Fish Bioindicators

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Fish as bioindicators
Chapter in Trace Metals and other Contaminants in the Environment · July 2003

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Bioindicators and biomonitors
B.A. Markert, A.M. Breure, H.G. Zechmeister, editors
© 2003 Elsevier Science Ltd. All rights reserved. 639
Chapter 18
Fish as bioindicators
Andreas Chovanec, Rudolf Hofer and Fritz Schiemer

Abstract
In this article, the role offish as bioindicators is discussed. The comprehensive knowledge of
taxonomy, habitat requirements, and physiology offish is a key prerequisite of using fish as
indicators. No other aquatic organism is suitable for the application of so many different
methods which allow the evaluation of the severity of toxic impacts by determining the accu-
mulation of toxicants in tissues, by using histological and haematological approaches or by
detecting morphological anomalies. Due to its complex habitat requirements the fish fauna is
a crucial indicator of the ecological integrity of aquatic systems at different scales, from micro-
habitat to catchment. The fitness of fish species both at the individual level (e.g. growth
performance) and at population level (e.g. population structure) is determined by the connec-
tivity of different habitat elements in a broad spatial-temporal context. Thus bioindication
using fish represents a good monitoring tool especially with regard to both pollution aspects
and to river engineering, e.g. river restoration and management.
Keywords: Toxicant, Pollutant, Accumulation, Ecological Integrity, Connectivity, Habitat

Structures, Water Framework Directive
1. Introduction
Over the last 150 years, aquatic systems worldwide have been impacted by a wide
array of anthropogenic factors (e.g. Falkenmark and Allard, 1991 ; Dynesius and
Nilsson, 1994; Rahel, 2000). Human activities may alter the physical, chemical or bio-
logical processes associated with water resources and thus modify the resident
biological community. Karr (1991) identified five primary classes of environmental
factors, that, when affected by human activities, result in ecosystem degradation:
• food/energy source: e.g. type, amount, and particle size of organic material;
seasonal pattern of available energy;
• water quality: e.g. dissolved oxygen, nutrients, toxic substances;
• habitat structure: e.g. substrate type, sinuosity, channel morphology, connectivity
aspects;
• flow regime: e.g. temporal distribution of floods and low flows ;
• biotic interactions: e.g. competition, parasitism.
In most cases biological communities are sound and precise indicators of the status
of the aquatic system as they are subject to the full range of chemical and physical
influences, additive and synergistic effects included. In this context fish play a crucial
role as bioindicators in water resource management and applied limnological research:
640 A. Chovanec, R. Hofer, F. Schiemer
fish serve as "ecological indicators", "keystones", "umbrellas'', "flagships" and "vul-

nerables" (Noss, 1990).
According to Markert (1994) a bioindicator is an organism (or a part of an organism
or a community of organisms) that contains information on the quality of the environ-
ment. Thus, the use of bioindicators should help to describe the natural environment,
to detect and assess human impacts and to evaluate restoration or remediation
measures; in all these cases fish are intensively used for indication purposes.
The spatial changes of fish communities along the course of river systems and the
use of fish zonation patterns for river classification are examples of some of the most
traditional bioindication approaches (Fritsch, 1872; Thienemann, 1912, 1925). Fish
have also been traditionally used for classifying different types of standing waters. The
nature of the fauna in stagnant water bodies reflects their morphometry, trophic status,
thermal and oxygen stratification and the extent of littoral development.
There are several reasons why fish are widely used to describe natural characteris-
tics of aquatic systems and to assess habitat alterations (Noss, 1990; Cairns et al., 1993;
Chovanec and Spindler, 1997; Boon et al., 2000; Schiemer, 2000; Schmutz et al.,
2000) :
• A long tradition of ecological, physiological and ecotoxicological research on fish
has led to an advanced knowledge of the ecological requirements of a large number
offish species. The effectiveness ofbioindication approaches depends on the sound
knowledge of the indicators' ecological demands and physiology (Schiemer et al. ,
2001).
• A large number of abiotic environmental variables at different spatio-temporal
scales are linked to the complex habitat requirements of particular species and their
ontogenetic stages. Due to the specific habitat requirements and habitat shifts during
the larval and juvenile stages, O+ fish for example are suitable indicators of the
ecological status of river systems (Schiemer et al. , 1991 ; Keckeis et al., 1996).
• As migratory organisms fish are suitable indicators of habitat connectivity or frag-
mentation (e.g. Jungwirth, 1998; Chovanec et al. , 2002). Waidbacher and Haidvogl
( 1998) point out that members of the families Clupeidae (Alosa pontica, Alosa caspia
nordmanni) and Acipenseridae (Huso huso, Acipenser gueldenstaedti, Acipenser
stellatus) migrate distances > 300 km in the Danube River system. Species typical
of the upper reaches of the Danube like the highly abundant barbel Barbus barbus
and nase Chondrostoma nasus migrate distances of more than 50 km.
• Due to the size of fish (and their organs) a great variety of analytical procedures
can be carried out. Pathological results concerning fish illustrate the effects of water
pollution to the scientific community, water management and the public. Some
methods, such as haematological and histo-pathological approaches, are taken from
human medicine.
• Due to the longevity of fish certain indication effects, e.g. accumulation processes,
are increased.
• As primary and secondary consumers at different levels fish reflect trophic condi-
tions in aquatic systems.
• The reconstruction of pristine reference communities is possible due to the exist-
ence of historical information (Muhar et al., 2000).
Fish as bioindicators 641
• Fishery and sport fishing have a long history, in which fish play an important role
as indicators of water quality; because of the use offish by man particularly as food
resource, the condition of fish communities is an important factor in water resource
management.
• Depending on the problem and the indication approach selected, bioindication by
using fish often meets the requirements of both top-down approaches (assessing
changes in communities in the natural environment and testing for sources and
causes of possible problems) and of bottom-up assessments (using laboratory data
to model changes in the more complex natural ecosystems).
• The number of species is relatively small and species are already determinable in
the field.
When using fish as bioindicators problems may arise:
• Fishery-caused alterations, such as species transfer, stocking, overfishing, make it
more difficult to discuss other man-induced degradations of aquatic ecosystems.
• The mobility of many species makes it difficult to identify not only the exact source
of pollution, but also the time and duration of exposure.
Bioindication based on the use of fish generally satisfies the criteria against which
biological monitoring programmes should be judged (Halbwachs and Arndt, 1992;
Cairns et al., 1993 ; Yoder and Rankin, 1995; Chovanec and Koller-Kreimel, 1999;
Karr and Chu, 1999; Chovanec et al., 2000a):
• Sensitivity to stressors: The range of responses must be suitable for the intended
application; factors of different strength should lead to reactions of different inten-
sity (no all or none response, no extreme natural variability).
• The range of response has to be sensitive to the environmental factors and condi-
tions being observed.
• Methods have to be broadly applied in a wide range of stressors and sites.
• The results obtained by bioindication programmes have to be representative of
many parts of the aquatic communities.
• Information has to be provided fast enough to initiate effective management action
before unacceptable damage has occurred.
• Standardised methods are necessary for obtaining comparable results.
• Bioindicators should be cost-effective to collect and identify.
• The application of bioindicators should be possible at a local scale as well as at a
regional or landscape scale.
• Bioindicators should be at least one of the following three major types (Cairns
etal., 1993):
- compliance indicators, which are chosen to assess the attainment and mainte-
nance of ecosystem objectives related to the restoration and maintenance of
environmental quality;
- diagnostic indicators, which provide insight into the cause of noncompliance;
- early warning indicators, which allow for management actions to be imple-
mented before conditions have deteriorated to the point where compliance
indicators become relevant.
In many bioindication programmes fish meet the requirements of all three types.
This chapter provides an overview of different assessment approaches using fish as

