the affected females become sterile and eventually
die. As a result of reduced reproductive output and individual
death, populations decline. Extinctions of populations of N.
lapillus and O. aciculata have even been reported [43, 44].
In spite of the role of N. lapillus in shore communities as a
necrophagous species, as investigated by experimental manipulations of field populations, no community level effects
were clearly demonstrated as a consequence of dogwhelk
population decline. This may result from the lack of longterm observations of dogwhelks in the context of the whole
community on such shores, and also from compensatory
mechanisms which are able to maintain the communities
functional (e.g. replacement by other necrophagous species
such as decapod crustaceans), except in the case of catastrophic events such as oil spills [38].
Since the use of TBT in antifouling paints has been restricted in 1982 in France and in 1987 throughout Europe, North
America, Australia and Japan [45-47], the degree of imposex
in some dogwhelk populations has decreased [48], but the
process of recovery of all affected populations and communities is likely to be slow as bioaccumulation still occurs in
some organisms that now recolonize the contaminated areas
[38, 46, 47].
This case-study demonstrates that the effects of reproductive impairement on marine molluscs populations and consequences on communities can conceivably be predicted from
individual measurements of biomarkers which represent
potent early-warning indicators of environmental pollution
by endocrine-disrupting chemicals.
C) EFFECTS OF POLLUTANTS ON INVERTEBRATE
BIOENERGETICS : CHANGES IN THE PHYSIOLOGICAL ENERGETICS OF FRESHWATER CRUSTACEANS
The demonstration of mechanistic linkages between effects
at different levels of biological organisation has been achieved using the freshwater amphipod Gammarus pulex in
various experimental contexts [49]. Physiological energetics
assessed through measurements of scope for growth have
been used to predict the concentrations of pollutants that
impair growth and reproduction as well as the magnitude of
this impairment. Reduced scope for growth which results
from lower individual feeding rate have been shown to be
correlated with decreased reproductive patterns, through
reduced offspring size and brood viability [50, 51].
Stress-induced reductions in G. pulex feeding rate have
been shown to be correlated to reductions in the rate of incorporation of leaf organic material into freshwater food webs
[51]. Field trials further indicated that between-site differences in G. pulex feeding rate were correlated to differences
586
in community structure, but this correlation did not result
from causal relationships between G. pulex energetics and
community structure [49]. Similarly JONES et al. [53] have
indicated that changes in the feeding behaviour of Daphnia
catawba induced by sublethal concentrations of toxicants
may have more rapid and pronounced effects at the community (i.e. algae populations) than on the cladoceran population itself.
Energetic biomarkers certainly have a real potential for
predicting effects of pollutants on invertebrate population
structure and dynamics [23, 27]. On the basis of experimental and field investigations, a conceptual framework has been
elaborated, which supports modelling approaches [54, 55].
However, compensatory population mechanisms and natural
variations of the parameters related to individual bioenergetics may act as confusing factors so that the regular use of
these latter as predictive biomarkers still requires further
investigations.
These two examples show that mechanistic links can be
established between biomarkers measured in individuals and
changes at the population level, the key-process that links the
individual to the population being reproduction. In invertebrates, biomarkers related to reproduction through hormone
metabolism and energetic balance appear as highly relevant
to predict effects at the population level. Prediction of further
consequences on communities and ecosystems relies on a
sound knowledge of the functional role of the population and
of the interactions between populations.
Assessment of the ecological
impact of chemicals through the
use of biomarkers : concluding
remarks
A large amount of data show that environmental contaminants may exert deleterious effects on organisms and ecological processes. However, even if responses of organisms or
processes to pollutants can been demonstrated in controlled
conditions (e.g. laboratory, microcosms or mesocosms), this
does not necessarily imply that the same responses (or any
response) will be observed in the field. Intrinsic unpredictability of the natural environment generally impedes the identification of precise causal relationships between effects of
toxicants on individuals and subsequent consequences on
populations and communites. The demonstration of such
relationships implies that the component of biological responses due to background fluctuations (e.g. natural variations) and to confounding variables (e.g. natural factors) is
accurately known [56].
Physiological compensation in individuals and/or natural
heterogeneity within populations, that usually ensure survival of species within a community [57], frequently make it
difficult to extrapolate from biochemical and physiological
changes to population-level effects of exposure [58-59].