bioindicators. Special attention is paid to the indication of different pollution aspects
and to the assessment of running water habitat degradation and the loss of connec-
tivity. The chapter describes indication approaches in the field, laboratory tests under
controlled conditions are not discussed in detail. Recent developments concerning the
role of fish as indicators in integrated assessment procedures are also considered, such
as the requirements of the new EU Water Framework Directive.
2. Fish as indicators of environmental pollution
Despite rising efforts of many industrialised countries to reduce toxicants from indus-
trial and motor vehicle exhausts and to purify industrial and communal waste waters,
our ecosystems still contain harmful concentrations of an increasing number of chem-
icals. They accumulate in soils and sediments from which they can be remobilised
after changing their physico-chemical condition, and many of these substances persist
for decades (e.g. DDTs, PCBs). Concentrations of heavy metals in sediments may
exceed those of the overlying water by a factor of one to ten thousand (Bryan and
Langston, 1992). Even remote areas such as high mountains and arctic regions receive
significant amounts of pollutants by atmospheric deposition after transport over long
distances (Wania, 1999). Relatively small quantities of toxicants may threaten these
highly vulnerable ecosystems (Skjelkvale and Wright, 1998).
The water quality of many rivers and lakes has improved significantly due to the
increasing number of purification plants. However, the treatment of waste water
reduces not only the concentration of toxic substances but also that of non-toxic
organic compounds. This may lead to changes in the bioavailability of chemicals and
their toxicity, in particular of those entering the water by run-off and atmospheric depo-
sition. Suspended inorganic and organic particles have a large surface area and thus a
high capacity for physically absorbing toxicants. Toxic chemicals have been shown to
interact with dissolved or colloidal organic matter by various modes of binding and
absorption (Spry and Wiener, 1991). Many of these complexes are too large or too
polar to diffuse across the gill membrane (Haitzer et al., 1998). Some metal cations
can form lipophilic complexes with specific organic compounds used in agriculture,
forestry and industry (e.g. ditiocarbamates, diethyldithiophosphate) which easily pass
the gill membrane. This leads to both higher levels of metal accumulation than
expected from water concentrations and an altered distribution pattern, with the highest
increase in the brain and eyes of fish (Tjalve and Gottofry, 1991 ). Uptake and toxi-
city of mercury strongly depends on methylation by bacterial activity (Boening, 2000).
Due to its lipophilic character, methyl mercury is absorbed about ten times faster than
the ionic form. On the other hand, several studies have shown that selenium may
reduce mercury toxicity (Cuvin-Aralar and Furness, 1991 ).
Bioavailability and toxicity of metals are controlled not only by suspended particles
and dissolved organic matter but also by water parameters such as hardness, alkalinity,
pH, temperature, and oxygen concentration (Kock and Hofer, 1998). Some of these
factors modulate the speciation of trace metals (Davies et al., 1976). Hydrate ions and
hydroxo-complexes are the most bioavailable forms of metals absorbed by fish gills
(Erickson et al., 1994). However, metals behave differently in natural waters: The
speciation of Pb, Cu, Hg, and Al is highly affected by pH, whereas that of Cd and Zn
is only slightly sensitive to pH alterations (Campbell and Stokes, 1985). The calcium
concentration of the water has a major impact on metal speciation and the permeability
of gill membranes. Competition between divalent metal ions and calcium for binding
sites on the gill surface and the passage through ion-sensitive channels reduce the
uptake and toxicity of metals in hard water (Wicklund and Runn, 1988; Kock et al.,
1995). Uptake of chemicals across gill membranes is also a function of water flow
along the gills (McKim and Erickson, 1991 ). As a consequence, rising temperature,
oxygen depletion and metabolic stimulation (e.g. during reproduction or stress) accel-
erate gill ventilation and thus the uptake of toxicants.
These examples demonstrate that simple approaches of chemical water analyses
often fail to detect environmental changes that are harmful for aquatic organisms. The
complex situation in natural waters, with their synergistic and antagonistic effects,
makes it difficult to predict the impact of toxicants on the ecosystem. In many cases,
the input of toxicants is not constant but intermittent and may remain undetected.
Bioindicators and, in particular, long-living organisms such as fish are sensitive to
the impact of a complex mixture of chemicals on a specific aquatic ecosystem, inte-
grating the environmental load over time and space. Pollutants usually cause a wide
spectrum of effects and responses in organisms ranging from the cellular and biochem-
ical level to the level of behaviour, growth and reproduction. During low and limited
exposure to toxicants, fish respond at a sub-cellular level, but usually organisms can
compensate for the toxic effect, and their health is not seriously affected. Prolonged
and severe exposure, however, may induce a sequence of functional and structural
changes which impair vital functions. Tissue concentrations of chemicals are excel-
lent indicators of the environmental load of a specific toxicant but usually do not
directly reflect the physiological and ecological consequences. Most of the biomoni-
toring techniques, however, focus on different kinds of stress responses which are often
more or less general responses and cannot be attributed to specific toxicants. Permanent
stress - even if it is moderate - interferes with hormonal and biochemical processes
leading to increased metabolism, immunosuppression, disturbed osmoregulation,
failure of reproduction or tissue damages. The low toxicant specificity of many stress
responses is not just a disadvantage, it increases the value of bioindicators for moni-
toring the general environmental load in natural water bodies which may contain
several out of hundreds of different harmful chemicals. For practical use in the field,
biomonitoring methods based on fish should be insensitive to the stress of capture
which may mask the effects of toxicants. The biological parameters analysed in the
assay should be well understood and their modulation induced by endogenous and
exogenous factors other than toxicants should be known. Data on commercially manip-
ulated fish species should be handled with caution, and possible loads of geogenic
origin (e.g. metals) have to be considered.
2.1. Toxicant accumulation in fish tissues
Tissue concentrations of chemicals are a function of uptake, storage, and excretion.

In fish, two different routes of uptake are important, (1) directly from the water, in
Table I. Definition of terms used in ecotoxicology
Bioaccumulation (BA) The accumulation of contaminants in organisms

resulting from water or food uptake.
Bioconcentration (BC) The accumulation of water-borne contaminants directly
from the water by a non-dietary route .
Biomagnification The accumulation of toxicants resulting from ingestion
of contaminated diet.
Bioconcentration factor Quotient of the concentration of a chemical in an
(BCF) aquatic organism and in the water. The BCF can be
predicted from the concentration of a lipophilic
chemical in the water and its Kow·
Octanol-water partition coefficient: In most cases, the
BCF is proportional to the logarithm of K0 w (Banjeree
and Baughman, 1991).
freshwater fish almost exclusively via the gills, in marine species at a low percentage
also through the drinking of water, and (2) the oral uptake and assimilation of conta-
minated food. Hydrophilic molecules are unlikely to pass the gill membrane unless
they are very small (diffusion along an osmotic gradient) or transported by ionic pumps
or channels. Lipophilic compounds, however, are soluble in biological membranes and
cross all barriers. The relatively low oxygen solubility in water requires an extremely
large respiratory surface and a high pumping rate of water. Consequently, the direct
uptake of water-borne toxicants (whose concentration is two orders of magnitude
higher than in the air) is the main route in fish (bioconcentration; see Table 1).
Diet, as the most significant source of toxicants leading to biomagnification along
the food chain, is usually restricted to lipophilic compounds which are almost insol-
uble in water (compounds with log K0 w values of 5- 8) and slowly metabolised, e.g.
halogenated contaminants and pesticides which resist biotransformation (Thomann,
1989; Suedel et al., 1994; Mackay and Fraser, 2000). Lipophilic contaminants are
predominantly stored in lipids including biological membranes and muscles, thus being
of major concern for human nutrition. On the other hand, lipids serve as a protective
reservoir for lipophilic chemicals, and therefore their toxicity decreases with rising
lipid content of fish (Geyer et al., 1994). Top predators (e.g. piscivorous fish) and
species with high lipid contents have been shown to be the most sensitive indicators
for environmental contamination with lipophilic compounds (Geyer et al., 1997).
Liver and kidney are the main sites of accumulation for most toxicants including
metals. These organs are rich in metallothioneins with high affinities to Cd, Hg, Zn,
and Cu. The liver is also involved in a variety of detoxification processes transforming
harmful compounds into less toxic and water-soluble metabolites which are excreted
into the bile. These metabolites are either eliminated with the faeces or reabsorbed
from the gut and returned to the liver by enterohepatic circulation which may increase
the half-life of toxicants in the fish. In the bile of trout exposed to several labelled
organic substances Statham et al. (1976) found concentrations between 11 and 10,000
times higher than in the water. Even under field conditions it has been shown that bile
analysis is a useful tool to evaluate the environmental load of xenobiotics (Pointet and
Milliet, 2000).
The proportion of accumulated toxicants between different tissues of the fish largely
depends on dynamic processes between uptake, storage, and elimination. After short-
term exposure, gills or the digestive tract and the liver usually show a high load of
toxicants, whereas concentrations in kidney, bones (Pb, Zn), and muscles (lipophilic
substances) increase more slowly after a time-lag, but the accumulated chemicals are
more persistent than in other organs (Olson et al. 1978; Kock et al., 1996). Due to
active regulation tissue accumulation of essential metals (Cu, Zn) is saturated at low
levels, and thus a relatively weak indicator of environmental contamination (McGeer
et al., 2000). Acute intoxication stimulates mucus secretion which can act as a chelator
(Shephard, 1994). This may explain at least some of the elevated metal concentrations
observed in fish gills (Felts and Heath, 1984). Strongly varying proportions of in-
organic and organic contaminants between tissue concentrations in wild captured fish
presented in Kime (1998) are not only due to different environmental conditions and
exposure times but also to species- or family-specific patterns. Salmonids, e.g., have
higher copper concentrations in the liver than other families.
2.2. Detoxification and cell protection
2.2.1. Biotransformation
The liver of fish is the major site of the biotransformation of lipophilic chemicals into
more hydrophilic compounds (phase I reaction), followed by their conjugation with
endogenous substances such as glucuronic acid, sulfate, and glutathione (phase II;
Goksoyr and Husoy, 1999). Phase I reaction includes oxidation catalysed by multiple
forms of enzymes known under various names (mixed function oxidase, monoxi-
genase, cytochrome P-450, CYPlA), located on the endoplasmatic reticulum of cells
(microsomal fraction). In most cases, these metabolites are less toxic, but there are
also examples where toxicity develops through this transformation (e.g. parathione ).
The conjugated products are water-soluble and easily excreted into bile, urine or
through the gills.
Under normal conditions the mixed function oxygenases are involved in the meta-
bolism of steroid hormones. Specific forms of these enzymes cover a broad substrate
specificity including several kinds of lipophilic xenobiotics such as PAHs, PCBs,
dioxins, and halogenated compounds which are able to induce the synthesis of these
enzyme complexes. It has been shown that in fish from areas polluted with oil, indus-
trial or domestic wastes, hepatic microsomal cytochrome P-450 activity is highly
elevated and can be used as an early dose indicator (Payne et al., 1987; Bucheli and
Fent, 1995; Goksoyr, 1995). Meanwhile, the cytochrome P-450 system in fish has been
incorporated as a routine method in many monitoring programmes. However, the
degree of induction varies with species, sex, hormonal status, season, and temperature
(Kleinow et al., 1987). Some toxicants, such as organotin compounds, inhibit the
646 A . Chovanec, R. Hofer, F. Schiemer
activity of cytochrome P-450 and glutathione S-aryl-transferase, and thus impair

metabolism and elimination of other toxicants (Fent, 1999). Distinct changes in the
activity of cytochrome P-450 may also interfere with the steroid metabolism of fish
and affect their hormonal balance.
2.2.2. Oxidative stress
The metabolism of xenobiotics frequently results in the formation of reactive oxygen

species (radicals) which significantly contribute to their toxicity. Due to their high reac-
tivity, radicals damage all kinds of biological structures including nucleic acids
(mutation, carcinogenesis), proteins, and membranes (lipid peroxidation). Peroxidation
of unsaturated fatty acids is the most common phenomenon induced by reactive
oxygen species. Peroxidation of fatty acids is a chain reaction modifying many mole-
cules until it is interrupted by either dimerisation of two radicals or by the reaction
with "radical scavengers" such as tocopherol and r3-carotene. In a cascade of reactions,
low molecular weight antioxidants including ascorbic acid, uric acid and glutathione
take up or release single electrons and form relatively stable radicals with low reac-
tivity (Lackner, 1998). Key enzymes for the detoxification of reactive oxygen species
are superoxide dismutase, glutathione peroxidase, peroxidase, and catalase, in conjunc-
tion with enzymes providing reducing equivalents (glucose-6-phosphate dehydro-
genase, glutathione reductase). Glutathione (GSH), a tripeptide, plays a central role
in detoxification processes: Not only does it act as an antioxidant but it is also the
substrate of glutathione peroxidase and the co-factor of glutathione-S-transferase
involved in the conjugation of xenobiotics, and because of its sulfhydryl group, GSH
can also bind metals. When GSH scavenges a radical or is oxidised it undergoes a
dimerisation to the oxidised glutathione disulfide (GSSG) or mixed disulphides with
proteins. In particular, the GSH/GSSG ratio is a sensitive measure of oxidative stress
(Lackner, 1998).
Most components of this complex detoxification system are induced by intracellular
radicals, toxicants and stress, and can be used as an unspecific but powerful early
warning system for environmental pollution (Filho, 1996; Lackner, 1998).
2.2.3. Metallothioneins (MTs)
MTs are low molecular weight proteins with many sulfhydryl groups binding a variety
of metals. MTs are found in all tissues, particularly in the liver and kidney, and play
an important role in the intracellular regulation of the essential metals Zn and Cu.
However, the affinity of Cd and Hg to MTs is even higher so that they may displace
essential metals. MT concentrations in tissues increase by exposure of fish to Cu, Zn,
Cd, or Hg. The changed pattern of metals bound to the protein may serve as an indi-
cator for specific metal pollution (Hamilton and Mehrle, 1986; Dallinger et al., 1997).
However, tissue levels of MTs are also affected by other factors such as reproduction
and different kinds of stress (Overnell et al. , 1987; Hyllner et al. , 1989). For routine
work tissue concentrations of metals are easier to obtain and more informative than
MT analyses.
2.2.4. Heat-shock proteins (HSPs)
Cells contain a family of various low molecular weight proteins (28- 100 kDa) with a
high degree of identity among different organisms. Heat-shock proteins (HSPs) guar-
antee that cellular protein integrity and function are maintained, in particular under
stressful conditions. HSP 70 is the most commonly known representative. Several
studies with cell lines and cell cultures from fish tissues have shown that stressors such
as heat shock and various environmental contaminants induce the de novo synthesis
of HSPs (Iwama et al., 1998, 1999). Fewer investigations have been performed with
the whole fish and they mainly refer to effects of heat shock. It has been shown that
metals, bleached kraft mill effluents but also bacterial and viral diseases increase the
cellular level of HSPs in various tissues. Although HSPs studies in fish are still at an
early stage they may serve as a sensitive but unspecific indicator of the stress status
of fish. Handling stress, however, does not induce HSP70 expression (Vijayan et al.,
1997), but there is only limited knowledge on the relation between stress hormone
levels and the formation of HSPs.
2.3. Inhibition of enzyme activities
2.3.1. 8 Aminolevulinic acid dehydratase (ALA-D):
ALA-D condenses two molecules of aminolevulinic acid to one molecule of porpho-

bilinogen, a component of haemoglobin and haem-containing enzymes involved in
detoxification (cytochromes, catalases, and peroxidases). ALA-D activity in erythro-
cytes is extremely sensitive and highly specific to inorganic lead intoxication, but the
more toxic organic lead compounds have only little effect (Johansson-Sjobeck and
Larsson, 1979; Hodson et al., 1984). Therefore, simultaneous analyses of lead and
ALA-D in the blood may give valuable information on the proportion of alkyl-lead in
the environment (high blood levels of lead but little inhibition of ALA-D).
Although ALA-D is a sensitive and highly specific indicator for pollution with inor-
ganic lead, even severe inhibition by more than 50% of its activity is not associated
with any signs of anaemia, probably due to the large reserve capacity of this enzyme.
"Normal" ALA-D activity varies considerably between species and size classes offish,
and is activated by zinc and tetrachloro-1,2-benzoquinone, a component of bleached
kraft pulp mill effluents (Andersson et al., 1988).
2.3.2. Acetylcholinesterase (AchE)
AchE has a key function in the regulation of nerve impulse transm1ss10n by

hydrolysing the accumulated acetylcholin in cholinergic synapses. Insecticides, in
particular organophosphates and carbamate insecticides, but also toxins of blue green
algae inhibit the activity of this enzyme, leading to behavioural dysfunctions (Brewer
et al., 2001 ). Fish die when more than 70-80 % of the activity is lost (Dembele et al.
2000). Both the highest activity of AchE and the highest sensitivity to inhibition were
found in the brain. However, the activity is not uniformly distributed within the brain,
and the sensitivity to inhibition is species-specific (Perkins and Schlenk, 2000). Other
tissues suitable for environmental monitoring are muscles and blood (cholinesterase).
2.4. llistolol:Jl
Increased levels of stress proteins and specific detoxification systems are typical
responses of organisms to toxicant exposure reflecting their compensatory potential.
Alterations at molecular levels manifest themselves rapidly and do not necessarily
imply impaired cellular functions. Changes at a structural level, however, reflect the
gradual impact on the metabolism ranging from adaptive to degenerative responses
with severe consequences for the survival of fish . Due to the limited set of structural
responses of cells and organelles histopathological changes have been considered
rather unspecific, but they often specify responses of specific physiological functions .
It has been shown that at least at an ultrastructural level toxicants induce a highly
specific pattern of cellular alterations (Braunbeck, 1998). However, the knowledge of
these responses is restricted to a limited number of toxicants investigated. Confronted
with a variety of different potential toxicants, often acting simultaneously, the situa-
tion in the field is much more complex. In contrast to analytical methods the majority
of histopathological investigations is of a descriptive nature, and the number of semi-
quantitative and quantitative studies is small (e.g. Rocha et al., 1995, Braunbeck, 1998,
Bernet et al., 1999).
Gills, liver, and kidney are the organs mostly used for histopathological investiga-
tions. As these organs are also impaired during infections by bacteria, viruses, and
parasites, a comprehensive assessment of the health status offish is necessary to differ-
entiate between toxicant-induced changes and diseases. As tissues start to degrade very
quickly after the death of fish, particularly at high temperatures, only samples of
freshly killed fish can be used for histological evaluations. In this respect, gills are
among the most delicate organs.
As gills have a large and permeable surface directly exposed to the water, they are
highly sensitive to toxicants and are the main site for their uptake. During acute expo-
sure to high concentrations, gills are the first and often most severely damaged organs
of the fish. Typical responses to acute and chronic exposure to toxicants are lifting and
necrosis of the lamellar epithelia and fusion of gill lamellae (Mallatt, 1985). More
chronic effects include hyperplasia (proliferation) of the filamental epithelia which
gradually reduces the respiratory surface, and the rise of mucus cell numbers caused
by physical and chemical irritants and pathogens. Among many other functions, the
mucus plays an important role in trapping toxicants as it provides a renewable surface
and anything that attaches to mucus is rapidly removed (Shephard, 1994). Hypertrophy
of gill epithelia, in particular the activation and proliferation of chloride cells, indi-
cates a disturbance of the ionic balance induced by toxicants or simply by all kinds of
prolonged stress as a result of increased corticosteroid levels (Perry and Laurent,
1993).
The liver is of high diagnostic value as it is not only the key organ for the basic
metabolism of fish but also the major site for biotransformation, accumulation, and
excretion of toxicants. Pollutant-induced changes in the liver have been reviewed by
Couch (1975), Hinton and Lauren (1990), and Braunbeck (1998). Severe pathological
changes induced by both toxicants and diseases include focal inflammations (hepatitis,
perivasculitis, pericholangitis), necroses, and fibroses. The liver of fish is the most
sensitive target organ of carcinogenic toxicants which may induce tumors (hepatoma
and cholangioma; Bailey et al., 1996). Cloudy swelling of hepatocytes followed by
hydropic degeneration and vacuolisation are the result of a disturbed Na/K membrane
pump. An increased number of pycnotic hepatocytes reflects a high cell turnover,
which is not only observed in intoxicated fish but also in females during vitellogen-
esis. Glycogen depletion in the liver often indicates a high metabolic status as it is
found in females during vitellogenesis as well as in fish involved in detoxification
processes and under chronic stress, but it might also be the result of starvation.
In species with glycogen as the main energy source of the liver (e.g. salmonids),
various pesticides may cause a lipid vacuolisation of hepatocytes (lipid degeneration,
steatosis), found also in cultured fish due to dietary imbalance or aflatoxin contami-
nated diet. The diagnostic value of the abundance of melanomacrophages in the liver
is equivocal (Haaparata et al., 1996). Besides species and age dependence,
melanomacrophages have also been correlated with detoxification processes (binding
of metals and radicals, phagocytosis of cell material) during intoxication, diseases, and
starvation (Agius, 1985, Meinelt et al., 1997).
Light microscopical alterations mainly describe degenerative processes, but ultra-
structural changes also reflect fast-responding adaptive processes of high indicative
value in which all cell organelles are involved (Braunbeck, 1998). The proliferation
of the smooth endoplasmatic reticulum is associated with the induction of xenobiotic
biotransformation processes. Differences in numbers and staining activity of peroxi-
somes indicate changes in oxidative stress responses, and the formation of autophagic
vacuoles reflects the turnover of cellular components. Substantial alterations are also
seen in the structures of the rough endoplasmatic reticulum and mitochondria.
The supplementation of routine histological investigations by the more time-
consuming ultrastructural analysis of the liver from a selected number of specimens
is recommended.
2.5. Haematology
Any kind of acute stress leads to an immediate release of stress hormones (cate-
cholamines followed by corticosteroids) which causes a general activation of the
metabolism and, consequently, a better chance of survival in extreme situations
(Pickering, 1981 ). Prolonged stress, however, leads to exhaustion, osmotic imbalance,
and immunosuppression. The use of haematological stress responses as biomarker for
acute or chronic intoxication is limited as they are difficult to separate from effects
induced by handling stress during the capture of wild fish. Within only a few minutes
of stress, blood concentrations of glucose and lactate, and the number and volume of
red blood cells increase significantly (Soivio and Oikari, 1976; Nikinrnaa, 1992).
Slower responses include rising numbers of immature erythrocytes released from the
erythropoietic tissues (indicating an increased turnover of red blood cells), and the
decline of lymphocyte numbers (lymphopenia). The high abundance of neutrophilic
granulocytes, however, is a sign of disease rather than intoxication. Suitable
biomarkers are more independent of acute stress and include anaemia, micronuclei
(small nuclear segments constricted from the erythrocyte nucleus), amitotic divisions
and deformations of erythrocytes (Nikinmaa, 1992). The latter should be evaluated
with caution as they might also be the result of artefacts, in particular when blood
smears are prepared under unfavourable conditions in the field. The amitotic division
of erythrocytes is probably the response to severe respiratory stress caused either by
oxygen depletion or toxicants (Murad et al., 1993). Increased levels of tissue enzymes
in the blood plasma such as GOT (glutamate oxalacetate transaminase) and GPT
(glutamate-pyruvate-transaminase) indicate lesions in liver and kidney during acute
intoxication or diseases rather than chronic exposure to toxicants (Bucher and Hofer,
1990). Reduced activities of ALA-D caused by lead (see above) and the oxidation of
haemoglobin to methaemoglobin in fish exposed to oxidants such as nitrite or mono-
chloramine have proved to be useful indicators of specific intoxication (Buckley, 1982;
Jensen, 1990). In general, blood composition is modified by natural environmental
parameters including temperature and season, and is often sex- and species-specific
(Luscova, 1997).
2.6. Endocrine disrupture
Many natural and synthetic substances interfere with the hypothalamus-pituitary-