Compensatory mechanisms have themselves a cost which
can, in turn, interfere with the performances of individuals
LAGADIC (L.)
(Darwinian fitness). Even adaptation or genotype selection
may have a cost in term of population performances (e.g.
decrease of tolerance to other stresses in tolerant populations
with reduced genotype variability) [60-62].
Surprinsingly, population biology is rarely considered in
ecotoxicological studies, even though modelling approaches
of population dynamics, which take into account the effects
of pollutants on various biological responses, have been proposed [63-66].
Population-level effects are sometimes measurable only
after several generations when affected endpoints are longterm parameters such as juvenile recruitment or age to first
reproduction [67, 68]. The age-structure of natural populations may also results in age-specific stress that will not
necessarily affect the whole population survival and dynamics [69]. On the other hand, field observations suggest that
populations are frequently interconnected, especially in
large-scale ecosystems (e.g. sea shore) or spatially complex
landscapes so that the real object of interest for ecotoxicologists should consist in metapopulations rather than in isolated
populations [70].
Therefore, even when laboratory experiments or model
outputs predict either population decrease or survival,
various natural fluctuation processes (e.g. immigration, food
availability, etc) may considerably modify actual demographic parameters, especially in unpredictable or short-lived
systems (e.g. temporal ponds and rivers, coastal ecosystems)
or when pollution is spatially restricted and that juvenile
organisms may colonise from surrounding non-contaminated
areas [56, 71]. Conversely, populations living in uncontaminated environments may be affected by the recruitment of
juveniles from areas which can be polluted. In the case of
such a metapopulation approach, the impact of human activities on habitat fragmentation and/or conservation is of primary importance.
Acknowledgement
Parts of the present contribution were previously discussed
in LAGADIC, L., 1999. Biomarkers in Invertebrates :
Evaluating the effects of chemicals on populations and communities from biochemical and physiological changes in
individuals, in PEAKALL D.B., WALKER C.H. &
MIGULA P. (eds.), 1999. Biomarkers : A Pragmatic Basis
for Remediation of Severe Pollution in Eastern Europe.
NATO Science Series. 2. - Vol. 54. Kluwer academic publishers, Dordrecht, The Netherlands, 323 p, and LAGADIC
L., AMIARD J.-C. & CAQUET Th., 2000. Biomarkers and
evaluation of the ecotoxicological impact of pollutants, in
LAGADIC L., CAQUET TH., AMIARD J.-C. & RAMADE
F. (eds.), 2000. Use of Biomarkers for Environmental Quality
Assessment. Science Publishers, Inc., Enfield, NH, USA. 324
p. I am therefore indebted to all the persons for their contribution to the discussions that have been summarized in the
present review.
Revue Méd. Vét., 2002, 153, 8-9, 581-588
BIOMARKERS : USEFUL TOOLS FOR THE MONITORING OF AQUATIC ENVIRONMENTS
References
1. — WILSON R.C.H., HARDING L.E. and HIRVONEN H. : Marine ecosystem monitoring network design. Ecosystem Health, 1995, 1, 222227.
2. — McCARTHY J.F. and SHUGART L.R. : Biomarkers of
Environmental Contamination. Lewis Publishers, Boca Raton, 1990.
3. — HUGGETT R.J., KIMERLE R.A., MEHRLE P.M. Jr. and BERGMAN H.L. (eds) : Biomarkers. Biochemical, Physiological, and
Histological Markers of Anthropogenic Stress. Lewis Publishers,
Boca Raton, 1992.
4. — WALKER C.H. : The role of biomarkers in ecotoxicology. Toxicol.
Ecotoxicol. News, 1995, 2, 67.
5. — PEAKALL D.B. and WALKER C.H. : Comment on van Gestel and
van Brummelen. Ecotoxicology, 1996, 5, 227.
6. — LAGADIC L., CAQUET Th. and AMIARD J.-C. : Biomarqueurs en
écotoxicologie : principes et définitions. In L. LAGADIC, Th.
CAQUET, J.-C. AMIARD and F. RAMADE (éds.) : Biomarqueurs
en Ecotoxicologie : Aspects Fondamentaux. Collection d’Ecologie,
Masson Editeur, Paris, 1997, 1-9.
7. — LAGADIC L., CAQUET Th. and RAMADE F. : The role of biomarkers in environmental assessment (5). Invertebrate populations and
communities. Ecotoxicology, 1994, 3, 193-208.