gonadal axis leading to alterations in secondary sexual characteristics and in the
development of gonads affecting sexual behaviour and fertility (Crews et al., 2000).
These substances mimic or block the action of hormones or affect their synthesis,
metabolism, and transport. Specific responses depend on the exposure during sensitive
periods of development, in particular during embryonic stages. Effects on reproduc-
tion are thus often delayed and may not be observed for years. Domestic and industrial
effluents may contain a variety of endocrine disruptors such as natural and synthetic
oestrogens originating from anti-baby pills and farm animals, natural phytosterols
(pulpmill effluents), alkylphenols (non-ionic surfactants, e.g. p-nonylphenol), and
organochlorine compounds (e.g. PCBs; Matthiessen and Sumpter, 1998). Many of
these substances are highly persistent with a tendency to accumulate in organisms.
Waste waters usually contain a mixture of hormone-like substances leading to addi-
tive or synergistic effects on the reproduction of fish which are difficult to predict.
The vitellogenin induction in males, analysed in the blood plasma using antibodies,
is the most sensitive indicator of the presence of many kinds of endocrine disrupting
substances in the water (Purdom et al., 1994; Allen et al., 1999). Vitellogenin is the
protein precursor of yolk synthesised in the liver under the control of oestrogen, a
process which does not occur in normal males. On the other hand, vitellogenin
synthesis in vitro has been found to be depressed by polycyclic and halogenated
aromatic hydrocarbons (Anderson et al., 1996). Alternative biomarkers for endocrine
disruptors in fish include changes in the secondary sexual characteristics or the occur-
rence of intersexes which are seen just after dissection or may require histological
techniques to detect more subtle changes in the testes (Ankley et al., 1998). Gonado-
somatic indices (reduced testicular growth) and liver-somatic indices (increased
relative liver weight) as well as sex ratios are other sensitive indicators of the pres-
ence of endocrine disruptors, but they are less specific as they may also depend on
other environmental factors. Although the feminisation of fish exposed to endocrine
disrupting compounds is the most common effect, many substances also interact with
androgen receptors (e.g. pp'DDE) and may lead to the masculinisation of females, e.g.
in the vicinity of kraft mill effluent (Taylor and Harrison, 1999). The effect of toxi-
cants on thyroid hormone receptors (e.g. certain hydroxylated PCBs) has not been
thoroughly investigated (Tyler at al., 1998).
2. 7. Morphological anomalies
The rising abundance of deformed fish larvae and fry may indicate the presence of
teratogenic substances, often without any visible effects on adult fish. As a conse-
quence, fish populations gradually decline without any apparent reason. Selenium,
progressively accumulating in food chains due to human activities, is one of these
substances leading to a massive reproduction failure and is predicted to be a major
threat to fish populations in several regions (Lemly, 1999). Most morphological anom-
alies found in fish concern bone malformations including skeletal anomalies,
deformations of opercula, gill arches and finrays, and scale disorientation (Bengtsson
et al., 1985; Janssens de Bisthoven, 1999). Substances affecting neuromuscular func-
tions (e.g. organochlorine pesticides, zinc) may also cause spinal deformations and
skeletal fractures due to an elevated muscle tone, even in adult fish. Non toxicant-
induced deformations are the result of mechanical damages or vitamin C deficiency.
Morphological anomalies are easily detectable indicators of a disturbed development
or genetic defects and are often only one of many symptoms including physiological
handicaps. Thus, with rising severity of deformation, larvae and fry will be eliminated
rapidly from the population due to natural mortality, predation, and competition
which considerably mask contamination effects. Fluctuating asymmetry, the random
deviation from perfect symmetry in an otherwise bilaterally symmetric trait, has proved
to be an excellent indicator of developmental instability being associated with reduced
fitness (Moller, 1997). Females of the brook stickleback Culaea inconstans with
symmetric pectoral fin ray numbers have about 15% more eggs per clutch than females
with asymmetric fin ray counts (Hechter et al., 2000). In fish, however, the few data
available do not support the theory that fluctuating asymmetry is a useful tool to
monitor environmental pollution (Parsons, 1990).
2.8. Active biomonitoring
Ecotoxicological laboratory experiments under controlled conditions yield valuable

basic data on threshold concentrations, dose-specific responses ranging from the mole-
cular to the behavioural level, detoxification processes, mechanisms of adaptation, and
modulation of toxicity caused by environmental factors. Although the body of know-
ledge of sublethal effects of pollutants is huge and rapidly growing, the toxicological
status under complex field conditions cannot be predicted adequately. In contrast,
studies on natural fish populations reflect the real situation, but, due to the mobility of
fish, their individual life history and, in particular, the duration of exposure are
unknown. Active biomonitoring using fish cages exposed to both a control site and the
contaminated area may combine the advantages oflaboratory and field studies (Grizzle
et al., 1988). However, the use of cages may cause other serious problems: Destruction
of the experimental set-up by storms, floods, and vandalism make such experiments
risky. In experiments with fish sensitive to social stress, e.g. salmonids, the resulting
immunosuppression combined with skin lesions in fish pushing against the net promote
fungal infections and fish mortality. As caged fish are usually fed with pellets, the
dietary input oftoxicants is excluded. As a consequence, data obtained by active moni-
toring in fish cages have to be evaluated very carefully and potential artefacts caused
by social stress or injuries have to be excluded.
The use of fish as sensors has been recommended for actively monitoring the water
quality of industrial effluents and drinking water systems in continuously running and
automatically working early warning systems, with the focus on short-term changes
of toxicity. Testing under controlled and exposed conditions consists of a flow-through
system supplying experimental chambers and recording units measuring a specific
physiological or behavioural activity of the fish. The biological responses are converted
into electronic signals feeding a data analysis system which discriminates between
"normal conditions" and abnormally high deviations caused by increasing levels of
toxicants. An alarm system should indicate rising toxic conditions. Automatic regis-
tration methods for monitoring rheodactil or locomotory behaviour, the frequency of
opercular ventilation, heart rates, coughing rates as a response to irritation of the gill
surface, and electric organ discharges of a weakly electric fish have been developed
or adapted (Cairns and Van der Schalie, 1980; Geller, 1984; Vogl et al., 1999).
Although these methods are useful and sensitive for short-term experiments, they
create serious problems when applied for routine monitoring in an automatic alarm
system. First, it is difficult to discriminate between the wide range of natural fluctua-
tions of fish behaviour or metabolism and the specific responses due to intoxication.
Second, some methods, e.g. the non-invasive registration of gill ventilation and heart
rate, do not give stable bioelectric signals over a long period of time.
2.9. Fish macroparasites as pollution indicators
Heavy metals play an important role as substances affecting aquatic organisms. Their
impact, particularly on fish, is receiving considerable attention. Investigations on
chronic exposure to sub lethal concentrations of pollutants and their effects on the host-
parasite interrelationship and the parasites in particular are often neglected (e.g.
Overstreet, 1997). The number of quantitative studies of heavy metals in both fish
and their parasites has increased recently (e. g. Bucher et al., 1992; MacKenzie et al.,
1995; Sures, 1999; Sures et al., 1999). Most investigations focus on either compara-
tive studies of parasite community changes subsequent to environmental stress (e.g.
Marcogliese and Cone, 1997; Dusek et al., 1998), or on single investigations of heavy
metal concentrations in fish and their parasites (Sures and Siddall, 1999; Sures et al.,
1999). Chubb (1997) confirms the results of Sures and co-workers (summarised in
Sures et al., 1997; Sures et al., 1999) where especially acanthocephalans accumulate
high burdens of lead and cadmium and therefore may be used as sensitive indicators
for monitoring heavy metal contaminations in aquatic ecosystems (see also Kuperman,
1995; Zimmermann et al., 1999).
If fish parasites are to be used as indicators of pollutants they must meet several
requirements to be comparable with free-living organisms. Kennedy (1997) suggested
that the following conditions are necessary if fish parasites are likely to be indicators
for pollution: the fish host must be abundant and easily accessible; parasite species,
despite their overdispersed distribution, must show a high prevalence and abundance
in the fish host population; parasites should be easily identified and not laborious to
remove and count; information on the ecology and biology of both fish host and para-
site should be available.
3. Fish as indicators of the ecological integrity of running waters
3.1. Habitat structures and connectivity aspects
Fish are used not only for the indication of pollution aspects but also to evaluate
compound and complex structural properties of the environment. It is well established
that river engineering has led to drastic changes in the ecological conditions with
regard to longitudinal continuity, lateral interactions with the bordering riparian zones
and the structural subunits within the instream channel. River engineering has led to
deficiencies in functional processes, in habitat diversity, and in the diversity of char-
acteristic biota (Noss, 1990; Townsend, 1996; Ward, 1998; Ward and Stanford, 1995).
Modem, ecologically orientated river engineering attempts to develop management
and restoration schemes in order to maintain and restore the major properties and func-
tional processes and the characteristic biodiversity. An approporiate indication and
monitoring system has to be developed to achieve this goal. Finding relevant descrip-
tors requires the merging of geomorphological, hydrological and biological
parameters. The physical indication system has to include the range and hierarchy of
spatial scales - from the scale of the catchment area to bed sediments, and to combine
the spatial properties with the relevant biological requirements of individual species
and the different stages during ontogeny.
Fish have proved to be of significance as bioindicators of the so-called ecological
integrity (Karr, 1991; Schiemer, 2000) because during their life cycle, the various
guilds integrate a wide range of riverine conditions including the properties of bed
sediments relevant for egg development and the longitudinal integrity for spawning
migrations (Copp, 1989; Gaudin, 2001; Persat et al., 1995; Schiemer et al., 1991;
(Schiemer et al., 2001a).
3.1.1. Structural properties of rivers at different scales
Over the past 20 years several concepts for understanding functional processes and
biodiversity patterns ofrivers have been developed emphasizing their four-dimensional
nature and hierarchical structure with regard to spatial and temporal properties (Frissell
et al., 1986; Noss, 1990; Gregory et al., 1991; Ward and Stanford, 1995; Townsend,
1996; Ward, 1998; Ward et al., 1999).
It is well known that the key factors for understanding running water ecosystems
are the hydrological connectivity between the river and its environment and - over a
longer time span - geomorphic processes within the river corridor controlled by
hydrology. Fluvial "disturbances" create characteristic patch dynamics, spatial hetero-

geneity, and the mosaic structure of densely packed ecotones and an array of
successions over a range of different scales. They also provide the habitat diversity
and the specific habitat conditions for characteristic species and result in high levels
of local species richness (alpha-diversity), habitat diversity and - differences between
habitats (beta-diversity) and consequently, overall species richness (Naiman et al.,
1988; Junk et al., 1989; Naiman and Decamps, 1990; Schiemer and Zalewski, 1992;
Bayley, 1995; Ward, 1998).
The floodpulse concept (Junk et al., 1989) refers specifically to these lateral inter-
actions and exchange processes between the river and the semi-terrestrial adjoining
area, which are inundated by regular or irregular floods. An "inshore retention concept"
recently formulated (Schiemer et al., 2001 b) highlights the significance of hydraulic
storage as a function of channel morphology, heterogeneity and the sinuosity of the
littoral zone. There is supportive evidence that the retentivity of a river reach is signif-
icant for the local microclimate, production processes, and the ability of channels to
retain particulate organic matter. With regard to fish, the production of food and refuge
capacity to withstand wash-out effects and population losses at early stages of their
life history is particularly relevant (Hildrew, 1996). In terms of hydraulics, inshore
retention also varies according to spatial scales: small storage zones will enhance the
growth and production of riverine phyto- and zooplankton while littoral diversifica-
tion along a river reach will be required as microhabitats and refugia for O+ fish. The
model thus proposes that hydraulic retention can be related to biological functions and
forms a general framework for the understanding of the ecology of large rivers.
A fish habitat is defined by structural conditions at various orders of magnitude.
Aspects of the catchment-scale, i.e. longitudinal integrity of the river (the upstream-
downstream connectedness), are very relevant for fish with regard to population
genetics, but also with regard to discharge and transport processes of nutrients and
organic matter. Sediment transport of a river and siltation are expressions of catch-
ment processes (but can also indicate the extent and quality of local buffer strips, see
below).
On the macroscale of the reach of a river, the overall form of the river, the riffle-
pool sequence, the relief of the floodplain, the connectedness between river and
sidearm habitats, longitudinal connectivity between spawning and nursery areas and
flood refugia are decisive. On the mesoscale, structural properties will define instream
habitat availability. The form and sinuosity of inshore structure (e.g. structure of grav-
elbanks) for example and the way it interacts with the hydrological dynamics of a river
determines microhabitat availability and the configuration and steepness of ecological
gradients.
At a microscale, the relief of gravelbanks for example defines the physical nature
of the quality of bed sediments as spawning substrate and the ontogenetically changing
microhabitats.
Because of the complex array of their habitat requirements, fish react sensitively to
the various aspects of ecological integrity, which refers to the functional entity of a
system with regard to its original state (Schiemer, 2000), which can be described by
the physical and abiotic conditions calibrated by the requirements of characteristic
species.
3.1.2. Fish assemblages and the identification of guilds
Fish can be classified according to habitat requirements, e.g. rheotopic or stagnotopic,