8. — DEPLEDGE M.H. and FOSSI M.C. : The role of biomarkers in environmental assessment (2). Invertebrates. Ecotoxicology, 1994, 3,
161-172.
9. — LAGADIC L., CAQUET Th., AMIARD J.-C. and RAMADE F.
(éds.) : Utilisation de Biomarqueurs pour la Surveillance de la
Qualité de l’Environnement.Tec & Doc Lavoisier, Paris, 1998.
10. — MONOD G. : L’induction du cytochrome P4501A1. In L. LAGADIC, Th. CAQUET, J.-C. AMIARD, F. RAMADE (éds.) :
Biomarqueurs en Ecotoxicologie : Aspects Fondamentaux.
Collection d’Ecologie, Masson Editeur, Paris, 1997, 33-51.
11. — NARBONNE J.-F. and MICHEL X. : Systèmes de biotransformation
chez les mollusques aquatiques. In L. LAGADIC, Th. CAQUET, J.C. AMIARD, F. RAMADE (éds.) : Biomarqueurs en
Ecotoxicologie : Aspects Fondamentaux. Collection d’Ecologie,
Masson Editeur, Paris, 1997, 11-31.
12. — BURGEOT Th. and GALGANI F. : Application of EROD in marine
fish in a multidisciplinary surveillance programme in the North Sea.
In L. LAGADIC, Th. CAQUET, J.-C. AMIARD, F. RAMADE
(eds.) : Use of Biomarkers for Environmental Quality Assessment.
Science Publishers, Inc., Enfield (NH), USA, 2000, 33-57.
13. — FLAMMARION P., GARRIC J. and MONOD G. : Use of EROD
enzymatic activity in freshwater fish. In L. LAGADIC, Th.
CAQUET, J.-C. AMIARD and F. RAMADE (eds.) : Use of
Biomarkers for Environmental Quality Assessment. Science
Publishers, Inc., Enfield (NH), USA, 2000, 59-77.
14. — BOCQUENÉ G., GALGANI F. and WALKER C.H. : Les cholinestérases, biomarqueurs de neurotoxicité. In L. LAGADIC, Th.
CAQUET, J.-C. AMIARD and F. RAMADE (éds.) : Biomarqueurs
en Ecotoxicologie : Aspects Fondamentaux. Collection d’Ecologie,
Masson Editeur, Paris, 1997, 209-240.
15. — GALGANI F. and BOCQUENÉ G. : Molecular biomarkers of exposure of marine organisms to organophosphorus pesticides and carbamates. In L. LAGADIC, Th. CAQUET, J.-C. AMIARD and F.
RAMADE (eds.) : Use of Biomarkers for Environmental Quality
Assessment. Science Publishers, Inc., Enfield (NH), USA, 2000, 113137.
16. — AMICHOT M., BERGÉ J.-B., CUANY A., PASTEUR N., PAURON
D. and RAYMOND M. : Molecular, genetic and population bases of
insect resistance to insecticides. In L. LAGADIC, Th. CAQUET, J.C. AMIARD and F. RAMADE (eds.) : Use of Biomarkers for
Environmental Quality Assessment. Science Publishers, Inc., Enfield
(NH), USA, 2000, 247-268.
17. — BLANCATO J.N., BROWN R.N., DARY C.C. and SALEH M.A.
(eds) : Biomarkers for Agrochemicals and Toxic Substances.
Applications and Risk Assessment. ACS Symposium Series, 643.
American Chemical Society, Washington, DC, 1996.
18. — ENGEL D.W. and VAUGHAN D.S. : Biomarkers, natural variability,
and risk assessment : can they coexist ? Hum. Ecol. Risk Assess.,
1996, 2, 257-262.
19. — HOLDWAY D.A. : The role of biomarkers in risk assessment. Hum.
Ecol. Risk Assess., 1996, 2, 263-267.
20. — SCHLENCK D. : The role of biomarkers in risk assessment. Hum.
Ecol. Risk Assess., 1996, 2, 251-256.
21. — US EPA (U.S. Environmental Protection Agency) : Framework for
Ecological Risk Assessment, Washington, DC, Risk Assessment
Forum, EPA/630/R-92/001, 1992.