or more specifically according to their requirements during specific life phases e.g. for
spawning. Balon (1975, 1981) has developed a classification scheme of reproductive
types based on spawning site selection, adaptive features of eggs and embryos and the
degree of parental care. The main groups distinquished are (a) non-guarders, (b)
guarders, and (c) bearers. Within the "non-guarders" different types are distinquished
according to spawning substrate, e.g. benthic spawners on coarse bottom substrate
(lithophilous), sand (psammophilous) or plants (phytophilous) and brood hiders, e.g.
cave spawners or spawners on invertebrates (e.g. Rhodeus sericeus amarus).
The various reproductive styles are obviously associated with specific habitat
requirements. The distinct sequence of fish assemblages occurring along the longitu-
dinal course of a river system can be related to river gradient and physical habitat
conditions: habitat structure, substrate types, current velocity temperature and oxygen
regime (Huet, 1959). Fish species richness generally increases with stream order
(Lotrich, 1973; Horwitz, 1978) along with increasing habitat diversity and complexity
and an enhanced trophic and energetic basis for the fish populations. The sequence of
assemblages along a river system can be characterised by the array of ontogenetic and
seasonal requirements of the characteristic species (e.g. Jungwirth et al. , 2000). They
define the ecological integrity of aquatic systems with regard to the connectedness of
supplementary and complementary habitats (see Schlosser, 1995) and source and sink
areas of populations.
Large rivers usually contain different guilds of fish according to life cycle ranges.
As far as spawning and nursery sites are concerned floodplain rivers provide a great
diversity of habitats which allows the existence of a variety of ecological guilds. For
European rivers we have distinguished five major guilds (Schiemer and Waidbacher,
1992) according to the preferred zones of occurrence of adults and the spawning and
nursery grounds (Fig. 1).
1. Riverine species dependent on the connectivity of the river with its tributaries. This
group requires rhithral conditions for spawning and during the early life history
stages (e.g. Hucho hucho).
2. Riverine species with spawning grounds and nurseries in the inshore zone of the
river itself (majority of species, e.g. Barbus barbus or Chondrostoma nasus) Group
1 and 2 are now frequently referred to as Rheophilic A.
3. Riverine species with a preference for low-flow conditions (e.g. connected back-
waters) during certain periods in the adult stage (e.g. feeding grounds or winter
refuge), but with spawning grounds and nurseries in the river (e.g. Aspius aspius,
Leuciscus idus). Such species are referred to as Rheophilic B.
4. Eurytopic species (habitat generalists found both in rivers and various types of stag-
nant water bodies. Some of these species require flooded vegetation as spawning
area, e. g. Esox lucius).
5. Lirnnophilic species confined to various microhabitats of the floodplain (e.g.
disconnected former river branches) with vigorous development of submerged
vegetation.
k I aquatic vegetation
f;/,~:1,~~d flooded vegetation
~ gravel banks
Figure J. Schematic presentation of main habitat requirements of five guilds of fish. Circles: preferred
habitats of adults; arrows: spawning and nursery sites (from Schiemer & Waidbacher, 1992).
Riverine species are either linked to the river only, or they spend phases in stagnant
connected water bodies. Stagnotopic forms are found in highly vegetated disconnected
water bodies of the floodplain. Stagnotopic species are characteristic of well dis-
connected, small water bodies and eurytopic forms are found in a wide range of
river-floodplain habitats.
Various structural properties are essential for the various guilds. Some stagnotopic
species such as Misgurnus fossilis are found exclusively in strongly fragmented and
vegetated pools in the wetlands. Such species belong to a highly endangered guild
which indicates that the wetland habitats of these species that border the flood-
plains have been reduced successively due to land reclamation and river restoration.
For such disconnectance specialists, ecological integrity means the long-term sustained
existence of the required habitat type as a result of floodplain development over the
scale of a century or more.
In the large rivers in Europe and North America, the rheophilic guilds contain the
highest number of species, but also the highest proportion of endangered taxa. This
endangerment and the population decline are strong indications of habitat loss and the
loss of the ecological integrity of aquatic systems. For large anadromous migrators
such as sturgeon, the integrity of the catchment area is required. Some of the species
require the connectance between the river and the floodplains, as complementary habi-
tats, e.g. Abramis ballerus in the Danube system, which is a riverine spawner but enters
connected backwaters for feeding and as a winter refuge. Such species are excellent
indicators of lateral connectivity between lotic and lenitic habitat types. In smaller
rivers, pools temporarily isolated along the shoreline have proved to be favourable for
larval fish and may function as local hot spots (Ulmann and Peter, in manuscript).
3.1. 3. Complex arrays of habitat requirements and critical phases
Fish vary dramatically in size and requirements during their ontogeny. Associated with
this variation is a complex array of habitat-use patterns being mediated by migratory
processes. Autecological requirements of the individual species and the match between
these requirements and environmental conditions are decisive for the survival of a
population. The habitat-template and niche concept provides the basis for this approach
(e.g. Winemiller, 1992).
The following scheme (Fig. 2) - based on stream fish - specifies these ontogenetical
and seasonal requirements for physical habitats. Interconnectivity of the various habitat
patches is required for spawning and embryonic development as well as a mosaic of
Spawning
habitat with
incubation
of eggs
~
Movement t o / vement to Feed
Spaw/ Movemen
Spaw
Mosaic of
Refugia from feeding habitat(s)
harsh environmental with favorable
Movement to Refuge growth conditions
conditions (e.g.,
extreme temperatures
Movement to Feed
or flows) with
unfavorable growth
conditions
Figure 2. The basic life cycle of stream fish with emphasis on patterns of habitat use and movement
(from Schlosser, 1995).
feeding habitats allowing for favourable growth conditions in the course of the life
cycle and the availability of refugia under harsh environmental conditions, e.g. during
the winter or in the case of environmental disturbances. Floods, for example, and
successful migration between the various subhabitat types are decisive for the com-
pletion of the life cycle. Suboptimal conditions and the restricted availability of
habitats or refugia will lead to reduced individual performances in growth or repro-
duction and population losses and ultimately to changes in the composition of the
fish community.
The success or failure of a species is largely determined during a few critical stages
of the life history. The value of fish as indicators is largely dependent on the match
or mismatch between environmental conditions and requirements during these critical
phases. At population level, the success of a species will be determined primarily by
reproductive effort and mortality rates during the embryonic and early larval phases.
The quality of the spawning substrates is critical especially in the lithophilous group.
The spawning substrate quality is crucial for the reproductive success as are the water
percolation in the bed sediments and the oxygen supply for the developing eggs. The
high sensitivity during the embryonic stage towards oxygen conditions has been docu-
mented for many species (see Kamler, 1992; Keckeis et al., 1996). Low oxygen levels
retard development and lead to a high egg mortality. Fish therefore act as sensitive
indicators of the quality of spawning grounds with respect to the content of fine sedi-
ment and siltation. Thus, the recruitment of a fish population is a good indicator of
conditions at the landscape level and the nature and quality of buffer strips (Berkman
and Rabeni, 1987; Bisson et al., 1992; Rabeni and Smale, 1995).
An especially critical phase - (particularly relevant for recruitment and year-class
strength) is the larval period. Mortality is high due to narrow niche dimensions. During
the larval and early juvenile phases, drastic changes in microhabitat requirements of
major environmental variables, food, water velocity, structural elements, etc. are
observed (Schiemer and Spindler, 1989; Sempeski and Gaudin, 1995; see overview in
Gaudin, 2001).
During the spawning and early life history period most riverine species are bound
to the inshore zone of the river. Their occurrence or disappearance is indicative of the
structural properties of the inshore zone. Inshore structure combines and integrates the
following elements required for successful recruitment on the micro- and mesoscale:
1. Appropriate stream bed structures for spawning must be in close proximity and
connectance to larval microhabitats. Emerging larvae drift passively to these
nursery zones. Population losses are generally higher in channelised rivers with
lower flow diversification.
2. Microhabitat gradients are required to cover ontogenetic niche shifts with regard
to the velocity of the water current, substrate type and food. The nurseries of
riverine species are almost exclusively found in richly structured littoral zones of
the river. Artificial linear shorelines with steeper slopes are inappropriate micro-
habitats for larval and juvenile fish . The ontogenetic niche profiles are the result
of changing microhabitat requirements. The larvae are bound to sheltered bays
along the river shoreline, where velocities are low despite changing water levels.
With increasing age and size, early juveniles shift into deeper water strata or to
adjoining shallow gravel banks (Fig. 3, Fig. 4).
Post-emergent larvae (15-20 mm)
"Old larvae"/ "Young parrs" (20-40 mm)
Fish location
9 DAY (feeding)
• NIGHT (resting)
Parrs (> 40 mm)

I
jcuANNELj DEAD ZONE
I
TRANSITION ZONE
Figure 3. Dynamics of habitat use in young grayling. The different compartments are schematically
represented by grey and black surfaces if the habitat is used by day or by night, respectively. Arrows
show the tendency of grayling to shift to the river channel with increasing size (from Sempeski & Gaudin,
1995).
3. An important quality of the littoral zone is the proximity to backwaters openly