Revue Méd. Vét., 2002, 153, 8-9, 581-588
587
22. — DARY C.C., QUACKENBOSS J.J., NAUMAN C.H. and HERN
S.C. : Relationship of biomarkers of exposure to risk assessment and
risk management. In J.N. BLANCATO, R.N. BROWN, C.C. DARY
and M.A. SALEH (eds) : Biomarkers for Agrochemicals and Toxic
Substances. Applications and Risk Assessment. ACS Symposium
Series, 643. American Chemical Society, Washington, DC, 1996, 223.
23. — CAQUET Th. and LAGADIC L. : Conséquences des altérations individuelles précoces sur la dynamique des populations et la structuration des communautés et des écosystèmes. In L. LAGADIC, Th.
CAQUET, J.-C. AMIARD and F. RAMADE (eds.) : Utilisation de
Biomarqueurs pour la Surveillance de la Qualité de l’Environnement,
Tec & Doc Lavoisier, Paris, 1998, 265-298.
24. — SUTCLIFFE D.W. (ed) : Water Quality and Stress Indicators in
Marine and Freshwater Ecosystems: Linking Levels of Organisation
(Individuals, Populations, Communities). Freshwater Biological
Association, Ambleside, 1994.
25. — WARD J.B. and HENDERSON R.E. : Identification of needs in biomarkers research. Environ. Health Perspect., 1996, 104 (suppl. 5),
895-900.
26. — WOLFE D.A. : Insights on the utility of biomarkers for environmental impact assessment and monitoring. Hum. Ecol. Risk Assess., 1996,
2, 245-250.
27. — LE GAL Y., LAGADIC L., LE BRAS S. and CAQUET Th. : Charge
énergétique en adénylates (CEA) et autres biomarqueurs associés au
métabolisme énergétique. In L. LAGADIC, Th. CAQUET, J.-C.
AMIARD and F. RAMADE (éds.) : Biomarqueurs en Ecotoxicologie : Aspects Fondamentaux. Collection d’Ecologie, Masson
Editeur, Paris, 1997, 241-285.
28. — MAYER F.L., VERSTEEG D.J., McKEE M.J., FOLMAR L.C.,
GRANEY R.L., McCUME D.C. and RATTNER B.A. : (1992)
Physiological and nonspecific biomarkers. In R.J. HUGGETT, R.A.
KIMERLE, P.M. MEHRLE Jr. and H.L. BERGMAN (eds) :
Biomarkers. Biochemical, Physiological, and Histological Markers
of Anthropogenic Stress, SETAC Special Publication Series, Lewis
Publishers, Boca Raton, FL, 1992, 5-85.
29. — DICKERSON R.L. and KENDALL R.J. (eds) : Endocrine disruptors.
Environ. Toxicol. Chem., Annual Review Issue, 17, 1998
30. — GRUNWALD C. : Steroids. In E.A. BELL, B.V. CHARLWOOD
(eds) : Secondary Plant Products, Encyclopedia of Plant Physiology,
Vol. 8 (A. PIRSON, M.H. ZIMMERMANN, eds), Springer Verlag,
1980, 221-256.
31. — WING K.D., SLAWECKI R.A. and CARLSON G.R. : RH5849, a
nonsteroidal ecdysone agonist: effects on larval Lepidoptera.
Science, 1988, 241, 470-472.
32. — SUNDARAM K.M.S., HOLMES S.B., KREUTZWEISER D.P.,
SUNDARAM A. and KINGSBURY P.D. : Environmental persistence and impact of diflubenzuron in a forest aquatic environment
following aerial application. Arch. Environ. Contam. Toxicol., 1991,
20, 313-324.
33. — KREUTZWEISER D.P. and THOMAS D.R. : Effects of a new moltinducing insecticide, tebufenozide, on zooplankton communities in
lake enclosures. Ecotoxicology, 1995, 4, 307-328.
34. — BALDWIN W.S., MILAM D.L. and LEBLANC G.A. : Physiological
and biochemical perturbation in Daphnia magna following exposure
to the model environmental estrogen diethylstilbestrol. Environ.
Toxicol. Chem., 1995, 14, 945-952.
35. — SHURIN J.B. and DODSON S.I. : Sublethal toxic effects of cyanobacteria and nonylphenol on environmental sex determination and
development in Daphnia. Environ. Toxicol. Chem., 1997, 16, 12691276.
36. — BALDWIN W.S., GRAHAM S.E., SHEA D. and LEBLANC G.A. :
Metabolic androgenization of female Daphnia magna by the xenoextrogen 4-nonylphenol. Environ. Toxicol. Chem., 1997, 16, 1905-1911.
37. — ZOU E. and FINGERMAN M. : Synthetic estrogenic agents do not
interfere with sex differentiation but do inhibit molting of the cladoceran Daphnia magna. Bull. Environ. Contam. Toxicol., 1997, 58,
596-602.
38. — HAWKINS S.J., PROUD S.V., SPENCE S.K. and SOUTHWARD
A.J. : From the individual to the community and beyond : water quality, stress indicators and key species in coastal systems. In D.W.
SUTCLIFFE (ed) : Water Quality and Stress Indicators in Marine and
Freshwater Ecosystems: Linking Levels of Organisation
(Individuals, Populations, Communities, Freshwater Biological
Association, Ambleside, 1994, 35-62.
39. — MATTHIESSEN P. and GIBBS P.E. : Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in mollusks.
Environ. Toxicol. Chem., 1998, 17, 37-43.
588
40. — BLABER S.J.M. : The occurrence of a penis-like outgrowth behind
the right tentacle in spent females of Nucella lapillus (L.). Proc.
Malacol. Soc. Lond., 1970, 39, 377-378.
41. — SMITH B.S. : Sexuality in the American mud snail, Nassarius obsoletus Say. Proc. Malac. Soc. Lond., 1971, 39, 377-378.
42. — ELLIS D.V. and PATTISINA A. : Widespread neogastropod
Imposex: a biological indicator of global TBT contamination ? Mar.
Pollut. Bull., 1990, 21, 248-253.
43. — OEHLMANN J., FIORONI P., STROBEN E. and MARKERT B. :
Tributyltin (TBT) effects on Ocinebrina aciculata (Gastropoda :
Muricidae) : Imposex development, sterilization, sex change and
population decline. Sci. Total Environ., 1996, 188, 205-223.
44. — BRYAN G.W., GIBBS P.E., HUMMERSTONE L.G. and BURT
G.R. : The decline of the gastropod Nucella lapillus around southwest England: Evidence for the effect of tributyltin from antifouling
paints. J. Mar. Biol. Assoc. UK, 1986, 66, 767-777.
45. — MATTHIESSEN P., WALDOCK R., THAI J.E., WAITE M.E. and
SCROPE-HOWE S. : Changes in periwinkle (Littorina littorea)
populations following the ban of TBT-based antifoulings on small
boats in the United Kingdom. Ecotoxicol. Environ. Saf., 1995, 30,
180-194.
46. — LANGSTON W.J. : Recent developments in TBT ecotoxicology.
Toxicol. Ecotoxicol. News, 1996, 3, 179-187.
47. — RUIZ J.M., BACHELET G., CAUMETTE P. and DONARD O.F.X. :
Three decades of tributyltin in the coastal environment with emphasis on Arcachon bay, France. Environ. Pollut., 1996, 93, 195-203.
48. — EVANS S.M., HUTTON A., KENDALL M.A. and SAMOSIR
A.M. : Recovery in populations of dogwhelks Nucella lapillus (L.)
suffering from Imposex. Mar. Pollut. Bull., 1991, 22, 331-333.
49. — MALTBY L. : Stress, shredders and streams: using Gammarus energetics to assess water quality. In D.W. SUTCLIFFE (ed) : Water
Quality and Stress Indicators in Marine and Freshwater Ecosystems:
Linking Levels of Organisation (Individuals, Populations,
Communities, Freshwater Biological Association, Ambleside, 1994,
98-110.
50. — MALTBY L. and NAYLOR C. : Preliminary observations on the ecological relevance of the Gammarus «Scope for Growth» assay: effect
of zinc on reproduction. Funct. Ecol., 1990, 4, 393-397.
51. — TATTERSFIELD L.J. : Direct and indirect effects of copper on the
energy budget of a stream detritivore. Proceedings of the first SETAC
World Congress, 28-31 March 1993, Lisbon, 88.
52. — MALTBY L. : Pollution as a probe of life-history adaptation in
Asellus aquaticus (Isopoda). Oikos, 1991, 61, 11-18.