connected with the river; such backwaters serve as a production zone of fine partic-
ulate organic food, e.g. zooplankton (in the sense of the "inshore retention concept"
see above).
4. Refugia to reduce wash-out effects at sudden flood pulses. Shallow sloping
embankments and littoral diversification can function as buffer zones for O+ fish
against wash-out effects in the event of floods.
Inshore structure is a significant requirement for the O+ stages, as far as the extent
of refugia under conditions of stochastic water level fluctuations and the connectivity
of complementary microhabitats are concerned. These conditions are particularly rele-
vant with regard to population losses especially in the early stages - when the ability
of the fish to search for adequate conditions or to escape critical conditions is limited.
The structural properties of the inshore constitute an important determinant for O+
Percent
100 50 0 50 100
n= 2 937
June
n=540 15 mm
July
n= 1 734
August
n= 1 317
September
n= 428
35-40mm
Bay Gravel bank
Figure 4. Habitat separation between eurytopic (white) and rheophilic (black) fish of the Danube River
downstream of Vienna (Austria) during the first months of life. The columns indicate the portion of the
total sample of fry found in adjacent bays and gravel banks. The average size offish in June and September
is indicated (from Schiemer & Spindler, 1989).
fish with regard to food, temperature and water velocity and will thus be decisive for
individual growth performance during the critical stages.
Ecological quality is not merely dependent on the structural properties but also on
the interaction between geomorphology and hydrology. Water level fluctuations lead
to a continuous shift of microhabitat positions and determine the availability,
connectance, and quality of microhabits and refugia. The quality of inshore zones
depends on the degree to which two dynamic processes are matched: (a) the onto-
genetic change in requirements and (b) the hydrological dynamics of the river which
result in the continuous change of microhabitat locations and conditions. Considering
the strong diurnal hydrological fluctuations occurring in large rivers, the inshore zones
represent a highly stochastic environment for the early life history stages. For example
in the Danube at Vienna the average daily amplitude lies between 20-40 cm. Structural
heterogeneity of the shoreline is a buffer again to population losses (Schiemer et al.,
200la).
Thus, the interaction between structural properties and water level defines eco-
logical qualities and the likeliness of disturbances at a microhabitat scale. Abrupt
changes of conditions, as often encountered in artificial shoreline constructions repre-
sent disturbances for fish. In this context, disturbances are considered to be abrupt
changes of habitat availability or of critical environmental conditions such as water
velocity, dry falling or strongly rising temperatures. Such conditions lead to popula-
tion loss if refugia are not available and appropriately connected.
Population loss is determined by a combination of 3 conditions:
(a) The hydrological extent and timing of water level fluctuations .
(b) Spatial heterogeneity determines the robustness against hydrological changes.
(c) Fish size, determining the escape range: small fish require higher spatial hetero-
geneity than larger ones.
For a detailed insight into bioindication and a causal understanding of environmental
constraints in the early life history period, the functional response towards major
environmental parameters has to be studied.
3.1.4. Individual fitness and habitat profitability in O+ riverine fish
The interaction of the geomorphology and the hydrological dynamics of the river is
not only significant for the population dynamics of riverine fish, but must be addressed
when mentioning habitat quality, which determines individual growth. O+ fish have to
grow fast through a narrow corridor of environmental constraints and threats, and the
match or mismatch between requirements and environmental conditions is particularly
important (Wieser et al., 1988).
Suboptimal conditions are critical because they lead to prolonged duration of larval
development, which makes it more likely that fish have to endure unfavourable or even
lethal conditions. Fast growth through critical periods increases the probability of
survival. A synoptic approach to defining the niche dimensions, environmental hard-
ships and limitations especially during the critical larval phase, is to a large extent
determined by the balance between energetic gains and costs. The knowledge of the
functional response to major environmental conditions during the critical early life
history phase - (temperature, current velocity and food availability) provides insight
into the causes behind the endangerment of individual species and improves the indi-
cation value of fish. For Chondrostoma nasus, a characteristic species of European
epipotamal rivers, such studies have shown the tight energetic balance espcially in the
larval phase. In a continuously shifting, stochastic environment as is the inshore zone
of large rivers, the costs of station maintenance are obviously high and such additional
costs or lower consumption will constrain growth and extend the duration of the crit-
ical period. With increasing body size and more advanced developmental stages, the
energetic scope widens and the escape range is enhanced.
3.1. 5. The indication value of riverine fish
Fish are not only used as indicators of environmental conditions but individual species
are targets for habitat quality assessments. Several models have been developed to
Table 2. The significance of various elements of"ecological integrity" of floodplain rivers for
community structure, population dynamics, and performance in fish (from Schiemer, 2000).
Biotic indicators Ecological parameters
Habitat Connectance Refugia Physiographic

diversity of comple- and trophic
mentary habitat
habitat condition
elements
Community structure
Biodiversity ++ +
Assemblage structure + ++ ++
Endangeredness + ++ ++
O+ assemblage ++ ++ ++
Population dynamics
Year class strength + ++
Recruitment/mortality rates + ++ +
Population exchange processes +
(e.g. migration, drift)
Bioenergetics
Growth ++
Condition ++
Egg size/egg quality ++
define river conditions and habitat quality for individual salmonid species with regard
to fisheries and the conservation of species stocks (e.g. Wesche et al., 1987; Barnard
and Wyatt, 1995; Bowlby and Roff, 1996).
The main value of fish, however, is their role within an overall environmental
assessment. The development of management criteria and restoration strategies for
river systems in order to improve ecological properties and functions requires appro-
priate biological indicators to analyse environmental deficiencies and to document
changes and improvements. In this respect fish are the most significant single indicator
group. Fish can be used within an integrative assessment of "biotic integrity" (Karr,
1991; Angermeier and Karr, 1994) and overall river corridor surveys. To use fish
successfully as indicators, the monitoring aspects have to be clearly defined and the
scope of indication has to be identified.
The matrix (Table 2) relates various elements of ecological conditions and integrity
and their significance for community organisation, population dynamics, and bio-
energetic performances of fish. It is quite obvious that the structure of the assemblage,
the presence or absence of individual species of fish, and their state of endangered-
ness provide a broad overview and a first overall indication of the situation.
A comparison with the original situation ("reference standard", "Leitbild") and char-
acteristic fish assemblages then (which is relatively well assessed for many river types
in Europe) reveals deficiencies.
For a more detailed evaluation the local distribution pattern of the fish fauna, its
population structure, seasonality of occurrence, and growth performance must be
assessed. Particularly the O+ stages of fish are excellent indicators of the diversity and
function of riparian ecotones and the structure of the shoreline. Simple indices of
shoreline diversification, e.g. the littoral development per unit river length, highly
correlate with species number, diversity and population density of O+ fish. Such para-
meters are valuable criteria for an ecologically oriented river engineering at a local
scale (Copp, 1989; Schiemer et al., 1991).
A detailed understanding of the requirements of a wide range of target species is
necessary to further enhance the value of the fish fauna as indicators. Fitness has to
be addressed at the level of both population dynamics and the ecophysiology of crit-
ical stages especially in the early life history period (Elliott, 1994; Keckeis and
Schiemer, 2001). The subject of a recent workshop was the state of the art of using
0+ fish as indicators of the ecological integrity of large rivers (Schiemer and Keckeis,
2001).
3.2. The Index of Biotic Integrity
The Index of Biotic Integrity (IBI) was developed by Karr (1981) for use in non-
salmonid, small warmwater streams in Illinois and Indiana. IBI incorporates many
attributes of fish communities to evaluate biological conditions at sites influenced by
different human activities (Karr and Chu, 1999). The original version of IBI included
12 metrics reflecting species richness and composition, trophic condition, and fish
abundance and condition (Karr, 1981; Karr et al., 1986): number of fish species,
number of darter species, number of sunfish species, number of sucker species, number
of intolerant species, relative abundance of green sunfish, relative abundance of omni-
vores, relative abundance of insectivorous cyprinids, relative abundance of top
carnivores, number of individuals (*), relative abundance of hybrids (*), relative abun-
dance of diseased individuals (asterisks indicate metrics that have been considered not
reliable).
Each metric is assigned a score based on expectations for that metric at minimally
disturbed sites for that region and stream size. Metrics that approximate what experts
would expect at reference sites are assigned a score of 5; those that deviate somewhat
from such sites receive a score of 3; those that deviate strongly are scored 1. The final
index is the sum of all the metrics' scores. The total IBI score determines the ranking
of the site in one of the integrity classes (excellent, good, fair, poor, very poor).
As the IBI became more widely used different versions were developed for different
regions and different types of ecosystems. Although these new versions had a multi-
metric structure, they differed from the original IBI in number, identity, and scoring
of metrics (e.g. Oberdorff and Hughes, 1992; Simon and Lyons, 1995; Gammon and
Simon, 2000).
3.3. The role offish in the EU "Water Framework Directive"
3.3.1. General principles of the Water Framework Directive
The European water management has to be fundamentally reorganised on the basis

of the new "Directive 2000/60/EC of the European Parliament and of the Council
establishing a framework for Community action in the field of water policy" (Water
Framework Directive - WFD; European Union, 2000). One major goal of the WFD
is to achieve the "good ecological status" and "good chemical status" in all surface
water bodies of the EU. The term ecological status corresponds to the general
philosophy of an integrated approach for evaluating the ecological integrity of water
bodies (Chovanec et al., 2000b).
The main principles for the assessment of the ecological status of surface waters
and, thus, the basis of the application of fish-oriented methods are:
• Ecosystem approach: As opposed to other water-relevant EU Directives, the key
issue of the WFD is not to guarantee the different aspects of water utilisation but
to maintain or restore the health of aquatic ecosystems. In this context fish play an
essential role as indicators within integrated assessment procedures.
• Type-specific approach: The assessment procedure is based on a comparison
between a type-specific pristine or near-pristine reference condition and the present-
day status of the water bodies (Muhar et al., 2000; Wimmer et al., 2000).
• Bioindication approach: According to the WFD, assessment has to be based on the
investigation of the aquatic communities, algae (phytoplankton, phytobenthos),
macrophytes, benthic macroinvertebrates, and fish.
• Classification: The degree of deviation has to be ranked in a five-class-system (high,
good, moderate, poor and bad ecological status).
• Heavily modified and artificial water bodies: The WFD permits the member states
to identify artificial and heavily modified water bodies, for which the objective is
the achievement of a good ecological potential. For these types of water bodies not
the type-specific natural condition but a so called "maximum ecological potential"
has to be established as the reference condition. Heavily modified water bodies are
bodies of surface water which are substantially changed in their character as a result
of physical alterations by human activities. Migratory fish species indicating habitat
fragmentation and landscape connectivity patterns will play an important role in
the assessment of e.g. channelised and I or impounded rivers.
• Monitoring: A monitoring network has to be designed in each country which
provides a comprehensive and representative overview of the ecological status
within each river basin.
The WFD provides general definitions of three of the five classes of ecological
status concerning biotic and abiotic parameters; definitions for the fish fauna are given
in Table 3. Fish also play an important role in the setting of chemical quality stan-
dards. Where possible, both acute and chronic data as well as accumulation data shall
be obtained for different taxa (e.g. fish) which are relevant for the water body type
concerned as well as any other aquatic taxa for which data are available.
~
;::-
~
c::i-
c;·
s·
l:l..
Table 3. Definitions for the high, good and moderate ecological status of river and lakes according to fish-based investigations (European Union, §"
2000). s;::;
High status Good status Moderate status
Species composition and abundance There are slight changes in species The composition and abundance of fish
correspond totally or nearly totally to composition and abundance from the species differ moderately from the type-
undisturbed conditions. type-specific communities attributable specific communities attributable to
to anthropogenic impacts on physico- anthropogenic impacts on physico-chemical
All the type-specific disturbance-sensitive chemical and hydromorphological or hydromorphological quality elements.
species are present. quality elements.
The age structures of the fish communities The age structures of the fish communities The age structure of the fish communities
show little sign of anthropogenic disturbance show signs of disturbance attributable to shows major signs of disturbance, attributable
and are not indicative of a failure in the anthropogenic impacts on physico-chemical to anthropogenic impacts on physico-chemical
reproduction or development of any or hydromorphological quality elements, or hydromorphological quality elements, to the
particular species. and, in a few instances, are indicative of a extent that a moderate proportion of the type-
failure in the reproduction or development specific species are absent or of very low
of a particular species, to the extent that abundance.
some age classes may be missing.
°'°'
Vo
0\
0\
0\
Table 4. Classification scheme for fish-based assessment of ecological integrity (Schmutz et al., 2000).
Criteria Levels of ecological integrity
High Good Moderate Poor Bad
Type-specific None or nearly Some species Several species Many species Most species
species none missing m1ssmg missing missing missing
Self-sustaining None or some Several species Many species Most species Nearly all species
species missing m1ssmg missing missing missing
Fish region No shift No shift Shift Shift Shift
Number of guilds No guild No guild Single guilds Many guilds Most guilds
missing missing m1ssmg missing missing ~
Guild composition No alteration Slight Substantial Complete Complete Q