53. — JONES M., FOLT C. and GUARDA S. : Characterizing individual,
population and community effects of sublethal levels of aquatic toxicants: an experimental case study using Daphnia. Freshwater Biol.,
1991, 26, 35-44.
54. — SIBLY R.M. and CALOW P. : A life-cycle theory of response to
stress. Biol. J. Linn. Soc., 1989, 37, 101-116.
55. — SIBLY R.M. : From organism to population: the role of life-history
theory. In D.W. SUTCLIFFE (ed) : Water Quality and Stress
Indicators in Marine and Freshwater Ecosystems: Linking Levels of
Organisation (Individuals, Populations, Communities, Freshwater
Biological Association, Ambleside, 1994, 63-74.
LAGADIC (L.)
56. — LUOMA S.N. : The developing framework of marine ecotoxicology:
pollutants as a variable in marine ecosystems ? J. Exp. Mar. Biol.
Ecol., 1996, 200, 29-55.
57. — MARSHALL J.D. and MELLINGER D.L. : Dynamics of cadmiumstressed plankton communities. Can. J. Fish. Aqua. Sci., 1980, 37,
403-412.
58. — KLUYTMANS J.H., BRANDS F. and ZANDEE D.I. : Interactions of
cadmium with the reproductive cycle of Mytilus edulis L. Mar.
Environ. Res., 1988, 24, 189-192.
59. — DEPLEDGE M.H., AGARD A. and GYORKOS P. : Assessment of
trace metal toxicity using molecular, physiological and behavioral
biomarkers. Mar. Pollut. Bull., 1995, 31, 19-27.
60. — GUTTMAN S.I. : Population genetic structure and ecotoxicology.
Environ. Health Perspect., 1994, 102 (suppl.12), 97-100.
61. — FORBES V.E. : Chemical stress and genetic variability in invertebrate populations. Toxicol. Ecotoxicol. News, 1996, 3, 136-141.
62. — HEBERT P.D.N. and LUIKER M.M. : Genetic effects of contaminant
exposure - Towards an assessment of impacts on animal populations.
Sci. Total Environ., 1996, 191, 23-58.
63. — KOOIJMAN S.A.L.M. and METZ J.A.J. : On the dynamics of chemically stressed populations: the deduction of population consequences from effects on individuals. Ecotoxicol. Environ. Saf., 1984,
8, 254-274.
64. — SUER J.R. and PENDLETON G.W. : Population modeling and ist
role in toxicological studies. In D.J. HOFFMAN, B.A. RATTNER,
G.A. BURTON Jr., J. CAIRNS Jr. (eds), Handbook of Ecotoxicology,
Lewis Publishers, Boca Raton, 1995, 681-702.
65. — BAVECO J.M. and DE ROOS A.M. : Assessing the impact of pesticides on lumbricid populations: an individual-based modelling
approach. J. Appl. Ecol., 1996, 33, 1451-1468.
66. — KLOK C. and DE ROOS A.M. : Population level consequences of
toxicological influences on individual growth and reproduction of
Lumbricus rubellus (Lumbricidae, Oligochaeta). Ecotoxicol.
Environ. Saf., 1996, 33, 118-127.
67. — SUNDELIN B. : Effects of cadmium on Pontoporeia affinis
(Crustacea: Amphipoda) in laboratory soft-bottom microcosms. Mar.
Biol., 1983, 74, 203-212.
68. — SCOTT J.K. and REDMOND M.S. : The effects of a contaminated
dredged material on laboratory populations of the tubicolous amphipod Ampelisca abdita. In U.M. COWGILL and L.R. WILLIAMS
(eds) : Aquatic Toxicology and Hazard Assessment, ASTM,
Philadelphia, 1989, 289-301.
69. — ZAJAC R.N. and WHITLACH R.B. : Natural and disturbance induced demographic variation in an infaunal polychaete, Nephtys incisa.
Mar. Ecol. Prog. Ser., 1989, 57, 89-102.
70. — MAURER B.A. and HOLT R.D. : Effects of chronic pesticide stress
on wildlife populations in complex landscapes: processes at multiple
scales. Environ. Toxicol Chem., 1996, 15, 420-426.
71. — UNDERWOOD A.J. : On beyond BACI : sampling designs that
might increases reliability detect environmental disturbance. Ecol.
Appl., 1994, 4, 3-15.
Revue Méd. Vét., 2002, 153, 8-9, 581-588