c
alteration alteration alteration alteration ..:
!:)
;::
(':>
_,...,
Biomass and No or nearly Slight Substantial Heavy Extremely
density no changes changes changes changes
?;i
changed
~
Population age No or nearly Slight Substantial Heavy Extremely ~
_..,
structure no changes changes changes changes changed
~
~
;:::,..
~·
~
._,
(':>
3.3.2. Implementation of the Water Framework Directive: need for action
Karr (1981) pointed out that "a key problem in classification is defining the baseline",
and the definition of reference conditions for river classification is no exception. The
implementation of the WFD requires the elaboration of a comprehensive abiotic (e.g.
Wimmer et al., 2000) and biotic typology of surface waters including the definition of
type-specific reference communities for fish as well as a sound scheme for ranking the
ecological status in a five-class system.
For lakes, a first approach of developing reference fish communities by analysing
historical data from between 1500 to 1940 was published by Gassner and Wanzenbock
(1999). The communities are described using factors such as species number and
composition, ecological guilds and abundance.
A five-tiered classification scheme for a fish-based assessment of the ecological
integrity of running waters was developed by Schmutz et al. (2000) and is close to the
requirements of the WFD (Table 4). The weighting of the criteria in an epirhithralic
stream will be different from that in a large potamalic river/floodplain-system. In
the first case, fish species diversity is low even under natural conditions and both
diversity and species composition are, thus, not sensitive criteria. On the other hand,
quantitative information on the population size and age structure of each species is
attainable at acceptable costs and without methodological sampling problems. In
river/floodplain-systems, species diversity is usually high: the sensitivity of the diver-
sity and species composition criteria is, therefore, much higher and quantitative
information becomes less important (Schmutz et al., 2000). As pristine reference sites
of rivers are generally rare in Europe and other parts of the world, the definition of
river-type-specific fish communities has to be based also on other information, such
as historical fish data, historical abiotic data (Muhar et al., 2000) and reference models
(Milner et al., 1993; Barnard and Wyatt, 1995).
4. Concluding remarks
Fish are one of the most frequently used group of bioindicators in ecotoxicological
field studies. The advantage of a comprehensive basic knowledge of toxicology, phys-
iology, and histology exceeds the disadvantage of fish mobility. No other aquatic
organism is suitable for the application of so many different methods which allow
the evaluation of the severity of toxic impacts ranging from compensatory responses
at a molecular and an ultrastructural level (serving as an early warning indicator)
to sublethal and pathological changes as alarm signals for population declines and
irreversible consequences for the whole ecosystem (Figure 5). Some biomarkers are
indicators of unspecific stress, others respond to a group of toxicants with comparable
attributes, and only a few biomarkers are highly substance-specific (Table 5). The
bioindication of the occurrence of specific substances and their impact on specific biota
and the ecosystem are the main focuses of ecotoxicological studies. Several methods
of ecological and toxicological relevance with varying specificity have to be applied
simultaneously to evaluate the ecotoxicological situation under the complex environ-
mental conditions in the field.
TOXICANTS
RESPONSE
T BIOMARKERS
~
i5
"§
">
Compensation
l B1ochem1cal and
phys1olog1cal responses
~
Early warning indicators
Induction of stress proteins and detoxification processes
Ultrastructu ral and haematological changes
---, _
-
"
a:
Stress syptomes, immune suppression,j Biomarkers indicating

decreased condition, disturbed behaviour a critical level
Development of
~
.c
Accumu lation of toxicants oi
-
sublethal injuries
J Tissue damages, deformation: . - !
vulnerabi lity to infections and parasites I
Haematological and histolopathological changes
Enzyme inhibition
Condition factor, storage products
Endocrine disruption
f
From sublethal
to
lethal changes --'
j Reduced reproduction
~c reased mortality
I
[ o e creasing population j
I Disturbed ecosystem I
Ecological
consequences
Figure 5. Different levels of responses of fish exposed to toxicants and the use of fish as a bioindicator
of environmental pollution.
The use of macroparasites as indicators of heavy metal contamination is of

increasing relevance in environmental control. There is a need to develop combined
approaches including both parasite community aspects and accumulation aspects.
Due to its complex habitat requirements the fish fauna is a crucial indicator of the
ecological integrity of aquatic systems at different scales, from microhabitat to catch-
ment. The fitness of fish species both at the individual level (e.g. growth performance)
and at population level (e.g. population structure) is determined by the connectivity of
different habitat elements in a broad spatio-temporal context. Thus bioindication
using fish represents a good monitoring tool especially with regard to river engineering,
e.g. river restoration and management.
In order to further strengthen the role of fish as valuable indicators of the ecolog-
ical integrity of aquatic systems, research is required ranging from the ecological
demands of certain target species to ecosystem processes.
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Chapter in Trace Metals and other Contaminants in the Environment · July 2003

Andreas Chovanec Rudolf Hofer

SEE PROFILE SEE PROFILE

Hydrobiological baseline survey for River Vjosa in Albania View project

Third edition of the "Fauna Aquatica Austriaca" View project

The user has requested enhancement of the downloaded file.

Andreas Chovanec, Rudolf Hofer and Fritz Schiemer

Keywords: Toxicant, Pollutant, Accumulation, Ecological Integrity, Connectivity, Habitat

fish serve as "ecological indicators", "keystones", "umbrellas'', "flagships" and "vul-

This chapter provides an overview of different assessment approaches using fish as

2. Fish as indicators of environmental pollution

2.1. Toxicant accumulation in fish tissues

Tissue concentrations of chemicals are a function of uptake, storage, and excretion.

Table I. Definition of terms used in ecotoxicology

Bioaccumulation (BA) The accumulation of contaminants in organisms

2.2. Detoxification and cell protection

activity of cytochrome P-450 and glutathione S-aryl-transferase, and thus impair

2.2.2. Oxidative stress

The metabolism of xenobiotics frequently results in the formation of reactive oxygen

2.2.3. Metallothioneins (MTs)

2.2.4. Heat-shock proteins (HSPs)

2.3. Inhibition of enzyme activities

2.3.1. 8 Aminolevulinic acid dehydratase (ALA-D):

ALA-D condenses two molecules of aminolevulinic acid to one molecule of porpho-

2.3.2. Acetylcholinesterase (AchE)

AchE has a key function in the regulation of nerve impulse transm1ss10n by

2.6. Endocrine disrupture

Many natural and synthetic substances interfere with the hypothalamus-pituitary-

2.8. Active biomonitoring

Ecotoxicological laboratory experiments under controlled conditions yield valuable

2.9. Fish macroparasites as pollution indicators

3. Fish as indicators of the ecological integrity of running waters

3.1. Habitat structures and connectivity aspects

3.1.1. Structural properties of rivers at different scales

hydrology. Fluvial "disturbances" create characteristic patch dynamics, spatial hetero-

3.1.2. Fish assemblages and the identification of guilds

Fish can be classified according to habitat requirements, e.g. rheotopic or stagnotopic,

f;/,~:1,~~d flooded vegetation

3.1. 3. Complex arrays of habitat requirements and critical phases

Post-emergent larvae (15-20 mm)

"Old larvae"/ "Young parrs" (20-40 mm)

Parrs (> 40 mm)

3. An important quality of the littoral zone is the proximity to backwaters openly

Bay Gravel bank

3.1.4. Individual fitness and habitat profitability in O+ riverine fish

3.1. 5. The indication value of riverine fish

Biotic indicators Ecological parameters

Habitat Connectance Refugia Physiographic

3.2. The Index of Biotic Integrity

3.3. The role offish in the EU "Water Framework Directive"

3.3.1. General principles of the Water Framework Directive

The European water management has to be fundamentally reorganised on the basis

Criteria Levels of ecological integrity

High Good Moderate Poor Bad

Fish region No shift No shift Shift Shift Shift

Guild composition No alteration Slight Substantial Complete Complete Q

3.3.2. Implementation of the Water Framework Directive: need for action

Stress syptomes, immune suppression,j Biomarkers indicating